Reproductive behavior of Cycloramphus dubius Miranda-Ribeiro (Amphibia, Anura, Leptodactylidae)

REPRODUCTIVE BEHAVIOR OF CYCLORAMPHUS DUBIUS

MIRANDA-RIBEIRO (AMPHIBIA, ANURA, LEPTODACTYLIDAE)

Ariovaldn A. Giart'tta I Adan J. Cardoso I

ABSTRACT. L~\'cI(I"(I",pJllIs clilhitts Mirallda-Rih~if(l. 1421l i~ a fn't! ~p~\.:il.!s fnlm

th...: "':\)(Islal Atlanti..: Fnfl.!st inSuulh...:ash:rll Bra/.il. 1I11sl.!~\\'ah:rf~dls\,rrllrl.!sh:d rivtlkt~

as hr...:...:ding sih!s. Thl.! ...:gg~ ar...: plal.'...:d llut:-.iLi...: .,1' wakr. h...:1\\"':"':11 rlll.:k ...:r...:\,ir.:...::-. 1)1'

fllots ..:nnstantly wdh:d hy wakr dripr'ing. CIUh:h...:s hav...: ahlnil nO I.!!!g's. and th...:

tadpnl\..'s !!t"I)\\' attal.:lh.:d tu rn..:ks. llut nl" wakr. t\lak~ ill" thi:-. ~Ih:...:i...:~ I.!\hihit par"':l1tal ,:arl.!, hiting aml/nr pushing a\\'a: strallt!1.! nhj...:\.'\:-. apprna .. :hint! th...: I.!c!t! 1lla:--~...::--. T\\(l

t)p...:s nf call:-. ",...:r...: idl."lltili...:d in th...: srh.!dnlgrams. Th...: "ad, ...:rtis"':1ll...:nt ..:all'" \,."lll:-.i:-.1 nfjllxtapns...:d puls...::-. lasting 200m:--: th...: "aggr..::-..:-;i\'..: I.: a 1(:,," . al~() hav~ Ih..: ~ht\rI J'ul:-...:~ slru...:tllf':. and la:--I aruuml 30()m:-.. Th..: (It!1:!I\::--:--i\o,! ...:aI1:-. ar..: I.!lllilt..:d durill~ h.:rrililrial illva~i(\Il.

KEY W( )RDS. Amphihia. Anura. Atlanti...: Fur..:st. hr..:~diJlt! :-it..:. krritnrialit:.

par..:ntal ...:ar..:

Species of the genus Cyc/orlllllpitll.l Tschudi. IS)8 are restricted to the

coastal Atlantic Forest. Brazil (HEYER 19S)), MIRANDA-RIBEIR() (102()) relnred

to direct development in two uncertainly determined spec'les of ('vcIIJ/w 1/1 ,I, 11,1 , LUTZ (1929) descrihed the reproductive heha\'ior of ('Vc/IIIWIII,IIII,I' hl'll,l'ili('l/.li,1

Steindachner. IS64, Besides these aJK'ient and hrief studies many ddails of the

reproductl\'e traits of the species of the genus ("c/lIl'lIlIlpllll,1 reillain UnKIH1\\'n.

Herein are desnlhed ~ome reproductive charal'teristlcs. as paternal care and

territorial heha\'ior, of CYc/Ii/'{//IIIJIIII.I' dllhill.l' (M Ir,-Rih,. 1920),

AREA DESCRIPTION AND METHODS

A populalion of CVc/Ii/'{//IIIJIIII.I' dllhill,l' was studied on a "Illall trihutary (ll

the Rio Quilolllho, Santos municipality. Sao Paulo State. Brazil (n"41'S

-46" IS·W). at different times from 19S8 to 1091, The local is typical Atlantic' Rain

Forest (SOm elevation. 3.400mlll nlln/year), The streams where the species lives

have a sandy or granite rock hed, They undergo large and sudden alterations in

volume hy local rain events, hut. under normal conditions. are ahout 20 CI11 in

depth and 1.4 m wide. In the field. it was performed Jirect ohservation on calling

and offspring guarding males, In order to study males aggressive heha\'ior, some

egg masses was touched with sticks and introduced foreign living indi\'iduals of

I) D..:partam":lltn d..: ZUI)ln!!ia. Univ..:rsidad..: E:-.tadllal d..: CltlllpinClS. C'ai'\CI PI):-.tal 61()lJ. 13(IX3 47() Caillpinas. San Pauh). Brasil.

234 GIARETTA & CARDOSO

the same species was introduced in previously occupied sites. Males also were tested in response to call playback. One clutch was collected and kept in a terrarium under laboratory observation. Vocalizations were recorded with a UHER 4000 IC

set at 19cm/s, and spectrograms were made using a Sound Spectrograph series

MD-700 from Voice Identification Inc .. A voucher specimen is housed at the Museu de Historia Natural, Universidade Estadual de Campinas (ZUEC 6690).

Fig. 1. Environment and life stages of Cycloramphus dubius; (A) adult male (ca. 48mm); (8) waterfall in the study site used by the species for reproductive activities; (C) tadpole

on a wet rock surface (ca. 29mm); (D) clutch guarded by an adult male (photo by E.

Ramirez).

RESULTS

Male

Cycloramphus

dubius

(Fig. lA) are about 46mm long and tlattened dorso-ventrally. Small noisy waterfalls (Fig. IB) are used by the species as breeding sites. Reproductive activity of the species occurs throughout the year, as

indicated by the presence of calling males, clutches and tadpoles. Clutches (Fig.

I D) were found in narrow crevices of rocks and between roots. All 16 clutches

found were outside of water, in places with constant water dripping or waterfall

spray, but never in places subject to washing by water flow. Clutches contain 30 to 80 eggs (X=60.3; SD=22.7; N=4). The eggs are deposited in a single layer, weakly adherent to the substrate and to one another. The yolk portion of the eggs

is cream color and measures about 3mm in diameter, each egg having a transparent

gelatinous-like capsule. The occurrence of gelatinous spheres without yolk (nurse eggs) and unfertilized eggs in the clutch is common. Embryos develop within the

egg capsules until stage 25 (GOSNER 1960), when they reach about ! 9111111. The

Reproductive behavior of Cycloramphus dubius ... 235

taupoles of C. dllhills (Fig. I C) were founu out of water, feeding ahovt' wd rocks.

From the 16 clutches encountereu, 15 hau a male sitting hy the side (Fig.

1 D). The males remaint'd with their eggs hoth day ami night. In the field two tests was performed with males that were near their clutches: I) a l'loth tied to the t'nd

of a stick was hung over a clutch. The male, uistant 10cm away . .iumpeu on to the

cloth, hit anu pusheu it away. Ahout half the clutch was colleckd anu the male

was expelled. On the t()lIowing day a male, prohahly the same one. was guaruing

the remaining eggs and. also at this time. responded aggressi\·e!y. hiting the cloth

on the stick. 2) It was introduced, separately. males near a guardeu clutch. One

of the introuuced males .iumped in the uirection of the l'lutch anu the guardian

reacteu hy emitting vocalizations (Fig. 2E) and engaged in a fight. When it was

inuuceu a foreign male to approach another resident male without eggs. the resiuent

reacteu hy emitting calls (Fig. 2E), hiting and pushing the intruuer away. Adult

males vocalize at night from rock crevices of the waterfalls. whereas uiurnal

vocalizations are rare. Tht' advertisemt'nt calls (Fig. 2A-D) or C dllhills is emitku

with an average rate of one l'all every 25 seconds. EaL'ilnllte l'()n~I~Il'U ofjuxtapost'd

pulses lasting ahout 200ms. During call emission. there is a disCJ't'le modulation

of the highest frequencies. The first pulse has a frequency range hetwet'n 1.2 and

3.lkHz: the last pulse has a lower frequency range hd\veen 1.5 and 2.3kHz.

Although the call resemhles a pure sound structure. it consists or pulses scparateu

hy wry short time intervals. The intervals hdwet'n tht' pulses are irregular (1.2

to 3.8ms). with marked variahility in the lower note frequenl'it's (Fig. 2A.C). The

call emitted hy a guardian when disturheu hy the introUUL'lion of another male into

its rol'k L'1'evice was characterized hy a Illultipulseunote with longer duration and

wiuer handwidth frequency (Fig. 2E), which was interpreteu as an aggressive call.

These vocalizations consist of calls given at a faster rate (around 1.2 seconds

hetween the calls) than the advertisement call: the pattern of emission appears to

he relateu to the degree of aggressi\'eness of the emitter. The uuration of the

aggressive call is arounu 300ms and the pulses are eillitted in ascendant frequencies

hetween 1.0 and 2.0kHz. In response to playhack of the aggressi\'e l'alls a guardian

emitted longer notes. in a faster rhythm: arounu400ms durati()n with ahout 700ms

hetween notes (Fig. 2F).

DISCUSSION

Some reproductive characteristics desnihed for Crc/(}I'IIIII/!/III.I' h/'{/si/i(,II.I'i,·

hy LUTZ (1929) are similar to those of (\'c/OI'lIlIl/,/iIiS dllhills. Including cgg laying

sites and clutch size. LUTZ (1972) hridly wrote ahout the genus (\d(}I'IIIII/I/IIIS:

"the large ((mns lay the spawn on the ledges of rocks and the male parent guard~

it". WELLS (1981) considereu parental l'are hehavior in frog~ as unU)Jllmon and.

in gt'neral. related to the terrestrialislll of pre-mdaillorphil' devel()pmental phases. mainly in tropical regions. Terrestrial salamanders with parental care. generally. have large eggs. low fecundity and an enhanced emhryonil' pcriod. Among them. hehavior such as parental care could reduce thc risk oremhryo I()ss during the long

emhryonic period (NUSSBAlJN & SrHULTZ 1989). Thcse statements could alsll he

kHz 236 4 A 2

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GIARETTA & CARDOSO

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Fig. 2. Spectrograms of the vocalizations of Cyc/oramphus dubius. lA-D) Different physical

structures of advertisement call found in the population; IE) aggressive calls emitted by a

resident male in presence of another male; IF) aggressive calls emitted in response to

playback of aggressive calls. The irregular marks of sounds up to 3.7kHz represent waterfall

noise. Air temperature 19°C. water 17"C.

true for

C.

dubius as evidenced by the simjlarities in egg/clutch size and

developmental characteristics. In

C.

dubills, as well as many species with paternal

care, the males also exhibit territorial behavior (WILLIAMS 1975). A general

characteristic of frog territorial behavior is the guarantee of access to limited

resources (WELLS 1977). Suitable laying sites appear to be a limjted resource for

C.

dub ius because, in spite of the numerous crevices between rocks, the majority

of them became inundated during rains or are outside of splash zones. The

advertisement calls of

C.

dub ius studied were similar to those described by HEYER

& MELLO (1979), later considered by HEYER (1983) as Cycloramphlls

bora-ceiellcis. The advertisement call is quite variable in some parameters. The

aggressive calls are also variable and are influenced by the behavioral context,

such as the presence of intruding males. ROSE

&

LEMON (1974) recognized space

maintenance by the existence of distinctive types of vocalization exclusively

emitted in emjnent physical combats, which were suppressed after elimination of

the neighbor calling male, as was found in

C.

dubius. Aggressive response to

conspecific aggressive calls was demonstrated for Hyla ebraccara by WELLS

&

SCHWARTZ (1984); and for Hyla minuta by CARDOSO

&

HADDAD (1984), two

Reproductive behavior of Cyc/ori/mphus dubius .. 237

specit:s whose males also show lighting heha\'ioL Two charaderistlcs app~'ar to he comnllln ill tht:st: aggressive L'alls: tht: lengthening of call dllration and the incrt:asing rate of t:mission. This rt:port is a tirst approaL'll to descrihe the

rt:prodllction of

C

dllhills. additional fidd experiments art: needed to explain the

main fundion of paternal care in this SpeCIt:S,

ACKNI JWLEDG~lENTS. W.W. lkllstlll alld W.R He\er pr"\ ided _""lllle"l, "" e<lrh draft:..: E Ralllif'~/lh:lpl..:d Ih~ lidd \\'tI11:--: I. Sa/illla mad\.! till.! hlad .. and \\hit..: pil..turL'~ (n)jll "I,d .... :..:

C.F H. Hadd"d I're,ellied help fll I ("'llmenl,. K. Facllre helpCli in Ihe pr"ie(1. FAI'ESI' lillan(i,,11\

slIl'l""'kd Ihe '111.1) (,rani 1(' X~'2/12X 0 1,\ AAG alld AP XAI2-lS, /1 ttl A.ICI alld Ihe SlIlill1,,,"i"lI

In .... tiwlit\1\ (Shllrl TL'rtli Vt:-.ihlr Prtlgral11) p~rlllitkd C'\(llllillatillllllftltL' tlriC!illal l\:~')ld . .., t'( (', dll hll I.'

and (', hOnlt't'/t'!I{'I.\.

REFERENCES

CARDOSII. A,J. & CF.B. HADDAD. 19R-l, Vartahilidade aL'llstica em dtlerc'llks

POPlll<H,l)eS e I Ilter,H/)eS agressi\'<ls de Hrill lIIilll/lli (Amphihla. r\nllra), Ci('Jll'ia ~ ('uHura

36

(8): 1393-1399.

GOSNER, K.L. i 960, A simplified tahle till' staging anuran emhryos a III I lar\'ae

with notes on identitiL'ation, lIerpctf)If)~ira 16: 183-190.

HEYER. W,R, & Cc. [\1ELUl, 1979. DesL'ription of the ad\'erti~ing L'all of ( \'dontIlI/J/IIIS 1I.'/l{''' and C\'c/UI'lIJII/J/IIIS dll!Jills (A mph ihia. Lept, Jdad ylldac). Pap. Antis D~pto Zool., Siio Paulo, ,12: 193-20(),

LUTZ. A, 1929. Taxonomla t; hiologia do genero ( \'c/II"lIl1l/JIIII,\, I\ll-nl. Ins!. Oswaldo Cruz 22: 5-16.

LUTZ. B. 1972, GellgraphiL'al and t:L'ologiL'al noks on cisandinc Ii I pia tine fro~s,

J. lI~rpctol. 6:9.1-100,

M IRANDA-RIBEIRI J, A, DE, 1926, Notas para servirem ao estudo dos

gylllno-hatrachios (Anura) hrasdt:lros, Arch. I\Ju.", Nac Rio Janeiro

27

:

1-227.

NlJSSBAUN. R,A, & D,l, SCHULTZ, 1989, Coe\'olution of parental care and t:gg size. Am. Nat.

1.'3:

591-603,

R()SE. M, & R. E, LHl! IN, 197-l, The \'()eal hcha\'ior of spring p""ppers. 1/.1'111

Ci'llci/l''', ('opeia

1974

(-l): 9-l0-950,

WELLS. K. D. 1977, The s(lL'ial heha\'ior of anman amphihians, Anim. Beha\'.

25: ()66-693.

- - - -.1981. Parental heha\'ioroflllaleand feillale frog, p, IR4-197, I,,: R.D.

ALEXANDER & D.W, TINKE (cds). Natural Sel~dion and Sorial Ikh'l\ior.

New York, ChInHl Prt:~s.

WELLS. K.D. & J.J, SCH\\',-\RTZ. 19R-l, Vocal L'omllllllli,'atl()11 III a IWtltr"pl,al

trccfrog. J-/r/II ('hl'l/('('(/lII: aggrt:ssive calls, Behaviour 91: L'.R-I-l5.

WILLlA~lS.

G.C

1975,

Sex

and E\'olution. PrtllL'don. I'rlllL'don 1 'Ili\'. l're~s.

ReceblC1Q em LOX!. 1994. acelto em 25 VI 1995