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This article was downloaded by: [The University of Manchester Library]On: 18 December 2014, At: 11:04Publisher: Taylor & FrancisInforma Ltd Registered in England and Wales Registered Number: 1072954 Registered office: MortimerHouse, 37-41 Mortimer Street, London W1T 3JH, UK
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Life history of Caprella grandimana (Crustacea:Amphipoda) reared under laboratory conditionsElena Baeza-Rojano a , José M. Guerra-García a , M. Pilar Cabezas a & Isabel Pacios aa Laboratorio de Biología Marina, Dpto. Fisiología y Zoología, Facultad de Biología ,Universidad de Sevilla , Sevilla, SpainPublished online: 04 Dec 2010.
To cite this article: Elena Baeza-Rojano , José M. Guerra-García , M. Pilar Cabezas & Isabel Pacios (2011) Life history ofCaprella grandimana (Crustacea: Amphipoda) reared under laboratory conditions, Marine Biology Research, 7:1, 85-92
To link to this article: http://dx.doi.org/10.1080/17451001003713571
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ORIGINAL ARTICLE
Life history of Caprella grandimana (Crustacea: Amphipoda) rearedunder laboratory conditions
ELENA BAEZA-ROJANO*, JOSE M. GUERRA-GARCIA, M. PILAR CABEZAS &
ISABEL PACIOS
Laboratorio de Biologıa Marina, Dpto. Fisiologıa y Zoologıa, Facultad de Biologıa, Universidad de Sevilla, Sevilla, Spain
AbstractGrowth, maturity, and reproduction of 112 juveniles of Caprella grandimana obtained from 26 ovigerous females werestudied under laboratory conditions at 178C, and with a 12-h photoperiod. The newly hatched juveniles were transferred tosmall glass containers and fed with a mixture of diatoms Phaeodactylum tricornutum and Tetraselmis chuii (1:1). Afteremerging from the brood pouch, caprellids were considered as Instar I (1 mm length). Sexes were not able to be identifieduntil Instar III. In males the moulting interval gradually increased up to Instar X, producing a final instar which livedsignificantly longer than the previous one. Female intermoult period remained constant until they died. The body lengthand flagellar articles increased faster in males than females at each instar. Females reached the mature stage at Instar V andVI with a mean of 38.4 days, producing their first brood 10 days later at 49.1 days. The mean of eggs produced by eachfemale was 7.6 and the number of offspring emerged was 5. There was a significant correlation between the average lengthof the female in each instar and the number of eggs and offspring per brood. This is the first time that a Mediterraneanspecies has been successfully reared under laboratory conditions. These studies are basic for future ecotoxicological researchand management of the caprellid species.
Key words: Amphipod, Caprella grandimana, laboratory culture, life cycle, Tarifa Island
Introduction
Caprella grandimana (Mayer, 1882) is a common
amphipod species spread throughout the Mediterra-
nean Sea (Krapp-Schickel 1993) and the Atlantic
African coast from Cape Spartel to Cap Blanc
(Morocco) (Bellan-Santini & Ruffo 1998). In the
Straits of Gibraltar, this species is mainly found
associated to the algae Corallina elongata (J. Ellis
and Solander) and Jania rubens ((Linnaeus) J.V.
Lamouroux) in low intertidal zones throughout the
year.
The body is smooth except for the 5th to 7th
pereonites, which carry small humps (Figure 1). The
head lacks a rostrum, with antenna 1 about half
the body length, and the flagellum slightly shorter
than the peduncle, with short setae. The gnathopod
2 propodus on the male is elliptical, nearly twice as
long as broad, the dorsal edge with a few short setae,
and convex palm with one very acute process which
delimits a concavity filled with a membranous sac,
distally with a triangular process. Guerra-Garcıa
et al. (2001) redescribed C. grandimana based on
specimens from the Straits of Gibraltar, and pointed
out the presence of two abdominal appendages in
males instead of one.
During the last decade, an effort has been under-
taken to contribute to the knowledge of the Caprel-
lidea from the Iberian Peninsula and nearby areas,
especially in the Straits of Gibraltar (e.g. Guerra-
Garcıa et al. 2000, 2001, 2002; Guerra-Garcıa 2001;
Guerra-Garcıa & Takeuchi 2002), since this is where
there is a very high proportion of endemic Caprelli-
dea species, contributing 30.8% to the endemism of
the Mediterranean population. However, nowadays,
the ecological knowledge and life history of peracarid
fauna including caprellids over this region is still very
scarce. No studies have been carried out on growth
*Correspondence: E. Baeza-Rojano, Laboratorio de Biologıa Marina, Dpto. Fisiologıa y Zoologıa, Facultad de Biologıa, Universidad de
Sevilla, Avda. Reina Mercedes 6, 41012, Sevilla, Spain. E-mail: [email protected]
Published in collaboration with the University of Bergen and the Institute of Marine Research, Norway, and the Marine Biological Laboratory,
University of Copenhagen, Denmark
Marine Biology Research, 2011; 7: 85�92
(Accepted 15 January 2010; Published online 2 December 2010; Printed 16 December 2010)
ISSN 1745-1000 print/ISSN 1745-1019 online # 2011 Taylor & Francis
DOI: 10.1080/17451001003713571
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rate and maturity periods of the Caprellids from this
zone and all the existing information is based on
species collected from other latitudes. In colder
waters, Caprella septentrionalis (Krøyer, 1839),
Pseudoprotella phasma (Montagu, 1804), and Caprella
acanthifera (Leach, 1814) showed short reproductive
periods or a limited number of generations per year
(Heptner, 1963; Hughes, 1978; Costello & Myers,
1989). On the other hand, Caprella danilevskii
(Czerniavski, 1868), Caprella tsugarensis (Utinomi,
1947), Caprella decipiens (Mayer, 1890), Caprella
verrucosa (Boeck, 1871), and Caprella okadai
(Arimoto, 1930), collected from warmer Japanese
waters, continued their reproductive cycle for almost
the whole year (Imada & Kikuchi 1984; Aoki 1988;
Takeuchi et al. 1990). Samples of C. grandimana
collected every two months during a two-year
period (Guerra-Garcıa et al. 2009a) proved that
C. grandimana reproduces all year around.
Currently, P. phasma, C. danilevskii, C. okadai, and
the invasive Caprella mutica (Schurin, 1935) have
been the only species successfully reared under
laboratory conditions in order to follow any signs
of moulting as well as spawning to attain knowledge
of their complete life history (Harrison 1940;
Takeuchi & Hirano 1991, 1992a; Cook et al. 2007).
Corallina elongata is one of the most abundant
calcareous macroalgae in the shallow waters of the
Mediterranean, and forms the ‘Corallina elongata
community’ between 0 and 5 m depth. Many authors
have indicated the presence of communities domi-
nated by C. elongata on the coasts of the western
Mediterranean (Gili & Ros 1985; Ballesteros 1988;
Soltan et al. 2001). This species constitutes one of
the dominant algae in the intertidal ecosystems in the
Straits of Gibraltar (Guerra-Garcıa et al. 2006).
Five species of caprellids have been recorded as
being associated with the intertidal algae Corallina
elongata in this area: C. acanthifera, C. grandimana,
Caprella hirsuta (Mayer, 1890), Caprella liparotensis
(Haller, 1879), and Caprella penantis (Leach, 1814).
Caprella grandimana and C. penantis are the most
common species showing a density up to 2000�3000
ind l�1 of algae, respectively (Guerra-Garcıa et al.
2009b).
In the present study, we focused on the life history
of C. grandimana, one of the dominant peracarid
species in the intertidal ecosystems of the Straits of
Gibraltar.
Material and methods
Tarifa Island (36800?00.7??N, 5836?37.5??W) is a
marine reserve located within the ‘Parque Natural
del Estrecho’ in the Gibraltar Straits. It represents
the southernmost enclave of Europe and its inter-
tidal ecosystems are among the most diverse of the
Iberian Peninsula. Caprella grandimana was collected
from Corallina elongata and Jania rubens in the low
intertidal zone of Tarifa Island at low tide, in
December 2007 and March 2008. The individuals
studied were taken directly off the algae in the field,
and in the laboratory 26 ovigerous females were
selected and isolated in small glass containers of
120 ml with a diameter of 6.5 cm and 6 cm in height.
A 1 mm plastic mesh, replaced weekly, was used as a
substratum for attachment. One hundred and twelve
newly hatched individuals were monitored through-
out their complete life cycle. The hatchlings were
introduced into new glass containers in groups of a
maximum of five individuals without the female,
since no evidence of maternal care was found for this
species; young did not cling to their mother, nor
did they remain together. During the first days, the
plastic mesh was substituted for small pieces of
J. rubens and C. elongata for the juveniles. Once
they reached maturity, a pair of females and males
were selected and placed in separate glass vessels.
The male was separated from the female when eggs
were present in the brood pouch. They were main-
tained at 178C with a photoperiod of 12 h light:
12 h dark. We selected this temperature because it
represents the average temperature throughout the
year in the sampling site at Tarifa Island (personal
observation, Guerra-Garcıa et al. 2004). The sea-
water used for culture was artificial water (ReefSalt
of SeachemTM) prepared with a salinity of 35.5. The
water in the glass containers was changed daily.
Individuals were fed with a mixture of algae,
made from lyophilized colonies of the diatom
Phaeodactylum tricornutum ((Bohlin) Lewin) and
Tetraselmis chuii (Butcher) (1:1). Previous studies
Figure 1. Schematic drawing of the lateral body shape of Caprella
grandimana from Tarifa Island. Refigured from Guerra-Garcıa
et al. (2001). Scale bar: 1 mm.
86 E. Baeza-Rojano et al.
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on total fatty acid composition of individuals col-
lected from the Strait of Gibraltar suggested a
greater contribution of diatoms and macroalgae in
the diet of C. grandimana (Guerra-Garcıa et al.
2004). These colonies were prepared daily, resus-
pended in the artificial seawater and introduced
once a day by pipette into each vessel. The caprellids
held the diatom colonies with their first gnathopods
and consumed them using their maxillipeds.
All the specimens were observed daily under a
binocular microscope for any signs of spawning,
moulting, or release of the young. Caprellids moulted
successively after their emergence from the brood
pouch, at Instar I (according to the system adopted by
Takeuchi & Hirano 1991), until their death. At each
instar stage after each moulting, body length was
measured while the caprellids remained with their
pereonites straightened over the mesh. The number
of flagellar articles on the first antenna was also
counted. The maturation stage of the female was
classified at immature, premature and mature stage
by the study of the morphology of the paired
oostegites located on pereonites III and IV (Takeuchi
1989).
The number of eggs could be counted through the
transparent oostegites of the brood pouch, as well as
the number of offspring that emerged from each
female in each reproduction event.
Mating behaviour was observed daily in each
container for 5 min.
Statistical analyses
Possible differences of life span, body length and
moulting intervals between males and females were
tested with a Kruskal�Wallis test. Univariate ana-
lyses were carried out using SPSS 17.
Results
Life span and survival
Forty-nine females and 53 males from 26 ovigerous
females of Caprella grandimana collected from Tarifa
Island were studied under laboratory conditions for
their whole life span, reaching on average, a survival
cycle of 104.5940.3 days, at 178C. Females lived
120.2944.7 days (mean9S.D.) and males 89.99
29.3 days (mean9S.D.), attaining a maximum of
209 days and 127 days, respectively (Table I);
females had a life span significantly longer than
males (Kruskal�Wallis�15.6, pB0.001).
Both females and males had a very high survival
rate during their first period of the life cycle, but it
began to decrease at Instar VI during the reproduc-
tive phase (Figure 2a). Males suffered a very marked
decrease of their survival rate during the last three
instars, with only 13% surviving at the last instar
(Figure 2b).
Moulting cycle
The moulting rate was found to be higher in
females than males, as females always moulted after
the release of their young from the brood pouch.
Figure 3 indicates the number and duration of each
instar in males and females. Males only reached
Instar X after nine moults while females continued
to Instar XVIII, moulting 18 times (Table I).
Caprellids have been observed eating their own
exuviae.
Newly hatched juveniles moulted every 6.4�10.8 days until reaching Instar IV, when their gender
could be identified under a binocular microscope.
The development in the young females of an
immature brood pouch in their pereonites was clear.
Later, the moulting intervals of males gradually
increased from 6.992.9 to 32.4911.4 days until
the last Instar X.
The time between the last moult and death among
all males was 32.5914.1 days, which was signifi-
cantly longer than all their previous moulting inter-
vals (Kruskal�Wallis�34.4, pB0.001). (In the final
period before they die, males of Caprella grandimana
have an accumulation of particles which completely
covers their body surface.)
Table I. Life history traits of Caprella grandimana reared in the laboratory (temperature 178C, salinity 35.5. M�male, F�female).
Life-cycle criteria M/F Range Mean 9SD n
Life span (days) M 36�127 89.9 29.3 53
F 38�209 120.2 44.7 49
Number of moults M 3�9 7 1.4 51
F 3�18 10 3.5 49
Mature body length (mm) M 4.5�6.7 5.4 0.8 51
F 2.9�4.8 4 0.4 42
No. of juveniles per brood (average) F 1�15 5 3.5 57
No. of eggs per brood (average) F 1�18 7.6 3.8 231
Incubation time (days) F 7�13 10.5 1.3 49
Sexual maturity of females (days) F 21�67 38.4 8.5 45
Life history of Caprella grandimana 87
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In females, the moulting frequency gradually
increased from 8.293.1 to 13.994.1 until Instar
V, and stabilized at 10.8�16.9 days from Instar V to
Instar XVIII. In contrast to males, the moulting
interval from last moult to death was not signifi-
cantly different to the rest of intervals.
Growth rate: body length and number of flagellar articles
of antenna 1
The growth rate was the same for males and females
before their gender was determined. After Instar IV,
the males had a higher size increment per moulting
within a shorter period compared to females.
Growth increment per instar is given in Figure 4.
Males increased the body length at each instar,
following a straight-line growth rate, reaching a
maximum value of 6.7 mm at Instar XI. The average
male body length was 5.4 mm for all mature stages.
However, in females, the rate of increase of body
length followed a polynomial curve, generally higher
in early developmental stages and decreasing after
Instar XVI. The maximum length was 6.7 mm in
males and 4.8 mm in females (Table I). Significant
differences could be found in body length between
males and females after Instar VI (Kruskal�Wallis,
pB0.001).
The number of flagellar articles in the antenna 1
was always two in newly born juveniles, plus three
basal articles at the peduncle. Males increased one
article in the flagellum before each moulting up to
Instar IX and females up to Instar VII. Afterwards,
males and females increased less than 1 article
per moulting (Figure 5). The number of flagellar
articles was always higher in males than females in all
instars from their gender differentiation stage. The
0
25
50
75
100(a)
(b)Instar
Sur
viva
l rat
e (%
)
0
25
50
75
100
I II III IV V VI VII VIII IX X XI XIII XIV XV XVI XVII XVIII XIX
IV V VI VII VIII IX X XI XII XIII XIV XVI XVII XVIII XIX
Instar
Sur
viva
l rat
e (%
) Females
Males
Figure 2. (a) General survival rate in Caprella grandimana at each
instar in laboratory conditions. (b) Survival rates of males and
females of Caprella grandimana reared in laboratory conditions.
Juvenile Instars I�III were not separated into males and females,
since their gender could not be identified under a binocular
microscope.
0
10
20
30
40
50
I II III IV V VI VII VIII IX X XI XII XIII XIV XV XVI XVII XVIII XIX
Instar
Dur
atio
n (d
ays)
MalesFemalesJuveniles
Figure 3. Duration of each instar (Mean9S.D.) in males, females and juveniles of Caprella grandimana. Instars I�III juveniles were not
separated into males and females, since the gender could not be identified under a binocular microscope.
Females;y = -0,019x2 + 0,6018x + 0,4397
R2 = 0,9976
Males;y = 0,6203x + 0,2015
R2 = 0,9899
0
2
4
6
8
I II III IV V VI VII VIII IX X XI XII XIII XIV XV XVI XVII XVIIIXIX
Instar
Bod
y le
ngth
(m
m)
Females
Males
Juveniles
Figure 4. Total body length and growth increment per instar
(Mean9S.D.) in males, females and juveniles of Caprella
grandimana. Juvenile Instars I�III were not separated into males
and females, since gender could not be differentiated.
88 E. Baeza-Rojano et al.
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maximum number of articles was 11 in males and 10
in females.
Maturation and sex ratio throughout the lifespan
Eighty-six per cent of the females reached the
mature stage at Instar V and VI and only 11% at
Instar VII. So a mature stage was achieved on
average of 38.498.5 days after emergence from the
brood pouch (Table I). Clutches of ovigerous
females collected from Tarifa resulted in a similar
number of females and males (49 females/53 males),
but the number of males decreased due to mortality
at an earlier age, consequently the number of males
was relatively lower than females towards the end of
the life cycle.
Mating behaviour and reproduction
Precopulatory mate-guarding was not observed in
Caprella grandimana during the study; males did not
carry the female until she could be fertilized to
guard her against other males. Instead, males only
came into contact with females to check if they were
receptive. After moulting took place, females were
ready to be fertilized, and the male would grasp
the female with the first gnathopods and pereiopods
5 and formed the precopulatory pair in the same way
described for the reproductive behaviour of Caprella
laeviuscula by Caine (1991), and Caprella scaura by
Lim & Alexander (1986). After oviposition, a mass of
eggs appeared into the brood pouch. No females were
found with eggs in the brood pouch in the absence of
males. The incubation period of the embryos was
recorded as the period from copulation to release of
juveniles from the brood pouch. The average incuba-
tion period for this species was 10.591.3 days. Thus,
the average generation length of this species was
estimated to be 48.9 days at 178C (Table I).
Fertility
The average number of embryos produced from
a single female in a single brood was 7.693.8,
increasing from 4 at Instar V to 18 at Instar XVIII.
The number of offspring that finally emerged from
the brood pouch was 5.093.5, half of the total
number of eggs released into the brood pouch, and a
maximum of 15 juveniles emerged at Instar XVIII
(Table I). Therefore, the number of eggs/juveniles
produced from a single brood increased with the age
of the female, and a positive correlation was also
0
2
4
6
8
10
12
I II III IV V VI VII VIII IX X XI XII XIII XIV XV XVI XVII XVIII XIX
Instar
Art
icle
num
bers
Males
Females
Juveniles
Figure 5. Number of flagellar articles (Mean9S.D.) of antennae I per instar in Caprella grandimana. Up to Instar IV females and males
could not be differentiated, so article numbers were the same in juveniles.
Nº of offspring;y = 2,4036x - 4,794
R2 = 0,1552
Nº of eggs;y = 4,0106x - 7,9391
R2 = 0,4829
0
2
4
6
8
10
12
14
16
18
20
2,5 3 3,5 4 4,5 5 5,5 6
Body length (mm)
Num
ber
of e
ggs
0
2
4
6
8
10
12
14
16
18
20
Num
ber
of o
ffspr
ing
Number of eggs
Number of offspring
Figure 6. Correlation of number of eggs and number of offspring with female total body length in Caprella grandimana. Number of eggs
(n�231 broods). Number of offspring (n�57 broods with offspring). Both correlations were significant at pB0.001.
Life history of Caprella grandimana 89
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found between body length and the number of eggs/
juveniles produced (Figure 6).
Decaying or disappearing of eggs during the
incubation period was observed in 31% of cases.
Discussion
Despite the importance of caprellids in Mediterra-
nean ecosystems, this is the first time in which a
Mediterranean species has been successfully reared
under laboratory conditions throughout all instars of
their cycle until completion of their life history.
These studies are elemental for future ecotoxicolo-
gical research and management of caprellid species.
Caprella grandimana was characterized by a lack
of maternal care behaviour in early stages of growth;
small first instar juveniles used Corallina elongata
thalli as habitat substrata, and no young were seen
clinging to the mother or staying near to her.
According to Aoki (1999), caprellids which produce
small first instar young (B1.3 mm) and live on
seaweed with thick thalli and branches such as
Sargassum patens (Agardh, 1820) need to use an
epiphytic secondary habitat or depend on maternal
care to hold on to the substratum and be able of
survive. However, C. elongata has thin branches
which allow the small first instar to hold them tight,
and this allows for C. grandimana juveniles not to
need the help of epiphytic or maternal care at their
first stage of life.
With regard to the moulting cycle, males and
females had different numbers of moults throughout
their life, following a similar process as described in
Pseudoprotella phasma by Harrison (1940). Males
only lived up to Instar X, while females continued
moulting up to Instar XVIII. Takeuchi & Hirano
(1991, 1992a) found the same pattern in Caprella
okadai, and Caprella danilevskii, where females had
more moults rate than males, and had a survival time
significantly longer than males.
The duration of each instar in females from VI
onward remained stable until they died, but in males
it gradually increased from Instar IV up to their last
instar, which was significantly longer than their
previous moulting interval. This case has not been
reported in any other species of Caprellidea or
Gammaridea in laboratory experiments. During
this last instar, larger males began to be covered by
detritus and other particles until all the gnathopods
and pereonites were completely covered with detri-
tus. During sampling in the field, well-developed
males also showed their bodies completely covered
with detritus, so it seems that males at their last
instar cannot moult and retain the same cuticule
without growing until their death. The pattern of
flagellar articles added to antenna 1 also differed
between males and females as reported for
C. danilevskii and C. okadai (Takeuchi & Hirano
1991, 1992a), so in this species it is necessary to
know the flagellar pattern to be able to determine the
instar only by the number of flagellar articles. Males
had a higher number than females. Upon reaching
sexual maturity, males continued to increase the
number articles, and females remained more or less
constant with 10 articles, so with this flagellar
pattern it is easy to determine the instar stage in
the field, and to know if females and males are able
or not to reproduce according to the number of
articles in their antenna 1.
Caprella grandimana had a generation period of
49.1 days at 178C, nearly double that of the caprellid
species reared by Takeuchi at 208C. It can be
understood because growth and reproduction are
strongly affected by temperature in marine crusta-
ceans, causing a rapid growth at high temperatures
and a slower growth at low temperatures. However,
if generation length of C. grandimana at 178C is
compared with that of gammarids at 178C (Wildish
1972), such as Orchestia mediterranea (Costa, 1853),
Orchestia gammarellus (Pallas, 1766), or Orchestia
remyi roffensis (Wildish, 1969), C. grandimana has a
faster generation period than gammarids at the same
temperature. Takeuchi & Hirano (1991) reported
that generation length for gammarids was longer
than the average of four Caprella species examined
by them at 208C (C. danilevskii, C. okadai, Caprella
generosa (Arimoto, 1977), Caprella brevirostris
(Mayer, 1903)). They suggested that in the Caprel-
lidea the reason may be attributable to the lack
of abdominal appendages, which in the Gammar-
idea are used for producing respiration and for
swimming.
The number of offspring that finally emerged from
the brood pouch of C. grandimana in a single brood
was only five, increasing in successive instars with
the increase in body length of the female, reaching a
maximum of 15 juveniles. In other species, this
increase in number of eggs and offspring is also
associated with an increase in female size. However,
the number of offspring emerging from C. grand-
imana was very low compared with a maximum of
82 hatchlings produced by a single female of Caprella
mutica in a single brood (Cook et al. 2007), or
50 and 32, in C. danilevskii and C. okadai, respec-
tively (Takeuchi and Hirano 1992b). The differences
in body length of each instar of different species with
different body length probably plays an important
role in fecundity, where females with small bodies in
earlier instars of their cycle have fewer offspring than
longer females in late instar, and small species like
C. grandimana (4.2 mm) also have fewer offspring
than longer species like C. mutica (7 mm).
90 E. Baeza-Rojano et al.
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During the reproduction of mature females, it was
found that many ovigerous females lost or dropped
their eggs from the brood pouch. This also occurred
in other two species: C. mutica females showed a
decay or loss of eggs during the incubation period
when reared at very low temperatures (5�108C)
(Hosono 2009), and the number of juveniles that
finally emerged from the brood pouch of Caprella
laeviuscula was about half of the number of
eggs carried within the brood pouch. Caine (1991)
suggested that juveniles may have eaten some of the
unhatched eggs prior to emergence from the brood
pouch.
Even so, the survival rate of juveniles of
C. grandimana that finally emerged from the
brood pouch was very high at 94%, proving that
C. grandimana seems to be a resistant species that can
be reared in laboratory conditions, supporting un-
favourable conditions such as water quality produced
by ammonia build-up from excess food (Chen et al.
1990), low oxygen concentration in small containers,
or stress caused by the manipulation of individuals
during the study.
The results of this study have implications for
future development in ecotoxicological testing with
C. grandimana. This species is capable of growing and
reproducing in captivity, and this can represent the
first step in evaluating the effects of different con-
taminants upon the growth and reproduction of this
species. Furthermore, our study provides a baseline
for knowledge of the life span of the species and its
length of survival, growth rate, maturation time and
fecundity. As pointed out by Woods (2009), caprellid
amphipods are an overlooked marine finfish aqua-
culture resource and this kind of study dealing with
life history is essential to properly address applied
studies in the future.
Acknowledgements
Financial support of this work was provided by
the Ministerio de Educacion y Ciencia (Project
CGL2007-60044/BOS) co-financed by FEDER
funds, and by the Consejerıa de Innovacion, Ciencia
y Empresa, Junta de Andalucıa (Project P07-RNM-
02524). The first author was awarded a grant-in-aid
(BES-2008-004520) from the Ministerio de Ciencia
e Innovacion in support of the present study. Special
thanks to Angela Ruiz-Cortina for English revision
of the manuscript.
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