Embed Size (px)
Citation preview
This article was downloaded by: [Dalhousie University]On: 25 August 2012, At: 22:00Publisher: Taylor & FrancisInforma Ltd Registered in England and Wales Registered Number: 1072954 Registeredoffice: Mortimer House, 37-41 Mortimer Street, London W1T 3JH, UK
Journal of Natural HistoryPublication details, including instructions for authors andsubscription information:http://www.tandfonline.com/loi/tnah20
Natural history of Phyllomedusamegacephala (Miranda-Ribeiro, 1926)(Anura: Hylidae) in southeasternBrazil, with descriptions of its breedingbiology and male territorial behaviourFrancisco Fonseca Ribeiro de Oliveira a , Pedro Augusto GuimarãesNogueira b & Paula Cabral Eterovick aa Laboratório de Ecologia Evolutiva de Anfíbios e Répteis,Programa de Pós-Graduação em Zoologia de Vertebrados,Pontifícia Universidade Católica de Minas Gerais, Belo Horizonte,Minas Gerais, Brazilb Instituto Superior de Ciências da Saúde: INCISA/IMAM, BeloHorizonte, Minas Gerais, Brazil
Version of record first published: 10 Nov 2011
To cite this article: Francisco Fonseca Ribeiro de Oliveira, Pedro Augusto Guimarães Nogueira &Paula Cabral Eterovick (2012): Natural history of Phyllomedusa megacephala (Miranda-Ribeiro,1926) (Anura: Hylidae) in southeastern Brazil, with descriptions of its breeding biology and maleterritorial behaviour, Journal of Natural History, 46:1-2, 117-129
To link to this article: http://dx.doi.org/10.1080/00222933.2011.626127
PLEASE SCROLL DOWN FOR ARTICLE
Full terms and conditions of use: http://www.tandfonline.com/page/terms-and-conditions
This article may be used for research, teaching, and private study purposes. Anysubstantial or systematic reproduction, redistribution, reselling, loan, sub-licensing,systematic supply, or distribution in any form to anyone is expressly forbidden.
The publisher does not give any warranty express or implied or make any representationthat the contents will be complete or accurate or up to date. The accuracy of anyinstructions, formulae, and drug doses should be independently verified with primarysources. The publisher shall not be liable for any loss, actions, claims, proceedings,
demand, or costs or damages whatsoever or howsoever caused arising directly orindirectly in connection with or arising out of the use of this material.
Dow
nloa
ded
by [
Dal
hous
ie U
nive
rsity
] at
22:
00 2
5 A
ugus
t 201
2
Journal of Natural HistoryVol. 46, Nos. 1–2, January 2012, 117–129
Natural history of Phyllomedusa megacephala (Miranda-Ribeiro, 1926)(Anura: Hylidae) in southeastern Brazil, with descriptions of its breedingbiology and male territorial behaviour
Francisco Fonseca Ribeiro de Oliveiraa*, Pedro Augusto Guimarães Nogueirab
and Paula Cabral Eterovicka
aLaboratório de Ecologia Evolutiva de Anfíbios e Répteis, Programa de Pós-Graduação emZoologia de Vertebrados, Pontifícia Universidade Católica de Minas Gerais, Belo Horizonte,Minas Gerais, Brazil; bInstituto Superior de Ciências da Saúde: INCISA/IMAM,Belo Horizonte, Minas Gerais, Brazil
(Received 16 March 2011; final version received 19 September 2011; printed 10 November 2011)
The breeding biology and male territorial behaviour of the large-headed leaf-frog(Phyllomedusa megacephala) were studied in three temporary altitudinal streamslocated in the Cerrado biome of southeastern Brazil, during three consecutive years(2007–2009). Phyllomedusa megacephala showed significant sexual dimorphism,with females being bigger and heavier than males. Acoustic and physical interac-tions between males defending or not defending territories including amplectantand non-amplectant males, patrolling behaviour by males without established terri-tories, and triple amplexus were observed. Neither males nor females were observedusing visual cues when searching for mates. We found that males that were presentat breeding sites in previous years bred more successfully and maintained territorybetter.
Keywords: Anura; Phyllomedusa megacephala; behaviour; reproduction; terri-toriality
Introduction
The genus Phyllomedusa (leaf-frogs) comprises 32 species (Frost 2011) with neotropicaldistributions, and is represented by medium-sized frogs that occur in a great diversityof environments, from dense tropical jungles to gallery forests and tiny vegetation relicsalongside rivers and ponds. Phyllomedusinae exhibits a derived mode of reproductionwithin the hylid clade, with egg clutches deposited on leaves of vegetation above water;initial larval development takes place here and larvae are subsequently flushed by rain-fall to the water below. The evolution of terrestrial modes of reproduction is a commonpattern in many anuran lineages and is possibly related to decreased predation ratesupon eggs and early larval stages (Magnusson and Hero 1991).
The large-headed leaf-frog, Phyllomedusa megacephala (Miranda-Ribeiro, 1926),is a species belonging to the Phyllomedusa hypocondrialis group (Caramaschi 2006)and is found in the southern portion of the Espinhaço Mountain Range, in the stateof Minas Gerais, Brazil. It occurs in streams formed in altitudinal meadows above1000 m after heavy rains and therefore has a restricted reproductive period. Although
*Corresponding author. Email: [email protected]
ISSN 0022-2933 print/ISSN 1464-5262 online© 2011 Taylor & Francishttp://dx.doi.org/10.1080/00222933.2011.626127http://www.tandfonline.com
Dow
nloa
ded
by [
Dal
hous
ie U
nive
rsity
] at
22:
00 2
5 A
ugus
t 201
2
118 F.F.R. de Oliveira et al.
some studies have been carried out on the reproductive biology of some species of thisgenus (Jungefer and Weygoldt 1994; Vaira 2001; Abrunhosa and Wogel 2004; Wogelet al. 2005, 2006), there is a lack of data for P. megacephala in particular. Indeed, alack of general information regarding its natural history, population aspects, distri-bution and ecology has caused the IUCN to categorize this species as Data Deficient(IUCN 2011). Occasional observations on the species’ ecology and natural history canbe found in Eterovick (2003), Eterovick and Barros (2003) and Eterovick and Sazima(2004). Giaretta et al. (2007) described its advertisement call from a population atSerra do Cipó.
Population studies undertaken during more than one reproductive season arescarce for anuran species in general (e.g. Tejedo 1993; Skidds and Golet 2005), withonly a small number of published works to date from the Neotropics (e.g. Guimarãesand Bastos 2003; Giaretta and Menin 2004; Neckel-Oliveira and Gascon 2006; Wogeland Pombal Jr. 2007; Muniz et al. 2008).
In this study we aimed to evaluate several aspects of the natural history of P. mega-cephala, including its reproductive biology and behaviour in an area of altitudinalrocky meadows inside the Espinhaço complex, in the central portion of Minas Geraisstate, southeastern Brazil. We studied some of the species’ basic natural history traitsduring three consecutive reproductive seasons (during the months of November andDecember, from 2007 to 2009), such as mating and male territorial behaviours, malemating success and egg clutch parameters on three distinct populations located in threetemporary altitudinal streams.
Study area and methods
We studied populations of P. megacephala at three temporary streams located onaltitudinal rocky meadows, between altitudes of 1356 and 1441 m, at the Rio PretoState Park (RPSP; 43◦30.767’W, 18◦00.799’S; São Gonçalo do Rio Preto municipal-ity), a conservation area in the Cerrado biome at the Espinhaço Mountain Range,southeastern Brazil. The studied streams form following the first heavy rains, whichgenerally begin in the second half of October, at the start of the warm, wet season.The streams have rocky outcrops with riparian vegetation of herbaceous and bushystrata along their margins, which provide suitable sites for P. megacephala females tolay their eggs.
We walked the whole length of the section occupied by calling males of P. mega-cephala at each stream for two to four consecutive nights in each sampling period.These sections varied between 50 and 100 m. We mapped these stream sections andthen recorded the position of each individual found, including distance and heightfrom water and type of vegetation and substrate, with the aim of determining spa-tial distribution and territorial behaviour. We also recorded distance from the nearestindividuals, as well as the occurrence of male groupings. To evaluate site fidelity bycalling males, we compared their position along the stream on two or more consecu-tive nights. We considered a male to be territorial when it used the same calling sitefor two or more consecutive nights and defended it using territorial calls and physicalcombats.
We recorded egg clutch features (height and distance from stream margin). Fieldobservations always started after sunset and lasted until we could no longer registerand observe active individuals.
Dow
nloa
ded
by [
Dal
hous
ie U
nive
rsity
] at
22:
00 2
5 A
ugus
t 201
2
Journal of Natural History 119
Figure 1. Photographs taken during field work to show the colour patterns on the right flanksof Phyllomedusa megacephala for individual recognition. The figure shows pictures of twoindividuals.
We used two methods to mark the individuals. First, we photographed all individ-uals on their right flank (Figure 1) using a digital camera (a compact Canon
®model
Powershot A-630, with 4 × optical zoom) to try to identify them through the mottledpatterns along their flanks. This procedure proved to be very effective for distinguish-ing each individual, and did not seem to cause any physical harm or stress or interferewith individual fitness. To confirm the efficacy of this method, we also used toe clip-ping to mark frogs (n = 80) in the first breeding season. Toe clipping was adaptedfrom Martof (1953), with no more than two toes being clipped from one foot. We usedonly the feet for marking and never the hands, in an attempt to minimize decreases inmovement and hanging ability of the frogs.
We sexed all recorded individuals, measured them with callipers to the nearest1.0 mm and weighed them to the nearest 0.05 g using a Pesola
®scale. We calculated
the operational sex ratio (Emlen and Oring 1977) at each studied stream during eachreproductive season by dividing the number of females by the number of males.
We recorded any observation on the territorial behaviour of males and the matingbehaviour of P. megacephala. We observed any related behaviour until it was finished;i.e. until either all individuals involved left the site (in the case of breeding behaviour)or until one male departed from another male’s territory. We employed the focal andad libitum sampling methods to record behaviour (Altmann 1974; Martin and Bateson1993). We used headlamps with red light to minimize the chances of interfering withfrogs’ natural behaviour. Thirty-seven egg clutches were collected, preserved in 5%formalin and taken to the laboratory for egg counting and measuring. We presentquantitative data as (mean ± SD, n), and compare means using Student’s t-test.
Results
In all, 197 different individuals were recorded and photographed in the three studiedstreams during the three consecutive reproductive seasons (2007–2009). In addition,we recorded but did not photograph another four individuals (two males and twofemales), totalling 201 individuals (142 males and 59 females). In 40 observation nights(248 h) we accumulated 497 visual registers (including recaptures).
Dow
nloa
ded
by [
Dal
hous
ie U
nive
rsity
] at
22:
00 2
5 A
ugus
t 201
2
120 F.F.R. de Oliveira et al.
Sexual dimorphism was significant, with females longer [snout–vent length(SVL) Student’s t-test = 16.12, p < 0.001] and heavier (Student’s t-test = 13.74,p < 0.001) than males (Table 1). Operational sex ratios were 0.369 (2007 season), 0.264(2008 season) and 0.355 (2009 season). Operational sex ratio during the entire studyperiod was 0.415. There was a total of 82 male recaptures in 2008–09 compared withonly six female recaptures.
Males vocalized in distances from water varying from 0 to 6.5 m (0.56 ± 1.02,n = 269) and in heights varying from 0 (on the ground) to 2.1 m (0.75 ± 0.42,n = 269). However, most individuals were within 1 m (height and distance) of water(n = 221). We observed calling activity before the formation of breeding sites (sec-ond half of October), when males emitted territorial calls and started establishingterritories. However, we did not gather quantitative data on this period.
Male territorial behaviourThirty-three males displayed territorial behaviour during the entire study period(moving less than 2 m from their first recorded position on successive samplingnights). Males called from the same sites for two or more consecutive nights (werecorded male permanence up to four nights, corresponding to the maximum num-ber of successive sampling nights at the same stream) and interacted agonistically(acoustically or physically). The “patrolling behaviour” (sensu Wogel et al. 2005) wasalso observed for some males (n = 27, Table 2), which tended to walk amidst thevegetation and so were observed in many different sites on consecutive nights. Malesthat successfully defended territories were not significantly different in SVL (Student’st-test = 1.24, p = 0.08) or bodyweight (Student’s t-test = 1.13, p = 0.12, Table 1) fromnon-resident males.
We observed eight territorial contests (Figure 2A). On six occasions physicalcombats between resident and intruder males occurred. There were two acoustic-only interactions, with both males standing near to each other, emitting territorialcalls. These contests occurred inside a male’s territory, in stream sections with manypotential egg-laying sites (dense herbaceous and shrub vegetation). The physical con-frontations lasted from about 3 minutes to a maximum of 21 minutes. They involvedgrasping and pushing each other over the cephalic region or over the arms with theuse of both hands, while hanging over the vegetation. All observed physical con-tests started with the intruder male slowing approaching the resident male’s territorywhile the resident stood on the vegetation and started emitting territorial calls tothe intruder. Then two possible behaviours occurred. In four cases, the intruder malestayed amidst the vegetation, within 1 m of the territorial male and also started emit-ting territorial calls. The duration of these acoustic confrontations varied from 12 to57 minutes, after which physical combat took place. In the other two cases, malesimmediately engaged in physical confrontation.
Three of these contests with previous acoustic confrontation happened more thanonce (two to four times) spaced by 20 seconds to 16 minutes. During all observa-tions, the resident male succeeded in staying on its calling site, with the intrudermale retreating to a greater distance sometime (12 to 32 minutes) after the end of theconfrontation.
Dow
nloa
ded
by [
Dal
hous
ie U
nive
rsity
] at
22:
00 2
5 A
ugus
t 201
2
Journal of Natural History 121
Tab
le1.
Snou
t–ve
ntle
ngth
(SV
L,m
m)a
ndbo
dym
ass
(BM
,g)
ofP
hyllo
med
usa
meg
acep
hala
mal
esan
dfe
mal
esfr
omth
ree
stre
ams
atth
eR
ioP
reto
Stat
eP
arqu
ein
Min
asG
erai
s,so
uthe
aste
rnB
razi
l.
Mal
esF
emal
esR
ange
tp
nM
ean
+SD
Ran
gen
Mea
n±
SD
SVL
142
39.9
4±
1.86
36.5
–44.
5SV
L59
46.0
9±
2.67
43.5
–60.
216
.12
<0.
001
BM
142
5.18
±1.
163.
0–6.
5B
M59
9.01
±1.
665.
0–10
.013
.74
<0.
001
Mat
edm
ales
Unm
ated
mal
es
nM
ean
±SD
Ran
gen
Mea
n±
SDR
ange
tp
SVL
1341
.12
±1.
9437
.5–4
4.5
SVL
128
39.0
1±
1.83
35.2
–43.
21.
360.
17B
M13
6.22
±1.
353.
0–9.
0B
M12
85.
05±
1.16
3.5–
7.0
2.54
0.35
Mal
esw
ith
terr
itor
yM
ales
wit
hout
terr
itor
ies
nM
ean
±SD
Ran
gen
Mea
n±
SDR
ange
tp
SVL
3341
.05
±1.
8536
.8–4
4.5
SVL
9840
.2±
1.58
35.2
–43.
61.
240.
08B
M33
5.2
±1.
23.
5–8.
0B
M98
4.93
±1.
143.
0–7.
01.
130.
12
Not
es:S
VL
and
BM
valu
esar
egi
ven
for
mat
edm
ales
they
are
show
non
lyfo
rth
em
ale
next
toth
efe
mal
ein
the
case
oftr
iple
ampl
exus
.
Dow
nloa
ded
by [
Dal
hous
ie U
nive
rsity
] at
22:
00 2
5 A
ugus
t 201
2
122 F.F.R. de Oliveira et al.
Table 2. Number of males of Phyllomedusa megacephala recorded during three consecutiveyears (2007–2009) at streams at the Rio Preto State Park.
Year Malesobserved
(n)
Firstcaptures
(n)
Recapturesfrom 2007
(n)
Recapturesfrom 2008
(n)
Territorialmales (n)
Patrollingmales (n)
Matedmales (n)
2007 60 66 – – 10 (2007) 6 (2007)2008 72 31 42 – 7 (2007); 7 (2008) 4 (2007);
3 (2008) 1 (2008)2009 85 45 25 15 6 (2007); 5 (2008); 2 (2007);
5 (2008); 15 (2009) 1 (2009)2 (2009)
Total 217 142 67 15 33 27 14
Note: The years shown in parenthesis relate to the first record of the males considered.
On three such occasions, we observed the presence of a static gravid female amidstthe vegetation inside the resident male’s territory. On two occasions, the female stoodover a broad leaf, folding it with its arms in amplexus position; amplexus occurred withthe resident male after the male–male confrontation. In one observation, following aphysical contest, the resident male climbed into amplexus position over the intrudermale, which stood over the vegetation. This behaviour lasted for about 25 minutes,then the intruder male walked away and resumed emitting territorial calls.
Resident males in any given year were likely to have been recorded the previ-ous year. Patrolling males with no established territories were less likely to have beenrecorded previously (Table 2).
Description of mating behaviourAmplectant individuals were observed 13 times. Five of these records involved anamplectant trio (two males and one female, Figure 3) and eight involved an amplectantpair. All amplectant individuals were measured (SVL) and weighed. Amplectant maleswere not significantly different in length (SVL) (Student’s t-test = 1.36, P = 0.17) orbodyweight (Student’s t-test = 2.54, p = 0.35) from non-amplectant males. In addi-tion, on three occasions when amplectant trios were observed (once in 2008 andtwice in 2009) the second male had been previously marked in the 2008 breedingseason, whereas the first male (the one directly above the female) was marked in2007. The use of visual cues by males or females when searching for mates was notobserved.
The mating behaviour of P. megacephala, including the whole sequence ofbehaviours from male–female encounter to egg laying, was observed six times dur-ing the study period (Figure 2B). In all observations, the female approached one ormore calling males, which were close together amidst the vegetation. The female thenstayed motionless for a varied period of time (from 6 to 44 minutes, n = 4) thenmoved to fold a leaf or immediately climbed on and folded a nearby leaf (n = 2).Following this, when only one male was present, it immediately approached thefemale and started an axillary amplexus (n = 2). When two or more males were
Dow
nloa
ded
by [
Dal
hous
ie U
nive
rsity
] at
22:
00 2
5 A
ugus
t 201
2
Journal of Natural History 123
Figure 2. (A) Summary of the events observed as part of the territorial behaviour ofPhyllomedusa megacephala males. (B) Summary of the events observed as part of the breedingbehaviour of P. megacephala.
Dow
nloa
ded
by [
Dal
hous
ie U
nive
rsity
] at
22:
00 2
5 A
ugus
t 201
2
124 F.F.R. de Oliveira et al.
Figure 3. Triple amplexus in Phyllomedusa megacephala, with two males on top of a female.
Dow
nloa
ded
by [
Dal
hous
ie U
nive
rsity
] at
22:
00 2
5 A
ugus
t 201
2
Journal of Natural History 125
involved, two behaviours could occur. First, the males stood in their calling sites,emitting territorial calls without any movement. The duration of these contests was6 to 28 minutes, after which one of the males moved and entered amplexus withthe female (n = 3). In the second situation, one of the calling males immediatelyformed amplexus with the female as she first folded a leaf (n = 1). In one observation,an amplectant couple formed amplexus with another amplectant couple positionednearby, after finishing egg laying (the amplectant female which had just ended egg lay-ing climbed onto the back of another amplectant male). They formed therefore anamplectant quartet for about 112 minutes, after which the climbing couple (whichfirst finished egg laying and then moved upon the other couple) moved away andthe other couple continued in amplexus. However, before the end of this quartet, apatrolling male also joined amplexus, climbing over the upper male’s back, formingthus an amplectant quintet. This amplected male from the upper couple immedi-ately started emitting release calls, with the patrolling male leaving the quartet after38 minutes.
During most observations, one or more (up to five) adjacent males tried to disrupta couple (n = 4). They tried to end amplexus in two ways (Figure 2B). In the firstscenario the intruder tried to physically disrupt the amplectant male by pushing itaway from the female’s back. In general, when that happened, both males engaged inphysical combat, which lasted from 5 to 13 minutes (n = 3). On two occasions, theamplectant male succeeded in pushing away the intruder and immediately re-enteredamplexus. On another occasion, both the amplectant and intruder males stayed nearbythe female, emitting advertisement calls and the amplexus did not restart. The intrudermale was never observed successfully disrupting the amplectant male and taking overits place in the amplexus. In the second scenario, the intruder male did not attemptphysical combat, but rather tried to spawn with the couple, climbing over the male’sback (n = 1, Figure 3).
On some occasions (n = 2), in the presence of other nearby males, the amplectantpair started moving away following the beginning of the amplexus, and the femaleactively searched for another broad leaf to hang up and fold. These movementswere sometimes followed by falls of the couple, scarring the dorsal region, limbsand head. After falls, non-amplectant males followed the couple, and stayed nearbyemitting advertisement calls (n = 1) or tried to disrupt the amplectant pair again(n = 1).
Egg clutches were deposited at heights that varied from 0.1 to 1.8 m (0.69 ± 0.40,n = 31) above water and at distances from 0 to 1.5 m (0.25 ± 0.58, n = 31) fromthe margins. Total number of eggs per clutch varied from five to 52 and the numberof gelatinous spheres adhered to the clutch varied from 165 to 2150. Fertilized eggswere yellow-cream when alive, with mean diameter of 4.44 mm (± 0.63, n = 215). Allcounted clutches had larvae in stages one to 18, following the classification of Gosner(1960) (n = 37). Another two collected clutches had well-developed larvae at stages23 and 24.
We observed egg laying five times, with total deposition period varying from 43 to192 minutes. Although we did not observe laying of more than one egg clutch percouple in a single night, it is possible that the same female bred with the same maleon consecutive nights. This pattern is proposed because we observed several clutches(two to six) on the same plant stems (n = 8) present within a male’s territory, wherethe same female was encountered for two or more consecutive nights (n = 3).
Dow
nloa
ded
by [
Dal
hous
ie U
nive
rsity
] at
22:
00 2
5 A
ugus
t 201
2
126 F.F.R. de Oliveira et al.
Discussion
Some observed behavioural and breeding aspects were similar to all studies with otherPhyllomedusa species, such as the occurrence of physical contests between males andthe oviposition of a great number of gelatinous capsules around fertilized eggs insidethe leaf nests, which probably function to create a microenvironment provided withhumidity, as well as a protection against UVB radiation (Pyburn 1980; Woehl Jr. andWoehl 2000; Wogel et al. 2005).
The limited availability of foraging, courtship and oviposition sites have been pro-posed to influence the evolution of territoriality in frog lineages (sensu Wells 1977).In this study we observed that resident males were always successful in maintain-ing their territories against intruder males. Matos et al. (2000) and Vaira (2001) alsoregistered the superiority of resident males in territorial contests for Phyllomedusahypochondrialis and Phyllomedusa boliviana, which won all observed contests. Thispattern occurs in other anuran lineages. Toledo and Haddad (2005) found that res-ident males of Scinax fuscomarginatus were competitively superior to other males.In contrast, Abrunhosa and Wogel (2004) observed that some intruder males ofPhyllomedusa burmeisteri were successful in winning physical combats. As a generalrule, many distinct anuran clades evolved different acoustic and physical strategiesas responses to intra-specific competition, such strategies contributing to breedingsuccess (Wells 1977).
It has been proposed that a higher level of male aggression and consequentlyhigher success in maintaining territories is the result of higher levels of testosteroneproduced by individuals that arrive first at the reproductive sites (Wogel et al. 2002).Establishment of territories by males before the beginning of breeding activity is a pat-tern that has been observed in other species of the P. hypochondrialis group (Matoset al. 2000), as well as in another neotropical frog genus (Dendropsophus, Bastos andHaddad 1996), with longer breeding seasons. However, given the short reproductiveperiod of P. megacephala (FFRO, personal observation) and consequently the syn-chronous arrival of individuals on reproductive sites, another pattern is proposed toexplain the higher success of territorial and mated males on this study. The elevatedrecapture rate of frogs in the present study (n = 88 individuals in 128 registers) denotesa prolonged lifespan for sexually active individuals, as we observed that a large pro-portion of individuals survived for at least three seasons. In fact, the higher malerecaptures (n = 82 individuals) compared with female recaptures (n = 6 individu-als) possibly denotes a higher male survivorship or an easier male detection by activesearch because of territorial behaviour. Older individuals may become better com-petitors after gaining experience and overcoming natural selection (through survivingsuccessive seasons) and therefore achieve an increased fitness, possibly explaining thesuccess of individuals marked earlier in the study in relation to younger frogs. We foundthat males recorded in the first year successfully maintained their territories and weobserved them mating more compared with males first recorded in 2008 and 2009(Table 2).
Some other patterns of male territoriality seem to be conservative among distinctclades of Phyllomedusa species. Abrunhosa and Wogel (2004) also observed that malecontests in P. burmeisteri started with intruder males approaching the resident’s ter-ritory, when the latter started emitting territorial calls. Wogel et al. (2005), studyingPhyllomedusa rohdei, postulated that a higher male breeding success was the resultof calling longer, as well as active search for females (patrolling behaviour). Indeed,
Dow
nloa
ded
by [
Dal
hous
ie U
nive
rsity
] at
22:
00 2
5 A
ugus
t 201
2
Journal of Natural History 127
we also observed the occurrence of patrolling males without established territoriesfor P. megacephala. We found that patrolling males were in most cases individualsmarked during later breeding seasons, possibly denoting again the influence of com-petitive capacity and age in determining territory establishment and mating success.Only once (in the 2009 breeding season) a patrolling male was found to mate success-fully, and this was an individual marked in the 2007 breeding season. The occurrenceof patrolling behaviour and of active searching for females has been recorded for otherPhyllomedusa species (Matos et al. 2000; Vaira 2001). However, Rodrigues et al. (2007)observed this behaviour neither for Phyllomedusa azurea (also of the P. hypochondrialisgroup) nor Phyllomedusa sauvagii. We observed three intruder males successfully dis-rupt an amplectant couple. Matos et al. (2000) observed that intruder males could notdisrupt amplexus in P. hypochondrialis, possibly denoting a greater competitive abilityfor territorial males in this species.
The occurrence of triple amplex has been recorded in other Phyllomedusa species(Woehl Jr. and Woehl 2000 for P. distincta; Wogel et al. 2005 for P. rohdei) althoughVaira (2001) did not observe this behaviour for P. boliviana. Woehl Jr. and Woehl(2000) reported the fertilization of egg clutches by both males, although genetic testswere not conducted for confirmation of these results.
Vaira (2001) noted a short duration for egg laying in P. boliviana (less than30 minutes). We recorded much longer oviposition for P. megacephala, possibly relatedto the occurrence of a single (maybe partial) oviposition event per night. A singlefemale may be breeding with the same male more than once, given the presence ofobserved (gravid) females inside a male’s territory for two or more continuous nights.Alternatively, it is possible that a male may be mating with more than a single femaleduring a short timespan, because several egg clutches were observed on the same plantstems within some males’ territories. Woehl Jr. and Woehl (2000) observed during a3-week period that a single male mated with five different females that entered itsterritory.
Vaira (2001; for P. boliviana); Neckel-Oliveira and Wachlevski (2004; forPhyllomedusa tarsius) and Rodrigues et al. (2007; for P. sauvagii) found that femalesmay use two or more leaves to fold and build a nest, possibly reducing predation ofegg clutches (Neckel-Oliveira and Wachlevski 2004), a pattern not observed in thepresent study, where females always used only one leaf. Wogel et al. (2005; for P. rohdei)and Rodrigues et al. (2007; for P. azurea) also observed nest construction with onlya single leaf, a pattern which may also be reflective of the P. hypochondrialis group.As for P. rohdei (Wogel et al. 2006) we found that P. megacephala did not show lekkingbehaviour, as oviposition sites were located inside the calling territories of males.
Rodrigues et al. (2007) postulated that a greater reproductive effort is accomplishedin small bodied species for vertebrates in general, which tend to live for only one repro-ductive season. We found that individuals of P. megacephala live for at least threereproductive seasons, but longevity alone is not enough to assess the fertility rates ofa given species. Another possible factor influencing reproductive effort is reproductionduration on a seasonal scale. The two species studied by Rodrigues et al. (2007) –P. azurea and P. sauvagii – had a longer breeding season than P. megacephala, whichin turn bred for more years.
In conclusion, P. megacephala can be classified as having an intermediate repro-ductive strategy in between the extremes defined by Wells (1977), regarding explosiveand continuous breeders, where the synchronous arrival of both males and females at
Dow
nloa
ded
by [
Dal
hous
ie U
nive
rsity
] at
22:
00 2
5 A
ugus
t 201
2
128 F.F.R. de Oliveira et al.
the reproductive sites and active female search by males are typical aspects of explo-sive breeding species, and the maintenance and high fidelity to established territoriesby males is typical of continuous breeders.
Acknowledgements
This research was financially supported by the Fundo de Incentivo à Pesquisa (FIP) ofthe Pontifícia Universidade Católica de Minas Gerais, and the Conselho Nacional deDesenvolvimento Científico e Tecnológico (CNPQ). We would like to thank the InstitutoBrasileiro de Meio Ambiente e Recursos Naturais Renováveis (IBAMA), as well as the InstitutoEstadual de Florestas (IEF) for providing the permits for capture and collection of specimensin the field (15330-2 and 15330-3). Special thanks to the two anonymous reviewers for their sug-gestions on this manuscript. Additional thanks to the whole team of the Rio Preto State Park,which provided important logistical support, and to I. Ottoni, R. Campos, and Juan Espanha,for their help during fieldwork. A Research Productivity grant (301077/2010-0) was provided toP. C. Eterovick by CNPq.
References
Abrunhosa PA, Wogel H. 2004. Breeding behaviour of the leaf-frog Phyllomedusa burmeisteri(Anura: Hylidae). Amphibia-Reptilia 25(2):125–135.
Altmann J. 1974. Observational study of behaviour: sampling methods. Behaviour 49(3/4):227–267.
Bastos RP, Haddad CFB. 1996. Breeding activity of the Neotropical Treefrog Hyla elegans(Anura, Hylidae). J Herpetol. (30)3:355–360.
Caramaschi U. 2006. Redefinição do Grupo de Phyllomedusa hypocondrialis com Redescrição dePhyllomedusa megacephala (Miranda-Ribeiro, 1926), Revalidação de Phyllomedusa azureaCope, 1862 e Descrição de uma Nova Espécie (Amphibia, Anura, Hylidae). Arquiv MusNacl, Rio de Janeiro. 64(2):159–179.
Emlen ST, Oring LW. 1977. Ecology, sexual selection, and the evolution of mating systems.Science. 197:215–223.
Eterovick PC. 2003. Distribution of anuran species among montane streams in south-easternBrazil. J Trop Ecol. 19:219–228.
Eterovick PC, Barros IS. 2003. Niche occupancy in south-eastern Brazilian tadpole communitiesin montane–meadow streams. J Trop Ecol. 19:439–448.
Eterovick PC, Sazima I. 2004. Anfíbios da Serra do Cipó – Amphibians from the Serra do Cipó,Minas Gerais, Brasil. Belo Horizonte, Brazil: Ed. PUC Minas.
Frost D. 2011. Amphibian Species of the World, 5.4, An Online Reference [Internet]. Availablefrom research.amnh.org/herpetology/amphibia/index. Accessed on 9 February 2010.
Giaretta AA, Menin M. 2004. Reproduction, phenology and mortality sources of a species ofPhysalaemus (Anura: Leptodactylidae). JNat Hist. 38:1711–1722.
Giaretta AA, Oliveira Filho JC, Kokubum MN. 2007. A new Phyllomedusa Wagler (Anura,Hylidae) with reticulated pattern on flanks from Southeastern Brazil. Zootaxa 1614:31–41.
Gosner KL. 1960. A simplified table for staging anuran embryo and larvae with notes onidentification. Herpetologica 16:183–190.
Guimarães LD, Bastos RP. 2003. Vocalizações e Interações Acústicas em Hyla raniceps(Anura, Hylidae) Durante a Atividade Reprodutiva. Iheringia, Sér. Zool. Porto Alegre.93(2):149–158.
IUCN 2011. International Union for Conservation of Nature and Natural Resources. TheIUCN red list of threatened species. Available at: www.iucnredlist.org. Accessed on 13March 2010.
Dow
nloa
ded
by [
Dal
hous
ie U
nive
rsity
] at
22:
00 2
5 A
ugus
t 201
2
Journal of Natural History 129
Jungefer KH, Weygoldt P. 1994. The reproductive biology of the leaf frog Phyllomedusa lemurBoulenger, 1882, and a comparison with other members of the Phyllomedusinae (Anura:Hylidae). Rev Franc Aquariol. 21:57–64.
Magnusson EW, Hero JM. 1991. Predation and the evolution of complex oviposition behaviourin Amazon rainforest frogs. Oecologia 86:310–318.
Martof BS. 1953. Territoriality in the green frog, Rana clamitans. Ecology 34:165–174.Martin P, Bateson P. 1993. Measuring behaviour: an introductory guide. 2nd ed. New York:
Cambridge University Press.Matos RHR, Andrade GV, Hass A. 2000. Reproductive biology and territoriality of
Phyllomedusa hypocondrialis in Northeastern Brazil. Herpetological Review 31 (2) : 84–86.Muniz KPP, Giaretta AA, Silva WR, Facure KG. 2008. Auto-ecologia de Hypsiboas albopuncta-
tus (Anura, Hylidae) em área de Cerrado no sudeste do Brasil. Iheringia, Sér. Zool., PortoAlegre. 98 (2) : 254–259.
Neckel-Oliveira S, Wachlevski M. 2004. Predation on the arboreal eggs of three species ofPhyllomedusa in Central Amazônia. J Herpetol. 38:244–248.
Neckel-Oliveira S, Gascon C. 2006. Abundance, body size and movement patterns of a trop-ical treefrog in continuous and fragmented forests in the Brazilian Amazon. Biol. Con.128:308–315.
Pyburn WF. 1980. The function of eggless capsules and leaf in nests of the frog Phyllomedusahypochondrialis (Anura: Hylidae). Proc Biol Soc Wash. 93:153–167.
Rodrigues DJ, Uetanabaro M, Lopes FS. 2007. Breeding biology of Phyllomedusa azurea Cope,1862 and P. sauvagii Boulenger, 1882 (Anura) from the Cerrado, Central Brazil. J Nat Hist.41(29–32):1841–1851.
Skidds DE, Golet FC. 2005. Estimating hydroperiod suitability for breeding amphibians insouthern RhodeIsland seasonal forest ponds. Wetlands Ecol Manag. 13:349–366.
Tejedo M. 1993. Do male Natterjack toads join larger breeding choruses to increase matingsuccess? Copeia (1):75–80.
Toledo LF, Haddad CFB. 2005. Reproductive biology of Scinax fuscomarginatus (Anura,Hylidae) in south-eastern Brazil. J Nat Hist. 39:3029–3037.
Vaira M. 2001. Breeding biology of the leaf-frog (Phyllomedusa boliviana (Anura, Hylidae).Amphibia-Reptilia 22:421–429.
Wells KD. 1977. The social behavior of anuran amphibians. Anim Behav. 25:666–693.Woehl Jr G, Woehl EM. 2000. Pererecas protetoras da Mata Atlântica sob ameaça. Ciênc Hoje
28 (164) : 72–74.Wogel H, Abrunhosa PA, Pombal JP Jr. 2002. Atividade Reprodutiva de Physalaemus signifer
(Anura, Leptodactylidae) em Ambiente Temporário. Iheringia, Ser Zool. Porto Alegre.92(2):57–70.
Wogel H, Abrunhosa PA, Pombal JP Jr. 2005. Breeding behaviour and mating suc-ces of Phyllomedusa rohdei (Anura, Hylidae) in south-eastern Brazil. J Nat Hist.39(22):2035–2045.
Wogel H, Abrunhosa PA, Pombal JP Jr. 2006. Chorus organization of the Leaf-FrogPhyllomedusa rohdei (Anura, Hylidae). Herpetol J. 16:21–27.
Wogel H, Pombal JP Jr. 2007. Comportamento reprodutivo e seleção sexual em Dendropsophusbipunctatus (Spix, 1824) (Anura, Hylidae). Papéis Avuls Zool. 47(13):165–174.
Dow
nloa
ded
by [
Dal
hous
ie U
nive
rsity
] at
22:
00 2
5 A
ugus
t 201
2
