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1996 Cantos Dendrobatidos PDF
1996 Cantos Dendrobatidos PDF
To cite this article: I. De la Riva , R. Márquez & J. Bosch (1996): The advertisement calls of
three South American poison frogs (Amphibia: Anura: Dendrobatidae), with comments on their
taxonomy and distribution, Journal of Natural History, 30:9, 1413-1420
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JOURNAL OF NATURAL HISTORY, 1996, 30, 1413-1420
The advertisement calls of three species of dendrobatid frogs from Bolivia and
Peru are described. For each species we present a characteristic audiospectogram
and oscillogram. We also provide numerical information about the spectral and
temporal features of the calls. Our recordings of these species are compared with
previously described calls of the same species from other locations. Comparisons
between the calls of three different populations of Colostethus from Peru and
Bolivia support their conspecificity. Characteristics of the call of a Peruvian
population of Epipedobates differ from those of E. hahneli, suggesting that further
taxonomic research is needed. The distribution of the genus Colostethus and
Epipedobates in Bolivia is reassessed.
Introduction
The anuran fauna of tropical South America is the richest in the world, and it is
difficult to estimate how m a n y species of frogs and toads occur in the region. Beside
the fact that m a n y new species are discovered each year, the study of populations
already known often leads to the discovery that new species are included under old
names. Nomenclatural problems accumulated over m a n y years m a y obscure our
understanding of the distribution and variation of m a n y species. A great advance
would be achieved by revisiting type localities and applying modern approaches, such
as bioacoustics, to the systematics of anurans (Cardoso and Vielliard, 1985; H a d d a d
and Martins, 1994; De la Riva et al., 1996). Given the importance of the anuran
mating calls as a pre-zygotic species isolating mechanism, there are commonly
remarkable inter-specific differences (Blair, 1995; 1959; Gerhardt, 1988). Thus, the
description of the advertisement calls of anurans is often necessary if a proper species
identification is to be made. In cases of cryptic species, calls may be a more reliable
way to discriminate these pecies than is visual appearance (Barrio, 1965; 1966).
Furthermore, becoming fa niliar with the different sorts of vocalizations of the
anurans in a particular regk n, leads to an easy and fast way to carry out inventories,
estimates of reproductive a~ tivity, phenology, abundance, and so on (Amiet, 1975;
1978; Zimmerman, 1994; [ e la Riva, 1993; 1994). Comparisons of advertisement
calls of different populations supposedly belonging to the same species can be a useful
tool in assessing their taxonomic status. However, because many different factors
influence the recording and the analyses of calls, this approach has to be applied
consistently if reliable conclusions are to be reached (De la Riva et al., 1996). In this
study we contribute to the l~nowledge of the anurans of southwestern Amazonia by
describing and comparing |he advertisement calls of three species of dendrobatid
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frogs.
Table 1. Summary of numerizal parameters of vocalizations (mean 4- SD, over range). The
two characteristic notes of C. t,~ilineatus are analysed separately (A and B).
C. trilineatus A C. trilineatus B E. hahneli E. pictus
Notes analysed 13 13 30 30
Note duration (ms) 27.8 _~:2.7 24.1 4- 5.5 12-8 4- 1.0 28-1 4- 2.1
24.6 32.5 13.2-32.2 10.7-14.9 25'5-32-5
Fundamental 1431-1 4- 133-6 1375-6± 104-5 5028-64- 13-5 1919-94- 24-6
frequency (Hz) 1212-0-1615-0 1191.0-1535.0 5007-7-5048-1 1878-0-1959-0
Dominant 5343.2 4- 117.9 5419.34- 40.8 5028-64- 13.5 3843-24- 31'5
frequency (Hz) 5149"0-5451.9 5330.8-5492.3 5007.7-5048.1 3776-0-3897'1
Notes minute -1 1562"6 i 48-8 - 312-9 + 66.6 252"9 4- 42-7
1507'5-1699.7 -- 160'6-437.9 108"3-294-0
Calls minute 1 213-1 4-48.1 312-94-66.6 252-94-42.7
121.2 281.6 -- 160.6-437-9 108.3-294.0
Calls of Dendrobatid frogs 1415
~.~ ~ ~,t
........ ..... l~ _ I~ ,,,i~..,,,,.-.,. ~ k .....~ix.
'- ....~' ......rr .....~ ......rr ........
F ........ - " - - ~ r F .....r r ......
Hz.
160 460 700 10.00 1300 1400 1900 2i00 msec.
10000'
9000'
8000'
7000'
6000'
5000 ~ ~.~- ~ ~ ~- it-
4000'
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3000'
2000,
1000'
O'
160 460 760 10.00 1300 1400 1900 2iOOmsec.
1o000
16o 460 700 lO"OO ]3oo 1400 1900 2i00 msec.
9000
8000
7000
6000
5000 t,-~ ~- P'!~.~- ~-p. ~ I,- ~ f. !~
4000
3000
2000
1000
0
160 400 760 10.00 1300 1600 1900 2200msec.
k_ .....
i.......L... ...... L ......L
It....... ..........L.......It_._
.... It..,,it.....
" r ........ir...........If ....... ! .... Ir ...... r ......... r " ~ ! ....... ir. . . . It-
Uz.
10000 160 460 760 10"00 1300 1600 1900 2i00 msec.
9000
8000
7000
6000
5000
4000
3000
2000
1000
0
160 460 700 1600 13"00 16LO 1900 2200 msec.
1416 I. De la Riva et al.
Epipedobates hahneli were deposited in the Natural History Museum, The University
of Kansas (KU), and the Museo de Historia Natural, U.N.M.S.M., Lima, Peru. In
addition, specimens were examined at the United States National Museum of Natural
History, Smithsonian Institution (USNM).
Results
The numerical values for the calls of the three species are summarized in Table 1.
Recordings of Colosthetus trilineatus were obtained at Cuzco Amaz6nico, Depart-
mento de Madre de Dios, Peril (12 ° 33 ~S; 69 ° 03' W) (for a description of the site see
Duelhnan and Koechlin, 1991). Males called during the day from the leaf litter on the
forest floor. Recordings were made at an air temperature o f 24°C. Calls were emitted
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continuously in rapid succession. The call (Fig. 1) was composed of two extremely
short notes (mean duration, 27-8 and 24.1 ms respectively) repeated in quick succes-
sion, the second one having a slightly higher dominant frequency than the first one
(mean dominant frequencies 5343.2 and 5419-3 Hz). The call was repeated regularly
at a fast rate (mean call repetition rate 231.1 calls min -1) in call groups of approx-
imately nine calls.
Male advertisement calls of Epipedobates hahneli were also recorded at Cuzco
Amaz6nico. Isolated males called during the day from the leaf litter or fallen logs on
the forest floor. Air temperature at the time of recording was 24°C. The call (Fig. 2)
was a brief single note (mean duration 12.8 ms), with a high dominant frequency
(mean dominant frequency at peak amplitude 5028"6 Hz). The call was emitted in
rapid succession (mean call repetition rate, 312.9 calls min 1) at relatively regular
intervals in long calling bouts of 31 or more calls.
Advertisement calls of Epipedobates pictus were recorded in Puerto Almac6n,
northwestern Departmento de Santa Cruz, Bolivia (15 ° 46 ~S; 62 ° 15'W), an Ama-
zonian locality in wet subtropical forest (Tosi et al., 1975; for a description of the site,
see De la Riva, 1993). Males called from the ground or standing on fallen logs or
leaves during most of the day, though more intensely in the late afternoon.
Temperature of the air at the time of recording was 25.5°C. The call (Fig. 3) was a
loud, high-pitched, short note (mean duration, 28-1 ms) which was repeated rapidly
(mean, 252.9 callsmin -1, resulting in a hammering sound. The mean dominant
frequency at peak amplitude was 3843.2 Hz.
This suggestion was followed by Duellman (1979). Myers (1987), however, included it
in the genus Epipedobates, and this decision has been followed by subsequent authors.
Epipedobates bolivianus remains one of the less well known species of South American
anurans, being only known from the type series (Rodriguez and Myers, 1993).
Edwards (1974) described a new species of Bolivian Colostethus from 6.5kmN
Chipiriri (Departmento de Cochabamba, Bolivia), but the description was never
formally published. One of us (ID1R) examined the holotype of this form (KU
137865) and concluded that it is undistinguishable from C. trilineatus. Indiv.iduals of
Colostethus recorded at Valle de Sajta (Departmento de Cochabamba, Bolivia) called
in an identical manner to those at Cuzco Amazdnico, and comparisons of specimens
from both localities also show a concordance in pattern and morphology, supporting
conspecific status as C. trilineatus. Fugler (1983) reported an unidentified species of
Colostehus from Tumi Chucua (Departmento del Beni). The examination of these
specimens (USNM 279896-7) leads to the conclusion that they also belong to C.
trilineatus (Morales, 1994b; pers. obs). Another specimen (USNM 336192) from San
Juan del Nuevo Mundo (Departmento de Pando) also is C trilineatus. Thus C.
trilineatus seems to be a widespread species in northern Bolivia, where it probably
reaches the area of Ambord National Park (Departmento de Santa Cruz). Finally,
Reynolds and Foster (1992) described C. mcdiarmidi, a distinctive species occurring in
cloud forests of the Departmento de Cochabamba. The advertisement call of C.
mcdiarmidi is unknown.
Morales (1992) described the call of individuals considered to be Dendrobates
pictus from Cuzco Amaz6nico, which are now considered to be E. hahneli. The calls
described are similar to those recorded by us at the same locality. The advertisement
calls of E. hahneli from Presidente Figueiredo (state of Amazonas, Brazil), were
described by Haddad and Martins (1994)~ These authors described a short call (about
15 ms duration), with a wide frequency range (2.5-7.0 KHz), emitted at intervals of
15-300ms. The numerical description and the audiospectrogram shown for the
Brazilian specimens are similar to those of our recordings from Peru. Comparison
with the data provided by Schlfiter (1980) is more complicated. He described the call
of Phyllobates pictus (following the nomenclature of Silverstone, 1976) from Pan-
guana. This population is considered to be E. hahneli by Haddad and Martin (1974)
on the basis of the physical appearance of the specimens. However, Haddad and
Martins (1994) found some differences between the bioacoustical data presented by
Schlfiter (1980) and their recordings ofE. hahneli, and on this basis they conclude that
perhaps two species are involved. Our recordings are structurally similar to those of
Schlfiter (1980), although he showed a call with a dominant frequency of 4000-
4700 Hz, i.e. lower than ours. Also, the call repetition rate he recorded is lower than
1418 I. De la Riva et al.
that of the specimens from Cuzco Amazdnico. Thus, the calls of P. pictus presented
by Schlfiter (1980) seem to possess intermediate features between those of E. pictus
and E. hahneli. Hence, we agree with Haddad and Martins (1994) that the taxonomic
status of the Panguana population remains unclear from a bioacoustical point of
view, and deserves future attention.
Haddad and Martin (1994) described the calls of Epipedobates pictus from the
type locality in Santa Cruz de la Sierra, Bolivia. They describe it as frequency
modulated notes, emitted at 220-280 ms intervals, in a narrow frequency range (3"4-
4.3KHz). These characteristics and, to a minor extent, their audiospectrogram
resemble the calls obtained by us, although the duration of the calls recorded by
Haddad and Martins (1994) was about 50ms, and we found our calls to be
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substantially shorter (25.5 32.45 ms). Overall, however, the calls they described are
rather similar to those described by us.
Haddad and Martin (1994) suggested that some of the Bolivian localities reported
by De la Riva (1990) for E. pictus could actually relate to E. hahneli and that both
species could occur in sympatry at some localities of northern Bolivia, and Acre and
Rond6nia (Brazil). We cannot confirm this, but we found E. hahneli in Bolivia. The
senior author heard the species calling in rainforest at Nareuda (Department of
Pando). Upon examination of the voucher specimens at the USNM, we confirm that
at least the following Bolivian localities listed by De la Riva (1990) correspond to
those of E. pictus: Rurrenabaque (280 558), Guayaramerin (123 967), Tumi Chucua
(279898), Ixiamas (147221), and San Buenaventura (281 567). Thus, in Bolivia E.
pictus occurs from northern Departmento de La Paz to the Brazilian border on the
extreme east, reaching at least up to 1300m on the Amazonian Andean slopes. A
related species, Epipedobates braccatus occurs in Matto Grosso, very close to the
Bolivian border, and probably enters Bolivia. However, at Serrania de Huanchaca,
on the Bolivian-Brazilian border, only E. pictus has been found (De la Riva, pers.
obs.). Haddad and Martins commented that the tadpoles of Dendrobates pictus
described by Lescure (1976) from french Guiana resemble those of E. hahneli.
However, Heatwole et al. (1965) considered Dendrobates pictus guayanensis more
closely related to D. pictus pictus than to D. pictus hahneli. Little is known about the
systematics of the E. pictus complex in northern South America, and the taxonomic
status of populations from the Guianan region needs to be reassessed.
Acknowledgements
We are indebted to the Museo de Historia Natural 'Noel Kempff Mercado', of
Santa Cruz de la Sierra, Bolivia, for its support. Field work in South America was
possible through a grant from the Asociacidn de Amigos de Dofiana to I. De la Riva.
Edwin Chacdn allowed us to record calls in his ranch, Puerto Almac~n. W. E.
Duellman kindly invited I. De la Riva to participate in the Biotrop project at Cuzco
Amaz6nico, and W. R. Heyer, R. McDiarmld, and R. Reynolds provided facilities
during his stay at the Smithsonian Institution. L. Coloma and E. Wild made useful
comments that improved the manuscript. Sound analyses were funded by project
CYCIT PB 89-0045C (PI: P. Alberch), Ministerio de Educaci6n y Ciencia (Spain),
and were performed in the facilities of the Estacidn Bio-Geol6gica E1 Ventorrillo
(C.S.I.C). J. Schwartz provided invaluable methodological advice.
References
AMIET, J.-L., 1975, Ecologie et distribution des Amphibiens Anoures de la r+gion de
Nkongsamba (Cameroun), Annales de la Facultd des Sciences de Yaoundd, 20, 33-107.
Calls o f D e n d r o b a t i d frogs 1419
AMIET,J.-L., 1978, Les Amphibiens Anoures de la r6gion de 1~ amfe, Annales de la Facultd des
Sciences de Yaoundd, 25, 189-219.
BARRIO,A., 1965, E1 g6nero Physalaemus (Anura, Leptodactyli,tae) en la Argentina, Physis, 25,
421-448.
BARRIO, A., 1966, Divergencia acfistica entre el canto nupical de Leptodactylus ocellatus
(Linn6) y L. chaquensis Cei (Anura, Leptodactylidae), ~hysis, 26, 275-277.
BLAIR, W. F., 1955, Differentiation of mating call in spadefgots, genus Scaphiopus, Texas
Journal of Science, 7, 183-188.
BLAIR, W. F., 1955, Call differences as an isolation mechanist 1 in southwestern toads, Texas
Journal of Science, 8, 87-106.
CARDOSO,A. J. and VIELLIARD,J. M. E., 1985, Caracterizaqgo Ce uma populaq~o topotipica de
Hyla rubicundula (Amphibia, Anura), Revista Brasileira de Zoologia, 2, 423-426.
DE LA RIVA, I., 1990, Lista preliminar comentada de los anfibic s de Bolivia con datos sobre su
Downloaded by [University of Tennessee, Knoxville] at 09:49 25 March 2013
RODRi~UEZ, L. O., CORDOVA,J. H. and ICOCHEA,J., 1993, Lista preliminar de los anfibios del
Peril, Publicaciones del Museo de Historia Natural UNMSM (A), 45, 1-22.
RODRiGUEZ, L. O. and MYERS, C. W., 1993, A new poison frog from Manu National Park,
southeastern Peru (Dendrobatidae, Epipedobates), American Museum Novitates, 3068,
1-15.
SCHLOTER,A., 1980, Bio-akustische Untersuchungen an Dendrobatiden in einem begrenzten
Gebiet des tropischen Regenwaldes von Peru, Salamandra, 16, 149-161.
SILVERSTONE,P. A., 1976, A revision of the poison-arrow frogs of the genus Phyllobates Bibron
in Sagra (Family Dendrobatidae), Natural History Museum, Los Angeles County Science
Bulletin, 27, 1-53.
Tosi, J. A., UNZUETA,O., HOLDR~DOE,L. R. and GONZALES,A., 1975, Mapa ecoldgico de Bolivia,
(La Paz: M.A.C.A.), 9 sheets.
ZIMMERMAN, B. L., 1994, Audio Strip Transects, in W. R. Heyer, M. A. Donnelly, R. W.
Downloaded by [University of Tennessee, Knoxville] at 09:49 25 March 2013