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Arquipelago - Life and Marine Sciences ISSN: 0873-4704
1
Apletodon gabonensis, a new species of clingfish (Teleostei:
Gobiesocidae) from Gabon, eastern Atlantic Ocean
RONALD FRICKE AND PETER WIRTZ
Fricke, R. and P. Wirtz 2018. Apletodon gabonensis, a new species of clingfish
(Teleostei: Gobiesocidae) from Gabon, eastern Atlantic Ocean. Arquipelago. Life
and Marine Sciences 36: 1 - 8.
The clingfish Apletodon gabonensis sp. nov. is described on the basis of seven specimens
and colour photographs from Gabon, eastern Atlantic Ocean. The species is small,
apparently not exceeding 20 mm total length; it is characterized by having 5 dorsal-fin rays,
4-5 anal-fin rays, 25-27 pectoral-fin rays, head width in males 2.6-4.7 in SL, anus in males
with urogenital papilla present but not pronounced; snout long, broad, anteriorly truncate in
male, narrower and rather pointed in female; preorbital length 1.8-3.8 in head length;
conspicuous maxillary barbel absent in both sexes; disc with 10-12 rows of papillae in
region A, 5 rows of papillae in region B, and 5-7 rows of papillae in region C. The new
species is compared with the other species of the genus; a key to the males of the 6 known
species of the eastern Atlantic genus Apletodon is presented.
Key words: clingfishes, systematics, Gabon, distribution, identification key.
Ronald Fricke (e-mail: [email protected]), Im Ramstal 76, 97922 Lauda-Königshofen,
Germany. PeterWirtz (e.mail: [email protected]), Centro de Ciências do Mar,
Universidade do Algarve, PT-8005-139 Faro, Portugal. Zoo-Bank registration:
http://zoobank.org/urn:lsid:zoobank.org:pub:97E49008-039E-4500-B8FF-
CFAF1A3FAA65.
INTRODUCTION
The clingfishes of the family Gobiesocidae are
distributed worldwide in tropical and temperate
seas, some also living in freshwater streams of the
tropics. They occur on hard substrata, usually on
rocky bottom or in coral reefs, mostly in shallow
waters. Clingfishes are characterized by
possessing an adhesive disc formed by the pelvic
fins, the head depressed, the skin naked, one
dorsal and anal fin each, and several specialized
osteological characters. The family was revised
by Briggs (1955), who distinguished 9 species
from the eastern Atlantic and the Mediterranean,
all belonging to the subfamily Lepadogastrinae.
In addition, there was a single species of Chorisochisminae from the southeastern Atlantic
[Chorisochismus dentex (Pallas, 1769) from South
Africa]. In a recent review of the Gobiesocidae of
the eastern Atlantic, a total of 13 species was
recognized to occur in the area (Fricke et al.
2016). Subsequently, Diplecogaster umutturali
was described from Turkey by Bilecenoğlu et al.
(2017), and Lecanogaster gorgoniphila from São
Tomé and Principe by Fricke &Wirtz (2017).
The clingfish genus Apletodon was first
described by Briggs (1955) on the basis of
Lepadogaster microcephalus Brook,1890 (a
junior synonym of Apletodon dentatus); the genus
was characterized within the subfamily
Lepadogastrinae by having 3 1/2 gills, the gill
membranes attached to the isthmus, the disc
double, the dorsal and anal fins with strong rays,
normal, the subopercular region without a spine,
20-29 pectoral fin rays, the presence of small
incisors in front of each jaw followed by 1-3 well
Fricke and Wirtz
2
developed canines, and 6 rakers on the first gill
arch. Hofrichter & Patzner (1997) found that
Apletodon species have often been confused with
the closely related genus Diplecogaster; they
distinguished Apletodon by its 3 pores of the
lacrymal canal (2 in Diplecogaster), the first anal-
fin ray usually situated below the 1st and 2nd
dorsal-fin ray (usually below 3rd dorsal-fin ray in
Diplecogaster), by the presence of anal papillae
(absent in Diplecogaster), the presence of
caniniform and incisiform teeth (absent in
Diplecogaster), and the thickening and dark
pigmentation of the fin membrane of the anterior
part of the dorsal and anal fin (normal in
Diplecogaster). Briggs (1986a, b) and Hofrichter
& Patzner (1997) distinguished 3 species of
Apletodon from the eastern Atlantic Ocean and
Mediterranean: A. dentatus, Mediterranean and
Black Seas to Scotland; A. incognitus, NW
Mediterranean Sea and Azores; A. pellegrini,
Madeira and Canary Islands along the west coast
of Africa to Port Alfred, South Africa. Apletodon
pellegrini was listed by Briggs (1990) from the
the Cape Verde, Canary, and Annobon Islands,
north to Madeira, and south to South Africa, and
by Vakily et al. (2002) from the Cape Verde
Islands and Senegal. Hofrichter et al. (2000)
described the habitat and ecological aspects of
Apletodon dentatus, and found the species off
Brittany/France in hollow bulbs of the seaweed
Saccorhiza polyschides. Apletodon incognitus
was recorded from the eastern Mediterranean by
Bilecenoğlu and Kaya (2006). Apletodon wirtzi
Fricke, 2007 was described from São Tome and
Principe, tropical eastern Atlantic (Fricke 2007:
69; Wirtz et al. 2007: 17). Apletodon barbatus
Fricke, Wirtz and Brito, 2010 was described by
Fricke et al. (2010) from the Cape Verde Islands.
A sixth, previously unknown species of
Apletodon was observed and collected on 22 Nov.
2017 by the second author in Gabon. It is
described in the present paper.
MATERIALS AND METHODS
Methods follow Briggs (1955) and Hofrichter &
Patzner (1997). The abbreviation 'SL' refers to the
standard length (measured from the tip of the the
snout to the middle of the caudal fin base), 'TL' to
snout to the middle of the caudal fin base), 'TL' to
total length (measured from the tip of the snout to
the end of the caudal fin). The adhesive disc is
divided into 3 different areas: region A is the
anterior portion, region B the posterior portion,
and region C the centre of the disc (as illustrated
by Briggs, 1955). In the description, data of the
holotype are given first, followed by data of the
paratypes in parentheses. Fin rays are counted
using the method of Fricke (1983), where spines
are expressed as Roman numerals, unbranched
soft rays are expressed as lower case Roman
numerals and branched rays as Arabic numerals.
Subspecies classification is no longer used,
following the method of Fricke et al. (2007);
valid taxa of the species group formerly treated as
subspecies are raised to species level. Specimens
cited in the present paper are deposited in the
following collections: CCML (Colección
Ictiologica, Departamento de Biología Animal,
Ciencias Marinas, Facultad de Biología,
Universidad de La Laguna, Tenerife, Spain); HUJ
(Hebrew University of Jerusalem, Fish
Collection, Jerusalem, Israel); MNHN (Muséum
National d'Histoire Naturelle, Paris, France);
SMNS (Staatliches Museum für Naturkunde
Stuttgart, Germany); ZSM (Zoologische
Staatssammlung München, Germany).
RESULTS
TAXONOMY
Apletodon gabonensis, n. sp.
Gabon clingfish (Figs. 1-3, Tab. 1)
Zoo-Bank registration:
http://zoobank.org/urn:lsid:zoobank.org:act:57A
8D1D6-C499-4A92-872C-8058BF5B90F6
TYPES
Holotype. ZSM 47025, male, 19.6 mm SL,
eastern Atlantic Ocean, Gabon, Commune
d’Akanda, 2.4 km southwest of Cap Esterias, 28
km northnorthwest of Libreville, 0°35.641'N
9°18.431'E, 1-2 m depth, P. Wirtz, 22 Nov. 2017.
Paratypes. HUJ 20847, 1 male, 14.3 mm SL;
ZSM 47026, 2 males (12.4-12.8 mm SL) and 3
females (8.2-15.9 mm SL); collection data as for
holotype.
Apletodon gabonensis, a new species of clingfish from Gabon
3
Fig. 1. Apletodon gabonensis sp. nov., ZSM 47025, holotype, male, 19.6 mm SL, Gabon. A Lateral
view; B dorsal view of head showing lateral-line system; C disc. Scale bar 4 mm.
DIAGNOSIS
A species of Apletodon with 5 dorsal-fin rays, 4-5
anal-fin rays, 25-27 pectoral-fin rays; head width
in males 2.6-4.7 in SL; anus in males with
urogenital papilla present but not pronounced;
anal-fin length in distance between anus and anal-
fin origin 1.2-1.5; snout long, broad, anteriorly
truncate in male, narrower and rather pointed in
female; preorbital length 1.8-3.8 in head length;
conspicuous maxillary barbel absent in both
sexes; disc with 10-12 rows of papillae in region
A, 5 rows of papillae in region B, and 5-7 rows of
papillae in region C; head and body of male light
brown, snout and cheeks green with white spots,
top of head with red spots, sides of body with five
dark brown bars bearing white spots.
DESCRIPTION
Dorsal-fin v (v); anal-fin iv (v); pectoral-fin xxvi
(xxv-xxvii); pelvic-fin I, 4 (I, 4); caudal-fin xi(xi).
Gill rakers on 3rd arch 10 (8-10). Measurements
of the type specimens in Table 1.
Upper jaw with 2 (2) canines and 5 (4) incisors,
surrounded by numerous undifferentiated conical
teeth. Lower jaw with 2 (2) canines and 6 (6)
incisors, surrounded by undifferentiated conical
teeth.
Head lateral line system with 2 pores in nasal
canal, 2 pores in postorbital canal, 3 pores in
lacrymal canal, 1 upper and 1 lower pore in
preopercular canal, and no pores in mandibular
canal.
Head broad, depressed. Head length 32.6 (42.7-
44.1) % SL (2.3-3.1 in SL). Maximum body
depth 14.3 (16.8-18.3) % SL (5.5-7.0 in SL).
Maximum head width 22.4 (21.4-38.3) % SL
(2.6-4.7 in SL). Maximum (horizontal) orbit
diameter 8.7 (6.8-9.8) % SL (3.8-6.5 in head
length). Snout long, broad, anteriorly truncate in
male (Figure 1B); narrower and rather pointed in
female. Preorbital length 17.9 (10.5-14.6) % SL
(1.8-3.8 in head length), in males significantly
longer than in females. Interorbital distance 9.7
(8.8-11.0) % SL (3.4-4.6 in head length). Upper
Fricke and Wirtz
4
jaw length 14.3 (14.5-19.5) % SL. Lower jaw
length 10.2 (12.1-16.9) % SL. Maxillary barbel
absent. Anus situated closer to anal-fin origin
than to disc; male with a short urogenital papilla
which is present but not pronounced; distance
between disc and anus 18.9 (15.3-22.0) % SL,
distance between anus and anal-fin origin 11.2
(9.8-14.6) % SL. Preanus length 65.3 (71.2-75.8)
% SL (1.3-1.5 in SL). Caudal-peduncle length 3.6
(3.4-4.4) % SL (22.7-29.5 in SL). Caudal-
peduncle depth 13.3 (8.1-12.7) % SL (7.5-12.4 in
SL) (Figure 1A).
Predorsal-fin length 80.6 (76.1-84.1) % SL
(1.2-1.3 in SL). Preanal-fin length 75.0 (81.8-
92.2) % SL (1.1-1.3 in SL). First rays of dorsal
and anal fins basally slightly thickened in males.
Prepectoral-fin length 42.9 (35.4-48.4) % SL
(2.1-2.8 in SL). Prepelvic-fin length 28.6 (25.0-
31.2) % SL (3.2-4.0 in SL). Predisc length 24.5
(19.4-26.8) % SL (3.7-5.2 in SL). Disc length
21.9 (21.4-32.8) % SL (3.0-4.7 in SL). Disc
membrane inserting at base of 15th (15th-20th)
pectoral-fin ray. Disc with 12 (10-12) rows of
papillae in region A, 5 (5) rows of papillae in
region B, and 5 (5-7) rows of papillae in region C
(Figure 1C). 5 (5) rows of lateral papillae in disc
region A. Caudal-fin length 19.2 (13.4-25.2) %
SL (4.0-7.4 in SL).
Colour in life. Ground colouration cream to
light brown, depending on sea-floor colour. In
colour photos taken by L. Berenger and C.
Serval-Roquefort (Figures 2-3), the male has the
snout and cheeks green with white spots, eyes
cream with brown spots and streaks, and the top
of the head with red spots (Figure 2); sides of
body with five interrupted dark brown bars
bearing white spots, with the white vertebral
column visible through the flesh; fins reddish.
Head of female with brown spots, sides of body
with several dark brown bars, white vertebral
column visible through the flesh.
Colour in alcohol. Similar to live colouration,
but green and red colours fade away.
ETYMOLOGY
The name of the new species, gabonensis,
refers to the type locality off the coast of
Gabon, West Africa.
Fig. 2. Apletodon gabonensis sp. nov., male, Gabon.
Photograph by Lucas Berenger.
Fig. 3. Apletodon gabonensis sp. nov., female, Gabon.
Photograph by Cathy Serval-Roquefort.
DISTRIBUTION AND HABITAT
This new species is currently known only from
Gabon (Figure 5). It was collected at 1-2 m depth,
where it was moderately common on and below
shallow rocks covered with algae. The most
common other species in this habitat were several
members of the family Gobiidae, including
undescribed species (Schliewen et al. in prep.).
COMPARISONS Within the genus Apletodon, the new species is
characterized by 10-12 rows of papillae in disc
region A (versus 3-6 in other species), and 6
incisors in the lower jaw (versus 2-4 in other
species) (see Table 2). The head shapes of the 6
known species of Apletodon differ considerably
in males. Males of Apletodon gabonensis have a
rather long snout (seen from above) similar to
Apletodon gabonensis, a new species of clingfish from Gabon
5
Fig. 5. Geographical distribution of the species of Apletodon. A Apletodon barbatus; B Apletodon dentatus; C
Apletodon gabonensis n. sp.; D Apletodon incognitus; E Apletodon pellegrini; F Apletodon wirtzi.
Fig. 4. Apletodon wirtzi Fricke, 2007, male, São Tomé
Island. Photograph by Claudio Sampaio.
Apletodon wirtzi, but the tip less pointed and
broader; the snouts of the males of the other four
species are distinctly shorter. Unfortunately, the
females of A. gabonensis n. sp. examined in the
present study are too small to show sufficiently
distinguishing characters to differentiate them
from females of A. incognitus, A. pellegrini and
A. wirtzi, except that they show a colouration
which is very similar to that of male A.
gabonensis n. sp. Apletodon wirtzi and A.
gabonensis are not only similar in the head shape
of males but also in the greenish colour of the
head of males (compare Figures 2, 4). They are
probably sister species.
DISCUSSION
The small species of the genus Apletodon are
cryptic and easily overlooked. Because of their
external similarity, they have probably often been
confused in the past. Old distribution records
must therefore be considered with caution. An
example is the alleged presence of A. pellegrini at
Fricke and Wirtz
6
Annobon Island, which is probably a
misidentification of A. wirtzi. Previous records of
Apletodon pellegrini from the Cape Verde Islands
were probably based on A. barbatus. The record
of this species from Madeira Island also appears
doubtful.
Five small specimens of Apletodon from
Cameroon (SMNS 25472, Limbe, Province de
Sud-Ouest, 3°59'49''N 9°12'18''E) were identified
as A. wirtzi by Fricke et al. (2010). However, it is
highly likely that these specimens are actually A.
gabonensis n. sp.. Additional material is
necessary to confirm this record.
It is surprising to find two similar but different
species of Apletodon at the islands in the Gulf of
Guinea and at the coast of Gabon. However, in a
similar distribution pattern, the small stomatopod
Protosquilla calypso Manning, 1974 has been
recorded from the islands of Annobon, São Tomé,
Príncipe and Bioko, while the closely related and
similar Protosquilla folini (Milne-Edwards, 1867)
occurs at the Cape Verde Islands, Senegal, Ghana
and Congo (Manning 1977).
The genus Apletodon is mostly confined to the
eastern Atlantic (including the Mediterranean and
Black Sea). While the short-snouted species are
apparently distributed antiequatorically (A.
barbatus, A. dentatus, A. incognitus, A.
pellegrini), they are replaced in the equatorial
Atlantic by two long-snouted species (A.
gabonensis n. sp., A. wirtzi). Further research on
the occurrence of this cryptic genus is needed, as
there are still large gaps along the coasts of West
Africa where the occurrence of the genus could
not yet be confirmed.
Key to the Species of the Genus Apletodon. The key to species mainly identifies male specimens;
females are often difficult to distinguish. Specimens are sexed by the presence of ovaries, and sexes are
often distinguishable by their head shape (females usually have small and pointed snouts, while males
usually have broader heads).
1a. Maxilla with a conspicuous white barbel in male; upper jaw with 4-5 incisors. ...Apletodon barbatus
1b. Maxilla without a barbel in male; upper jaw with 1-5 incisors. ..........................................................2
2a. No mandibular-canal pores. ………………………………………………………………………….3
2b. Three mandibular-canal pores. ............................................................................................................4
3a. Snout in males short, rounded; rows of papillae in disc region A 4-5; gill rakers on 3rd arch 6;
incisors in upper jaw 1-2; incisors in lower jaw 2-3; pectoral-fin rays 21-24. ..……...Apletodon dentatus
3b. Snout in males long, blunt; rows of papillae in disc region A 10-12; gill rakers on 3rd arch 8-10;
incisors in upper jaw 5; incisors in lower jaw 6; pectoral-fin rays 25-27. ….Apletodon gabonensis n. sp.
4a. Males: head width 3.6-4.0 (mean 3.8) in SL; snout long, more or less pointed, conical, preorbital
length 3.1-4.0 in head length. …………………………………………………………... Apletodon wirtzi
4b. Males: head width 2.4-3.4 in SL; snout short, rounded, preorbital length 2.7-3.4 in head length. ….5
5a. Males: head width 2.9-3.4 (mean 3.3) in SL; anal papillae small, indistinct; both sexes: anal-fin
length in distance between anus and anal-fin origin1.0-1.7 (1.4)…………………..Apletodon incognitus
5b. Males: head width 2.4-3.0 (2.7) in SL; anal papillae large, distinct; both sexes: anal-fin length in
distance between anus and anal-fin origin 1.5-2.3 (1.9). …………………………...Apletodon pellegrini.
Comparative material Apletodon barbatus: SMNS 26427 (holotype,
14.2 mm SL), Santiago Island, Cape Verde
Islands; MNHN 2009-1592 (1 paratype, 13.5 mm
SL), SMNS 26428 (19 paratypes, 6.3-11.4 mm
SL), USNM 396967 (1 paratype, 13.5 mm SL),
Santiago Island, Cape Verde Islands; SMNS
24604 (1, 13.5 mm SL), SMNS 24605 (1, 15.0
mm SL), Sal Island, Cape Verde Islands.
Apletodon dentatus: CCML uncat., 2 specimens,
14.0-14.5 mm SL, Alegranza Island, Canary
Islands, 35 m depth, A. Brito; CCML uncat., 2
specimens, 11.5-17.5 mm SL, northern Lanzarote
Island, Canary Islands, 30 m depth, A. Brito;
SMNS 12664, 1 specimen, 19.1 mm SL, Italy,
Genoa, 44°25’N, 8°57’E, R. A. Kossmann, 1891.
A. incognitus: NMW 93029, holotype, male, France,
Banyuls-sur-mer; CCML uncat., 2 specimens, 21.1-
21.6 mm SL, Punta de La Sal, Gran Canaria, Canary
Islands, 12 m depth, A. Brito; CCML uncat.,1
Apletodon gabonensis, a new species of clingfish from Gabon
7
specimen, 12.2 mm SL, La Graciosa, Canary Islands,
15 m depth, A. Brito; SMNS 21814, 1 specimen, 22.0
mm SL, Azores Islands, Faial Island, Porto Pim,
38°31' N, 28°37'20''W, P. Wirtz, Apr. 1999. A.
pellegrini: SAIAB 10255, 1 specimen, South Africa,
Knysna, under railroad bridge, D. Watts, 21 Nov
1978; SAIAB 10852, 11 specimens, South Africa,
Knysna lagoon, Western Cape area, 34°02’S,
23°02’E, 8 Dec. 1979; SAIAB 14599, 7 specimens,
South Africa. SAIAB 43756, 5 spec., South Africa,
False Bay, Cape Province, 34°10’S, 18°37’E, R.
Winterbottom, 27 Nov. 1975; USNM 198169, 1
paratype, South Africa, Knysna estuary, J.L.B. Smith,
Jan. 1964; USNM 270272, 2 specimens, South
Africa, Bird Island, Algoa Bay. A. wirtzi: SMNS
24130, holotype, male, 14.2 mm SL, Bombom Island,
Principe Group, São Tomé and Principe, 1 m depth,
P. Wirtz, Feb. 2004; MNHN 2005-0170, paratype, 1
male, 10.7 mm SL, same data as the holotype; SMNS
24446, paratypes, 5 specimens, 9.4-12.1 mm SL,
same data as the holotype; SMNS 24132, paratypes, 2
specimens, 9.0-12.1 mm SL, same data as the
holotype; USNM 381374, paratype, 1 male, 11.5 mm
SL, same data as the holotype. Diplecogaster
bimaculata: HUJ 20575, 1 specimen, Balearic
Islands, north of Cabrera, 39°13'55.08''N
2°58'58.62''E - 39°13'51.54''N 2°59'08.58''E, 57 m
depth, R/V Miguel Oliver, 8 June 2016; HUJ 20623,
1 specimen, Balearic Islands, southsoutheast of
Mallorca, 39°13'58.44''N 3°08'35.28''E -
39°14'50.22''N 3°09'16.20''E, 95-87 m depth, R/V
Miguel Oliver, R9 June 2016; HUJ 20577, 7
specimens, Balearic Islands, south of Mallorca,
39°22'05.16''N 2°41'08.64''E - 39°22'06.78''N
2°41'10.68''E, 52 m depth, R/V Miguel Oliver, 9 June
2016; HUJ 20593, 1 specimen, Balearic Islands,
northeast of Mallorca, Menorca Channel,
39°51'06.84''N 3°28'15.84''E - 39°50'59.40''N
3°28'14.04''E, 57 m depth, R/V Miguel Oliver, 10
June 2016; HUJ 20602, 2 specimens, Balearic
Islands, northwest of Menorca, 39°58'54.12''N
3°39'23.46''E - 39°59'01.26''N 3°39'21.48''E, 63-64 m
depth, R/V Miguel Oliver, 15 June 2016; SMNS
12541, 1 specimen, France, Pyrenées Orientales,
Racou, 22 km SSE Perpignan, 42°32’30’’N, 3°1’E, 5
m depth, M. Grabert, Sep. 1991; SMNS 13177, 1
specimen, Italy, Giglio Island, Bay of Campese, at
Faraglione, 42°22’N, 10°52’E, 20 m depth, I. Koch,
28 Apr. 1992; SMNS 14049, 2 specimens, Italy,
Giglio Island, Bay of Campese, at Tralicci, 42°22’N,
10°52’E, 8 m depth, I. Koch, 18 Apr. 1993; SMNS
19061, 2 specimens, Northern Cyprus, Karavas
Alsavcak Bay, 9 km W Kyrenia/Girne, 35°21’13’’N,
33°13’15’’E, 0-1 m depth, R. Fricke, 19 May 1997;
SMNS 19204, 2 spec., Italy, Giglio Island, Bay of
Campese, 42°22’35’’N, 10°52’58’’E, 10 m depth, I.
Koch, 14 June 1985; SMNS 20163, 8 specimens,
Madeira, off Hotel Roca Mar, Caniço de Baixo, 40-
70 m depth, P. Wirtz, 22 Sep. 1996; SMNS 20347, 1
specimen, Tunisia, 4 km E Tabarca, 6 km E
Bone/Annaba, 36°57’22’’N, 8°47’52’’E, 0-6 m
depth, R. Fricke, 23 May 1998; SMNS 21202, 2
specimens, Madeira, Porto Novo, 1-2 m depth, P.
Wirtz, 16 Oct. 1998. D. pectoralis: SMNS 11916, 4
specimens, Azores Islands, Faial Island, Horta,
38°32’N, 28°38’W, P. Wirtz, Dec. 1990.
ACKNOWLEDGMENTS
We would like to thank A. Brito (CCML), D.
Golani (HUJ), P. Pruvost (MNHN), M.E.
Anderson and V. Mthombeni (SAIAB,
Grahamstown) and J.T. Williams (USNM,
Washington D.C.) who gave access to specimens
in their care. D. Golani (HUJ), U. Schliewen and
D. Neumann (ZSM, München) provided
catalogue numbers for type specimens.
The second author is grateful to Lucas Berenger
and Thomas Menut for their invitation to
participate in the expedition of the French
environmental organization BIOTOPE to the
rocky coast of Gabon. This expedition was
organized by the Gabonese National Parks
Agency in collaboration with Fondation
BIOTOPE and financed by the French
Development Agency. This study received
Portuguese national funds through FCT -
Foundation for Science and Technology - through
project UID/Multi/04326/2013.
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Apletodon incognitus Hofrichter et Patzner 1997
(Gobiesocidae) in the eastern Mediterranean Sea.
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Bilecenoğlu, M., M.B. Yokeş and M. Kovačić 2017. A new
species of Diplecogaster (Actinopterygii: Gobiesocidae)
Fricke and Wirtz
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from the Mediterranean Sea. Zoology in the Middle East
2017: 1-9.
Briggs, J.C. 1955. A monograph of the clingfishes
(order Xenopterygii). Stanford Ichthyological
Bulletin 6: i-iv + 1-224.
Briggs, J.C. 1986a. Gobiesocidae. Pp. 1351-1359. in:
Whitehead, P.J.P., Bauchot, M.-L., Hureau, J.-C.,
Nielsen, J. and E. Tortonese (Eds): Fishes of the
Northeastern Atlantic and the Mediterranean, vol
3. UNESCO, Paris.
Briggs, J.C. 1986b. Family no. 110: Gobiesocidae. Pp.
378-380, pl. 14. in: Smith, M.M. and P.C.
Heemstra (Eds): Smith’s sea fishes. Macmillan
South Africa, Johannesburg, 1047 pp..
Briggs, J.C. 1990. Gobiesocidae. Pp. 474-478. in:
Quéro, J.C., J.-C. Hureau, C. Karrer, A. Post and L.
Saldanha (Eds): Check-list of the fishes of the
eastern tropical Atlantic. UNESCO, Lisbon.
Fricke, R. 1983. A method of counting caudal fin rays of
actinopterygian fishes. Braunschweiger Naturkundliche
Schriften 1: 729-733.
Fricke, R. 2007. A new species of the clingfish genus
Apletodon (Teleostei: Gobiesocidae) from Sao
Tome and Principe, Eastern Central Atlantic.
Ichthyological Research 54(1): 68-73.
Fricke, R., M. Bilecenoglu and H.M. Sari 2007. Annotated
checklist of fish and lamprey species (Gnathostomata
and Petromyzontomorphi) of Turkey, including a Red
List of threatened and declining species. Stuttgarter
Beiträge zur Naturkunde, Serie A (Biologie) 706: 1-169.
Fricke, R., J.C. Briggs and J.D. McEachran 2016.
Gobiesocidae. Clingfishes. Pp. 2807-2809. in:
Carpenter, K.E. and N. De Angelis (Eds). The
living marine resources of the Eastern Central
Atlantic. Volume 4. Bony fishes part 2 (Perciformes
to Tetradontiformes) and Sea turtles. FAO, Rome.
Fricke, R. and P. Wirtz 2017. Lecanogaster
gorgoniphila, a new species of clingfish (Teleostei:
Gobiesocidae) from São Tomé and Principe,
eastern Atlantic Ocean. Arquipelago - Life and
Marine Sciences 35: 1-10.
Fricke, R., P. Wirtz and A. Brito 2010. A new species
of the clingfish genus Apletodon (Teleostei:
Gobiesocidae) from the Cape Verde Islands,
Eastern Central Atlantic. Ichthyological Research
57 (1): 91-97.
Hofrichter, R., T. Breining and R.A. Patzner 2000.
Habitat selection and feeding ecology of two
Atlantic clingfish species, Apletodon dentatus and
Diplecogaster bimaculata in Brittany, France.
Zeitschrift für Fischkunde 5: 71-81.
Hofrichter, R. and R.A. Patzner 1997. A new species of
Apletodon from the Mediterranean Sea and the
eastern Atlantic with notes on the differentiation
between Apletodon and Diplecogaster species (Pisces:
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Manning, R.B. 1977. A monograph of the West
African stomatopod Crustacea. Atlantide Report
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B. Samb, A.J. Dos Santos, M.F. Sheriff, M. Ould
Taleb Sidi and D. Pauly 2002. Poissons marins de
la sous-région nord-ouest africaine. EUR 20379
FR, Commission Européenne, Bruxelles.
Wirtz, P., C.E.L. Ferreira, S.R. Floeter, R. Fricke, J.L.
Gasparini, T. Iwamoto, L. Rocha, C.L.S. Sampaio
and U.K. Schliewen 2007. Coastal fishes of São
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(Eastern Atlantic Ocean) – an update. Zootaxa
1523: 1-48.
Submitted 13 June 2018. Accepted 20 July 2018.
Published online 14 Dec 2018.
Arquipelago - Life and Marine Sciences ISSN: 0873-4704
9
Snake eels (Ophichthidae) of the remote St. Peter and St.
Paul’s Archipelago (Equatorial Atlantic): Museum records
after 37 years of shelf life
OSMAR J. LUIZ AND JOHN E. MCCOSKER
Luiz, O.J. and J.E. McCosker 2018. Snake eels (Ophichthidae) of the remote St.
Peter and St. Paul’s Archipelago (Equatorial Atlantic): Museum records after 37
years of shelf life. Arquipelago. Life and Marine Sciences 36: 9 - 13.
Despite of its major zoogeographical interest, the biological diversity of central Atlantic
oceanic islands are still poorly known because of its remoteness. Incomplete species
inventories are a hindrance to macroecology and conservation because knowledge on
species distribution are important for identifying patterns and processes in biodiversity and
for conservation planning. Records of the snake-eel family Ophichthidae for the St. Peter
and St. Paul’s Archipelago, Brazil, are presented for the first time after revision of material
collected and deposited in a museum collection 37 yrs ago. Specimens of Apterichtus
kendalli and Herpetoichthys regius were collected using rotenone on sand bottoms and one
Myrichthys sp. was observed and photographed swimming over a rocky reef. Remarkably,
these species were not seen or collected in the St. Peter and St. Paul’s Archipelago ever
since despite the substantial increase of biological expeditions over the past two decades,
suggesting that the unjustified rotenone sampling prohibition in Brazil is hindering
advancement of the nation’s biological diversity knowledge.
Key words: Central Atlantic islands, Anguilliformes, sampling bias, rotenone prohibition.
Osmar J. Luiz (e-mail: [email protected]), Research Institute for the Environment and
Livelihoods, Charles Darwin University, Darwin, NT 0810 Australia. John E. McCosker,
California Academy of Sciences, San Francisco, CA 94118 USA.
INTRODUCTION
Museum collections are an invaluable resource
for biodiversity research, having provided, among
other things, innumerable new species that were
discovered among preserved specimens.
However, species ‘shelf life’ - i.e. the period from
the first collection of a specimen of a new species
to its formal description and naming in the
scientific literature - is decades long on average
(Fontaine et al. 2012). Consequently, long shelf-
life periods of new species in museum collections
delays taxonomic progress and is a major factor
contributing to the Linnean shortfall (i.e. the
knowledge discrepancy between formally
described species and the number of species that
actually exist; Hortal et al. 2015).
Likewise, known species that have been
collected in a given locality for the first time can
also face a long shelf life period until the new
occurrence is reported in the literature, potentially
resulting in incomplete knowledge about their
geographical distribution, or the Wallacean
shortfall (Hortal et al. 2015). The Wallacean
shortfall has important implications for
biogeography and macroecology because data on
the distribution of species are vital for identifying
broad-scale patterns in biodiversity and the
processes driving those patterns. The Wallacean
shortfall can also influence estimates of conservation
Luiz and McCosker
10
threat status since geographic range size is frequently
used in conservation planning, in which species with
small ranges are given higher priority (Hoffmann et
al. 2008).
New occurrences of species’ geographic
records are acquiring momentum in the context of
climate change (Fogarty et al. 2017) and
biological invasions (Luiz et al. 2013; Pajuelo et
al. 2016). Consequently, effort towards
diminishing specimens’ shelf life in museum
collection records is becoming increasingly
important, especially for remote places where
sampling is scarce due to logistic and financial
constraints. Here we bring to light details of the
first geographic records of two snake eel species
(Anguilliformes: Ophichthidae) from the remote
Saint Peter and Saint Paul’s Archipelago
(hereafter SPSPA) that were collected 37 years
ago and another that was subsequently
photographed in 1981 by a scuba diver.
The SPSPA - formerly known in the biological
literature as Saint Paul’s Rocks (Lubbock and
Edwards 1981; Luiz and Edwards 2011) - is a
group of barren islets in the equatorial Atlantic
Ocean, on the mid-Atlantic ridge (00°55’N,
29°21W), located at 960 km off Cape of São
Roque, north-eastern coast of Brazil and 1890 km
south-west off Senegal, West Africa. The fauna
of SPSPA is of considerable zoogeographical
interest because of peculiar characteristics of
isolation, small area and high endemism. Despite
the SPSPA’s renown as a regular stopover during
important 19th century expeditions, including
those of Charles Darwin on the H.M.S. Beagle in
1832 and of H.M.S. Challenger in 1873 (Luiz &
Edwards 2011), detailed studies of its
ichthyofauna are relatively recent. The first
inventory of demersal fishes of the SPSPA was
done in 1979 (Lubbock & Edwards 1981).
Subsequent expeditions primarily intended to
study demersal fishes in the SPSPA took place
only after 1998 after the construction of a
research station by the Brazilian Navy. Currently,
there are approximately 60 species of demersal
fishes recorded in the SPSPA (Feitoza et al. 2003;
Ferreira et al. 2009). So far, the order
Anguilliformes were represented in the SPSPA
only by the family Muraenidae, with seven
species recorded (Feitoza et al. 2003, Vaske et al.
2005). In this note we report the occurrence of
three additional species of anguilliforms
belonging to the snake eel family (Ophichthidae).
MATERIALS AND METHODS
The snake eel specimens were collected in 1981
by Alex Smart, a former zoology student in the
University of Florida (UF) and a photograph
taken (the specimen was not collected) by
Alexander MacPherson while scuba diving in
1981. Those specimens, along with further
material photographed and collected by A. Smart
in the SPSPA, are deposited in the Florida
Museum of Natural History (FLMNH) and the
California Academy of Sciences (CAS).
Specimens were analysed and identified by JEMC
and the late Eugenia Böhlke. Voucher numbers
are given below.
RESULTS AND DISCUSSION
Apterichtus kendalli (Gilbert, 1891) (Figure 1)
Sphagebranchus kendalli Gilbert 1891. Type
locality: Off Florida, Gulf of Mexico, USA.
Fig. 1. Specimens of Apterichtus kendalli collected
with rotenone in the Saint Paul’s archipelago
Examined material: FLMNH —UF 44624 (8), Center Islands Bay, St. Paul’s Rocks, Brazil,
Snake eels of St. Peter and St. Paul’s Archipelago
11
Atlantic Ocean, 01 July 1981, Coll. Alex Smart, at a depth of 10 m, rotenone station. Distribution: From the western Atlantic from the Carolinas, Florida, Bermuda, Bahamas, Lesser Antilles and Brazil, and from St. Helena Island, and now St. Paul’s Rocks. Known from 6-401 m (mostly 30-80 m) depth (Edwards & Glass 1987; Robertson & Van Tassell 2017, McCosker & Hibino 2015). Remarks: These distinctive specimens were
identified by the late Eugenia B. Böhlke and the
second author.
Herpetoichthys regius (Richardson, 1848)
(Fig. 2)
Ophisurus regius Richardson, 1848. Type
locality: St. Helena Island, South Atlantic.
Fig. 2. Herpetoichthys regius collected with rotenone
in the Saint Peter archipelago.
Examined material: FLMNH - UF 172077 (2)
and CAS 227182 (2), St. Paul’s Rocks, Brazil,
Atlantic Ocean, 04 July 1981, Coll. Alex Smart,
at a depth of 15m, rotenone station.
Distribution: Ascension Island, St. Helena Island
and St. Paul’s Rocks in the South Atlantic and
Mauritania Coast in Eastern Atlantic (Edwards “
Glass 1987; Wirtz et al. 2017). Santa Catarina
State on the Brazilian Coast, south-western
Atlantic (Anderson et al. 2015). Known from 15-
170 m (McCosker 2016).
Remarks: Our specimens do not differ in
morphology or in meristics from specimens reported
by McCosker et al. (1989).
Myrichthys sp. (Fig. 3)
Examined material: A photograph taken by
Alexander MacPherson, at a depth between the
surface and 10 m at St. Peter’s Rocks during
May/June 1981.
Fig. 3. Myrichthys sp. Photo: Alexander MacPherson
taken at St. Peter’s Rocks, between 0 - 10 m.
Distribution: See Remarks below.
Remarks: Our identification of this eel is based
solely on a photograph, however its appearance is
unique and clearly that of a Myrichthys.
Myrichthys is easily recognized within the family
due its prominent dorsal-fin origin and usually
spotted or striped coloration. It is also unlike most
ophichthids which spend the majority of their
lives buried in the substrate. There are two
closely related gold-spotted Myrichthys in the
Atlantic, M. ocellatus (Lesueur, 1825) and M.
pardalis (Valenciennes, 1839), separated by their
vertebral numbers. They have previously been
synonymized (Gunther 1870; Fowler 1936).
However, McCosker et al. (1989) recognized
them as distinct species. Myrichthys ocellatus,
described from a Barbados specimen, has 151-
159 total vertebrae, and is an insular species,
known from Bermuda, the Florida Keys,
throughout the West Indies, and south to Brazil
(McCosker & Rosenblatt 1993). Myrichthys
pardalis, described from a Canary Island
specimen has 164-173 total vertebrae and is also
an insular species, known from the “islands of the
eastern Atlantic including São Tomé, the Cape
Verde Islands, the Canaries and Annoban, and the
Gulf of Guinea (McCosker 2016). Lacking a
specimen and the ability to examine its meristics
and morphometrics, and ultimately its
cytogenetics, we are unable to identify
Luiz and McCosker
12
this species and are prepared for the possibilities
that it might be an endemic species or that the two
species are synonymous.
The occurrence of these three snake eel species
in the SPSPA is not unexpected given that they
are found in the relatively close St. Helena Island
and Ascension Island. Nevertheless, to the best of
our knowledge, this represents the first record of
Apterichtus kendalli for Brazilian waters. It is
intriguing, however, that those species have never
been found in the many expeditions to the SPSPA
performed by Brazilian researchers during the last
decade. The sharp snouts and tails and muscular
and cylindrical bodies of snake eels are well
adapted for burrowing, and many of those species
(especially A. kendalli) spend most of their adult
lives buried in the shallow sand and soft
sediment. It is necessary to use specific methods
to catch them, the most efficient being rotenone
ichthyocides over sand bottoms.
Sampling with rotenone is prohibited in Brazil
since the late 1990’s despite being one of the best
tools available for discovering vital information
about the biodiversity of marine fishes (Robertson
& Smith-Vaniz 2008). Over the past decades, the
use of rotenone has become a concern to
environmental and animal rights groups. As a
result, its use has been challenged, halted, or
discouraged based on evidence of effects on non-
target fauna and health concerns on mammals
(Pan-Montojo et al. 2012; Dalu et al. 2015; Melo
et al. 2015). Nevertheless, rotenone sampling can
be completely safe and potential environmental
impacts largely minimized if rotenone is used
with caution (Finlayson et al. 2000; Robertson &
Smith-Vaniz 2008).
Rotenone use is not an alternative sampling
method, but a complementary one that is essential
for ensure broad taxa coverage in fish assemblage
surveys around the globe, especially of
cryptobenthic, turbid-habitat and deep-reef
species (Ackerman & Bellwood 2000; Ross &
Quattrini 2007; Grubich et al. 2009; Ilves et al.
2011). It is well known that fish biodiversity
surveys relying only on visual sampling fail to
detect a large proportion of species present in the
area, particularly cryptic species that live within
the habitat matrix and out of sight of divers
(Ackerman & Bellwood 2002, Ilves et al. 2011).
Therefore, it is very likely that modern
researchers are overlooking an important section
of the nation’s fish diversity because of sampling
limitations.
ACKNOWLEDGMENTS
We thank R. Robins and G. Burgess for tracking
down specimens and photographs at FLMNH and
A. MacPherson for his advice and permission to
use his photograph.
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Received 26 Sep 2018. Accepted 01 Oct 2018.
Published online 14 Dec 2018.
15
SHORT COMMUNICATION
First record of the Sculptured Mitten Lobster Parribacus
antarcticus (Crustacea, Decapoda, Scyllaridae) from the Cabo
Verde Islands (eastern Atlantic)
RUI FREITAS AND PETER WIRTZ
Freitas, R. and P. Wirtz 2018. First record of the Sculptured Mitten Lobster
Parribacus antarcticus (Crustacea, Decapoda, Scyllaridae) from the Cabo Verde
Islands (eastern Atlantic). Arquipelago. Life and Marine Sciences 36: 15 – 18.
Key words: Slipper lobster, biodiversity, West Africa, Cape Verde
Rui Freitas (email: [email protected]) Faculdade de Engenharia e Ciências
Marinhas, Universidade de Cabo Verde, CP 163 Mindelo, Cabo Verde; P. Wirtz
([email protected]): Centro de Ciências do Mar, Universidade do Algarve,
Campus de Gambelas, PT-8005-139 Faro, Portugal.
INTRODUCTION
The lobster genus Parribacus contains six living
and one fossil species (Holthuis 1991; Chan
2010; Nyborg & Garassino 2017). In the Atlantic
Ocean, only one living species is known,
Parribacus antarcticus (Lund, 1793); it has been
recorded in the western Atlantic from Florida to
Brazil and recently also from the mid-Atlantic
island of Ascension (Brown et al. 2016). It is
nocturnal and is often found hiding in crevices
during daytime (Holthuis 1991). We here note the
presence of Parribacus antarcticus at the Cabo
Verde Islands, the first record of the species from
the eastern Atlantic.
RESULTS
The mitten lobster Parribacus antarcticus is
recorded from four different islands in the Cabo
Verde archipelago: 1) Santa Luzia Island: The
photo of the first specimen (Figure 1A), taken by
Kiyotaka Hatooka, came from a research project
on marine biodiversity in the Cabo Verde
Exclusive Economy Zone (OFCF, Overseas
Fishery Cooperation Foundation of Japan). An
ovigerous female of about 11 cm carapace length
(CL) was captured at Santa Luzia Island during a
purse seine operation in the night of 04 November
2003 in 25-30 m depth. 2) São Vicente Island:
The second specimen came from SCUBA diving
in 18-25m depth. It was collected off Salamansa
bay, São Vicente Island, in January 2012 by the
experienced fisherman Roberto dos Santos. He
told the first author that in 25 years of fishing he
had never seen the species until a few years ago,
but that it was now becoming more common,
found only in dark shelters, particularly on the
north of the island. The specimen (64 mm CL)
was sent to Ehud Spanier and Kari Lavalli at the
University of Boston, USA, who kindly took photos
and measurements (Figure 1B); 3) Sal Island: The
dive instructor White Oliveira observed and
photographed P. antarcticus in a lava tunnel at
Palmeira, in 11m depth, on 23 November 2017
(Figure 2A). 4) Santiago Island: A film taken in April
2010 by João Sá Pinto at Ponta Grande (13m depth),
Cidade Velha, Santiago Island
(https://vimeo.com/82012872) shows a specimen of
P. antarcticus at 02:35 (video-frame, Figure 2B).
DISCUSSION
Eight lobster species were until now known to
occur at the Cabo Verde Islands. Panulirus
regius, the endemic Palinurus charlestoni and
Freitas and Wirtz
16
Fig. 1. A) Ovigerous female (11 cm CL) of Parribacus antarcticus from Santa Luzia Island (photos by Kiyotaka
Hatooka in 2003); B) Dried specimen of P. antarcticus (6 cm CL) from São Vicente Island captured in 2012 (photo
by Kari Lavalli in 2018).
Scyllarides latus used to be common species but
their populations have been severely reduced by
fishery (including illegal fishery using SCUBA).
Other species are Scyllarus pygmaeus, Panulirus
echinatus, Panulirus argus, Enoplometopus
antillensis and Enoplometopus callistus (Wirtz et
Parribacus antarcticus in Cabo Verde
17
al. 1988; Holthuis 1991; Merino & Lindley 2003;
Freitas & Castro 2005). Distinctively with a more
flattened body than S. latus, P. antarcticus has a
dorsal surface with tubercles and the lateral
margin shows large teeth banded with yellow and
orange (Holthuis 1991). We do not know if
Parribacus antarcticus is a recent arrival at the
Cabo Verde archipelago or, due to its small size
and secretive habits, has simply been overlooked
in the past. In a similar case, Freitas & Castro
(2005) discussed possible scenarios of the arrival
of the Caribbean lobster species Panulirus argus
in the Cabo Verde archipelago (larval dispersal or
human transport). The capture of an ovigerous
female of Parribacus antarcticus and the
presence of the species at four different islands
indicates a reproducing population.
Fig. 2. A) P. antarcticus from Sal Island in a lava tunnel (photo by White Oliveira in 2017); B) frame capture of
video (https://vimeo.com/82012872) showing P. antarcticus in a cave in 13 m depth off Cidade Velha, Santiago
Island (video by João Sá Pinto in 2010).
ACKNOWLEDGEMENTS
We are grateful to Kiyotaka Hatooka for the
photo of the Santa Luzia specimen, to Roberto
dos Santos for the specimen from São Vicente
Island and comments on the species, and to White
Oliveira of the ecodiveschool at Santa Maria, Sal
Island, for a photo and information on the third
specimen. João Sá Pinto kindly confirmed that his
film showing P. antarcticus was taken at Santiago
Island. Thanks also to Kari Lavalli and Ehud
Spanier for comments and data on the second
specimen sent to USA in 2012. This study
received Portuguese national funds through FCT -
Foundation for Science and Technology - through
project UID/Multi/04326/2013.
REFERENCES
Brown, J., K. Downes, R.J. Mrowicki, E.L. Nolan, A.J.
Richardson, F. Swinnen & P. Wirtz 2016. New
records of marine invertebrates from Ascension
Island (central Atlantic). Arquipélago. Life and
Marine Sciences 33: 71-79.
Chan, T.Y 2010. Annotated checklist of the world’s
marine lobsters (Crustacea: Decapoda: Astacidea,
Glypheidea, Achelata, Polychelida). The Raffles
Bulletin of Zoology 23: 153-181.
Freitas and Wirtz
18
Freitas, R. & M. Castro 2005. Occurrence of Panulirus
argus (Latreille, 1804) (Decapoda, Palinuridae) in
the northwest islands of the Cape Verde
Archipelago (Central-East Atlantic). Crustaceana
78: 1191-1202.
Holthuis, L.B. 1991. FAO Species Catalogue. Vol. 13.
Marine lobsters of the world. An annotated and
illustrated catalogue of species of interest to
fisheries known to date. FAO Fisheries Synopsis
No. 125, 13, Rome, FAO. 292 pp.
Merino, S.E. & J.A. Lindley 2003. First record of
Enoplometopus callistus (Crustacea: Decapoda:
Nephropidae) in the Cape Verde Islands. Journal of
the Marine Biological Association of the United
Kingdom 83: 1233-1234.
Nyborg, T. & A. Garassino 2017. A new genus of
slipper lobster (Crustacea: Decapoda: Scyllaridae)
from the Eocene of California and Oregon (USA).
Neues Jahrbuch für Geologie und Paläontologie -
Abhandlungen 283: 309-316.
Wirtz, P., B. Müller & P. Nahke 1988. The Caribbean
shrimp Tuleariocaris neglecta Chace 1969 found in
association with Diadema antillarum at Madeira,
and two new records of decapod crustaceans from
the Cape Verde islands. Courier Forschungsinstitut
Senckenberg 105: 169-171.
Submitted 07 Nov 2018. Accepted 13 Nov 2018. Published online 18 Jan 2019.
Arquipelago - Life and Marine Sciences ISSN: 0873-4704
19
SHORT COMMUNICATION
The polychaete Lygdamis wirtzi at Ascension and St Helena
Islands (Annelida, Polychaeta, Sabellariidae)
JUDITH BROWN, EJIROH NISHI AND PETER WIRTZ
Brown, J., E. Nishi and P. Wirtz 2019. The polychaete Lygdamis wirtzi at Ascension
and St Helena Islands (Annelida, Polychaeta, Sabellariidae). Arquipelago. Life and
Marine Sciences 36: 19 -21.
Key words: Polychaeta, Sabellariidae, central Atlantic
Judith Brown ([email protected]), Ascension Island Government, Ascension
Island, South Atlantic; Eijiroh Nishi ([email protected]), College of Education, Yokohama
National University, Hodogaya, Yokohama 240-8501, Japan; Peter Wirtz
([email protected]): Centro de Ciências do Mar, Universidade do Algarve,
Campus de Gambelas, PT-8005-139 Faro, Portugal.
Little is known about the polychaete fauna of the
two mid-Atlantic Islands, Ascension and St
Helena. Baird (1864), Monro (1930), and
Hartmann-Schröder (1992) documented the
polychaetes from Ascension Island while Day
(1946) reported polychaetes from St Helena
Island. Lastly, Yáñez-Rivera & Brown (2015)
reported on Hermodice and Eurythoe from both
Ascension and St Helena Islands. We do not know
any other publications on polychaetes for these
two remote islands.
The genus Lygdamis (Family Sabellariidae)
currently contains 20 species (Hutchings et al.
2012; Capa et al. 2015). Lygdamis wirtzi Nishi and
Núñez, 1999, was originally described from
Madeira Island and the Canary Islands and has also
been found at the Cape Verde Islands and at São
Tomé Island (Wirtz 2001, 2003).
New observations of this species were made
while SCUBA diving at the coasts of Ascension
and St Helena Islands in 2013 and 2015.
The specimens were collected from coarse sandy
habitats in depths of ~10-12m. The animals (two
specimens from St Helena and one from
Ascension), were photographed in-situ and then
collected by hand and stored in 70-80% ETOH.
Preserved specimens were sent to the second
author for identification. They are now deposited
in the Coastal Branch, Natural History Museum
and Institute, Chiba, Japan.
Morphological study by the second author
confirmed the initial, provisional identification of
the specimens as Lygdamis wirtzi. An animal from
St. Helena Island is shown in a colour photo in a
popular book by Brown (2014, p. 40). Figure 1
shows an animal from Ascension Island. In both
places, the species was common in bottoms of
coarse sand or gravel in shallow water.
Despite actively searching for it, the third author
has not found Lygdamis wirtzi when diving on the
coasts of Senegal, Sierra Leone, and Gabon. Until
now, the species is only known from (sub) tropical
Brown et al.
20
Fig. 1. Lygdamis wirtzi at Ascension Island (Photo J. Brown)
islands in the eastern and central Atlantic Ocean.
Lygdamis species are notoriously difficult to
observe and to collect as they quickly retract into
their tubes when approached. These new records
increase the known distribution of Lygdamis wirtzi
and it is likely that this and other Lygdamis species
are much more wide-spread than currently known.
ACKNOWLEDGMENTS
The record from Ascension Island was made
during several expeditions in 2013 and 2015
funded by grants to the Shallow Marine Surveys
Group from the Darwin Initiative (EIDCF012).
Thanks to the staff of the Conservation
Department on Ascension Island for continuing
support. The record from St Helena Island was
made while the first author was part of a Darwin
Initiative funded marine biodiversity project
(Project 19-031) which was in joint partnership
with the Joint Nature Conservation Committee
(JNCC) and the Environmental Management
Department (EMD) of St Helena Government. P.
Wirtz wishes to thank the Centre for Marine
Sciences (CCMAR) of the University of Algarve
for partially funding two trips to Ascension Island
and one trip to St Helena Island. This study
received national funds through FCT -Foundation
for Science and Technology project
UID/Multi/04326/2013.
REFERENCES
Baird, W. 1864. Description of a new species of
Annelide belonging to the family Amphinomidae.
Transactions of the Linnean Society of London 24:
449–450.
Brown, J. 2014. Marine Life of St Helena. Pisces
Lygdamis wirtzi at Ascension and St Helena
21
Publications, Newbury. 220 pp.
Capa, M., L. Faroni-Perez & P. Hutchings 2015.
Sabellariidae from Lizard Island, Great Barrier
Reef, including a new species of Lygdamis and
notes on external morphology of the median organ.
Zootaxa 4019 (1): 184–206.
Day, J.H. 1949. On the Polychaeta collected by Mr. J.
Colman at St. Helena. Journal of the Linnean
Society of London, Zoology 41: 434–451.
Hartmann-Schröder, G. 1961. The Polychaetes of the
Amsterdam Expedition to Ascension Island (Central
Atlantic). Bijdragen Tot De Dierkunde 1961: 219-
235.
Hutchings, P., M. Capa and R. Peart 2012. Revision of
the Australian Sabellariidae (Polychaeta) and
description of eight new species. Zootaxa 3306: 1-
60.
Monro, C.C.A. 1930. Polychaete worms. Discovery
Reports 2: 1–222.
Nishi, E. & J. Nunez 1999. A new species of shallow
water Sabellariidae (Annelida, Polychaeta) from
Madeira Island, Portugal, and Canary Islands, Spain.
Arquipelago. Life and Marine Sciences 17A: 37-42.
Yáñez-Rivera, B. and J. Brown 2015. Fireworms
(Amphinomidae: Annelida) fromAscension and
Saint Helena Island, Central South Atlantic Ocean.
Marine Biodiversity Records 8(e149); doi
10.1017/S1755267215001244
Wirtz, P. 2001. New records of marine invertebrates
from the Cape Verde Islands. Arquipelago. Life and
Marine Sciences 18A: 81-84.
Wirtz, P. 2003. New records of marine invertebrates
from São Tome Island (Gulf of Guinea). Journal of
the Marine Biological Association of the United
Kingdom 83: 735-736.
Submitted 03 Jan 2019. Accepted 01 Feb 2019.
Published online 11 Mar 2019
Arquipelago - Life and Marine Sciences ISSN: 0873-4704
23
A first assessment of operator compliance and dolphin
behavioural responses during swim-with-dolphin
programs for three species of Delphinids in the Azores
ARIANNA CECCHETTI, KAREN A. STOCKIN, JONATHAN GORDON AND JOSÉ M.N.
AZEVEDO
Cecchetti, A., K.A. Stockin, J. Gordon and J.M.N. Azevedo 2019. A
first assessment of operator compliance and dolphin behavioural responses during
swim-with-dolphin programs for three species of Delphinids in the Azores.
Arquipelago. Life and Marine Sciences 36: 23 - 37.
The popularity of swim-with wild dolphin programs around the world is fast growing, with
the studies required to investigate their impact lagging behind. In the Azores, species
targeted include the short-beaked common (Delphinus delphis), the bottlenose (Tursiops
truncatus) and the Atlantic spotted dolphin (Stenella frontalis). To evaluate the effects of
this activity on local dolphin populations, and thus provide support for management
decisions, dolphin response data were collected onboard commercial boats off São Miguel
Island between 2013 and 2015. All three species revealed high degree of neutral and
avoidance behaviours, and very low approach rates. Tursiops showed higher frequency of
neutral responses than Delphinus, while Stenella both avoided and approached more
frequently than the other species. When boats intersected the path of dolphin groups,
avoidance responses were more likely and the duration of swims was shorter. Swims were
also shorter when animals were resting and travelling, and when groups were smaller. The
operators generally complied with the legislation, except in respect to the number of swim
attempts per dolphin group, which was higher than the legal maximum. Improvement of the
current legislation and concurrent reinforcement of controls is essential to avoid detrimental
long-term effects of this activity on dolphin populations in the Azores.
Key words: dolphin tourism, management, Delphinus delphis, Tursiops truncatus, Stenella
frontalis.
Arianna Cecchetti1 (e-mail: [email protected]), K.A. Stockin2, J. Gordon3 and
J.M.N. Azevedo1. 1CE3C - Centre for Ecology, Evolution and Environmental Changes/
Azorean Biodiversity Group, University of the Azores, Biology Department, 9501-801
Ponta Delgada, Azores, Portugal. 2C-MRG - Coastal Marine Research Group, School of
Natural and Computational Sciences, Massey University, Private Bag 102 904, North
Shore Mail Centre, Auckland, New Zealand 0745. 3SMRU - Sea Mammal Research Unit,
Scottish Ocean Institute, University of St. Andrews, St. Andrews, Fife KY16 8LB, UK.
INTRODUCTION
Swimming with free-ranging dolphins (hereafter
abbreviated as swim-with-dolphin) is offered
commercially as an ecotourism activity in various
parts of the world (Samuels et al. 2000). Swim-
with-dolphin encounters pose similar or greater
levels of disturbance than whale watching
(Scarpaci et al. 2000; Courbis & Timmel 2009),
an activity which has raised concerns in relation
to potential negative effects on the long-term
viability of cetacean populations (Christiansen &
Cecchetti et al.
24
Lusseau 2014; Meissner et al. 2015). Swim-with-
dolphin programs generally involve more
disruptive forms of interaction than conventional
whale and dolphin watching. Thus, understanding
of long-term effects is imperative. Surprisingly,
despite their more intrusive nature the impact of
these activities remains poorly investigated, with
only a few studies currently available and
focusing on the effects of swim-with programs on
dolphin behavioural responses and group
structure (Martinez et al. 2011; Peters et al. 2013;
Peters & Stockin 2016). For example, Hector’s
(Cephalorhynchus hectori hectori), bottlenose
(Tursiops spp.) and common dolphins (Delphinus
delphis) in New Zealand and Australia were
reported showing direct avoidance behaviour
when subjected to swim-with operations
(Neumann & Orams 2006; Martinez et al. 2011;
Filby et al 2014).
A study of responses of bottlenose dolphins to
swim-with-dolphin tourism in Port Phillip Bay,
Australia, compared observations made during
two study periods 15 years apart and showed
evidence of increasing sensitivity to disturbance
over this period. Both the sighting success and the
mean encounter duration decreased between the
two periods. The proportion of “neutral”
encounters also decreased while the probability
that dolphins would show either avoidance or
approach behaviour was higher in the later study.
Dolphins that were scored as resting before the
encounters were particularly likely to show
avoidance (Filby et al. 2014).
Several studies suggest that the strategy used
by tour operators to approach dolphin groups
affects with the dolphins’ response. The J-
approach, where the dolphin’s path is intersected
by the boat, generates greater avoidance reactions
than a parallel approach (Martinez et al. 2011;
Peters et al. 2013). Other factors, such as group
size and age class have also been shown to
influence dolphins’ responses: smaller groups are
more likely to avoid swimmers, while juveniles
are more likely to engage (Neumann & Orams
2006; Peters et al. 2013).
In the Azores, swim-with-dolphin programs
started in early 1990s in combination with whale
watching tours, with tourists engaging in swim-
with-dolphin activities in an opportunistic
manner. As this activity became more popular
and also provided anappealing economic revenue,
operators started to offer dedicated swim-with-
dolphins tours. Currently, there are twenty-four
companies on four of the nine islands of the
Archipelago, of which seven on the largest island
São Miguel. On average two to three trips are
scheduled daily by the operators with each trip
lasting 2-3 hours. The variety of dolphin species
and their high sighting frequency in the Azores
(Silva et al. 2003, 2014) has facilitated the
development of these activities. The target
species are common (Delphinus delphis),
bottlenose (Tursiops truncatus), Risso’s
(Grampus griseus), and Atlantic spotted dolphins
(Stenella frontalis). Operators may target specific
groups based on species, group size, activity state
or distance from the harbour. For instance,
operators tend to prefer Atlantic spotted dolphins
and bottlenose dolphins over common dolphins,
while large gatherings of surface feeding common
dolphins are preferred over smaller ones. A
shorter distance from the harbour is also preferred
(Filipe Ferreira, tour company lookout, personal
communication).
The fact that multiple species are targeted in
the same area is different from the situation
typical in other locations such as New Zealand
and Australia, where dolphin operators mostly
focus on a single species e.g. bottlenose dolphins
in Gulf of St. Vincent (Peters et al. 2013) and Port
Phillip Bay (Scarpaci et al. 2000; Filby et al.
2014), Australia; Hector’s dolphins in Akaroa
Harbour (Martinez et al. 2011) and Porpoise Bay
(Bejder et al. 1999), common and bottlenose
dolphins in Bay of Islands (Stockin et al 2008;
Peters & Stockin 2016) and Mercury Bay
(Neumann & Orams 2006), dusky dolphins
(Lagenorhynchus obscurus) in Kaikoura
(Markowitz 2012), New Zealand.
Swim-with-dolphin operators in the Azores
release tourists, equipped with a mask and snorkel
but no fins, into the water within 10 m of dolphin
groups. In New Zealand, swimmers are also
provided with snorkelling gear (Martinez et al.
2012) while in Australia, there is more variability,
free snorkelling, underwater scooters or the use of
a rope are offered by different operators (Zeppel
2007; Peters et al. 2013). In Australia, mermaid
Assessment of operator compliance and dolphin behavioural in the Azores
25
lines are used. These are 15 m long ropes which
swimmers hold while pulled by a slowly moving
boat. Mermaid lines were found to minimize
inappropriate approaches by swimmers towards
the dolphins; thus reducing dolphins’ behavioural
changes and possibly disturbance (Peters et al.
2013; Filby et al 2014).
Regulations are important for managing tourist
operations and to minimize potential impacts.
However, to be able to issue effective guidelines,
it is imperative to understand the effects these
activities have on subjects, bearing in mind these
may be species, habitat and operation dependent.
In the Azores, all matters related to whale and
dolphin watching, including swim-with-dolphin
programs, are regulated by regional legislation
(Decreto Legislativo Regional 13/2004/A) first
issued in 1999, and currently under revision.
However, this offers no specific guidance on how
to approach dolphin groups: the regional
legislation states only that the type of approach
and the distance to the group is the exclusive
responsibility of the boat skipper, based on
his/her evaluation of the dolphins’ behaviour and
of the sea state. However, limitation is placed on
the number of swim attempts per group of
dolphins (maximum of 3), the number of
swimmers per swim attempt (maximum of 2), and
the duration of each swim episode (maximum of
15 minutes). A recent proposal for amending this
legislation suggests a limit of only one swim-
with-dolphin boat at any time per group of
dolphins, and no swim attempts are to be made in
the presence of other whale watching boats.
Further, at the first sign of disturbance from the
dolphins, the swimmers should return to the boat
and no further swim attempts should be allowed.
The legal definition of ‘disturbance’ is a
horizontal and/or vertical displacement of the
group or part of it.
Given the lack of detailed knowledge of
industry operational practices and the effects of
swim-with-dolphin operations in the Azores, this
study aims to provide an insight into swim-with-
dolphin operations off São Miguel Island.
Specifically, we test the operator’s preference for
species or group size and explore the relationship
between different boat approaches and dolphins’
response and resulting swim durations for
participants. We also investigate the extent of
compliance with existing guidelines. This study
offers first insights into swim-with dolphin
operations at a location where several dolphin
species are the subject of tourism focus.
MATERIALS AND METHODS
Field data collection
Boat-based data were collected off the south coast
of São Miguel Island (N 37º39’, W 25º26’),
Azores, during swim-with-dolphin operations
between June and September of 2013 to 2015
(Figure 1).
Whale watching companies rely on land-based
lookouts to detect cetaceans. Each company has
its own lookout, usually located in a fixed land
station along the south coast of the island. To its
own lookout, usually located in a fixed land
station along the south coast of the island. To
cover as much area as possible, we chose two
whale watching companies departing from two
different harbours (Ponta Delgada and Vila
Franca do Campo) for our study.
Typically, each company carried out separated
trips for observation and swim-with-dolphin
activities. Each swim-with-dolphin tour included
one or more group encounters, during which the
boat approached a group of dolphins while
attempting to place patrons in the water (swim
attempt). If successful, a swim attempt led to a
swim episode in which one or more swimmers
were released in the water.
We used group focal scan sampling (Altmann
1974; Mann 1999) to examine the dolphins’
Cecchetti et al.
26
Fig.1. Dolphin groups encounters during swim-with-dolphin operations between 2013 and 2015 off the south
coast of São Miguel with each dot representing a dolphin group.
response to the activity. A group was defined as
existing when >50% of individuals were engaged
in the same activity state, were heading in the
same direction when travelling and were within 5
body length of each other. We performed an
initial scan on first observation of the group and
then again, prior to the boat engaging directly
with the group. Data collected included the initial
activity state, group size best estimate and the
presence of calves and newborns. Vessels were
always farther than 100 m from the dolphin group
when these assessments were made. A second
scan was completed when swimmers were
released into the water. In addition to the
parameters recorded for the initial scan, we
recorded the dolphins’ behavioural responses, the
type of boat placement, the number of swimmers
and their placement relative to the dolphin group.
The probability of sampling the same group was
low given the fact that samples regarded not just
one species, but all dolphin species encountered
by the operators, e.g. a morning tour could
include a group of common dolphins and the
afternoon a group of bottlenose dolphins.
Typically, the activity was performed with just
one group per tour. Four activity state categories
(foraging, resting, travelling and socialising) were
defined based on Neumann (2001) and Stockin et
al. (2009), summarised in Table 1. A calf was
defined as an individual of approximately one-
half or less in size than an adult and consistently
associated with an adult (Fertl 1994). Newborns
were defined as individuals showing visible foetal
folds, consistently associated with an adult
(Shane 1990).
Cecchetti et al.
27
Table1. Definition of activity states recorded during swim-with-dolphins operations between 2013 and 2015 off
São Miguel island, Azores (adapted from Neumann 2001 and Stockin et al 2009).
Activity state Definition
Foraging Individuals engaged in coordinated directional movements and prolonged dives in
an attempt to pursue and capture prey. Cohesiveness of the group often varied and
changes in heading and circling movements could be observed during cooperative
foraging. When actual feeding occurred close to the surface, aerial activity was
observed. Seabirds were often associated with feeding dolphins.
Resting Involved slow movements up to absence of forward propulsion. Close distance
range between individuals, regular surfacing patterns and absence of active surface
behavior were observed.
Travelling An individual or group following a consistent direction over time.
Socialising Included high frequency of active surface events such as breaching, head slapping,
and tail slapping concerning at least two individuals (mother-calf excluded).
Chasing and body contact is observed.
Recording the time swimmers entered the water and re-boarded the boat allowed the duration of each swim episode to be calculated. When the swimmers entered the water, we recorded the dolphins’ response as: 1) neutral, dolphins did not show any apparent change of behaviour; 2) avoidance, dolphins changed their path direction or dived away from the swimmers or increase their speed and either changed direction or dived; 3) approach, at least one dolphin of the group changed direction and swam within 5 m of at least one swimmer (Martinez et al. 2011).
Data analysis
To investigate whether encounter frequency of
different dolphin species for swim-with operations
reflected their prevalence in the area or was instead
affected by operator preference, data collected during
swim-with-dolphin operations were compared with
observations from an opportunistic open database
(MONICET,
www.monicet.net) using a Chi-square test. The
MONICET database is compiled from regular whale
watching activity and includes data since 2009.
Dolphin response to swimmers was analysed with
a Generalised Estimating Equation (GEE)
model for multinomial responses using the
exchangeability time (“time.exch”) correlation
structure, recommended for nominal responses
(Toulomis 2015). The full model contained the
three-levels response variable (neutral, avoidance
and approach) and six explanatory variables:
species, year, group size, activity state, boat
placement and presence of calves/newborns. The
model was rerun excluding non-significant
explanatory variables. Similarly, we applied a
GEE model with exchangeable correlation
structure to explore the duration of swim episodes
with the same six explanatory variables. In the
exchangeable correlation structure, the within-
cluster observations (in this case the group
encounter) are assumed to be equally correlated.
This structure was preferred over the first-order
autoregressive, which assumes that correlations
are a function of time, i.e. correlation of
successive swim attempts would decrease over
time, and that measurements are equally spaced in
time. This was not the case in the present study,
as sampling depended on the activity; hence no
standardization of intervals between swim
attempts was applied. We did not include the
variable “swimmers placement” due to its high
Cecchetti et al.
28
collinearity with boat placement. We chose this
latter because effects from boat approach would
occur earlier than those due to swimmers.
Moreover, rules of best practice regarding boat
manoeuvres would be easier to implement. Only
the most frequent levels of “boat placement” and
“swim episode duration” were included in the
models. Waldts and QIC tests were used to select
the best models. We determined compliance rates
in respect to both current and proposed
legislation. All analysis was performed in R using
“geepack” (Højsgaard et al. 2006) and “multgee”
(Toulomis 2015) packages.
RESULTS
Target species and approach techniques
Data were collected on 135 trips run over 104
days between 2013 and 2015. We recorded a total
of 225 independent group encounters. Only one
trip resulted in no dolphin encounters. Operators
approached common dolphins on 110 occasions,
bottlenose dolphins on 62 and spotted dolphins on
34. Risso’s dolphins were approached only 3
times. Mixed species groups of common with
spotted or bottlenose dolphins were also
approached (12 and 4 times, respectively). No
statistical analysis was carried out using data
from mixed groups or for Risso’s dolphins
because of the small sample sizes.
The frequency of approaches to the various
species was not significantly different from their
sighting frequency in the overall whale-watching
trips, as recorded in the larger MONICET
database (N swim-with dataset = 206, N whale
watching dataset = 1265; Dd: X 2= 0.0861, df = 1,
p = 0.769; Tt: X2 = 0.3125, df = 1, p = 0.576; Sf:
X 2= 1.1108, df = 1, p = 0.291). However,
operators did select smaller groups for swim
attempts: the median group size of approached
dolphin groups was significantly smaller than that
recorded in the whale watching database (Table
2). Calves and newborns were present during the
majority of the swim attempts. Dolphins
approached thr boat in only 1% of cases. Five
different approach techniques were used by the
skippers (Figure 2). The J-approach strategy (a)
was the most frequently used (50%, N = 1367):
the boat would move parallel to the group at first,
then accelerate in order to pass ahead of it and
quickly position itself transversal to their track.
The second most frequent (35%, N = 1367) type
of approach involved the boat moving and
stopping parallel to the group of dolphins (b).
During 9% (N=1367) of approaches, the boat
would pass through and stop centred to the group
(c). Other less frequent strategies used were
approaching and placing the boat directly to the
front of the group facing their path (4%, N =
1367) or to the back (1%, N = 1367). In less than
1% (N = 1367) of cases the boat remained
Table 2. Differences between group sizes of dolphins approached for swim operations (SWD) and those recorded
during regular whale watching (WW). Group size is given as median (1st quartile, 3rd quartile). Percentage of
calves and newborns observed during swim operations are reported for each species. Dd=common dolphin,
Tt=bottlenose dolphin, Sf=Atlantic spotted dolphin.
Group size
% calves SWD WW U P
Dd 72 17.5 (10-30)
n= 110
30 (15-50)
n= 658
41528.5 <0.001
Tt 52 15 (10-25)
n= 62
20 (10-40)
n= 355
12941 0.012
Sf 79 30 (17-46)
n= 34
50 (30-80)
n= 252
5257.5 <0.01
Assessment of operator compliance and dolphin behavioural in the Azores
29
Fig.2. Boat placement strategies used to approach dolphin groups in the Azores: a) J-approach, b) parallel, c)
centred, d) to the front, e) to the back.
Cecchetti et al.
30
Table 3. Compliance with current and proposed (*) guidelines during swim-with-dolphins operations between 2013
and 2015 off São Miguel island, Azores.
Rule Set Value Median Maximum Compliance
Nr swimmers in the water 2 2 7 77%
Nr swim attempts with one group 3 6 23 33%
Duration of swim episode 15 2 15 100%
Stop interaction on avoidance* - - - 29%
stationary near the dolphins long enough to allow
a second swim turn. Swimmers entered the water
mostly to the front (50.7%, N = 1355), parallel
(35.2%, N = 1355) or in the middle (11.22%, N =
1355) of the group. In few cases, swimmers were
placed behind the dolphin group (1.4%, N =
1355) or were at some distance from it requiring
participants to swim to get to the group (1.4%, N
= 1355).
The percentage of each approach strategy
varied between species. The J-approach was
most often used to approach bottlenose dolphins
(43%, N = 683), while both the centred approach
(65%, N = 129) and parallel (61%, N = 472) were
most often used to approach common dolphins.
Spotted dolphins were approached with almost
equal percentages of all techniques. Approach
strategies varied significantly as a function of
group size for common (KW = 20.162, df = 2, p <
0.001) and spotted dolphins (Sf: KW = 14.0502,
df = 2, p < 0.001). A posthoc Dunn’s test showed
that for these two species, the centred approach
was used significantly more frequently with the
larger groups (p < 0.01, Figure 3).
Fig.3. The three most frequent boat placement strategies as a function of dolphins group size for each species (a)
common dolphin, b) bottlenose dolphin, c) Atlantic spotted dolphin). Note: C=centred, P= parallel, J= J-approach.
Horizontal lines are medians, vertical lines are the range of values, and boxes are the interquartile ranges.
Assessment of operator compliance and dolphin behavioural in the Azores
31
Compliance with regulations
Compliance with current and proposed
regulations is reported in Table 3. The median
number of swimmers entering the water during
each swimming episode was 2, which is the
maximum number specified by the current
regulation. In 23% of the episodes, 3 or more (up
to 7) swimmers were in the water concurrently.
On average, swim episodes lasted about 2
minutes, regardless of the species. (This includes
the time of placing the swimmers in the water and
recovering them back into the boat).
Regulations specify a maximum of 3 swim
attempts per dolphin group, but the median
number observed was 6, and 67% of the groups
were approached more than 3 (up to 23) times.
Only twelve swim attempts (N = 1367) were not
followed by the release of swimmers into the
water.
The new regulations under discussion propose
that at the first sign of disturbance, swimmers
should return to the boat and no further swim
attempts should be made. We considered
avoidance reactions as a sign of disturbance, and
found that only 29% of the encounters would
potentially follow this rule. The other proposed
rule is that only one swim-with dolphin boat is
allowed per group and that whale watching have
priority over the swim-with activity. Compliance
in this case could not be investigated as
information was not available for encounters
given the fact that it was not always possible to
distinguish the activity of all boats arriving and
departing during dolphin response data collection. Effects of swim-with-dolphin operations For all three species, dolphin response to swimmers was either avoidance (49.6%, N = 1354) or neutral (47.8%). Only in 2.6% of cases did the dolphins approach the swimmers. Atlantic spotted dolphins showed a high degree of avoidance (52%), but also the highest percentage of approach (10%, Figure 4a). The GEE model for multinomial responses showed that three variables: species, activity state
Table 4. Dolphin responses to swim-with programs resulting from multinomial GEE with time.exch correlation
structure. N=neutral, Av=Avoidance. Sf=Atlantic spotted dolphin, Tt=bottlenose dolphin.
Parameters Coefficient Estimate Standard Error Z P
beta01 3.2087 0.6839 4.69 <0.001 ***
Species
Sf: N
Tt: N
-1.0202
1.4949
0.9001
0.7530
-1.13
1.99
0.257
0.047 *
Boat placement
Parallel: N
J-approach: N
0.3651
1.3924
0.5589
0.7759
0.65
1.79
0.514
0.073
Activity state
Foraging: N
Travelling: N
Resting: N
0.0237
-0.8044
-1.1568
1.0432
0.8764
0.5349
0.02
-0.92
-2.16
0.982
0.359
0.031 *
beta02 2.8709 0.6550 4.38 <0.001 ***
Species
Sf: Av
Tt: Av
-0.6729
1.2178
0.8936
0.7551
-0.75
1.61
0.451
0.107
Boat placement
Parallel: Av
J-approach: Av
0.2643
1.5136
0.5031
0.7262
0.53
2.08
0.599
0.037 *
Activity state
Foraging: Av
Travelling: Av
Resting: Av
-0.3205
-0.1126
-0.8512
1.0011
0.8520
0.5323
-0.32
-0.13
-1.60
0.749
0.895
0.110
Assessment of operator compliance and dolphin behavioural in the Azores
32
and boat placement were significantly correlated with dolphin response (Table 4). In particular, a neutral response was more likely for bottlenose than for common dolphins (Figure 4a). Groups of resting dolphins were less likely to
respond in a neutral way than socialising groups (Figure 4b). Avoidance responses were more likely when the boat intersected the path of the dolphins than when it stopped centrally to the group (Figure 4c).
Fig. 4. Dolphins’ response during swim-with-dolphin operations in relation to species (a) activity state (b) and
boat placement (c). Dd=common dolphin, Tt=bottlenose dolphin, Sf=Atlantic spotted dolphin; C=centred,
P=parallel, J=J-approach.
Three of the five explanatory variables had
significant effects on the duration of the swim
episodes: group size, activity state and boat
approach technique (Table 5). Swim episode
duration tended to increase with larger groups
(Figure 5a). When the operator was using the
J-approach, the duration of the swims was shorter
than when the boat was centrally placed in the
group (Fig. 5b). Foraging groups also resulted in
longer swim episodes compared with travelling or
resting dolphins (Figure 5c).
Table 5. Effects of swim-with programs on the duration of swim episodes resulting from the GEE model with
exchangeable correlation structure.
Parameter Coefficient Estimate Standard Error Wald P
Intercept 2.54014 0.19277 173.63 < 0.001***
Group size 0.00454 0.00181 6.30 0.0121 *
Activity state
Foraging
Travelling
Resting
0.47078
-0.42777
-0.37697
0.22641
19.12
0.12528
4.32
0.09783
9.05
0.0376 *
<0.001***
0.0026 **
Boat placement
Parallel
J-approach
-0.26337
-0.44053
0.15115
0.16163
3.04
7.43
0.0814
0.0064 **
Assessment of operator compliance and dolphin behavioural in the Azores
33
Fig. 5. Swim episodes’ duration in relation to group size (a), boat placement (b) and activity state (c). C= centred,
P=parallel, J= J-approach. Horizontal lines are medians, vertical lines are the range of values, and boxes are the
interquartile ranges.
DISCUSSION
Species and group selection
Three dolphin species were the most targeted for
swim-with-dolphin operations off São Miguel,
Azores: common, bottlenose and Atlantic spotted
dolphin. The sighting frequency of these species
did not differ from that in the larger dolphin
watching database. Despite the perception that
certain species were preferred targets of the
industry, the current analysis did not reflect this.
However, other factors such as the distance from
the coast could have had priority over species
selection. For instance, the regular occurrence of
a small group of bottlenose dolphins outside of
Ponta Delgada (AC personal observation) makes
them potential easy targets for commercial
operations. A similar point was raised by
Hartman et al. (2014), who called for restrictions
on swim-with-dolphin activities after reporting
Risso’s dolphin females with calves using
periodically a specific area off the south coast of
Pico Island. Small resident populations targeted
by tourism activities may be vulnerable to
cumulative effects (Markowitz 2012), which
could ultimately lead to displacement or even
impacts on reproductive rates (Lusseau 2005;
Bejder et al. 2006). Monitoring the impact of
swim-with-dolphin activities should aim to
measure whether particular groups of animals
may be targeted more intensely than the general
population and, may thus, require specific
management measures to limit cumulative
impacts.
Effects of swim-with-dolphin operations
The analysis of the dolphin response to swim-
with-dolphin operation in the Azores revealed a
high degree of neutral or avoidance reactions, and
a very low approach rate for all three species.
Atlantic spotted dolphins had the highest
avoidance rates, followed by common dolphins,
while bottlenose dolphins were more frequently
neutral in their responses. Atlantic spotted
dolphins also showed a tendency for higher
approach rate, suggesting this species as the most
variable in terms of responses.
We did not find evidence for the presence of
calves and newborns affecting dolphin responses.
However, the high percentage of swim attempts
including these age classes might be the reason
for this missed effect. The well documented
vulnerability of calves, given their small size,
dependency from adults and lack of experience of
vessels (Stone & Yoshinaga 2000; Martinez &
Stockin 2013; Dwyer et al. 2014) should motivate
a precautionary approach. In New Zealand and
Australia, for instance, a ban on swimming with
groups containing calves has been enacted in
national swim-with-dolphin regulations
(Neumann & Orams 2006).
For all species, resting was associated with
fewer neutral responses with a tendency for
higher avoidance responses. The duration of
swim episodes was also reduced when dolphins
were resting and travelling as opposed to
socialising. This is consistent with observations
of bottlenose dolphins in Port Phillip Bay,
Australia which also showed a high degree of
Cecchetti et al.
34
neutral responses from groups of individuals that
were socialising and high avoidance when resting
(Filby et al. 2014). In other mammals including
humans, rest is fundamental for brain and cellular
function (Tartar et al. 2006; Benington & Heller
1995; Inoué et al. 1995), hence decrease in resting
may affect the physiology and metabolism of an
individual. An example of resting disruption has
been reported for Hawaiian spinner dolphins
(Stenella longirostris), which use in-bay waters
with sandy substrates to rest during the day and
predominantly travel when outside the bays (Tyne
et al. 2015). The presence of snorkelers, scuba
divers and kayakers (Danil et al. 2005; Courbis &
Timmel 2009) resulted in alteration of the spinner
dolphins resting patterns (Courbis & Timmel
2009) which are unlikely to be replaced outside
the bays where protection is lacking (Tyne et al.
2015). Common dolphins in the Azores have been
observed resting and engaging in less energetic
activities around midday (Cecchetti 2017). This
information would be useful to address in
management decisions, for example, regulating
the timing of tours either avoiding this time range
or delaying the tours.
The J-approach generated the greatest
percentage of avoidance reactions and the lowest
proportion of approaches from dolphins. Other
studies have reported similar results for
bottlenose, common and Hector’s dolphins
(Scarpaci et al. 2003; Martinez et al. 2011; Filby
et al. 2014). In the Azores, this was the approach
technique most frequently used by tour operators.
This may reflect the fact that the legislation does
not specify how the operators should approach
the dolphin group. However, guidelines from
other regions are more specific. For example, in
New Zealand and Australia, a parallel approach
is mandatory because it was reported to cause less
disturbance (Martinez et al. 2011; Filby et al.
2014). In our study, dolphins were less disturbed
by the centred approach, possibly because it was
used more often when groups were larger and
when dolphins are feeding close to the surface or
socialising. One of the functions of large groups
is to increase predator protection (Inman & Krebs
1987). Since responses to human disturbance
have been compared to anti-predator behaviour
(Frid & Dill 2002), individuals in large dolphin
groups would likely react less strongly to the
potential threat. Larger dolphin groups have in
fact been reported to approach swimmers and
boats more frequently (Neumann & Orams 2006;
Peters et al. 2013). Groups of spinner dolphins
smaller than 25 individuals were observed
avoiding entering Maku’a Beach, Hawaii, if the
number of swimmers was high (Danil et al.
2005), and swimmers in Mercury Bay, New
Zealand, had a higher chance of longer
interactions with common dolphins when groups
were larger than 50 individuals (Neumann &
Orams 2006). However, this does not necessarily
mean that the centred approach is per se the least
disturbing, as greater number of animals are
involved although to a lesser extent, so further
studies are needed to explore this more in detail.
In the present study, large group size was also
related to increased duration of swim episodes,
which is in line with the suggestion of lower
perceived risk for dolphins when gathered in
larger numbers.
Compliance with regulations Operators never exceeded the 15 minutes
maximum duration of each swim episode
specified in the regulations. In fact, the mean
duration of swim episodes was only 2 minutes for
all species. However, this result appears to be
determined by the avoidance response of dolphins
rather than the choice of the operators. A short
interaction time is usual for common dolphins,
which have shown to be one of the least receptive
species for swim-with tourism (Neumann &
Orams 2006) when compared to dusky (8-9
minutes, Markowitz et al. 2009) and Hector’s
dolphins (25 minutes, Martinez et al. 2011). In
the Azores bottlenose and spotted dolphins
exhibited similar levels of receptivity to common
dolphins. It is noteworthy however, that
bottlenose dolphins were the ones more often
approached with the most disturbing strategy (J-
approach), compared to the other two species.
Habituation and sensitisation due to cumulative
experience of anthropogenic activity has been
reported for some dolphin populations (e.g.
Markowitz et al. 2009), though whether the
bottlenose dolphins occurring out of Ponta
Delgada harbour have developed some degree of
Assessment of operator compliance and dolphin behavioural in the Azores
35
tolerance is hard to determine at this stage, thus
further investigation is warranted.
Most of the operators followed the legislation
for the number of swimmers simultaneously in
the water, but not for the number of attempts per
group. Regulations state that swimmers can be
released into the water no more than three times
per group of dolphins. Operators may increase the
number of simultaneous swimmers or the number
of swimmer releases, when they find a more
receptive dolphin group. Neumann & Orams
(2006) reported common dolphin encounters in
Mercury Bay were longer if the number of
swimmers did not exceed five. Hector’s dolphins
in Porpoise Bay did not show any avoidance
reaction towards swimmers, whereas boats led to
initial attraction followed by neutral and
eventually avoidance behaviours (Bejder et al.
1999). In the Azores, operators usually made a
large number of swim attempts, with little
account being taken of the reaction of the
dolphins, and often non-compliance with existing
and proposed regulations. This likely reflects the
low success of interactions, and is a way to
counteract the short time dolphins stay in the
presence of swimmers. Clearly, regulation in this
area is premature without a reference to current
practices and, ideally, to data on the impact of the
different alternatives. It would be useful to
investigate the impact of the number of swimmers
versus the impact of the number of attempts
performed to approach a group. This would help
identify the least disturbing method, and
potentially contribute to more effective
regulations that are easier to interpret and that
would result in higher compliance.
In order to increase the probability of
compliance, especially those regarding the
number of boats interacting with each group at
any moment, and the type of activity they are
engaged in, a clear definition of group must be
specified. For instance, a group which is
dispersed and includes many subgroups could be
perceived as many different groups. Within the
peer reviewed dolphin literature, group
definitions are typically based on distance
between individuals (e.g. 100m rule, Irvine 1981;
5 body-length, Smolker et al. 1992; 10-m rule,
Acevedo-Gutiérrez & Stienessen 2004), on
activity state and on direction of movement
(Shane 1990). Standardization of a group
definition would further aid enforcement as well
as compliance matters.
CONCLUDING REMARKS
Currently, there are no Azorean guidelines
advising on the best manner to approach dolphin
groups. If a given type of approach is considered
disturbing when observing dolphins, it would
seem rational to assume it is also disruptive
during swimming interactions. In light of the
current results, it is clear that the J-approach,
which is used with most frequency in the Azores,
is a poor option. A parallel approach, is preferred
while central placement should be reserved for
large (at least >50 individuals) and dispersed
groups. Resting groups of dolphins should be
avoided. Further investigation on the effects of
presence and number of calves should further be
undertaken, and it would be advisable to apply a
precautionary approach and, following the
example of international regulation, avoid
swimming with newborns.
ACKNOWLEDGMENTS
We would like to thank all the volunteers
involved in data collection, and the two whale
watching companies, Terra Azul and Picos de
Aventura, which offered their collaboration
throughout this study. Thanks to Anestis
Touloumis for clarifying issues about multgee
models package. We very much appreciate the
reviewer suggestions which improved the
manuscript. This research was partially supported
by the European Regional Development Fund
(ERDF) through the COMPETE – Operational
Competitiveness Programme and national funds
through FCT – Foundation for Science and
Technology, under the project PEst-
C/MAR/LA0015/2013, by the Strategic Funding
UID/Multi/04423/2013 through national funds
provided by FCT – Foundation for Science and
Technology and European Regional Development
Fund (ERDF), in the framework of the
programme PT2020 and by cE3c funding
(Ref:UID/BIA/003329/2013). It was also partly
supported by CIRN (Centro de Investigação de
Cecchetti et al.
36
Recursos Naturais, University of the Azores), and
CIIMAR (Interdisciplinary Centre of Marine and
Environmental Research, Porto, Portugal). A.
Cecchetti was supported by the Regional Fund for
Science through the scholarship M.3.1.2/F/036/2011.
K.A. Stockin was supported by a Royal Society of
New Zealand Te Aparangi Rutherford Discovery
Fellowship.
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Silva, M.A., R. Prieto, I. Cascão, M.I. Seabra, M.
Machete, M. Baumgartner and R. Santos 2014.
Spatial and temporal distribution of cetaceans in
the mid-Atlantic waters around the Azores. Marine
Biology Research 10(2):123-137.
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Pepper 1992. Sex differences in patterns of
association among Indian Ocean bottlenose
dolphins. Behaviour 123:38-69.
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and M.B. Orams 2009. Behavior of free-ranging
common dolphins (Delphinus sp.) in the Hauraki
Gulf, New Zealand. Marine Mammal Science
25(2):283-301.
Stockin, K.A., D. Lusseau, V. Binedell, N.J. Wiseman
and M.B. Orams 2008. Tourism affects the
behaviour budget of common dolphins (Delphinus
sp.) in the Hauraki Gulf, New Zealand. Marine
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(Cephalorhynchus hectori) calf mortalities may indicate new risks from boat traffic and habituation.
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Arrigoni, R.W. McCarley, R.E. Brown and R.E.
Strecker 2006. Hippocampal synaptic plasticity and
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Submitted 22 Jan 2019. Accepted 25 Mar 2019
Published online 22 May 2019.
Arquipelago - Life and Marine Sciences ISSN: 0873-4704
39
The marine macroalgae of Cabo Verde archipelago: an
updated checklist
DANIELA GABRIEL AND SUZANNE FREDERICQ
Gabriel, D. and S. Fredericq 2019. The marine macroalgae of Cabo Verde
archipelago: an updated checklist. Arquipelago. Life and Marine Sciences 36: 39 -
60.
An updated list of the names of the marine macroalgae of Cabo Verde, an archipelago of
ten volcanic islands in the central Atlantic Ocean, is presented based on existing reports,
and includes the addition of 36 species. The checklist comprises a total of 372 species
names, of which 68 are brown algae (Ochrophyta), 238 are red algae (Rhodophyta) and 66
green algae (Chlorophyta). New distribution records reveal the existence of 10 putative
endemic species for Cabo Verde islands, nine species that are geographically restricted to
the Macaronesia, five species that are restricted to Cabo Verde islands and the nearby
Tropical Western African coast, and five species known to occur only in the Maraconesian
Islands and Tropical West Africa. Two species, previously considered invalid names, are
here validly published as Colaconema naumannii comb. nov. and Sebdenia canariensis sp.
nov.
Key words: Cabo Verde islands, Macaronesia, Marine flora, Seaweeds, Tropical West
Africa.
Daniela Gabriel1 (e-mail: [email protected]) and S. Fredericq2, 1CIBIO -
Research Centre in Biodiversity and Genetic Resources, 1InBIO - Research Network in
Biodiversity and Evolutionary Biology, University of the Azores, Biology Department,
9501-801 Ponta Delgada, Azores, Portugal. 2Department of Biology, University of
Louisiana at Lafayette, Lafayette, Louisiana 70504-3602, USA.
INTRODUCTION
The Republic of Cabo Verde is an archipelago
situated in a region in the Northeast Atlantic
Ocean known as the Macaronesia, which also
contains the Portuguese archipelagos of the
Azores and Madeira (including the Selvagens)
and the Spanish archipelago of the Canaries
(Sangil et al. 2018). Cabo Verde archipelago is
located 570 km west of Senegal (West Africa),
and comprises 10 main islands and eight minor
islets divided in two groups, the Windward and
the Leeward islands, with a total coastline of 979
km and an Exclusive Economic Zone of 796.555
km2 (Menini et al. 2018).
The marine flora of Cabo Verde islands has been
studied since 1896 (see revision in Otero-Schmitt
1995), with the most recent checklist for the
archipelago published in 2005 by Prud’homme
van Reine et al. Since then, few studies and
reports have been published with the
characterization of the Caboverdean marine biota
(e.g. Silva 2012; Berecibar et al. 2013, Sangil et
al. 2018), but an updated list of the names of the
archiepelago's marine macroalgae is not available.
The Distribution Tool available on the AlgaeBase
Website delivers an incomplete species list for
Cabo Verde, mostly lacking the species that went
through taxonomic and nomenclatural changes
since 2005.
Gabriel and Fredericq
40
The present work aims to fulfill this gap, by
producing an updated list based on published
records, with recent additions (Afonso-Carillo et
al. 2006; Wilkes et al 2006; Almada et al. 2010;
Berecibar et al. 2013; Tronholm et al. 2013;
Sangil et al. 2018), nomenclatural corrections
(Guiry & Guiry 2019, present work), and the
inclusion of previously reported taxa (e.g. John et
al. 2004) which were not considered in
Prud’homme van Reine et al. (2005).
The resulting list comprises a total of 372
species, of which 68 are brown algae, 238 are red
algae and 66 are green algae, the removal of six
synonyms, nomenclatural correction of 84 taxa,
addition of 36 species and the valid publication of
two red algal species as Colaconema naumannii
comb. nov. and Sebdenia canariensis sp. nov.
New distribution records also resulted in the
recognition of 10 endemic species for Cabo
Verde, nine species geographically restricted to
Macaronesia and five species restricted to Cabo
Verde islands and the nearby Tropical Western
African coast. This confirms the African imprint
in the Caboverdean marine flora as reported by
Prud’homme van Reine (2005), though now with
less species restricted to only those two areas (a
reduction from 11 to five species). An African
imprint is also detected on the Macaronesian
marine flora, with five species limited to Tropical
West Africa and the Macaronesian islands. The
number of Caboverdean endemics is also reduced
from the 21 names reported by Haroun-Tabraue
(1998), since they have also been found in other
areas.
Future taxonomic work is necessary to assess
possible misidentifications in previous reports
(e.g. Prud’homme van Reine 1982; Price et al.
1986; Lawson et al. 1995; Leliaert & Coppejans
2004) as well as the clarification of general
taxonomic groups (e.g. Otero-Schmitt 1995;
Berecibar et al. 2013; Sangil et al. 2018).
Consequently, many species and genus names in
this checklist may not be accurate because the
taxonomic concepts of previous reports were
based nearly exclusively on superficial
morphological similarities without reference to
type collections or comparative molecular
systematics (with a few exceptions such as
Tronholm et al. 2013 and Belton et al. 2014).
Moreover, many of the listed names may be
outdated because many recent advances in
phycology and traditional morphology-based
species delimitation often yield inaccurate
estimates of seaweed diversity (Leliaert et al.
2013).
In a changing world with mounting evidence of
global climate change and its related effects,
changes in ocean circulation, ocean acidification,
and spread of invasive species, the need for
precise biodiversity assessment has never been
greater. Therefore, it is of prime importance that
the algae from Cabo Verde archipelago, as well
as worldwide, be well characterized
taxonomically and the short- and long-term trends
in the diversity of their assemblages thoroughly
examined with regard to seasonality in
ephemeral, annual and perennial species (Brodie
et al. 2009; Zenetos et al. 2010). The framework, taxonomy, nomenclature, and authorities in this checklist are predominantly built upon the current synthesis of taxa in AlgaeBase (Guiry & Guiry 2019). Taxa indicated with an asterisk (*) denotes those listed in Prud’homme van Reine et al. (2005). It is beyond the scope of this paper to provide a rigorous assessment about the misapplication of species and genus names reported for Cabo Verde islands without a critical examination of the seaweed vouchers from the region. Nevertheless, this checklist is the first step to start estimating the true diversity of the seaweeds from Cabo Verde in relation to global marine biogeography.
Kingdom Chromista
Phylum Ochrophyta
Class Phaeophyceae
Subclass Dictyotophycidae
Order Dictyotales
Family Dictyotaceae
1. Canistrocarpus crispatus (J.V. Lamouroux) De
Paula & De Clerck (as Dictyota crispata J.V.
Lamouroux)*
2. Dictyopteris delicatula J.V. Lamouroux*
3. Dictyopteris divaricata (Okamura) Okamura
(in Price et al. 1978)
Marine macroalgae of the Cabo Verde archipelago
41
4. Dictyopteris prolifera (Okamura) Okamura (in
Price et al. 1978)
5. Dictyota bartayresiana J.V. Lamouroux* 6. Dictyota canariensis (Grunow) Tronholm (in
Tronholm et al. 2013) 7. Dictyota crenulata J. Agardh* 8. Dictyota dichotoma (Hudson) J.V. Lamouroux* 9. Dictyota fasciola (Roth) J.V. Lamouroux* 10. Dictyota friabilis Setchell (as Dictyota
pfaffii Schnetter; in Sangil et al. 2018) 11. Dictyota humifusa Hörnig, Schnetter &
Coppejans* 12. Dictyota implexa (Desfontaines) J.V. Lamouroux
(as Dictyota divaricata J.V. Lamouroux)* 13. Dictyota jamaicensis W.R. Taylor (in
Tronholm et al. 2013) 14. Dictyota liturata J. Agardh* 15. Dictyota menstrualis (Hoyt) Schnetter,
Hörning & Weber-Peukert (in John et al.
2004) 16. Dictyota mertensii (C. Martius) Kützing* 17. Dictyota pinnatifida Kützing (as Dictyota
alternans (J. Agardh) Hörnig, Schnetter &
Prud'homme van Reine)* 18. Lobophora variegata (J.V. Lamouroux)
Womersley ex E.C. Oliveira*
Note: The genus Lobophora is the subject of
recent revisions (e.g. Camacho et al. 2019)
and material from Cabo Verde needs to be
critically examined in order to designate the
correct species name.
19. Padina gymnospora (Kützing) Sonder*
20. Padina pavonica (Linnaeus) Thivy* 21. Rugulopteryx suhrii (Kützing) De Clerck &
Coppejans (as Dictyota suhrii (Kützing) I. Hörnig, R. Schnetter & W.F. Prud'homme van Reine)*
22. Stypopodium zonale (J.V. Lamouroux) Papenfuss*
23. Zonaria tournefortii (J.V. Lamouroux) Montagne*
Subclass Fucophycidae
Order Ectocarpales
Family Acinetosporaceae
24. Acinetospora crinita (Carmichael)
Sauvageau*
25. Feldmannia irregularis (Kützing) Hamel*
26. Feldmannia mitchelliae (Harvey) H.-S. Kim (as
Hincksia mitchelliae (Harvey) P.C. Silva)*
Family Chordariaceae
27. Levringia brasiliensis (Montagne) A.B. Joly* 28. Levringia natalensis (Kützing) Kylin*
Family Ectocarpaceae
29. Ectocarpus hamulosus Harvey & Bailey*
Note: Endemic.
30. Ectocarpus simpliciusculus C. Agardh (as
Feldmannia irregularis (Kutzing) Hamel; in
John et al. 2004)
31. Spongonema tomentosum (Hudson) Kützing*
Family Scytosiphonaceae
32. Chnoospora minima (Hering) Papenfuss*
33. Colpomenia sinuosa (Mertens ex Roth)
Derbès & Solier*
34. Hydroclathrus clathratus (C. Agardh) M. Howe* 35. Rosenvingea intricata (J. Agardh) Børgesen
(in Sangil et al. 2018) 36. Stragularia clavata (Harvey) Hamel*
Order Fucales Family Sargassaceae
37. Cystoseira abies-marina (S.G. Gmelin) C. Agardh* 38. Cystoseira compressa (Esper) Gerloff &
Nizamuddin*
39. Cystoseira foeniculacea (Linnaeus) Greville*
Gabriel and Fredericq
42
40. Cystoseira humilis Schousboe ex Kützing* 41. Cystoseira nodicaulis (Withering) M. Roberts* 42. Cystoseira sauvageauana Hamel* 43. Cystoseira selaginoides Naccari (as Cystoseira
sauvageauana Hamel)* 44. Cystoseira sonderi (Kützing) Piccone*
Note: Endemic.
45. Cystoseira tamariscifolia (Hudson) Papenfuss*
46. Cystoseira usneoides (Linnaeus) M. Roberts* 47. Sargassum acinarium (Linnaeus) Setchell* 48. Sargassum cymosum C. Agardh* 49. Sargassum natans (Linnaeus) Gaillon* 50. Sargassum platycarpum Montagne* 51. Sargassum rigidulum Kützing (as Sargassum
cymosum C. Agardh)* 52. Sargassum subrepandum var. [rueppellii] f.
turneri (Kützing) Grunow (as Sargassum
turneri (Kützing) Montagne)* 53. Sargassum vulgare C. Agardh*
Note: John et al. (2003:57, 164) did not
distinguish between S. vulgare and S. vulgare
var. foliosissimum.
Order Laminariales
Family Lessoniaceae
54. Ecklonia biruncinata (Bory) Papenfuss (as
Ecklonia muratii Feldmann)* 55. Ecklonia muratii Feldmann*
Note: Restricted to Tropical West Africa and
Macaronesia. 56. Ecklonia radiata (C. Agardh) J. Agardh (as
Ecklonia muratii Feldmann)*
Order Ralfsiales
Family Neoralfsiaceae
57. Neoralfsia expansa (J. Agardh) P.-E. Lim &
H. Kawai ex Cormaci & G. Furnari (as Ralfsia
expansa (J. Agardh) J. Agardh)*
Family Ralfsiaceae
58. Ralfsia verrucosa (Areschoug) Areschoug*
Order Scytothamnales
Family Asteronemataceae
59. Asteronema breviarticulatum (J. Agardh) Ouriques
& Bouzon (as Hincksia breviarticulata (J. Agardh)
P.C. Silva)*
Family Bachelotiaceae
60. Bachelotia antillarum (Grunow) Gerloff*
Order Sphacelariales
Family Sphacelariaceae
61. Sphacelaria brachygonia Montagne*
62. Sphacelaria cirrosa (Roth) C. Agardh* 63. Sphacelaria fusca (Hudson) S.F. Gray (in
Prud'homme van Reine 1982) 64. Sphacelaria novae-hollandiae Sonder (in
John et al. 2004) 65. Sphacelaria rigidula Kützing* 66. Sphacelaria solitaria (Pringsheim) Kylin
(misspelled as Sphacelaria soliaria (Pringsheim)
Kylin; in John et al. 2004) 67. Sphacelaria tribuloides Meneghini*
Family Stypocaulaceae
68. Halopteris scoparia (Linnaeus) Sauvageau (as
Stypocaulon scoparium (Linnaeus) Kutzing)*
Marine macroalgae of the Cabo Verde archipelago
43
Kingdom Plantae
Phylum Rhodophyta
Subphylum Eurhodophytina
Class Bangiophyceae
Subclass Bangiophycidae
Order Bangiales
Family Bangiaceae
1. Porphyra umbilicalis Kützing*
Class Florideophyceae Subclass Ahnfeltiophycidae
Order Ahnfeltiales
Family Ahnfeltiaceae
2. Ahnfeltia elongata Montagne (as Chondrus
elongatus Montagne)*
Subclass Corallinophycidae
Note: The systematics of the Corallinophycidae is in a constant flux and has undergone major recent taxonomic changes at the family, subfamily, genus and species level (e.g. Nelson et al. 2015; Rösler et al. 2016; Caragnano et al. 2018; Liu et al. 2018; Peña et al. 2018). For this reason, the classification of this group did not follow Guiry & Guiry (2019). Members of the subfamilies of the family Corallinaceae (previously viewed as families in the Corallinales) are here listed alphabetically. Likewise, members of the previously known Lithothamniaceae and Mesophyllaceae are here listed under the Hapalidiaceae (Hapalidiales).
Order Corallinales Family Corallinaceae
3. Amphiroa fragilissima (Linnaeus) J.V. Lamouroux* 4. Amphiroa rigida J.V. Lamouroux* 5. Corallina officinalis Linnaeus*
6. Ellisolandia elongata (J.Ellis & Solander) K.R.
Hind & G.W. Saunders (as Corallina 7. Floiophycus africanus (Foslie) R.A. Townsend &
Huisman (as Spongites africanus (Foslie) J.
Afonso-Carrillo; M. Chacana & M. Sanson)*
8. Goniolithon orotavicum Foslie (as Neogoniolithon
orotavicum (Foslie) Me. Lemoine ex Afonso-
Carrillo)*
Note: Restricted to Tropical West Africa and
Macaronesia. 9. Harveylithon samoënse (Foslie) A. Rösler;
Perfectti; V. Peña & J.C. Braga (as
Hydrolithon samoense (Foslie) Keats & Y.M.
Chamberlain and Neogoniolithon illitus (Me.
Lemoine) Afonso-Carrillo)* 10. Hydrolithon farinosum (J.V. Lamouroux)
Penrose & Y.M. Chamberlain* 11. Jania adhaerens J.V. Lamouroux* 12. Jania capillacea Harvey* 13. Jania crassa J.V. Lamouroux* 14. Jania cubensis Montagne ex Kützing (as
Haliptilon cubense (Montagne ex Kutzing)
Garbary & H.W. Johansen)* 15. Jania cultrata (Harvey) J.H. Kim; Guiry &
H.-G. Choi (as Cheilosporum elegans (J.
Hooker & Harvey) Areschoug)* 16. Jania longifurca Zanardini (in Berecibar et al.
2013) 17. Jania rubens (Linnaeus) J.V. Lamouroux* 18. Jania tenella (Kützing) Grunow* 19. Jania verrucosa J.V. Lamouroux* 20. Jania virgata (Zanardini) Montagne (as
Haliptilon virgatum (Zanardini) Garbary &
H.W. Johansen)* 21. Lithophyllum aninae Foslie*
Note: Endemic. 22. Lithophyllum byssoides (Lamarck) Foslie (in
John et al. 2004)
23. Lithophyllum esperi (Me. Lemoine) South &
Tittley*
Note: Restricted to Macaronesia.
24. Lithophyllum geometricum Me. Lemoine*
25. Lithophyllum gracile Foslie*
Note: Endemic.
Gabriel and Fredericq
44
26. Lithophyllum incrustans Philippi*
27. Lithophyllum lobatum Me. Lemoine* 28. Lithophyllum polycephalum Foslie* 29. Lithophyllum simile Foslie* 30. Lithophyllum vickersiae Me. Lemoine* 31. Lithoporella melobesioides (Foslie) Foslie* 32. Lithoporella sauvageaui (Foslie) Adey*
Note: Restricted to Macaronesia.
33. Neogoniolithon caribaeum (Foslie) Adey*
34. Neogoniolithon hauckii (Rothpletz) R.A. Townsend &
Huisman (as Neogoniolithon mamillosum (Hauck)
Setchell & L.R. Mason)* 35. Neogoniolithon mamillare (Harvey) Setchell
& L.R. Mason* 36. Pneophyllum amplexifrons (Harvey) Y.M.
Chamberlain & R.E. Norris* 37. Porolithon oligocarpum (Foslie) W.H. Adey*
Note: Restricted to Macaronesia. 38. Porolithon onkodes (Heydrich) Foslie (as
Hydrolithon onkodes (Heydrich) Penrose &
Woelkerling)* 39. Pseudolithophyllum mildbraedii (Pilger) De Toni (as
Lithophyllum retusum (Foslie) Foslie)*
Note: Restricted to Tropical West Africa and
Cabo Verde islands. 40. Spongites absimilis (Foslie & M. Howe)
Afonso-Carrillo* 41. Spongites fruticulosus Kützing (in John et al.
2004) 42. Titanoderma mediterraneum (Foslie)
Woelkerling* 43. Titanoderma pustulatum (J.V. Lamouroux)
Nägeli (as Lithophyllum pustulatum (J.V.
Lamouroux) Foslie)*
Order Hapalidiales
Family Hapalidiaceae
44. Capensia fucorum (Esper) A. Athanasiadis
(as Lithophyllum capense Rozanov)*
45. Leptophytum bisporum (Foslie) W.H. Adey
(as Phymatolithon bisporum (Foslie) Afonso-
Carrillo)* 46. Lithothamnion corallioides (P. Crouan & H. Crouan)
P. Crouan & H. Crouan (as Lithothamnion solutum
(Foslie) Me. Lemoine)* 47. Melobesia membranacea (Esper) J.V. Lamouroux* 48. Melyvonnea erubescens (Foslie) Athanasiadis &
D.L. Ballantine (as Mesophyllum erubescens
(Foslie) Me. Lemoine)* 49. Mesophyllum ectocarpon (Foslie) W.H. Adey*
Note: Restricted to Tropical West Africa and
Macaronesia. 50. Mesophyllum lichenoides (J. Ellis) Me.
Lemoine* 51. Phymatolithon lenormandii (Areschoug)
W.H. Adey* 52. Phymatolithon purpureum (P. Crouan & H.
Crouan) Woelkerling & L.M. Irvine*
Order Sporolithales
Family Sporolithaceae
53. Sporolithon africanum (Foslie) Afonso-
Carillo*
Subclass Nemaliophycidae Order Colaconematales
Family Colaconemataceae
54. Colaconema naumannii (Askenasy) Prud'homme
van Reine, R.J. Haroun & L.B.T. Kosterman ex D.
Gabriel & Fredericq comb. nov. Basionym:
Chantransia naumannii Askenasy (naumani),
published in Forschungsreise S.M.S. "Gazelle".
Theil 4: Botanik, p.31, 1888.
Note: John et al. (2004:54) indicated that
Stegenga (pers. comm.) suggested that
Acrochaetium naumannii (Askenasy)Askenasy
should be referable to the genus Colaconema. The
new combination Colaconema naumannii
(Askenasy) Prud'homme van Reine, R.J. Haroun &
Marine macroalgae of the Cabo Verde archipelago
45
L.B.T. Kostermans* was proposed by Prud'homme
van Reine et al. (2005: 21, nom. inval.), who failed
to cite the place of publication of the basionym.
The complete citation is here refered to validate the
new combination, according to Article 46 of the
Shenzhen Code (Turland et al. 2018).
55. Colaconema nemalii (De Notaris ex L.
Dufour) Stegenga* 56. Colaconema savianum (Meneghini) R. Nielsen (as
Colaconema byssaceum (Kutzing) J.H. Price)*
Order Nemaliales Family Galaxauraceae
57. Dichotomaria obtusata (J. Ellis & Solander)
Lamarck (as Galaxaura obtusata (J. Ellis &
Solander) J.V. Lamouroux)* 58. Galaxaura rugosa (J. Ellis & Solander) J.V.
Lamouroux* 59. Tricleocarpa cylindrica (J. Ellis & Solander)
Huisman & Borowitzka* 60. Tricleocarpa fragilis (Linnaeus) Huisman &
R.A. Townsend*
Family Liagoraceae
61. Ganonema farinosum (J.V. Lamouroux) K.C.
Fan & Yung C. Wang* 62. Helminthocladia calvadosii (J.V. Lamouroux
ex Duby) Setchell* 63. Liagora albicans J.V. Lamouroux* 64. Liagora ceranoides J.V. Lamouroux* 65. Liagora distenta (Mertens ex Roth) J.V.
Lamouroux* 66. Liagora viscida (Forsskål) C. Agardh* 67. Titanophycus validus (Harvey) Huisman, G.W.
Saunders & A.R. Sherwood (as Liagora valida
Harvey)*
68. Trichogloea requienii (Montagne) Kützing*
Family Liagoropsidaceae
69. Liagoropsis schrammii (P. Crouan & H. Crouan) Doty
& I.A. Abbott*
Family Scinaiaceae
70. Scinaia furcellata (Turner) J. Agardh*
Subclass Rhodymeniophycidae
Order Acrosymphytales
Family Acrosymphytaceae
71. Acrosymphyton purpuriferum (J. Agardh)
Sjöstedt (as Helminthiopsis purpuriferum (J.
Agardh) Pappenfuss)*
Family Schimmelmanniaceae
72. Schimmelmannia bollei Montagne*
Note: Restricted to Macaronesia.
Order Bonnemaisoniales
Family Bonnemaisoniaceae
73. Asparagopsis taxiformis (Delile) Trevisan*
Order Ceramiales
Family Callithamniaceae
74. Aglaothamnion boergesenii (Aponte & D.L.
Ballantine) L'Hardy-Halos & Rueness* 75. Aglaothamnion tenuissimum (Bonnemaison)
Feldmann-Mazoyer (as Ceramium
tenuissimum (Roth) J. Agardh)* 76. Callithamnion corymbosum (Smith)
Lyngbye* 77. Callithamnion ellipticum Montagne*
Note: Restricted to Macaronesia. 78. Callithamnion granulatum (Ducluzeau) C.
Agardh* 79. Callithamnion tetragonum (Withering) S.F.
Gray*
Gabriel and Fredericq
46
80. Crouania attenuata (C. Agardh) J. Agardh* 81. Gaillona hookeri (Dillwyn) Athanasiadis (as
Aglaothamnion hookeri (Dillwyn) Maggs &
Hommersand)* 82. Gaillona rosea (Roth) Athanasiadis (as
Aglaothamnion roseum (Roth) Maggs &
L'Hardy-Halos)* 83. Gulsonia ecorticata Lawson & John*
Note: Restricted to Tropical West Africa and
Cabo Verde islands.
Family Ceramiaceae 84. Antithamnion cruciatum (C. Agardh) Nägeli*
85. Antithamnionella boergesenii (Cormaci & G.
Furnari) Athanasiadis* 86. Antithamnionella elegans (Berthold) J.H.
Price & D.M. John (as Antithamnionella
boergesenii (Cormaci & G. Furnari)
Athanasiadis)* 87. Centroceras clavulatum (C. Agardh)
Montagne* 88. Centroceras hyalacanthum Kützing (as
Centroceras clavulatum (C. Agardh)
Montagne)* 89. Ceramium ciliatum (J. Ellis) Ducluzeau* 90. Ceramium codii (H. Richards) Mazoyer* 91. Ceramium cornutum P.J.L. Dangeard*
Note: Restricted to Tropical West Africa and
Cabo Verde islands. 92. Ceramium diaphanum (Lightfoot) Roth (as
Ceramium nodosum (Kutzing) Harvey)* 93. Ceramium nitens (C. Agardh) J. Agardh* 94. Ceramium poeppigianum Grunow (as
Reinboldiella poeppigianum (Grunov)
Feldmann & Mazoyer)* 95. Ceramium strobiliforme G.W. Lawson &
D.M. John* 96. Ceramium tenerrimum (G. Martens) Okamura
(in Almada et al. 2010)
97. Compsothamnion thuioides (Smith) Nägeli* 98. Gayliella flaccida (Harvey ex Kützing) T.O.
Cho & L.J. McIvor (as Ceramium flaccidum
(Kutzing) Ardissone)*
Family Dasyaceae
99. Dasya baillouviana (S.G. Gmelin) Montagne
(in Sangil et al. 2018) 100. Dasya schmidtiana Sonder*
Note: Endemic. 101. Halydictyon mirabile Zanardini* 102. Heterosiphonia crispella (C. Agardh) M.J.
Wynne*
Note: Lipkin & Silva (2002:32) indicates that
H. crispella var. laxa appears to be a shaded
habitat ecophene.
Family Delesseriaceae
103. Acrosorium ciliolatum (Harvey) Kylin (as
Acrosorium venulosum (Zanardini) Kylin)* 104. Apoglossum ruscifolium (Turner) J. Agardh* 105. Haraldia lenormandii (Derbès & Solier)
Feldmann* 106. Hypoglossum hypoglossoides (Stackhouse)
Collins & Hervey* 107. Phrix spatulata (E.Y. Dawson) M.J. Wynne,
M. Kamiya & J.A. West (as Apoglossum
gregarium E.Y. Dawson) M.J. Wynne; in
Almada et al. 2010) 108. Taenioma nanum (Kützing) Papenfuss* 109. Taenioma perpusillum (J. Agardh) J.
Agardh*
Family Rhodomelaceae
110. Alsidium triquetrum (S.G. Gmelin) Trevisan
(as Bryothamnion triquetrum (S.G. Gmelin)
M. Howe)*
111. Bryocladia cuspidata (J. Agardh) De Toni*
Marine macroalgae of the Cabo Verde archipelago
47
112. Bryocladia thyrsigera (J. Agardh) F.Schmitz*
113. Carradoriella denudata (Dillwyn) A.M.
Savoie & G.W. Saunders (as Polysiphonia
denudata (Dillwyn) Greville ex Harvey)* 114. Chondria densa P. [J.L.] Dangeard* 115. Chondrophycus glandulifer (Kützing) Lipkin
& P.C. Silva (in John et al. 2004) 116. Digenea simplex (Wulfen) C. Agardh* 117. Herposiphonia secunda (C. Agardh)
Ambronn* 118. Herposiphonia secunda f. tenella (C.
Agardh) M.J. Wynne* 119. Janczewskia verruciformis Solms-Laubach* 120. Laurencia dendroidea J. Agardh (as
Laurencia majuscula (Harvey) Lucas)* 121. Laurencia galtsoffii M. Howe* 122. Laurencia intricata J.V. Lamouroux (as
Laurencia implicata J. Agardh)* 123. Laurencia microcladia Kützing* 124. Laurencia nidifica J. Agardh* 125. Laurencia obtusa (Hudson) J.V. Lamouroux* 126. Laurencia tenera C.K. Tseng* 127. Laurencia viridis Gil-Rodríguez & Haroun*
Note: Restricted to Macaronesia. 128. Leptosiphonia brodiei (Dillwyn) A.M.
Savoie & G.W. Saunders (as Polysiphonia
brodiaei (Dillwyn) Sprengel)* 129. Leptosiphonia schousboei (Thuret) Kylin (in
John et al. 2004) 130. Lophocladia trichoclados (C. Agardh) F.
Schmitz* 131. Lophosiphonia obscura (C. Agardh)
Falkenberg* 132. Melanothamnus collabens (C. Agardh) Díaz-
Tapia & Maggs (as Streblocladia collabens
(C. Agardh) Falkenberg)*
133. Melanothamnus ferulaceus (Suhr ex J.
Agardh) Díaz-Tapia & Maggs (as
Polysiphonia ferulacea Suhr ex C. Agardh)* 134. Melanothamnus gorgoniae (Harvey) Díaz-
Tapia & Maggs (as Polysiphonia gorgoniae
Harvey)* 135. Osmundea hybrida (A.P. de Candolle) K.W.
Nam* 136. Osmundea pinnatifida (Hudson) Stackhouse* 137. Palisada corallopsis (Montagne) Sentíes,
Fujii & Díaz-Larrea (as Chondrophycus
corallopsis (Montagne) K.W. Nam)* 138. Palisada intermedia (Yamada) K.W. Nam
(as Chondrophycus intermedia (Yamada)
Garbary & J.T. Harper)* 139. Palisada patentiramea (Montagne) Cassano,
Sentíes, Gil-Rodríguez & M.T. Fujii (as
Chondrophycus patentiramea (Montagne)
K.W. Nam)* 140. Palisada perforata (Bory) K.W. Nam (as
Chondrophycus papillosa (C. Agardh)
Garbary & J.T. Harper and Chondrophycus
perforata (Bory) K.W. Nam)* 141. Palisada thuyoides (Kützing) Cassano,
Sentíes, Gil-Rodríguez & M.T. Fujii (as
Laurencia paniculata (C. Agardh) J. Agardh)* 142. Polysiphonia pulvinata (Roth) Sprengel* 143. Polysiphonia scopulorum Harvey* 144. Polysiphonia stricta (Mertens ex Dillwyn)
Greville* 145. Polysiphonia subtilissima Montagne* 146. Vertebrata foetidissima (Cocks ex Bornet)
Díaz-Tapia & Maggs (as Polysiphonia tepida
Hollenberg)* 147. Vertebrata fruticulosa (Wulfen) Kuntze (as
Boergeseniella fruticulosa (Wulfen) Kylin)* 148. Vertebrata reptabunda (Suhr) Díaz-Tapia &
Maggs (as Lophosiphonia reptabunda (Suhr)
Kylin)*
Gabriel and Fredericq
48
149. Yuzurua poiteaui (J.V. Lamouroux) Martin-
Lescanne (as Laurencia poiteaui (J.V.
Lamouroux) M. Howe)*
Family Sarcomeniaceae
150. Cottoniella filamentosa (M. Howe)
Børgesen* 151. Platysiphonia caribaea D.L. Ballantine &
M.J. Wynne (in Lawson et al. 1995) 152. Platysiphonia delicata (Clemente)
Cremades* 153. Platysiphonia intermedia (Grunow) M.J.
Wynne*
Family Spyridiaceae
154. Spyridia clavata Kützing (in John et al.
2004)
155. Spyridia filamentosa (Wulfen) Harvey* 156. Spyridia hypnoides (Bory) Papenfuss*
Family Wrangeliaceae 157. Anotrichium barbatum (C. Agardh) Nägeli*
158. Anotrichium furcellatum (J. Agardh)
Baldock*
159. Anotrichium tenue (C. Agardh) Nägeli* 160. Halurus flosculosus (J. Ellis) Maggs &
Hommersand (in John et al. 2004) 161. Tiffaniella gorgonea (Montagne) Doty &
Meñez* 162. Vickersia baccata (J. Agardh) Karsakoff* 163. Wrangelia argus (Montagne) Montagne* 164. Wrangelia penicillata (C. Agardh) C.
Agardh*
Order Gelidiales
Family Gelidiaceae
165. Gelidium corneum (Hudson) J.V.
Lamouroux (as Gelidium sesquipedale
(Clemente) Thuret)* 166. Gelidium pusillum (Stackhouse) Le Jolis* 167. Gelidium spinosum (S.G. Gmelin) P.C.
Silva*
Family Gelidiellaceae
168. Gelidiella acerosa (Forsskål) Feldmann &
Hamel* 169. Millerella pannosa (Feldmann) G.H. Boo &
Le Gall (as Gelidiella pannosa (Bornet ex
Feldmann) Feldmann & Hamel)*
Family Pterocladiaceae
170. Pterocladiella capillacea (S.G. Gmelin)
Santelices & Hommersand*
Order Gigartinales
Family Areschougiaceae
171. Anatheca montagnei F. Schmitz*
Note: Restricted to Tropical West Africa and
Cabo Verde islands.
Family Caulacanthaceae
172. Caulacanthus ustulatus (Mertens ex Turner)
Kützing*
Family Cystocloniaceae
173. Hypnea arbuscula P.J.L. Dangeard*
Note: Restricted to Tropical West Africa and
Macaronesia.
174. Hypnea cenomyce J. Agardh*
175. Hypnea cervicornis J. Agardh (as Hypnea
spinella (C. Agardh) Kutzing)* 176. Hypnea divaricata (C. Agardh) Greville* 177. Hypnea flagelliformis Greville ex J.
Agardh*
Marine macroalgae of the Cabo Verde archipelago
49
178. Hypnea musciformis (Wulfen) J.V. Lamouroux* 179. Hypnea pannosa J. Agardh* 180. Hypnea spinella (C. Agardh) Kützing* 181. Hypnea valentiae (Turner) Montagne* 182. Hypneocolax stellaris Børgesen*
Family Dumontiaceae
183. Dudresnaya verticillata (Withering) Le
Jolis*
Family Gigartinaceae
184. Chondracanthus teedei (Mertens ex Roth)
Kützing*
185. Chondrus crispus Stackhouse* 186. Chondrus crispus var. lonchophorus
Montagne*
Note: Endemic.
187. Chondrus uncialis Harvey & Bailey*
Note: Endemic.
Family Kallymeniaceae
188. Austrokallymenia schizophylla (J. Agardh)
G.W. Saunders (as Kallymenia schizophylla
(Harvey) J. Agardh)* 189. Kallymenia reniformis (Turner) J. Agardh* 190. Meredithia microphylla (J. Agardh) J.
Agardh*
Family Phyllophoraceae 191. Ahnfeltiopsis concinna (J. Agardh) P.C.
Silva & DeCew* 192. Ahnfeltiopsis devoniensis (Greville) P.C.
Silva & DeCew (as Gymnogongrus
devoniensis (Greville) Schotter)* 193. Ahnfeltiopsis gigartinoides (J. Agardh) P.C.
Silva & DeCew* 194. Gymnogongrus crenulatus (Turner) J. Agardh*
195. Stenogramma interruptum (C. Agardh)
Montagne*
Family Solieriaceae
196. Meristotheca decumbens Grunow*
Note: Restricted to Macaronesia.
197. Meristotheca gelidium (J. Agardh) E.J. Faye
& M. Masuda (as Meristiella echinocarpum
(Areschoug) D.P. Cheney & P.W.
Gabrielson)* 198. Solieria filiformis (Kützing) P.W.
Gabrielson* 199. Wurdemannia miniata (Sprengel) Feldmann
& Hamel*
Order Gracilariales
Family Gracilariaceae
200. Gracilaria bursa-pastoris (S.G. Gmelin) P.C.
Silva*
201. Gracilaria isabellana Gurgel, Fredericq &
J.N. Norris (as Gracilaria lacinulata (H.
West) M. Howe)*
202. Gracilaria multipartita (Clemente) Harvey*
203. Hydropuntia rangiferina (Kützing) Gurgel &
Fredericq (as Gracilaria rangiferina
(Kutzing) Piccone)*
Order Halymeniales
Family Halymeniaceae
204. Cryptonemia seminervis (C. Agardh) J.
Agardh* 205. Grateloupia filicina (J.V. Lamouroux) C.
Agardh* 206. Grateloupia scutellata Kützing*
Note: Endemic.
207. Halymenia duchassaingii (J. Agardh) Kylin*
208. Halymenia elongata C. Agardh*
Gabriel and Fredericq
50
Order Nemastomatales
Family Nemastomataceae
209. Predaea feldmannii Børgesen*
Family Schizymeniaceae
210. Platoma confusum (Kraft & D.M. John)
Gabriel & Fredericq (as Nemastoma confusum
Kraft & D.M. John)* Note: Restricted to Tropical West Africa and
Macaronesia.
Order Peyssonneliales
Family Peyssonneliaceae
211. Peyssonnelia dubyi P. Crouan & H. Crouan*
212. Peyssonnelia harveyana P. Crouan & H.
Crouan ex J. Agardh* 213. Peyssonnelia heteromorpha (Zanardini)
Athanasiadis (as Peyssonnelia polymorpha
(Zanardini) F. Schmitz)* 214. Peyssonnelia inamoena Pilger* 215. Peyssonnelia magna Ercegovic* 216. Peyssonnelia rosa-marina Boudouresque &
Denizot* 217. Peyssonnelia rubra (Greville) J. Agardh* 218. Peyssonnelia squamaria (S.G. Gmelin)
Decaisne ex J. Agardh (in Berecibar et al.
2013) 219. Polystrata fosliei (Weber Bosse) Denizot*
Order Plocamiales
Family Plocamiaceae
220. Plocamium cartilagineum (Linnaeus) P.S.
Dixon* 221. Plocamium concinnum Areschoug*
Note: Endemic. 222. Plocamium corallorhiza (Turner) J.D.
Hooker & Harvey*
223. Plocamium telfairiae (W.J. Hooker &
Harvey) Harvey ex Kützing*
Order Rhodymeniales
Family Champiaceae
224. Champia parvula (C. Agardh) Harvey*
225. Champia vieillardii Kützing (in Almada et
al. 2010) 226. Coelothrix irregularis (Harvey) Børgesen
(in Sangil et al. 2018)
Family Faucheaceae 227. Leptofauchea rhodymenioides W.R. Taylor*
Family Lomentariaceae
228. Ceratodictyon intricatum (C. Agardh) R.E.
Norris*
Family Rhodymeniaceae 229. Botryocladia botryoides (Wulfen) Feldmann*
230. Botryocladia macaronesica Afonso-Carillo,
Sobrino, Tittley & Neto (in Afonso-Carillo et
al. 2006)
Note: Restricted to Macaronesia. 231. Botryocladia papenfussiana Ganesan &
Lemus (in Wilkes et al. 2006) 232. Rhodymenia pseudopalmata (J.V. Lamouroux)
P.C. Silva*
Order Sebdeniales
Family Sebdeniaceae
233. Sebdenia canariensis Soler-Onis, Haroun,
Viera-Rodríguez & Prud’homme van Reine ex
D. Gabriel & Fredericq sp. nov. First
published in XI Simposio Nacional de
Botánica Criptogámica: resúmenes de
comunicaciones, pp. 15-16, 1995, nom. inval.
Holotype: BCM 2206 (tetrasporophyte),
Marine macroalgae of the Cabo Verde archipelago
51
collected by R. Haroun, on 19-June-1993, at
23 m depth. Deposited in the Herbarium of
University of Las Palmas de Gran Canaria
(BCM).
Type locality: Las Lanzas (28º 49’ 54”
N, 13º 51’ 32” W), in the Strait of Bocaina,
between Lanzarote and Fuerteventura,
Canary Islands.
Etymology: The species name refers to
its type locality, from the Canary Islands.
We here present an English translation
of the original description and formally
instate the species as Sebdenia
canariensis.
Original description (sensu Soler-Onis et
al. 2015: 15-16): Foliose, gelatinous
thallus, 380-400 m thick, at least 35 cm
tall and 25-30 cm wide, brownish-pink in
colour, attached to the substratum by a
small basal disc (up to 5 mm of diameter),
from which a cylindrical stipe about 2 cm
long develops, becoming flattened at the
basis of the blade. Blade has a swollen
basis, with pseudo-dichotomous lobes,
ending in round apices, with smooth edges.
Cortex composed of one layer of very
pigmented isodiametric cells that are 7-11
m in diameter. Subcortex with two layers
of cells 14-16 m and 40-50 m in
diameter, respectively. Medulla formed by
star-like cells 50-55 m in diameter and
filaments 12-17 m long, connecting
neighbouring star-like cells in the
subcortex. Usually, adjacent filaments
become linked with one another, but also
bifurcated filaments are merged again.
Gland cells, 10-12 m in diameter, develop
from star-like cells and filaments, and
frequently observed throughout the thallus.
Subspherical, cruciate tetrasporangia, 20-
25 m in diameter, are spread among
cortical cells on both blade surfaces.
Note: Woelkerling et al. (1998: 121,
nom. inval.) suggests S. canariensis Soler-
Onis, Haroun & Prud’homme van Reine is
a synonym of S. macaronesica Soler-
Onis*, without giving any diagnosis or
justification for the new species,
combination or replacement, therefore
constituting an invalid name according to
Article 38 of the Shenzhen Code (Turland
et al. 2018). S. canariensis was described
by Soler-Onis et al. (1995: 15-16, nom.
inval.) based on a description in Spanish,
also constituting an invalid name according
to Article 39 of the Shenzhen Code. Since
neither of the two species was validly
published, the species epithet ‘canariensis’
does not have priority over ‘macaronesica’
(Article 11 of the Shenzhen Code),
nevertheless it is here maintained in honor
of its first authors. The new species seems
restricted to Macaronesia with all records
(except that of Soler-Onís et al. 1995)
previously reported as S. macaronesica.
234. Sebdenia rodrigueziana (Feldmann)
Codomier ex Parkinson*
Subphylum Proteorhodophytina
Class Compsopogonophyceae
Order Erythropeltales
Family Erythrotrichiaceae
235. Erythrocladia irregularis Rosenvinge*
236. Erythrotrichia carnea (Dillwyn) J.
Agardh*
Class Stylonematophyceae
Order Stylonematales
Family Stylonemataceae
237. Chroodactylon ornatum (C. Agardh)
Basson*
238. Stylonema alsidii (Zanardini) K.M. Drew*
Phylum Chlorophyta
Class Ulvophyceae
Order Bryopsidales
Family Bryopsidaceae
1. Bryopsis duplex De Notaris*
2. Bryopsis myosuroides Kützing (as Bryopsis
setacea Hering)*
3. Bryopsis pennata J.V. Lamouroux (in
Berecibar et al. 2013)
Gabriel and Fredericq
52
Note: Ballesteros (1990: 42) considers this
species as conspecific with B. plumosa.
4. Bryopsis plumosa (Hudson) C. Agardh*
5. Bryopsis stenoptera Pilger*
Note: Restricted to Tropical West Africa and
Cabo Verde islands.
Family Caulerpaceae
6. Caulerpa ambigua Okamura (as Caulerpella
ambigua (Okamura) Prud'homme van Reine
& Lokhorst)* 7. Caulerpa cupressoides (Vahl) C. Agardh*
8. Caulerpa mexicana Sonder ex Kützing* 9. Caulerpa prolifera (Forsskål) J.V. Lamouroux* 10. Caulerpa racemosa (Forsskål) J. Agardh* 11. Caulerpa chemnitzia (Esper) J.V. Lamouroux
(as Caulerpa racemosa var. peltata (J.V.
Lamouroux) Eubank; in Berecibar et al. 2013)
Note: Belton et al. (2014:48) reinstated C.
chemnitzia, including C. racemosa var.
peltata as an environmentally induced form. 12. Caulerpa sertularioides (S.G. Gmelin) M.
Howe*
13. Caulerpa taxifolia (M. Vahl) C. Agardh* 14. Caulerpa verticillata J. Agardh* 15. Caulerpa webbiana Montagne*
Family Codiaceae 16. Codium adhaerens C. Agardh*
17. Codium decorticatum (Woodward) M. Howe* 18. Codium guineënse P.C. Silva ex G.W.
Lawson & D.M. John (in John et al. 2004) 19. Codium intertextum Collins & Hervey* 20. Codium repens P. Crouan & H. Crouan* 21. Codium taylorii P.C. Silva* 22. Codium tomentosum Stackhouse*
Family Derbesiaceae
23. Derbesia tenuissima (Moris & De Notaris) P.
Crouan & H. Crouan*
Family Halimedaceae
24. Halimeda discoidea Decaisne*
25. Halimeda tuna (J. Ellis & Solander) J.V.
Lamouroux*
Family Ostreobiaceae
26. Ostreobium quekettii Bornet & Flahault*
Family Udoteaceae
27. Boodleopsis pusilla (Collins) W.R. Taylor,
A.B. Joly & Bernatowicz*
28. Flabellia petiolata (Turra) Nizamuddin* 29. Pseudochlorodesmis furcellata (Zanardini)
Børgesen (in Sangil et al. 2018) 30. Udotea flabellum (J.Ellis & Solander) M.
Howe*
Order Cladophorales
Family Anadyomenaceae
31. Anadyomene stellata (Wulfen) C. Agardh*
32. Anadyomene saldanhae A.B. Joly & E.C.
Oliveira (in Almada et al. 2010) 33. Microdictyon umbilicatum (Velley) Zanardini
(as Microdictyon calodictyon (Montagne)
Kutzing)*
Family Boodleaceae
34. Boodlea composita (Harvey) F. Brand*
35. Cladophoropsis membranacea (Hofman Bang
ex C. Agardh) Børgesen* 36. Phyllodictyon anastomosans (Harvey) Kraft
& M.J. Wynne*
37. Phyllodictyon pulcherrimum J.E. Gray (in Leliaert
& Coppejans 2004)
Marine macroalgae of the Cabo Verde archipelago
53
Family Cladophoraceae 38. Chaetomorpha antennina (Bory) Kützing*
39. Chaetomorpha clavata Kützing* 40. Chaetomorpha nodosa Kützing* 41. Chaetomorpha pachynema (Montagne) Kützing* 42. Cladophora laetevirens (Dillwyn) Kützing* 43. Cladophora lehmanniana (Lindenberg)
Kützing* 44. Cladophora prolifera (Roth) Kützing* 45. Cladophora ruchingeri (C. Agardh) Kützing* 46. Cladophora vagabunda (Linnaeus) van den
Hoek* 47. Lychaete pellucida (Hudson) M.J. Wynne (as
Cladophora pellucida (Hudson) Kutzing)* 48. Rhizoclonium riparium (Roth) Harvey (as
Rhizoclonium tortuosum (Dillwyn) Kutzing)* 49. Rhizoclonium tortuosum (Dillwyn) Kützing*
Family Siphonocladaceae
50. Dictyosphaeria cavernosa (Forsskål) Børgesen* 51. Dictyosphaeria ocellata (M. Howe) Olsen-
Stojkovich (in John et al. 2004) 52. Ernodesmis verticillata (Kützing) Børgesen*
Family Valoniaceae
53. Valonia utricularis (Roth) C. Agardh*
54. Valonia ventricosa J. Agardh (in Sangil et al.
2018)
Order Dasycladales
Family Dasycladaceae
55. Neomeris annulata Dickie*
56. Neomeris mucosa M. Howe*
Family Polyphysaceae
57. Parvocaulis polyphysoides (P. Crouan & H.
Crouan) S. Berger, U. Fettweiss, S.
Gleissberg, L.B. Liddle, U. Richter, H.
Sawitzky & G.C. Zuccarello (as Acetabularia
polyphysoides P. Crouan & H. Crouan)*
Order Ulvales
Family Ulvaceae
58. Kallonema caespitosum Dickie*
Note: Endemic.
59. Ulva clathrata (Roth) C. Agardh (as
Enteromorpha clathrata (Roth) Greville)*
60. Ulva compressa Linnaeus (as Enteromorpha
compressa (Linnaeus) Nees)* 61. Ulva fasciata Delile* 62. Ulva flexuosa Wulfen (as Enteromorpha
flexuosa (Wulfen ex Roth) J. Agardh)* 63. Ulva intestinalis Linnaeus (as Enteromorpha
intestinalis (Linnaeus) Nees)* 64. Ulva lactuca Linnaeus* 65. Ulva rigida C. Agardh*
Family Ulvellaceae
66. Ulvella viridis (Reinke) R. Nielsen, C.J.
O'Kelly & B. Wysor (as Acrochaete viridis
(Reinke) R. Nielsen)*
ACKNOWLEDGMENTS
The present work was generated in the context of
the Project PADDLE - Planning in the liquid
world with tropical stakes, funded by the
European Union’s Horizon 2020 Research and
Innovation Programme under Grant 734271. DG
was supported with the FCT postdoctoral grant
SFRH/BPD/64963/2009. CIBIO-Açores is
maintained with Portuguese
(UID/BIA/50027/2013) and Azorean (POCI-01-
0145-FEDER-006821) funding. We also thank
Dr. García-Soto for her valuable suggestions to
improve this manuscript.
Gabriel and Fredericq
54
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Published online 20 Sep 2019.
Gabriel and Fredericq
56
APPENDIX
Taxonomic index – Families and genera
Acinetospora ..................................................... 41
Acinetosporaceae .............................................. 41
Acrosorium ....................................................... 46
Acrosymphytaceae ........................................... 45
Acrosymphyton ................................................. 45
Aglaothamnion ................................................. 45
Ahnfeltia ........................................................... 43
Ahnfeltiaceae .................................................... 43
Ahnfeltiopsis ..................................................... 49
Alsidium ............................................................ 46
Amphiroa ......................................................... 43
Anadyomenaceae .............................................. 52
Anadyomene ..................................................... 52
Anatheca ........................................................... 48
Anotrichium ...................................................... 48
Antithamnion .................................................... 46
Antithamnionella .............................................. 46
Apoglossum ...................................................... 46
Areschougiaceae ............................................... 48
Asparagopsis .................................................... 45
Asteronema ....................................................... 42
Asteronemataceae ............................................. 42
Austrokallymenia .............................................. 49
Bachelotia ......................................................... 42
Bachelotiaceae ..................................................42
Bangiaceae ........................................................43
Bonnemaisoniaceae ...........................................45
Boodlea .............................................................52
Boodleaceae ......................................................52
Boodleopsis .......................................................52
Botryocladia ......................................................50
Bryocladia ................................................... 46, 47
Bryopsidaceae ...................................................51
Bryopsis ...................................................... 51, 52
Callithamniaceae ...............................................45
Callithamnion ...................................................45
Canistrocarpus ..................................................40
Capensia ...........................................................44
Carradoriella ....................................................47
Caulacanthaceae ................................................48
Caulacanthus ....................................................48
Caulerpa ...........................................................52
Caulerpaceae .....................................................52
Centroceras .......................................................46
Ceramiaceae ......................................................46
Ceramium ..........................................................46
Ceratodictyon ....................................................50
Chaetomorpha...................................................53
Marine macroalgae of the Cabo Verde archipelago
57
Champia ........................................................... 50
Champiaceae .................................................... 50
Chnoospora ...................................................... 41
Chondracanthus ............................................... 49
Chondria ........................................................... 47
Chondrophycus ................................................. 47
Chondrus .......................................................... 49
Chordariaceae ................................................... 41
Chroodactylon .................................................. 51
Cladophora ....................................................... 53
Cladophoraceae ................................................ 53
Cladophoropsis ................................................ 52
Codiaceae ......................................................... 52
Codium ............................................................. 52
Coelothrix ......................................................... 49
Colaconema ................................................ 44, 45
Colaconemataceae ............................................ 44
Colpomenia ...................................................... 41
Compsothamnion .............................................. 46
Corallina .......................................................... 43
Corallinaceae .................................................... 43
Cottoniella ........................................................ 48
Crouania ........................................................... 46
Cryptonemia ..................................................... 49
Cystocloniaceae ................................................ 48
Cystoseira ................................................... 41, 42
Dasya ................................................................46
Dasyaceae .........................................................46
Dasycladaceae ...................................................53
Delesseriaceae ...................................................46
Derbesia ............................................................52
Derbesiaceae .....................................................52
Dichotomaria ....................................................45
Dictyopteris ................................................ 40, 41
Dictyosphaeria ..................................................53
Dictyota ............................................................41
Dictyotaceae ......................................................40
Digenea .............................................................47
Dudresnaya .......................................................49
Dumontiaceae ...................................................49
Ecklonia ...........................................................42
Ectocarpaceae ...................................................41
Ectocarpus ........................................................41
Ellisolandia .......................................................43
Ernodesmis ........................................................53
Erythrocladia ....................................................51
Erythrotrichiaceae .............................................51
Faucheaceae ......................................................50
Feldmannia .......................................................41
Flabellia ............................................................52
Floiophycus .......................................................43
Gaillona ............................................................46
Gabriel and Fredericq
58
Galaxaura ......................................................... 45
Galaxauraceae .................................................. 45
Ganonema ........................................................ 45
Gayliella ........................................................... 46
Gelidiaceae ....................................................... 48
Gelidiella .......................................................... 48
Gelidiellaceae ................................................... 48
Gelidium ........................................................... 48
Gigartinaceae .................................................... 49
Goniolithon ....................................................... 43
Gracilaria ......................................................... 49
Gracilariaceae ................................................... 49
Grateloupia ...................................................... 49
Gulsonia ........................................................... 46
Gymnogongrus ................................................. 49
Halimeda .......................................................... 52
Halimedaceae ................................................... 52
Halopteris ........................................................ 42
Halurus ............................................................. 48
Halydictyon ...................................................... 46
Halymenia ........................................................ 49
Halymeniaceae ................................................. 49
Hapalidiaceae ................................................... 44
Haraldia ........................................................... 46
Harveylithon ..................................................... 42
Helminthocladia ............................................... 45
Herposiphonia .................................................. 47
Heterosiphonia ..................................................46
Hydroclathrus ...................................................41
Hydrolithon .......................................................41
Hydropuntia ......................................................49
Hypnea ........................................................ 48, 49
Hypneocolax .....................................................49
Hypoglossum .....................................................46
Janczewskia ......................................................47
Jania..................................................................42
Kallonema .........................................................53
Kallymenia ........................................................49
Kallymeniaceae .................................................49
Laurencia ..........................................................47
Leptofauchea .....................................................50
Leptophytum ..................................................... 44
Leptosiphonia ....................................................47
Lessoniaceae .....................................................42
Levringia ...........................................................41
Liagora..............................................................45
Liagoraceae .......................................................45
Liagoropsidaceae ..............................................45
Liagoropsis .......................................................45
Lithophyllum ............................................... 43, 44
Lithoporella ......................................................44
Lithothamnion ...................................................44
Lobophora .........................................................41
Lomentariaceae .................................................50
Marine macroalgae of the Cabo Verde archipelago
59
Lophocladia ...................................................... 47
Lychaete ........................................................... 53
Melanothamnus ................................................ 47
Melobesia ......................................................... 44
Melyvonnea ...................................................... 44
Meredithia ........................................................ 49
Meristotheca ..................................................... 49
Mesophyllum .................................................... 44
Microdictyon .................................................... 52
Millerella .......................................................... 48
Nemastomataceae ............................................. 50
Neogoniolithon ................................................. 44
Neomeris ........................................................... 53
Neoralfsia ......................................................... 42
Neoralfsiaceae .................................................. 42
Osmundea ......................................................... 47
Ostreobiaceae ................................................... 52
Ostreobium ....................................................... 52
Padina .............................................................. 41
Palisada ............................................................ 47
Parvocaulis ....................................................... 53
Peyssonnelia ..................................................... 50
Peyssonneliaceae .............................................. 50
Phrix ................................................................. 46
Phyllodictyon .................................................... 52
Phyllophoraceae ............................................... 49
Phymatolithon ...................................................44
Platoma .............................................................50
Platysiphonia ....................................................48
Plocamiaceae.....................................................50
Plocamium ........................................................50
Pneophyllum .....................................................43
Polyphysaceae ...................................................53
Polysiphonia .....................................................47
Polystrata ..........................................................50
Porphyra ..........................................................43
Predaea .............................................................50
Pseudochlorodesmis .........................................52
Pseudolithophyllum ...........................................44
Pterocladiaceae .................................................48
Pterocladiella ....................................................48
Ralfsia ...............................................................42
Ralfsiaceae ........................................................42
Rhizoclonium.....................................................53
Rhodomelaceae .................................................50
Rhodymenia ......................................................50
Rhodymeniaceae ...............................................50
Rosenvingea ......................................................41
Rugulopteryx .....................................................41
Sarcomeniaceae .................................................48
Sargassaceae .....................................................41
Sargassum ........................................................42
Gabriel and Fredericq
60
Schimmelmannia .............................................. 45
Schimmelmanniaceae ....................................... 45
Schizymeniaceae .............................................. 50
Scinaia .............................................................. 45
Scinaiaceae ....................................................... 45
Scytosiphonaceae ............................................. 41
Sebdenia ..................................................... 50, 51
Sebdeniaceae ................................................... 50
Siphonocladaceae ............................................. 53
Solieria ............................................................. 49
Solieriaceae ...................................................... 49
Sphacelaria ....................................................... 42
Sphacelariaceae ................................................ 42
Spongites .......................................................... 44
Spongonema ..................................................... 41
Sporolithaceae .................................................. 44
Sporolithon ....................................................... 44
Spyridia ............................................................ 48
Spyridiaceae ..................................................... 48
Stenogramma .................................................... 49
Stragularia........................................................ 41
Stylonema ......................................................... 51
Stylonemataceae .............................................. 51
Stypocaulaceae ................................................. 42
Stypopodium ......................................................41
Taenioma ..........................................................46
Tiffaniella ..........................................................48
Titanoderma ......................................................44
Titanophycus .....................................................45
Trichogloea .......................................................45
Tricleocarpa ......................................................45
Udotea ...............................................................52
Udoteaceae ........................................................52
Ulva ..................................................................53
Ulvaceae ............................................................53
Ulvella ...............................................................53
Ulvellaceae ........................................................53
Valonia .............................................................53
Valoniaceae .......................................................53
Vertebrata .........................................................47
Vickersia ...........................................................48
Wrangelia ..........................................................48
Wrangeliaceae ...................................................48
Wurdemannia ....................................................49
Yuzurua .............................................................48
Zonaria ....................................................41
Arquipelago - Life and Marine Sciences ISSN: 0873-4704
61
Hawksbill (Eretmochelys imbricata) and Green Turtle
(Chelonia mydas) Nesting and Beach Selection at Príncipe
Island, West Africa
ROGÉRIO L. FERREIRA, HELEN R. MARTINS AND ALAN B. BOLTEN
Ferreira, R.L., H.R. Martins and A.B. Bolten 2019. Hawksbill (Eretmochelys
imbricata) and Green Turtle (Chelonia mydas) Nesting and Beach Selection at
Príncipe Island, West Africa. Arquipelago. Life and Marine Sciences 36: 61-77.
Hawksbills (Eretmochelys imbricata) and green turtles (Chelonia mydas) are the
predominant nesting sea turtle species on the beaches of Príncipe Island in the Gulf of Guinea.
The extent of nesting has been largely unknown, but such information is essential for
management and conservation. Our study is the first island-wide nesting assessment. Results
from the survey, conducted from 1 December 2009 to 18 January 2010 (during peak nesting
season), show that the potential suitable nesting area (10 km) is scattered around the island’s
50 beaches. Sea turtles nested on 32 of the beaches (hawksbills, 20; green turtles, 28) and
used 7.5 km of the suitable nesting habitat (hawksbills, 5.8 km; green turtles, 7.0 km). We
estimated that 101 (95% CI = 86–118) clutches were deposited by 17-29 hawksbills and 1088
(95% CI = 999–1245) clutches were deposited by 166-429 green turtles on Príncipe from
November 2009 to February 2010 (nesting season). Long-term green turtle nest count data
collected from 2007/08 to 2015/16 suggest a positive trend. Analyses of clutch densities in
relation to beach characteristics suggested that both species preferred areas where human
presence is lower, which coincided with the most sheltered areas. These findings should be
used to inform coastal planning and minimize impacts on nesting beaches, as Príncipe is
currently targeted for tourism development. Overall, results highlight that Príncipe beaches
are very important for the conservation of West African hawksbill and green turtle
populations.
Key words: assessment, Gulf of Guinea, population, reproduction, sea turtle
Rogério L. Ferreira1 (email:[email protected]), H.R. Martins2 and A.B. Bolten3, 1Centre of Marine Sciences, University of Algarve, Campus de Gambelas, 8005-139 Faro,
Portugal. 2Department of Oceanography and Fisheries, University of the Azores, 9901-862
Horta, Portugal. 3Archie Carr Center for Sea Turtle Research, University of Florida, PO
Box 118525, Gainesville, Florida 32611, USA.
INTRODUCTION
Príncipe, the smaller island of the São Tomé and
Príncipe Republic, located in the Gulf of Guinea,
has recently been designated as a UNESCO
Biosphere Reserve (2012). The Gulf of Guinea
harbours major nesting aggregations of hawksbill
(Eretmochelys imbricata) and leatherback
(Dermochelys coriacea) turtles as well as
regionally important populations of green turtles
(Chelonia mydas) and olive ridleys (Lepidochelys
olivacea) (Fretey 2001; Formia et al. 2006;
Mortimer and Donnelly 2008; Tomás et al. 2010;
Metcalfe et al. 2015). However, leatherbacks and
olive ridleys rarely nest on Príncipe; here the
beaches are mainly used by the critically
endangered hawksbill and by the endangered green
turtle (Fretey 2001; http://www.iucnredlist.org/).
Ferreira et al.
62
Both adult hawksbills and green turtles migrate
from foraging to nesting grounds, sometimes
thousands of kilometers, to lay several clutches of
more than 100 eggs in or near the area where they
hatched (philopatry), making most nesting
colonies different in regard to population genetic
structure (Miller 1997; Bowen & Karl 2007; Hays
& Scott 2013). Recent stable isotope analyses
suggested that most of Príncipe’s breeding female
hawksbills forage close to the nesting grounds, on
the insular platform (Ferreira et al. 2018), while
green turtle foraging grounds may cover a much
larger area, chiefly in the Gulf of Guinea (RLF,
unpubl. data). The longer migration of the green
turtles requires accumulation of large energy
reserves, meaning that this reproductive migration
is dependent on environmental conditions at
foraging grounds. The herbivorous green turtle is
typically affected more by this variation than the
carnivorous marine turtle species, and,
consequently, nesting numbers vary substantially
from year to year (Broderick et al. 2001; Solow et
al. 2002).
Quantifying nest numbers allows an estimation
of population size and trends, which are crucial
information for science, conservation, and
management (Gerrodette & Taylor 1999; Girondot
2010). These data can be readily obtained from
nesting surveys, representing a standardized and
repeatable record of nesting activity to assess and
monitor population status (Gerrodette & Taylor
1999; Schroeder & Murphy 1999; National
Research Council 2010). Nesting surveys are
based on the fact that each time a female turtle
emerges from the water to deposit a clutch, she
leaves a set of tracks in the sand (e.g. body pit) that
can be used to infer the number of nests (i.e.,
clutches) on the beach (Schroeder & Murphy
1999; National Research Council 2010). When
nesting occurs on a large number of small and
dispersed beaches, reliable nest estimates can be
attained with two to three weeks of monitoring
during peak nesting of a fraction of the available
beaches (Eckert 1999; Jackson et al. 2008;
Girondot 2010; Delcroix et al. 2013). Although
several sea turtle projects have been carried out in
São Tomé and Príncipe during the past 20 years,
they have focused on a small fraction of the
islands’ beaches, and information on the extent of
nesting and available habitat is incomplete.
Nesting surveys, in addition to being useful in
studying reproduction and nest biology (Miller
1997), can provide information about beach
selection. The locations where females emerge to
nest have consequences for their survival and that
of their offspring (Mortimer 1982; Bjorndal &
Bolten 1992). The small island of Príncipe, where
a large number of different types of beaches
occurs, is an ideal place to conduct an analysis of
beach selection.
Although no accurate information on population
sizes and status exists for the São Tomé and
Príncipe rookeries, hawksbill nesting in the
country is considered to be the most important in
the Eastern Atlantic and is the top priority for the
conservation of the species in the region (Fretey
2001: Mortimer & Donnelly 2008). The eastern
Atlantic hawksbill population was ranked as one of
the 11 most endangered sea turtle Regional
Management Units in the world (Wallace et al.
2011), highlighting the importance of nesting
surveys in São Tomé and Príncipe. Green turtle
nesting, however, has historically been lower than
other regions of the East Atlantic (e.g., Bioko,
Poilão and Ascension islands), but breeding
females exhibit a relatively higher mitochondrial
diversity in São Tomé and Príncipe (Formia et al.
2006).
In the present study, we identify and describe
sea turtle nesting along the entire coast of the
island of Príncipe to aid sea turtle conservation and
the sustainable development of the island’s littoral
habitat. We estimated the numbers of clutches
based on one-time body-pit counts per beach and
regular monitoring of a fraction of those beaches
during peak nesting season, complemented with
clutch data from the intensively monitored
Paciência beach. Our method was simple and
provided information on the nesting abundance
and distribution throughout Príncipe Island, as
well as an estimation of the breeding female
numbers. We also investigated possible patterns of
beach selection by nesting females by comparing
clutch densities with recorded beach
characteristics.
Sea turtle nesting and beach selection at Príncipe Island
63
MATERIAL AND METHODS
Study Site
The island of Príncipe (140 km2; 1º37’N; 7º23’E)
is located 220 km west of the African continent,
145 km northeast of São Tomé and 205 km
southwest of Bioko (Fig. 1). The warm and humid
equatorial climate supports dense vegetation.
Although it rains year-round, there are two drier
seasons: one from June to September (Gravana)
and another from mid-December to early-February
(Gravanita). The second drier season is
characterized by higher temperatures and lower
precipitation levels and largely overlaps with the
reported sea turtle nesting season, from November
to January (Graff 1996). Permanent fishing
communities, and most of Príncipe’s 7500 human
inhabitants (National Institute of Statistics 2013),
are located in the sheltered and less mountainous
northern half of this deeply eroded and ancient
volcanic island (ca. 30 Ma; Dunlop & Fitter 1979).
Currently, only two small, isolated fishing
communities exist in the south, which are mostly
accessed during fishing campaigns.
Fig. 1. Location of islands in the Gulf of Guinea relative to the African coast.
Data Collection
Beach surveys were undertaken during the peak of
the 2009-2010 nesting season, from 1 December
2009 to 18 January 2010. The entire shoreline of
Príncipe (ca. 100 km) was surveyed primarily on
foot, although boats and/or motorcycles were used
occasionally. Nesting activity was quantified by
one-time body-pit counts on each beach. More
frequent, systematic crawlcounts on all the
beaches were not feasible due to the island
geography and financial constraints (e.g., boat
rental). Species were distinguished based on their
Ferreira et al.
64
track morphology and nest location (Pritchard &
Mortimer 1999). In addition to the one-time survey
of the entire island, nine body-pit count surveys,
distributed over the 49 days, were conducted on
two nesting beaches in Infante Bay (Fig. 2, beaches
14 and 15) to develop accumulation curves of body
pits for each species throughout the season.
Finally, sporadic night patrols were conducted on
the two Infante Bay beaches and on three other
beaches (Rio São Tomé, Rio Porco, and Praia
Seca) to estimate the ratio of body pits to clutches
for each species. This ratio is essential to convert
body-pit counts to clutch counts because a female
may dig a body pit without depositing a clutch of
eggs.
Fig. 2. The island of Príncipe with estimated clutch abundance proportions for the beaches in the 2009/2010 nesting
season. Filled circles represent number of clutches, from 2 to 315, black for hawksbills and grey for green turtles.
X’s indicate beaches without observed turtle activities and arrows indicate prevailing winds and currents. Human
population is concentrated north of latitude 1o 37’ N. City of Santo António, airport and beach numbers (see
Appendix for names) are also illustrated.
Longitudinal beach lengths at the high tide line
were recorded with a global positioning system
(GPS) unit. The length of suitable nesting habitat
(i.e., no obstacles and enough sand to allow
digging of a nest cavity) was determined in
addition to total beach length. Also, information
was collected on beach characteristics that might
affect nesting (see Beach Selection Analysis
section, below).
Sea turtle nesting and beach selection at Príncipe Island
65
Abundance Analysis
To convert our body-pit counts on a single day (n)
for each beach to estimates of the total number of
clutches for each species deposited on each beach
in the 2009/2010 study period, we need three
conversion factors. First, we need the proportion of
total body pits for the year created for each survey
day (n) or daily cumulative value dc(n). These
proportions were generated by regressing
cumulative body-pit proportions from the nine
body-pit surveys on the two Infante beaches
against date and using this regression to generate
the proportion of body-pits created by each date.
The cumulative proportions from the Infante
beaches for both hawksbills and green turtles were
assumed to be representative for all beaches.
Second, we need to estimate the proportion of
body pits that have been obscured before the
survey day by spring tides, wave splashes, and
heavy rainfalls, which affect the persistence of
body-pits on the beach (Schroeder & Murphy
1999). We used a correction factor (cf) based on
the survey day (n from 1 to 49). At every spring
tide, we assumed that half of the body-pits were
wiped out by the sea or rain (RLF, pers. obs.): cf(n)
= 1, if n ≤ 16; 1.5, if 16 < n ≤ 30; 2, if 30 < n ≤ 45;
and 2.5, if n > 45.
Third, we need the ratio of clutches to body-pits to
convert the total number of body pits per beach to the
number of clutches per beach. We calculated this ratio
based on sporadic night patrols conducted on the two
Infante Bay beaches and on three other beaches (Rio
São Tomé, Rio Porco, and Praia Seca) and on observed
number of clutches laid on the intensively monitored
Paciência beach (reported by the local monitoring
program) and the expected number of body-pits for
Paciência beach during the study period. The clutch to
body-pit ratio was assumed to be similar among
beaches, except for Rio São Tomé beach where
discrepancies for green turtles were observed and
corrected.
As a result, the expected number of body-pits (epx)
for each beach (x) for the study period was obtained as
follows:
epx = [opx(n) + (opx(n) x cf(n))] / dc(n) Eqn. 1
where opx(n) = the observed number of body-pits
for beach x on day n, cf(n) = the correction factor
for proportion of nests obscured by day n, and dc(n)
= the proportion of body pits created by day n.
The number of clutches were estimated for each
beach (ncx) with the following formula:
ncx = epx × cbp Eqn. 2
where epx = expected number of body-pits for a beach
and cbp is the clutch to body pit ratio for the entire
nesting season (1 September 2009 to 28 February
2010) from Paciência beach (observed clutch number
/ expected body pit number). We incorporated
uncertainty by imposing an error level to each
estimated model input, resulting in a range of values
with 95% level of confidence (i.e., 95% CI). While the
regression coefficient (1- R2) was used for dc(n), which
differs between species, a 5% error was assigned to
cf(n) and to the quotient between observed clutches
and estimated body pits on Paciência beach.
An indirect method to estimate the annual number
of nesting females can be derived from dividing the
total number of clutches by the clutch frequency,
defined as the average number of nests laid per female
during a season (Alvarado & Murphy 1999). Since
estimates of Príncipe sea turtles were not available, the
values used were obtained from the literature: 4–5
nests per season for hawksbills nesting at Seychelles
(Indian Ocean) and Antigua (Caribbean) islands
(Mortimer & Bresson 1999; Richardson et al. 1999);
and 2.9–3.1 for green turtles nesting at Alagadi
(Mediterranean) and Bioko (Gulf of Guinea) islands
(Broderick et al. 2002; Tomás et al. 2010). However,
for green turtles, a value of six was used as the
maximum because recent tracking studies had shown
that clutch frequency might be underestimated in some
populations (Weber et al. 2013; Esteban et al. 2017).
Beach Selection Analysis
Because clutch abundances are expected to be
positively correlated with beach size (Mortimer
1982), densities (clutches/km of suitable sections
of beach) were used to explore the nesting
distribution in relation to the recorded beach
characteristics. Beaches with a large amount of
obstacles that impeded nesting (e.g., organic and
artificial debris, armoring) were not included in the
analyses. The observations were grouped in four
categories (Table 1) from each of the seven
recorded qualitative and quantitative
Ferreira et al.
66
Table 1. Recorded qualitative and quantitative beach characteristics, that might affect sea turtle nesting on Príncipe,
and the criteria and conditions used for their classification into four categories (1–4).
Characteristic Description Obtained 1 2 3 4 Condition
Total length longitudinal size (m) of the
beach
in situ
with a
GPS
≤100 >100;
≤300
>300;
≤600 >600 -
Suitable
length
longitudinal distances (m)
with minimal nesting
conditions
in situ
with a
GPS
≤75 >75;
≤225
>225;
≤450 >450 -
Sand color subjective rating, from
lighter to darker in situ yellow
light
brown brown
dark
brown -
Grain size
subjective rating, partially
based on the Wentworth
(1922) scale
in situ very fine fine medium coarse -
Slope
distance (m) from the
middle of the beach to the
10 m isobath
nautical
chart >900
>600;
≤900
>300;
≤600 ≤300 -
Exposure
beachfront orientation
relative to the prevailing
wind and current
nautical
chart and
in situ
- NE NW and
SE SW
minus 1 if
protected by
the shoreline
Threat
minimal distance (m) from
the beach to the nearest
settlement
nautical
chart and
in situ
>1000 >500;
≤1000 ≤ 500 -
plus 1 if
located north
of 1º37’N
characteristics of the beach (i.e., total and suitable
lengths, sand color and size, slope, exposure and
threat), allowing the use of continuous statistical
methods (Bentler & Chou 1987; Mason 1994).
Chi-square tests were used to evaluate whether the
numbers of beaches in each category for each
characteristic were similar and whether the
distributions of clutch abundance and density
among beaches, for both species, were different
from those expected by chance. Because all data
were not normally distributed, non-parametric
Spearmen R correlations were used to explore the
relationships between all pairs of variables.
Multiple regression was also employed to suggest
which beach characteristics might have a major
effect on clutch densities. Statistical significance
was assessed using Statistica software (StatSoft,
Inc.) with an alpha of 0.05.
RESULTS Eighty beaches were identified along the 100 km
coastline of Príncipe Island. Fifty beaches had a
total of 10 km shoreline with suitable
morphological conditions to support nesting (mean
± SD (range) = 200 ± 223.1 m (9–1255 m), n = 50),
and 17.8 km of total beach length (356 ± 295.6 m
(62–1500 m), n = 50) (Appendix). In general,
beaches were predominantly backed by coconut
plantations, although lowland rain forest and
scarps also occur. The nesting area under the over-
story vegetation was characterized by the presence
of more compact sand with higher organic matter
and a small degree of low-lying vegetation.
Beaches appeared to be homogeneous in widths
and in the proportion of sunny to shaded areas. All
had several permanent streams or rivers but
erosion by heavy rains or river flooding is not
common. Approachability from the sea was also
similar among beaches, except on Ponta Pedra
Furada and Ponta Marmita, where green turtles
could not emerge due to a rocky foreshore.
Abundances
Sea turtle nesting was observed on 32 of the 50
Sea turtle nesting and beach selection at Príncipe Island
67
suitable nesting beaches, 20 for hawksbills and 28
for green turtles (Fig. 2, Appendix). The best fit to
the cumulative body-pit frequencies, observed in
the two Infante beaches, was a nearly linear second
degree equation, for both hawksbills (total number
of body pits = 16; R2 = 0.94; cumulative body pits
= 0.004n2 + 0.014n + 5.157) and green turtles (total
number of body pits = 389; R2 = 0.99; cumulative
body pits = 0.075n2 + 3.651n + 29.694). Clutch
abundances for each beach (nests/beach) for the
entire nesting season, estimated using equations 1
and 2, and using 6 hawksbill and 315 green turtle
clutches reported for Paciência beach during the
entire nesting season in 2009/2010 (H. Carvalho,
pers. comm.; Loureiro et al. 2011), ranged from 2
to 12 hawksbill turtle clutches (mean = 5 ± 3.2
(SD), n = 20) and from 2 to 315 green turtle
clutches (38.8 ± 77.5, n = 28) (Fig. 2, Appendix).
Although clutch to body-pit ratios appeared similar
Fig. 3. Total number of green turtle clutches laid at Paciência beach, Príncipe Island, from 2007/08 to 2015/16
nesting seasons.
among beaches, in Rio São Tomé beach a large
amount of cut coconut palm logs blocked suitable
green turtle nesting area, increasing the ratio by
30% (7:2), in comparison to the ratio (32:13)
observed on the other beaches during night patrols.
This resulted in an estimate of 101 hawksbill (95%
CI = 86–118) and 1088 green turtle (95% CI =
999–1245) clutches laid during the 2009/2010
nesting season. Applying the range of clutch
frequencies from the literature to the total clutch
counts, approximately 17–29 (95% CI) female
hawksbills and 166–429 (95% CI) female green
turtles used the island during the 2009/10 nesting
season.
Long-term clutch data were available for green
turtles for 9 consecutive seasons from Paciência
beach: 2007/08, 219 clutches (Z. Rodriguez, pers.
comm.); 2008/09, 41 (E. Neto, pers. comm.);
2009/10, 315 (Loureiro et al. 2011); 2010/2011,
134; 2011/12, 102; 2012/13, 73; 2013/14, 541;
2014/15, 223; 2015/2016, 683 (H. Carvalho, pers.
comm.). These data (9 seasons) suggest a positive
trend of the nesting population (Fig. 3).
Although estimated clutch numbers were
significantly different among beaches for both
species (all P’s < 0.001, df = 49), hawksbill
abundances were not as clumped as observed for
green turtles (Fig. 2). However, two northwest
situated beaches, Ponta Marmita and Ponta Pedra
Furada, accounted for almost a quarter (23.5%) of
the hawksbill nests. These two beaches possessed
sharp rocks on the foreshore, and no green turtle
body-pits or tracks were observed there. Two
green turtle nesting beaches accounted for more
0
100
200
300
400
500
600
700
2007/08 2008/09 2009/10 2010/11 2011/12 2012/13 2013/14 2014/15 2015/16
n c
lutc
hes
Chelonia mydas - Paciência beach
Ferreira et al.
68
than half (55.4%) of clutches: Paciência in the
northeast (315 clutches, observed) and the larger of
the Infante beaches in the southeast (288 clutches,
95% CI = 257–321). If the two beaches located in
Infante Bay are combined, as represented on maps,
then 324 (95% CI = 290–361) green turtle clutches
were laid there. Although the great majority of the
potential nesting beaches (72.5%) and suitable
nesting habitat (78.5%) are located in the North (>
latitude 1o37’N), more than half of the total number
of clutches were laid in the South (58.6%)
(hawksbills, 43.7%; green turtles, 59.9%). Also,
79% of the green turtle clutches were laid on only 6
beaches, 5 of them located to the south of the island. Beach Selection
Clutch densities (nests/km) by beach, for both
species, also differed significantly among beaches
(all P’s < 0.001, df = 49) and were not normally
distributed. Estimated hawksbill nest densities
ranged from 4.8 to 150.7 (mean ± SD 38.8 ± 47.3, n
= 20), within 5.8 km of suitable habitat. For green
turtles, they ranged from 6.8 to 564.9 (mean ± SD
151.2 ± 164.2, n = 28), on 7 km of suitable habitat
(see Appendix). The beach with the combined
highest density of sea turtle nesting was Infante
(582.2 clutches/km), which ranked second in
abundance. Paciência, the longest beach with the
highest abundance, ranked eighth in nest density
(255.8 clutches/km). The seven beaches with nest
density higher than that of Paciência were all
located in the south, accounting for almost
half (49.4%) of the total number of clutches laid in
Príncipe.
Recorded beach characteristics (i.e., total length,
suitable length, sand color, grain size, slope,
exposure and threat) were not normally distributed
and, except for suitable length (P < 0.104, df = 3)
and almost for sand color (P < 0.016, df = 3),
differed significantly among beaches (all P’s <
0.002, df = 3). Two beaches, Candeia and Bom-
bom, had large amounts of obstacles on the beach
(e.g., organic and artificial debris, armoring), which
impeded sea turtle nesting, and these were removed
from the analysis for both species. In one of them
(Candeia), we observed a hawksbill track with no
body pit below high tide line, but no body-pits or
tracks were found (confirmed by other visits later in
the season). For green turtles only, two beaches with
sharp rocks on the foreshore that prevented this
species from nesting were removed from the
analyses (Ponta Pedra Furada and Ponta Marmita).
While hawksbill and green turtle densities were
correlated with one another (rs = 0.60, P < 0.001, n
= 46), also with excluded beaches (rs = 0.47, P <
0.001, n = 50), both were significantly correlated
with exposure and threat (Table 2). In addition,
exposure was correlated with threat, suitable length
with total length, and slope with grain size and
exposure (Table 2).
From the multiple regressions, although the
overall relationship of beach characteristics with
hawksbill clutch densities was significant, the fit
was poor and only the effects of exposure and total
length were significant. For green clutch densities,
the fit was a little better, the relationship was
significant, and the effect of threat was the only
significant parameter (Table 3).
Table 2. Spearman R correlations (rs) between densities (clutches/km) and beach characteristics (1–4) recorded at
Príncipe, for both species. Only significant results are presented (all P’s < 0.01).
Variable n Total length Grain size Exposure Threat
Density
Hawksbill 48 0.45 -0.43
Green turtle 46 0.44 -0.62
Beach characteristic
Suitable length 0.76
Slope 50 0.41 0.39
Exposure -0.52
Sea turtle nesting and beach selection at Príncipe Island
69
Table 3. Multiple regression output between clutch densities (clutches/km) and beach characteristics (1–4), for
hawksbill and green turtle nesting at Príncipe. Predictors with significant effects are also presented.
n Statistic R2adj P SE
Predictor
Hawksbill 48 F7.40 = 3.77 0.31 0.003 30.1
Exposure: t40 = 2.51; P = 0.016
Total length: t40 = -2.28; P = 0.028
Green turtle 46 F7.38 = 6.41 0.46 <0.001 104.6
Threat: t38 = -4.81, P < 0.001
DISCUSSION
Sea turtle nesting is scattered around Príncipe
Island, with reduced frequency on the more
exposed and rockier west coast and in sites with
high human population densities. On two beaches
with the highest abundance of hawksbill clutches,
Ponta Marmita and Ponta Pedra Furada in the
northwest (25% of total), green turtles did not
emerge due to a dangerous rocky foreshore. Two
beaches, Paciência in the northeast and Infante in
the southeast, hosted 55% of the green turtle
clutches. These observations overlapped with
earlier observations of Castroviejo et al. (1994)
and Juste (1994), who listed Infante and Paciência
beaches, among others, as the most important for
sea turtle nesting in Príncipe. Our results expand
upon the conclusions of more recent studies.
Monzón-Argüello et al. (2011) indicated that the
main hawksbill nesting beaches are located on the
northern, eastern, and southern coasts of the island,
while Loureiro et al. (2011), who only
monitored northern beaches, reported Paciência as
the most visited beach by nesting green turtles.
Abundances
Although there is uncertainty in our model, the
estimated annual number of hawksbill clutches for
Príncipe Island (86–118 clutches) was much
higher than that of any other West African location
where nesting has been reported (Mortimer &
Donnelly 2008). For example, at the neighbouring
Bioko Island, only 22 hawksbill clutches were
reported during two nesting seasons, 1996 and
1998 (Tomás et al. 2010). Although there are no
estimates for the entire island of São Tomé, almost
130 hawksbill nests were recorded on the
monitored beaches during the recent 2016/17
nesting season (S. Vieira, pers. comm.). Thus, it is
likely that hawksbill nesting in Príncipe ranks
among the highest in the region. Estimated clutch
abundance translates to 17–29 hawksbills nesting
at Príncipe in the 2009/10 nesting season. This
estimate may be biased low, as hawksbills leave
little or no body-pits in the littoral forest (Pritchard
& Mortimer 1999), and our estimated annual
abundance is 50% of that previously assumed (<50
females/year; N. Loureiro, pers. comm. in
Monzón-Argüello et al. 2011). Nonetheless, our
annual nesting hawksbill estimate represents a
large proportion of the total annual numbers of
nesting females expected for the entire West
African region (100 females/year; Mortimer &
Donnelly 2008). An estimated 100–150 adult
hawksbills were captured annually in Príncipe in
the early 1990’s (Castroviejo et al. 1994; Juste
1994). Although these figures include captures at
sea and males, based on informal interviews with
older inhabitants, sea turtle capture was on a small-
scale prior to independence in 1975, in part
because of the availability of other sources of
meat. The danger of losing important hawksbill
genetic diversity is a reality, particularly because
the high value of hawksbill scutes for craftwork
makes them a highly valued target (Ferreira 2015),
and other anthropogenic activities threaten every
life stage of sea turtles (e.g., bycatch and coastal
development; Donlan et al. 2010). Based on an 11-
year study with hawksbills from Antigua Island,
Richardson et al. (1999) calculated that one adult
female hawksbill must breed for at least 4.1
nesting seasons to replace herself, and some of
them must be reproductively active for decades to
compensate for the early mortality of others.
Emerging from the sea several times during the
Ferreira et al.
70
season makes sea turtles very vulnerable to
exploitation, but once effective protection is
provided, the increase in nesting activity can be
dramatic (Mortimer & Bresson 1999), even at sites
with low abundance (Mazaris et al. 2017).
Although inter-annual variation in nesting
numbers is very high for green turtles (Broderick
et al. 2001), the green turtle clutch estimate for
Príncipe (999–1245 clutches, 2009/10 season) fall
within the range reported on the neighboring island
of Bioko (1255–1681 clutches, 1996/97-1997/98
seasons, Tomás et al. 2010; ca. 180 to 3900
clutches, 2000/01 to 2013/14 seasons, Honarvar et
al. 2016). However, the extent of the nesting
habitat used in Bioko (19.3 km; Tomás et al. 2010)
was much greater than in Príncipe (7.5 km). All
these clutch estimates are small relative to those
reported from Ascension and Poilão, islands
located outside of the Gulf of Guinea (Catry et al.
2009; Weber et al. 2014). Although the Ascension
population is still recovering (Weber et al. 2014),
Poilão might be reaching the limit of nesting
supported by the available habitat, where 7000–
29000 clutches are laid annually in only 2.3 km of
beaches (Catry et al. 2009). If protection of nesting
females and their eggs is achieved, as occurs on
Ascension and Poilão (Catry et al. 2009; Weber et
al. 2014), the islands in the Gulf of Guinea could
stand out significantly since more nesting habitat
will be available. Although the present estimate of
166–429 nesting green turtle females for Príncipe
in 2009/10 more than double previous population
estimates (75–100/year; Formia et al. 2006), it
continues to be low. Low nesting has also been
documented elsewhere in the Gulf of Guinea (e.g.,
63–649 nesting females/year at Bioko; Honarvar et
al. 2016), and our results reinforce the urgency to
study and conserve all life stages. Even so, it is
possible that the positive trend observed at
Príncipe is connected to the recent great decrease
in female capture following the approval of the
regional sea turtle protection law in Príncipe
(Regional Legislative Decree 2009). Positive
trends in sea turtle populations are likely to be
associated with the protection of nesting females
and their eggs (Mazaris et al. 2017). Since Príncipe
has a small human population (7500 inhabitants;
National Institute of Statistics 2013), full
protection could be achieved if resources are used
effectively, transforming the island into a safe
habitat for sea turtles to buffer against their
extirpation in the region.
Beach Selection
Although nesting habitats were scattered around
Príncipe Island, clutch densities were not
distributed evenly. Nesting densities and
abundances were generally higher in southern
beaches, within the Natural Park limits (see
Albuquerque & Cesarini 2009), suggesting that the
human population, which is highly concentrated in
the north, may impact distribution. While both
exposure and threat were correlated with hawksbill
and green turtle clutch densities, although in
opposite directions, they were also negatively
correlated with each other. Considering that
human settlements occupy the most sheltered
areas, the effect of both threat and exposure is
expected. However, for hawksbills, the multiple
regression did not show threat as most relevant, as
it did for green turtles, but rather exposure and the
inverse influence of total beach length. We believe
these results might be a consequence of the two
most important hawksbill beaches being very small,
exposed, and situated in small rocky peninsulas on the
north inhabited area, that are not easily accessed by
people. Therefore, the risk of poaching might be
smaller than expected. In addition, hawksbills are
smaller than green turtles and dig much more shallow
body pits, allowing hawksbills to emerge, lay their
eggs, and return to sea much faster, sometimes during
the day (Miller 1997; Ferreira & Martins 2013).
Exposure, besides being correlated with threat, was
also correlated with beach slope. In turn, slope was also
correlated with grain size, which is typically larger on
higher slope beaches and on beaches exposed to high-
energy waves (Komar 1976). Hawksbills may prefer
high-slope beaches, that provide females and
hatchlings with reduced travel distances, costs, and
predation risk (Horrocks & Scott 1991).
Although hatching success is influenced by sand
characteristics (Ackerman 1997; Miller 1997), sea
turtles nested in all types of sand on Príncipe. The same
was reported for Ascension Island, where biotic factors
like predation and competition may be more relevant
than the characteristics of the sand or other geologic
factors (e.g., offshore approach, obstacles; Mortimer
Sea turtle nesting and beach selection at Príncipe Island
71
1982). This supports the hypothesis that it might
be better for females to select a nest site based on
their survival rather than on the survival of their
eggs (Bjorndal & Bolten 1992). Although habitat
availability is a relevant factor, results from this
study suggest that green turtle nest densities are
higher on beaches with lower threat, that is, farther
away from human settlements. This may be driven
by differences in mortality between beaches or
also by turtles actively avoiding the riskier areas,
as sea turtles do in foraging habitats to avoid
predators (Heithaus 2013). Further evidence
indicates that green turtles nesting on the isolated
Infante beaches have larger body sizes than in
Paciência beach (RLF, unpubl. data), where threats
are higher. This could be related to smaller
females, likely younger and less experienced,
preferring Paciência beach due to better nesting
conditions (space and approachability). Weber et
al. (2014) also found an inverse relationship
between nesting intensity and distance to the main
human settlement for green turtle nesting at
Ascension, which may reflect an increase in
nesting due to effective protection and
conservation measures after severe exploitation.
This suggests that if harvests of females and eggs
decrease at Príncipe, and other threats on the beach
(e.g., construction and denaturalization) do not
increase, nesting on the northern beaches has the
potential to surpass that on southern beaches
because more habitat is available.
Conservation Insights
The approbation of the local sea turtle protection
law (Regional Legislative Decree 2009) is the
result of a committed regional government
wanting to develop the island in harmony with the
local biodiversity and culture, despite the
constraints of being a small, poor and isolated
island where people are highly dependent on their
natural resources to subsist. Those actions pass
through attracting and supporting tourism
investors, in preference to less environmentally
friendly activities like extensive palm oil
plantations or hydrocarbon extraction
infrastructures. Recently, another seaside resort
became operational (in Sundi beach), where the
fishing community was relocated to areas around
the city bay. Besides the impacts on local people
lives, coastal development has recognizable
negative impacts on sea turtles that should be
prevented or mitigated (e.g., beach armoring,
lighting). In addition, a common negative practice
observed is the removal of organic matter and low-
lying vegetation on beaches and their backshores.
This practice compacts the sand under the over-
story vegetation (mostly coconuts) and may cause
that nesting habitat, mainly used by hawksbills, to
become unsuitable or decrease thermal variation
and impact sex-ratios, limiting the resilience to
changes in global temperatures (Kamel 2013). In a
recent visit to the island (January 2017), RLF
observed the tracks from a hawksbill unsuccessful
emergence that went through a large extension of
Banana beach backshore, a beach that just started
to be controlled by a resort (e.g., diving center, bar,
esplanades). Thanks to the positive results of the
protection and awareness initiatives following
legislation, a plan to construct a hatchery near
another tourist resort (Bom-bom) was abandoned,
thus reducing further negative impacts on
incubation conditions (Mortimer 1999; Mrosovsky
2006). Another emerging trend is cement-based
construction being encouraged instead of
traditional wooden houses, which leads to sand
extraction on the beaches and consequent negative
impact on tourism and sea turtles. Noteworthy, the
increase in dampness and mold in cement homes
might also have negative consequences on human
health (Krieger 2010), that may lead to an increase
in the demand for the local traditional medicine to
cure asthma, made from dried sea turtle penis.
CONCLUSIONS
Our main goal was to identify the extent of the
nesting habitat and provide an island-wide
estimate of clutch numbers – indispensable
information for assessment of population status
and trends (Schroeder & Murphy 1999; Girondot
2010). This study demonstrated that Príncipe
represents a significant nesting area for hawksbills
in the Eastern Atlantic, although nesting in other
potentially important areas should be assessed
(e.g., São Tomé, where more nesting habitat is
available). The small size of hawksbill and green
turtle nesting stocks in the Gulf of Guinea suggests
Ferreira et al.
72
that the illegal take of females at São Tomé and
Príncipe (Ferreira 2015), both on the beaches and
at sea, is a serious threat for these sea turtle
populations. Fortunately, recent sea turtle
conservation efforts involving turtle fishers and
turtle traders show very positive signs (Vieira et al.
2017a,b) and highlight the importance of
integrating local people that used to make a living
with sea turtles (Frazier 1999; Ferreira 2015). The
relative nest abundances observed among the
beaches, and their association with human
distribution, can now aid managers and
conservationists to adopt more informed and
efficient measures (e.g., in coastal development
planning and sea turtle monitoring). Our approach
can also be used for future population assessments,
especially if the robustness of the method is
increased by: (1) replicating the method to obtain
variances or year to year deviations; (2) evaluating
clutch to body-pit ratio variation between beaches
or beach types; (3) reducing the number of days
between beach counts and increase the total
numbers of counts; (4) obtaining accurate body-pit
persistence time for different beach types; (5)
regularly monitoring main beaches during the
nesting season; and (6) obtaining more precise data
on clutch frequency and remigration intervals.
Since hawksbill nesting was more dispersed than
that of green turtles, periodic monitoring of several
beaches will be necessary to assess population
status. On the other hand, the assessment of green
turtle population size and trends can be efficiently
conducted by integrating the monitoring and
protection of the two main beaches (Paciência and
Infante), increasing efficiency and allowing for
funds to be invested in other essential activities.
We recommend the adaptation of this method to
other regions where low-density nesting is also
scattered across numerous small, interspersed
beaches and where financial resources are limited.
ACKNOWLEDGEMENTS
Data collection was possible thanks to an
anonymous contribution and to the support of the
Regional Government of Príncipe, while data
analysis and manuscript writing were supported by
a PhD scholarship to RLF (Portuguese Foundation
for Science and Technology -
SFRH/BD/73947/2010). We are indebted to C.
Sousa, from University of Algarve, for initiating
RLF on the ethnographic field work that made the
integration in the small fishing community of Praia
Seca informed and fruitful; Archie Carr Center for
Sea Turtle Research at the University of Florida,
for material and continued support; Norberto from
São Tomé, for opening his Praia Seca hut to RLF
and for taking him to Príncipe in his F/V Carioco
(which funny and hardworking fishermen made
the foreign white guy’s arrival to the community,
during the night, as natural as possible); all the
people staying in Praia Seca, who warmly
welcomed RLF in their lives, especially to Dona
Xica, who fed him when he was hungry, and to
Tachada, Gabriel, Nuno Kuto and Anastácio, who
accepted him in their spear-fishing campaigns; to
Silvino, for accompanying RLF during the hard
surveys around the island, including the
preparation of shelters and fishing for food; to T.
Borges, from University of Algarve, for the
insightful and intelligent advice during the writing
of the manuscript; to N. Carvalho, University of
Azores and F. Leitão, University of Algarve for
helpful comments and suggestions in the early
stages of the draft; to J. Latas, University of Évora,
for help with the formulas and math; to J.
Huttemann for help with English; to K. Bjorndal
for editing the final manuscript; and finally to all
the anonymous reviewers whose contributions
greatly improved the manuscript.
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Ferreira et al.
76
APPENDIX
General beach characteristics for the 50 sandy beaches identified at Príncipe Island (*obstacles on the
beach preventing sea turtle nesting; **rocks on the foreshore precluding green turtle emergences),
including estimated clutch densities (clutches/km, based on the suitable length) for the 2009/10 nesting
season, for both hawksbills (Ei) and green turtles (Cm). N and S are north and south areas of Principe,
respectively.
# Beach name Area Lat, Long Total length
(m)
Suitable
length (m)
Sand
color
Grain
size
Clutch density
Ei Cm
1 Papagaio N 1.641 / 7.423 545 245 brown small 0 0
2 Hospital Velho N 1.644 / 7.429 106 38 brown small 0 0
3 Ponta Mina N 1.646 / 7.436 158 38 brown small 0 0
4 Évora (a) N 1.645 / 7.439 162 9 yellow small 0 0
5 Évora (b) N 1.642 / 7.441 447 53 yellow small 0 0
6 Portinho N 1.638 / 7.446 553 236 yellow small 0 0
7 Salgado N 1.633 / 7.452 167 93 light brown medium 0 0
8 Abade N 1.631 / 7.456 256 199 brown medium 0 0
9 D'Areia S 1.608 / 7.432 295 52 light brown medium 0 125.9
10 Bumbo (Abelha) S 1.604 / 7.426 566 319 yellow small 19.1 224.1
11 Espraínha S 1.597 / 7.424 152 57 yellow small 0 382.7
12 Cemitério S 1.569 / 7.426 406 153 yellow medium 16 133.7
13 Cabinda S 1.564 /7.422 209 86 yellow small 28.6 369.6
14 Infante (Grande) S 1.558 / 7.417 965 510 brown small 17.2 564.9
15 Infante S 1.556 / 7.411 366 77 dark brown medium 76 467.7
16 Seca S 1.546 / 7.399 417 246 yellow coarse 12.8 331.6
17 Candeia* S 1.540 / 7.398 157 17 dark brown small 0 0
18 Rio Porco S 1.550 / 7.376 273 57 dark brown coarse 110.9 357.8
19 Rio São Tomé S 1.560 / 7.355 427 225 light brown small 40 318.5
20 Novo (Formiga) S 1.595 / 7.337 94 12 yellow coarse 0 170.6
21 Maria Correia S 1.601 / 7.353 169 90 brown coarse 0 0
22 Lapa S 1.605 / 7.364 391 247 dark brown medium 0 0
23 Caixão N 1.619 / 7.370 760 235 brown medium 0 0
24 Praínha (a) N 1.631 / 7.368 279 25 light brown medium 0 0
25 Praínha (b) N 1.632 / 7.367 69 35 light brown coarse 0 0
26 Iola N 1.647 / 7.373 491 300 yellow medium 8.1 6.8
27 Pedra Furada N 1.656 / 7.369 165 66 brown medium 0 29.3
28 Ponta Pedra Furada** N 1.657 / 7.367 77 77 yellow coarse 150 0
29 Ponta Marmita** N 1.683 / 7.372 95 81 yellow coarse 150.7 0
30 Margarida N 1.681 / 7.373 127 75 yellow coarse 0 81.9
31 Sundi N 1.679 / 7.380 548 354 light brown coarse 6.9 0
32 Barraca N 1.680 / 7.384 199 144 light brown medium 0 14.2
33 Mocotó N 1.681 / 7.390 522 459 light brown medium 5.3 31.2
34 Ribeira Izé N 1.685 / 7.395 610 399 light brown medium 6.1 35.9
35 Côco N 1.691 / 7.401 611 400 light brown medium 5.8 14.5
36 Bom-bom* N 1.695 / 7.402 202 20 light brown medium 0 0
37 Santa Rita N 1.691 / 7.405 794 470 light brown medium 0 8.2
38 Seabra N 1.689 / 7.412 158 130 brown medium 0 15.8
39 Cana (Lagaia) N 1.687 / 7.419 120 56 brown medium 0 0
Sea turtle nesting and beach selection at Príncipe Island
77
# Beach name Area Lat, Long Total length
(m)
Suitable
length (m)
Sand
color
Grain
size
Clutch density
Ei Cm
40 Campanha N 1.684 / 7.426 293 290 light brown small 0 8.9
41 Popa (Sandida) N 1.686 / 7.429 134 78 yellow coarse 0 26.3
42 Burra N 1.684 / 7.435 1222 815 yellow medium 0 0
43 Banana N 1.690 / 7.442 231 213 yellow coarse 28.2 75.8
44 Franguinha N 1.684 / 7.449 374 242 light brown medium 0 8
45 Armazén N 1.682 / 7.453 334 261 light brown medium 11.5 51.6
46 Macaco N 1.681 / 7.456 159 128 light brown medium 0. 0 21
47 Boi N 1.680 / 7.460 289 277 yellow coarse 10.8 106.9
48 Uba N 1.674 / 7.459 80 45 yellow coarse 66.7 0
49 Paciência (Grande) N 1.671 / 7.447 1500 1255 yellow medium 4.8 251
50 Capitania N 1.643 / 7.421 62 19 brown small 0 0
Arquipelago - Life and Marine Sciences ISSN: 0873-4704
79
First record of an Odontaspidid shark in Ascension Island
waters ANDREW J. RICHARDSON, GEORGE H. BURGESS, CHARLES M. SHEPHERD AND SAM B.
WEBER
Richardson, A.J., G.H. Burgess, C.M. Shepherd and S.B. Weber 2019. First record
of an Odontaspidid shark in Ascension Island waters. Arquipelago. Life and Marine
Sciences 36: 79-84.
The occurrence of the poorly understood shark species Odontapsis ferox is reported at an
oceanic seamount in the central south Atlantic, within the Exclusive Economic Zone of
Ascension Island. The presence of the species at this location is confirmed by the discovery
of a tooth embedded in scientific equipment, and footage of at least one animal on
autonomous underwater video. The new record of this shark species at this location
demonstrates the knowledge gaps which still exist at many remote, oceanic structures and
their candidacy for status as important conservation areas.
Key words: Shark, Seamount, Tooth
Andrew J. Richardson1 (email: [email protected]), G.H. Burgess2, C.M.
Shepherd3and S.B. Weber4. 1Conservation & Fisheries Department, Ascension Island
Government, South Atlantic Ocean ASCN 1ZZ. 2Florida Program for Shark Research,
Florida Museum of Natural History, University of Florida, Gainesville, FL 326114. 3Pristine
Seas, National Geographic Society, Washington, DC, United States of America. 4Centre for
Ecology and Conservation, University of Exeter, Penryn Campus, Cornwall, UK, TR10 9FE.
INTRODUCTION
The smalltooth sand-tiger shark, Odontaspis ferox
(Risso, 1810) has a circum-global but irregular
distribution, often being associated with deep shelf
edges and upper slopes of continents (Compagno
1984; Compagno 2001; Acuna-Marrero, et al.
2013). However, the presence of O. ferox has also
been recorded at oceanic islands, including the
Canary Islands (Barria et al. 2018), Azores
(Barcelos et al. 2018), Madeira (Lloris et al. 1991),
Cape Verde (Menezes et al. 2004; Wirtz et al.
2013) and Fernando de Noronha (Garla & Garcia
Junior 2006) in the Atlantic Ocean. O. ferox location records from a single specimen are not uncommon in the literature, such as Bonfil (1995), Sheehan (1998), Garla & Garcia Junior (2006) and Santander-Neto et al. (2011). Despite their cosmopolitan distribution and large size, with mature females reaching at least 410 cm total length (Fergusson et al. 2008), relatively little is
known on the ecology and biology of O. ferox, though it is recognised as having low rates of reproduction (one litter of two pups every two years) and relatively fragmented populations (Garla & Garcia Junior 2006; Barcelos et al. 2018; Barria et al. 2018), contributing to it being listed as Vulnerable under the International Union for Conservation of Nature (Graham et al. 2016). Most of the first location records for O. ferox have, to date, been from sightings by SCUBA divers or, more commonly, shark encounters with fishing gears, including hooking and entanglement. In addition, the first record of O. ferox from the South Atlantic was identified from a preserved set of jaws taken from a fishery in northeastern Brazil (Menni et al. 1995). The current study, however, presents not only the first record of O. ferox from the mid-ocean Ascension Island, the site of an upcoming Marine Protected Area (MPA) designation, but also the first occurrence of O. ferox presence being initially identified from in-situ, discarded teeth.
Richardson et al.
80
MATERIAL AND METHODS
Between 19th May and 4th June 2017 a major
expedition was launched to study the marine
megafauna communities associated with three
largely unexplored seamounts lying within the
Exclusive Economic Zone of Ascension Island,
including two shallow water features (summits <
100 m depth) located close to the mid-Atlantic
Ridge 260 – 320 km south east of Ascension
(Grattan Seamount and a second unnamed sister
peak). In order to survey deep-water demersal
fauna, custom-made autonomous underwater
video systems, or ‘dropcams’, developed by the
National Geographic Society as described by
Turchik et al (2015), were deployed at various
locations around the seamounts at depths ranging
from 99-2100m. Camera rigs were baited with
sardines and suspended 2 m above bottom with a
high-definition Sony Handycam HDR-XR520V
12-megapixel camera angled down at the seabed
and illumination provided by powerful LED
illuminators.
Fig. 1. A. Location of Ascension Island within the Atlantic Ocean and position of the Grattan seamount relative to
the Ascension Island 200 NM Exclusive Economic Zone. B. Locations of the Dropcam deployment from which
digital stills of O. ferox are extracted and the acoustic receiver from which the embedded tooth was recovered on the
Grattan seamount.
As part of a longer-term telemetry study of marine
megafauna, arrays of acoustic receivers (VR2AR
Acoustic Release Receiver, Vemco –
Canada www.vemco.com) were also deployed on
the summits of both seamounts. Upon retrieval of
one unit using a transponding hydrophone on the
Grattan seamount (9.74˚S, 12.82˚W) (Figure 1)
damage to cold-shrink tape wrapping on the unit,
used as an anti-foul measure, was observed. The
receiver had been deployed to a depth of 130 m, on
First record of an Odontaspidi shark in Ascension Island
81
the 3rd June 2017 and retrieved at the surface on
the 24th January 2018. Upon further inspection a
tooth was found embedded in the tape wrapping
and had also penetrated a short distance into the
casing of the VR2AR receiver unit. The tooth was
removed and stored dry for subsequent
identification.
RESULTS
Examination of the embedded tooth found it to be
single-cusped, labio-lingually flattened and having
smooth cutting edges. Crucially to species
identification were two pairs of prominent lateral
cusplets adjacent to the basal edge of the crown
(Figure 2). Using these diagnostic features, the
tooth was unambiguously identified to the
smalltooth sandtiger, Odontaspis ferox (FAO,
2002). The tooth had an overall length of 12.60
mm, enamel height of 5.25 mm, maximum width
of 5.15 mm and maximum lateral cusplet length of
2.98 mm. Further information on shark size, jaw
position or orientation was not available from the
single tooth specimen.
Fig. 2. Lateral view of the tooth, following removal
from the acoustic receiver housing.
O. ferox presence at the Grattan Seamount was
further corroborated by dropcam footage filmed
contemporaneously with the initial deployment of
the acoustic array, but not analysed until 2018
following discovery of the discarded tooth. Upon
close examination of archived digital video
footage filmed at a depth of 765 m on the southern
flank of the seamount (9.771˚S, 12.817˚W), a
single O. ferox individual was visible for a period
of 49 seconds (Figure 3). Diagnostic features used
to identify the specimen on film as O. ferox were
the first dorsal fin being situated closer to the
pectoral fins than to the pelvic fins with its rear tip
anterior to the pelvic-fin origins, together with a
short, asymmetrical caudal fin having a distinct
subterminal notch (Bass & Compagno 1986; FAO
2002). Based on the estimated relative lengths of
multiple cutthroat eels (Synaphobranchidae) and
bluntnose sixgill shark (Hexanchus griseus) also
visible in footage, the total length of the O. ferox
specimen was approximated to be 2.0-2.5 m. A
CTD mounted on the camera rig indicated an
ambient water temperature of 5.0°C and dissolved
oxygen saturation of 44%. On-board temperature
sensors in the VR2AR receiver in which the
embedded tooth was recovered recorded a daily
average of 15.6 – 19.6 °C over the deployment
period.
DISCUSSION
This record of O. ferox increases the number of
shark species confirmed from the Ascension Island
Exclusive Economic Zone to 16 and is particularly
notable for the unusual circumstances surrounding
its collection. Forensic analysis of shark bite traces
and damage have been used extensively for
investigation of shark attacks on humans (Lowry
et al. 2009), but rarely as a method for contributing
to species inventories. Although it is not possible
to ascertain the exact circumstances or timing of
the tooth being embedded in the acoustic receiver
body, other incidences of shark species biting into
submarine equipment have been reported (Marra
1989). Regardless of the nature of these
interactions, the trace evidence left behind proved
to be of considerable value in confirming
Richardson et al.
82
Fig. 3. Digital video stills of O. ferox captured at a depth of 765m on the Grattan Seamount using a baited dropcam
system. Images were extracted from footage filmed by a camera rig deployed at 07:42 GMT on 29th May 2017 (photo
credit: National Geographic Pristine Seas)
the presence of O. ferox at a previously unrecorded
location.
The presence of O. ferox at Ascension Island’s
Grattan Seamount, as well as other oceanic island
locations such as Madeira and Fernando de
Noronha (Lloris et al. 1991; Garla & Garcia Junior
2006), indicates at least some limited movement
by the species across oceanic expanses of many
thousands of metres depth, thus necessitating at
least one pelagic phase in the life history of some
individuals. Indeed, this has been evidenced in the
Indian Ocean by recorded catches of O. ferox in
pelagic areas (Abe et al. 1981; Gubanov 1985).
Nonetheless, it is likely that remote seamounts
such as Grattan are important habitats in an
otherwise open ocean environment for this
demersal species of suspected low productivity
(Bonfil 1995; Fergusson et al. 2008). Combined
evidence from video footage and recovery of the
embedded tooth demonstrate that O. ferox is
present in benthic habitats at depths ranging from
130 m to at least 765 m on the Grattan Seamount
and is clearly active over the summit at times.
Given the relative vulnerability of such isolated
seamounts to fishing and other anthropogenic
pressures, and the often higher biodiversity they
support relative to surrounding pelagic habitat,
there is mounting evidence of the importance of
these submarine peaks as focal points for marine
conservation efforts in the deep sea (Watling &
Auster 2017). In addition to this uneven distribution
of biodiversity between pelagic and seamount
systems, the lack of global homogeneity in demersal
fish assemblages across seamounts identified by
Clark et al (2010) may suggest that the ecological and
conservation value of seamounts is not consistent on
a global scale. Considering the announcement, in
September 2016, that Her Majesty's UK Government
would, by 2019, create a marine protected area at
Ascension Island covering at least 50% of the island’s
~440,000 km2 exclusive economic zone, seamounts
and other bathymetric features around Ascension
Island are surely strong candidates for protection.
ACKNOWLEDGEMENTS
The 2017 Ascension Island seamounts expedition was
funded by the European Union’s BEST 2.0
programme (grant 1599), the UK Government’s
Darwin Plus initiative (project DPLUS063) and
National Geographic Pristine Seas. Funding for
acoustic telemetry equipment was provided through
the Conflict, Stability and Security Fund (CSSF),
administered by the National Security Council of Her
Majesty's Government. AR and SW were funded by
Darwin Plus through project DPLUS063. The authors
thank the crews of the RRS James Clark Ross and St
Helena fishing vessel Extractor for their assistance in
deploying and retrieving survey equipment.
First record of an Odontaspidi shark in Ascension Island
83
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Received 16 Aug 2019. Accepted 15 Oct 2019.
Published online 29 Oct 2019.
Arquipelago - Life and Marine Sciences ISSN: 0873-4704
85
Short term effects of irradiance on the growth of
Pterocladiella capillacea (Gelidiales, Rhodophyta)
RITA F. PATARRA, ANNA A. LLOVERAS, ANA S. CARREIRO, MARIA H. ABREU,
ALEJANDRO H. BUSCHMANN AND ANA I. NETO
Patarra, R.F., A.A. Lloveras, A.S. Carreiro, M.H. Abreu, A.H. Buschmann and A.I.
Neto 2019. Short term effects of irradiance on the growth of Pterocladiella
capillacea (Gelidiales, Rhodophyta). Arquipelago. Life and Marine Sciences 36:
85-94.
Pterocladiella capillacea has been economically exploited for agar extraction in the Azores
for many years. Harvesting dropped to a full stop in the early 1990s due to a population
collapse, but restarted in 2013. Since then it has been intensively harvested and
overexploitation must be prevented, with both sustainable harvesting and effective
cultivation practices. This study represents the first attempt to determine optimal conditions
for P. capillacea production in the Azores, and evaluates its vegetative growth in two
experiments using von Stosch’s medium designed to test entire thallus and tips portions
response to different irradiances (30, 70 and 150 μmol photons m-2 s-1). The best relative
growth rate (RGR) was recorded at 150 μmol photons m−2 s−1 for the entire thalli and tips
after two-weeks and three-weeks, respectively, indicating that an acclimation period is
necessary to assure the growth of this alga under experimental conditions. Higher RGR was
obtained at higher irradiance (3.98 ± 2.10% fm day-1), but overall, growth rates were low or
negative. Epiphytes were a serious problem towards the end of the entire thallus experiments,
where Feldmannia irregularis proliferate at all irradiances. Future cultivation approaches
complemented with other relevant environmental factors (e.g. pH, photoperiod, salinity), are
recommended.
Key words: epiphytes, growth, in vitro cultivation, light intensity, Pterocladiella capillacea
Rita F. Patarra1,5 (email: [email protected]), A.A. Lloveras2, A.S. Carreiro3, M.H.
Abreu4, A.H. Buschmann5and A.I. Neto1. 1cE3c - Centre for Ecology, Evolution and
Environmental Changes/ Azorean Biodiversity Group and University of Azores, Faculty of
Sciences and Technology, Department of Biology, 9501-801 Ponta Delgada, Azores,
Portugal. 2Facultad de Biologia, Universidad de Barcelona, Avenida Diagonal, núm. 643,
08028 Barcelona, Spain. 3University of Azores, Faculty of Sciences and Technology,
Department of Biology, 9501-801 Ponta Delgada, Azores, Portugal. 4ALGAplus, Prod. e
Comerc. de Algas e Seus Derivados, Lda. Travessa Alexandre da Conceição, 3830-196
Ílhavo, Portugal. 5Centro i-mar & CeBiB, Universidad de Los Lagos, Camino Chinquihue
km 6, Puerto Montt, Chile.
INTRODUCTION
Pterocladiella capillacea (S.G. Gmelin)
Santelices & Hommersand is a well-known red
alga, recognized to produce a very high quality
bacteriological agar and agarose (Bixler & Porse
2010; Boo et al. 2010; Rhein-Knudsen et al. 2015;
Lahaye & Rochas 1991). The demand for agar
producing seaweeds is high; nonetheless, all raw
materials are obtained from harvests of wild plants,
resulting in limited or overexploited natural seaweed
stocks (Bixler & Porse 2010; Callaway 2015;
Marinho-Soriano 2017). Wild plants of P.
capillacea are relatively small (up to 17cm), and
Patarra et al.
86
mostly inhabit tropical and subtropical waters,
although a few extend into temperate latitudes
(Lawson & John 1982; Santelices 1998; Patwary
et al. 1998; Santelices & Hommersand 1997; Neto
2000a, Neto 2000b; Boo et al. 2010). The growth
in length of its axes and branches, as in all genera
presently recognized in the Gelidiaceae, depends
on the activity of a dome-shaped apical cell
(Rodríguez & Santelices 1987; Abbott 1997; Lee
2008). Its erect fronds can persist for up to 7 years
although the average is only 2-3 years (Dixon &
Irvine 1977). P. capillacea growth is site specific
and influenced by irradiance, temperature and
water movement (e.g. Macler & Zupan 1991;
Santelices 1991; Oliveira & Berchez 1993;
Friedlander 2008).
Epilithic in the lower intertidal and shallow
subtidal (down to 15m), this species is widely
distributed in the Azores (Neto 2000b), where it
was considerably harvested between 1950-80 t,
reaching an annual biomass between 1000-2000 t,
(Fralick & Andrade 1981; Santos & Duarte 1991;
Melo 2002; Santos & Melo 2018), dried and then
exported for agar extraction (Neto et al. 2005). Due
to a population collapse in the early 1990s,
harvesting dropped to a full stop, but restarted in
2013 and, at the present, P. capillacea is being
harvested in six of the nine Islands of the
Archipelago (Terceira, São Miguel, Graciosa,
Faial, São Jorge and Pico Islands; LOTAÇOR
2019) and sold almost exclusively to IBERAGAR
S.A. and TAE Lda. companies (AOnline 2016;
unpublished observations). In 2016, 450 wet
weight (ww) tonnes of P. capillacea were
harvested, representing a total value of 450000 €
(GaCS 2017), corresponding grossly to 1 € Kg-1
ww. Due to this recent resurge of the exploitation,
there is an urgent need to implement good
management practices for the harvest of the wild
resource and to promote the species cultivation
(Patarra et al. 2014; Rebours et al. 2014; Netalgae
2012; Patarra 2018).
Today there is not any known commercial
cultivation of this Gelidiales (Melo 1998;
Friedlander 2008; Callaway 2015: Marinho-
Soriano 2017; Santos & Melo 2018), mostly due to
its slow growth rates (Friedlander & Lipkin 1982;
Friedlander & Zelikovitch 1984; Macler & Zupan
1991; Yokoya & Oliveira 1992; Oliveira &
Berchez 1993; Felicini et al. 2002; Fujimoto et al.
2014). However, land base studies on P. capillacea
in Israel, revealed promising growth rates per week
(28.3% in average) during winter time (Gal-Or &
Israel 2004). According to a revision of the
Gelidiales cultviation made by Friedlander (2008)
distinct types of seaweed material, namely
different sized portions from differents parts of the
thallus can have different growth. This was earlier
observed by Rodríguez (1996) who reported that
the vegetative growth in length and branch
proliferation of Gelidium sclerophyllum was
favored by medial fragments, whereas the
rhizoidal propagation was favoured by apices.
To our best knowledge, a single study on the
physiological responses of Azorean Gelidiales was
performed (Fralick et al. 1990), and authors
indicated that optimal photosynthesis activity
occurred at 177 µmol m-2 s-1, between 15 and 25ºC.
To move to an effective culture of this species, a
clarification of the most relevant factors and
constraints for its production is needed. The
present work is a first attempt to understand how
different irradiances affect the vegetative growth
of distinct portions of the thallus (entire thallus and
tips) of P. capillacea from the Azores.
MATERIAL AND METHODS
Experimental setup
Sterilized natural seawater (SNW) was prepared
by filtering the water with 0.2 µm pore size filter
and autoclaved. Von Stosch’s enrichment culture
medium (VSE) was prepared according to Guiry &
Cunningham (1984). All the material used during
media preparation and in the experiments was
sterilized either by autoclave (2 atm, 120ºC, 20
min) or by using a drying oven (150ºC, 2 hr).
Fronds were collected by hand, between
December 2013 and February 2014, from the low
intertidal zone of a rocky shore of the south coast
of São Miguel Island (37° 50′ N, 25° 30′ W;
Azores archipelago), where stable populations of
P. capillacea are known to occur (Neto 2000b,
Neto 2000a, Neto 2001, Wallenstein et al. 2008).
Fronds were transported to the laboratory within 4
hr of the collection and kept in natural seawater
tanks (5 L). At each collection time, voucher
Short term effects of irradiance on the growth of Pterocladiella capillacea
87
specimens were made and deposited in the
Herbarium Ruy Telles Palhinha (AZB) of the
Biology Department, University of the Azores (P.
capillacea, AZB- SMG-13-90, AZB-SMG-14-01,
AZB-SMG-14-07).
One week before the experiments, algae were
incubated in 1 L Erlenmeyer flasks containing 500
ml of SNW enriched with VSE and kept in
constant movement through bottom aeration.
A preliminary experiment was conducted to
evaluate the effect of different pre-cleaning
solutions (sodium hypochlorite 1%; betadine 10%
and SNW) on the growth of epiphytes and
endophytes of P. capillacea (Table 1). The pre-
cleaning solution Bleach promoted the growth of
the red endophytes Anotrichium spp. and
Epicladia spp. (unpublished data). Based on these
preliminary results, the pre-cleaning solution
Betadine 10% was used in all subsequent
experiments. For this, fronds of P. capillacea were
rinsed under tap water and visible epibionts and
surface sediments were removed by hand and
gently brushed if necessary. Then, algae were
checked under a dissecting microscope and the
healthy ones retained for the cultivation essays.
Entire thalli (of 2-3cm long) and tips portions (1cm
long) were cleaned in SNW, submerged for 30s in
the pre-cleaning solution of Betadine 10% and
cleaned again in SNW; then they were randomly
assigned to experimental units, 1 L Erlenmeyer
flasks each containing eight individual entire
thallus or tips portions (depending on the
subsequent experiment) and 500 ml of SNW
enriched with VSE. The growth of excised
fragments was evaluated in two experiments
designed to test if distinct algae material: i) entire
thallus (ET) and ii) tips portions (TP) respond
differently under different photon flux densities
(PFD, 30, 70 and 150 μmol photons m-2 s-1).
The experiments were carried in cultivation
chambers (Sanyo MLR-351; Japan) using a
photoperiod of 12L:12D and 18ºC temperature as
fixed factors and lasted 5 weeks. The temperature
of 18ºC was used to match natural conditions of
the collecting site and the average annual sea
surface temperature (SST) in the Azores
archipelago (DETRA 2013, Patarra et al. 2017).
The 12L:12D photoperiod chosen in the
experiments relies on the fact that there is no
consensus on the best L:D combination for P.
capillacea growth (e.g. 10:14 LD, Fralick et al.
1990, 12:12 L:D; Nasr et al. 1966, 16.8 LD;
Yokoya & Oliveira 1992, 12:12 LD; Felicini et al.
2002). The irradiance was measured with a LI-250
Light Meter (LI-COR, USA) inside the culture
chambers and whenever the algae were collected
in the field. When the culture medium was
changed, the algal material was blotted dry and
weighted as fresh mass (fm) using a digital balance
(Kern ALJ220-5DNM, Germany; ±0.0001 g
precision). In each of these occasions, algae were
placed on plasticized graph paper and
photographed (Sony α230 with an objective of 18-
55mm, Japan) for posterior length analyses. The
pH was monitored (three measurements per
replicate) with a pH sensor (Hanna Instruments,
HI98127 USA).
Growth responses
Once a week, fresh biomass (g) and length (cm)
were registered, and relative growth rate was
calculated (RGR; % fm day-1) for each replicate
(n=4, SE) in all treatments. Length of individual
thallus/portions was obtained from the above
mentioned images using the AxioVision LE
Digital Imaging Software (SE 64 Rel. 4.9.1.,
Germany) and by measuring each individual
thallus/portion from its base to the top. At each
sampling time the RGR was calculated for each
replicate flask according to the following formula
(Abreu et al. 2011):
RGR= [Ln (final fm)-Ln (initial fm)]
time (days) ×100
These calculations were based on the sum value of
the eight individual thallus/portions in each flask.
For the analysis (see section 2.3), the mean value
of weekly growth rates measured throughout the
experiment was used to account for temporal
growth rates variation.
Data analysis
For all analysis, we used flasks as sampling units.
One-way analysis of variance (ANOVA, e.g.
Underwood 1997; PFD as a fixed factor with 3
levels, 4 replicates each) was used to test for
differences in RGR in the different treatments.
Patarra et al.
88
Prior to the analysis, Cochran's test was used to test for
homogeneity of variances and transformations were
applied whenever necessary. When this was not possible,
analyses were run on the untransformed data, since
ANOVA is robust to departures from this assumption
when designs are balanced and replication is high
(Underwood 1997). However, a more conservative p-
value (α = 0.01) was used. The a posteriori Student–
Newman-Keuls (SNK) test was used to investigate
differences among levels within significant terms. All
statistical analyses were performed using the software
GMAV v5.
RESULTS
The abiotic factors (temperature, irradiance)
monitored during the experiment were kept in the
pre-defined range. Carbon availability was always in
optimal levels, as determined by the pH recorded
values, ranging between 7.00 ± 001 and 7.93 ± 0.02
in ET experiment and 7.02 ± 0.05 and 7.90 ± 0.02 in
TP experiment.
Table 1. List of epiphytes and endophytes identified at the end of the preliminary experiment. SNW - sterilized
natural seawater.
Taxa Authorities Occurrence Pre-cleaning solutions
SNW Betadine 10% Bleach
RHODOPHYTA
Anotrichium tenue Nägeli endophyte x
Bangia spp. Lyngbye epiphyte x
Ceramium rubrum C. Agardh epiphyte x
CLOROPHYTA
Cladophora spp. Kützing epiphyte x
Enteromorpha multiramosa Bliding epiphyte x
Epicladia spp. Reinke endophyte x
Ulva compressa Linnaeus epiphyte x x
Ulva rigida C. Agardh epiphyte x x
HETEROKONTOPHYTA
Feldmannia irregularis (Kützing) Hamel epiphyte x x
In the ET experiment there was no biomass
increase in any of the treatments for the first 3
weeks (Figure 1A, B). However, pronounced
weight and length increments were recorded after
the third week for the 150 μmol photons m−2 s−1
treatment (Figure 1A), and the same pattern
occurred from the fourth to the fifth week at 70
μmol photons m−2 s−1 (Figure 1A). However, in
both situations an increase in the epiphytes (mostly
Feldmannia irregularis) growth (from the base to
the top of the thalli) was recorded, as well as an
accumulation of a layer of died cells over the thalli
surface. Due to the amount of epiphytes growing
at 150 μmol photons m−2 s−1 at the fifth week, no
measurements were taken from that moment
forward and for RGR statistical analysis only 30
and 70 μmol photons m−2 s−1 treatments were used
(Table 2). The lower RGR was observed at 30
μmol photons m−2 s−1 (-2.02 ± 1.25% fm day-1)
indicating loss of tissue (Figure 1C, Table 2).
Overall, the best entire thalli RGR was recorded at
150 μmol photons m−2 s−1 (3.98 ± 2.10% fm day-1,
Figure 1C).
As for the TP experiment, there was a similar
growth pattern for the 70 and 150 μmol photons
m−2 s−1 treatments, with slight mass increments
Short term effects of irradiance on the growth of Pterocladiella capillacea
89
Fig. 1. Effect of photon flux density (PFD) on the growth of P. capillacea entire thallus (ET; panels A, B and C)
and tips portions (TP; panels D, E and F) cultivated at three PFD (30, 70 and 150 μmol photons m−2 s−1), 18 ºC and
12:12 L:D photoperiod, after five weeks in culture. Fresh mass and length (mean ± SE, n=4); relative growth rate
(RGR, mean ± SE, n=20; p < 0.05). # mean RGR of four weeks, not used in the statistical analysis.
after two weeks in culture (Figure 1D, E). No
recovery was observed but the growth was lower
at the higher irradiance (150 μmol photons m−2 s−1)
(Figure 1E, Table 2) and no epiphytes were
recorded. Nevertheless, RGR was negative at all
PFD (Figure 1F). As for the ET, the best growth
was obtained for the higher PFD used.
Experiments lasted 5 weeks, since then algae were
mushy and colorless (some of them even white).
Table 2. Univariate analysis of variance (ANOVA) examining the effect of photon flux density (two levels for entire
thallus experiment, ET; three levels for tips portions experiment, TP; fixed) on the relative growth rate of P.
capillacea cultivated at 18 ºC, and 12:12 L:D photoperiod, after 5 weeks in culture.
ET TP
Source df MS F P df MS F P
PFD 1 86.44 2.42 0.1280 2 6.70 0.21 0.8135
Residual 38 35.71 57 32.36
Cochran's test C = 0.67 ns C = 0.47 ns
Transformation none none PFD = photon flux density; ET = entire thalus experiment; TP = tips portions experiment; n.s., not significan
Patarra et al.
90
DISCUSSION
The best growth performance observed at high
PFD for both, the entire thallus and the tip
portions, submitted to an longer acclimation period
(seen as necessary to assure the growth of P.
capillacea under experimental conditions) is in
agreement with reports for this species by other
researchers (e.g. Nasr et al. 1966; Correa et al.
1999; Felicini et al. 2002). However, the
unexpected decrease in length observed for both
entire thallus and plant tips is in disagreement with
reports by other authors, which reported that,
although P. capillacea exhibited low growth rates,
it maintained a viable growth for several days or
weeks in artificial conditions (e.g. Stewart 1984;
Macler & Zupan 1991; Yokoya & Oliveira 1992,
Oliveira & Berchez 1993, Felicini et al. 2002;
Friedlander 2008; Fujimoto et al. 2014). This may
be related with the collection time of the algae
material used to run laboratory experiments. In
fact, Stewart (1984) reported a best initial growth
and survival for cultures initiated with Californian
of P. capillacea collected between October and
March, corresponding to local late autumn/winter
period. Similar results were reported by Gal-Or &
Israel (2004) for Israeli material. In the present
study all the laboratory trials were run at 18 ºC (the
mean annual SST in the Azores Archipelago,
DETRA 2013, Patarra et al. 2017), but the algae
were collected from December to early Spring
when SST varies between 16 and 17 ºC (DETRA
2013). It is likely that the observed negative
growth could be related to higher temperature
used. In fact, a poor growth performance of P.
capillacea at high temperatures has been reported
by several authors (Fralick et al. 1990; Yokoya &
Oliveira 1992; Gal-Or & Israel 2004; Fujimoto et
al. 2014). It is, however, worth considering, that P.
capillacea in the Azores is distributed from low
intertidal to shallow subtidal zones (Neto 2000a,
Neto 2000b, Neto 2001: Wallenstein et al. 2008),
being adapted to a wide range of irradiances and
water temperatures, although the temperature
range in shallow subtidal zones does not vary
greatly (HI 2000). Furthermore, Fralick &
Andrade (1981) observed that wild Azorean plants
exhibited optimal growth at 20-22 ºC, coinciding
to the period between June and October when the
irradiance level is higher in the Azores.
Regarding irradiance, the obtained mean growth
rates were negative/low at all PFD, and, even in the
higher irradiances, their was loss of tissue, and the
thallus was mushy, colorless or even white at the
end of the experiments. This is in disagreement
with reports by other researchers for Gelidiales:
Macler & West (1987) kept vegetative cultures of
Gelidium coulteri for more than a year with an
exponential growth rate less than 10% day-1 at 150
μmol photons m−2 s−1; Fralick et al. (1990) in a
research on the physiological responses of
Pterocladia and Gelidium (Gelidiales,
Rhodophyta) from the Azores reported optimal
photosynthesis for P. capillacea at 177 μmol
photons m−2 s−1 with oxygen production values
remaining high until 320 μmol photons m−2 s−1;
Rico (1991) reported maximum growth rates
(10.0% day-1) for Gelidium pulchellum at 130-
μmol photons m−2 s−1; Sousa-Pinto et al. (1999)
observed that the growth of Gelidium pulchellum
pieces increased with irradiance up to 130 μmol
photons m−2 s−1; Gal-Or & Israel (2004) recorded
maximal growth rates for P. capillacea, using a
gradient table, at 100 μmol photons m−2 s−1 with
winter plants; Harb et al. (2018) reported a higher
growth rate for P. capillacea at 300 μmol photons
m−2 s−1, as long as increasing photosynthetic
pigment and protein contents.
Worth considering, however, that Stewart
(1984) reported that higher levels of irradiance
favored contaminants and were correlated with
larger numbers of bleached P. capillacea thalli that
did not exhibit measurable growth. This is similar
to what we observed in the present study, in which
the growth of the epiphyte Feldmannia irregularis
at 150 μmol photons m−2 s−1 after 4 weeks in
culture was a serious problem (growing from the
base to the top of the thalli). According to
Friedlander (2008) one of the biological factors
that most affects Gelidium cultivation is indeed the
growth of epiphytes. Sousa-Pinto et al. (1999) in
their study on the effect of light on the growth of
Gelidium pulchellum reported that the algae were
heavily epiphytized (with cyanobacteria, fungi and
algae) at the higher irradiances (240-430 μmol
photons m−2 s−1). Fungi and cyanobacteria
Short term effects of irradiance on the growth of Pterocladiella capillacea
91
proliferation were inhibited with antibiotics, but
green algae persisted and were only marginally
contained after washing the thalli with distilled
water in-between medium changes. Buschmann et
al. (1997) also reported problems with
Ceramialean epiphytes on Gracilaria and
observed that their abundance increased
significantly from the apical (new tissues) to the
central parts of the thalli (older tissues). Probably
the lower load of epiphytes observed on the apical
tips portions of P. capillacea in the present study
is related to the new age of this tissue, but could be
also related with the adopted cleaning procedures.
From the known cleaning methods (e.g.: i)
cleaning the algae with a soft brush; ii) wash them
with distilled water; iii) using pre-cleaning
solutions, such as sodium hypochlorite, Betadine
10%, antibiotics) used by several authors (see
Salinas 1991; Sousa-Pinto et al. 1999; Redmond et
al. 2014), the one adopted in the present study (pre
cleaning followed by the use of Betadine 10%)
seemed to be effective for some epiphytes
identified in the preliminary experiments with the
tip portions (TP).
The obtained values for the culture medium pH
in all experiments suggest the algae were not CO2
limited (in accordance to Lignell & Pedersén 1989;
Hargreaves 1998; Mercado et al. 2001).
Altogether, the adopted combination of irradiance,
temperature, nutrients and water aeration in the
present study was not the best option for the
growth of P. capillacea from the Azores.
Nonetheless, small studies, as the present ones, are
an important tool for the collection of data on the
biology of the species, that could be used in future
long-term experiments. Considering the economic
importance of the species in the region, future
cultivation approaches using different culture
combinations, complemented with relevant
environmental factors (e.g. pH, photoperiod,
salinity) and a delicate selection of fast growing
ecotypes are recommended.
ACKNOWLEDGEMENTS
This study was partially supported by project
AQUAIMPROV, ON.2 – O Novo Norte,
(SAESCTN-PII&DT/1/2011); Portuguese National
Funds, through FCT – Fundação para a Ciência e
Tecnologia, within the projects
UID/BIA/00329/2013, 2015 - 2018 and
UID/BIA/00329/2019, CIRN (Centro de
Investigação de Recursos Naturais, University of
the Azores), and CIIMAR (Interdisciplinary
Centre of Marine and Environmental Research,
Porto, Portugal). RFP was supported by a doctoral
grant M3.1.2/F/024/2011, Fundo Regional para a
Ciência e Tecnologia. The authors are grateful to
Pedro Pereira and Natália Cabral (Department of
Biology, Azores University) for their technical
support during the experimental studies. We would
like to thanks Dr. Eva Cacabelos for her support on
the seawater collection along the experimental
period. Special thanks go to Dr. Gustavo Martins
for his helpful comments on the statistical analysis.
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Published online 18 Nov 2019.
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Woo, K.L. 2006. Testing Visual Sensivity to the Speed
and Direction of Motion in Lizards. Journal of
Visualized Experiments [Internet]. Available from:
http://www.jove.com/index/details.stp?id=127 (cited 18
February 2007)
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ISSN 0873-4704
ARQUIPELAGO - Life and Marine Sciences
No. 36 – 2018/2019
CONTENTS: PAGE
FRICKE, RONALD AND PETER WIRTZ
Apletodon gabonensis, a new species of clingfish (Teleostei: Gobiesocidae)
from Gabon, eastern Atlantic Ocean 1
LUIZ, OSMAR J. AND JOHN E. MCCOSKER
Snake eels (Ophichthidae) of the remote St. Peter and St. Paul’s Archipelago
(Equatorial Atlantic): Museum records after 37 years of shelf life 9 FREITAS, RUI AND PETER WIRTZ
First record of the Sculptured Mitten Lobster Parribacus antarcticus (Crustacea,
Decapoda, Scyllaridae) from the Cabo Verde Islands (eastern Atlantic) 15
BROWN, JUDITH, E. NISHI AND PETER WIRTZ
The polychaete Lygdamis wirtzi at Ascension and St Helena Islands
(Annelida, Polychaeta, Sabellariidae) 19
CECCHETTI, ARIANNA, K.A. STOCKIN, J. GORDON AND J.M.N. AZEVEDO
A first assessment of operator compliance and dolphin behavioural responses
during swim-with-dolphin programs for three species of Delphinids in the Azores 23
GABRIEL, DANIELA AND SUZANNE FREDERICQ
The marine macroalgae of Cabo Verde archipelago: an updated checklist 39
FERREIRA, ROGÉRIO L., HELEN R. MARTINS AND ALAN B. BOLTEN
Hawksbill (Eretmochelys imbricata) and Green Turtle (Chelonia mydas)
Nesting and Beach Selection at Príncipe Island, West Africa 61
RICHARDSON, ANDREW J., G.H. BURGESS, C.M. SHEPHERD AND S.B. WEBER
First record of an Odontaspidid shark in Ascension Island waters 79
PATARRA, RITA F., A.A. LLOVERAS, A.S. CARREIRO, M.H. ABREU, A.H.
BUSCHMANN AND A.I. NETO
Short term effects of irradiance on the growth of Pterocladiella capillacea
(Gelidiales, Rhodophyta) 85
