karen lips, decline of a tropical montane amphibian fauna, 1998.pdf

106

Conservation Biology, Pages 106–117Volume 12, No. 1, February 1998

Decline of a Tropical Montane Amphibian Fauna

KAREN R. LIPS*

Department of Biology, University of Miami, Coral Gables, FL 33124, U.S.A.

Abstract:

On the basis of surveys conducted between 1991 and 1996, I report a decline of the amphibianfauna at Las Tablas, Puntarenas Province, Costa Rica. I propose that the reduction in the abundance of

Atelo-pus chiriquiensis

and

Hyla calypsa

, the presence of dead and dying individuals of six species of frogs and sala-manders, and changes in population sex ratios of

A. chiriquiensis

and

H. calypsa

are evidence for “atypical”population fluctuations. Species with both aquatic eggs and aquatic larvae were most affected (e.g.,

Rana vibi-caria

,

Hyla rivularis

), whereas species with direct development or those that lack tadpoles, such as rainfrogs(

Eleutherodactylus

spp.) and some salamanders (e.g.,

Bolitoglossa minutula

), do not seem to have declined innumbers. In light of this evidence and in comparison with other declines in tropical upland Australia, Brazil,and Costa Rica, I conclude that environmental contamination (biotic pathogens or chemicals) or a combina-tion of factors (environmental contamination plus climate change) may be responsible for declines in theamphibian populations at this protected site.

Una Redución en las Poblaciones de Anfibios en una Localidad Tropical Ubicada en las Montañas

Resumen:

Basado en encuestas dirigidas por un período de 5 años, reporto una disminución de la faunaanura en un sitio elevado de la región sur central de Costa Rica. Yo propongo que la reducción en el númerode individuos, los individuos muertos o moribundos y los cambios en la proporción radial de los sexos, de-muestran que las fluctuaciones no son típicas o normales. Las especies más afectadas son aquellas que tienenposturas de huevos acuáticos y renacuajos acuáticos, mientras que aquellas con desarrollo directo (sin rena-cuajos) no parecen haber disminuido en la misma cantidad. Tomando en cuenta estos datos y comparándo-los a las disminuciones observadas en otros sitios montañosos del trópico, concluyo que la contaminación delmedio ambiente (causado por un microbio patógeno o químico) o quizás causado por una combinación defactores (contaminación del medio ambiente más cambios del clima) puede ser la causa de la disminución

de la población anfibia de este sitio protegido.

Introduction

Years after the first realization of global patterns of am-phibian declines (First World Congress of Herpetology1989), we are still uncertain about how to determinewhether declines are “normal population fluctuations”(Pechmann et al. 1991; McCoy 1994; Travis 1994) orwhether they are due to anthropogenic changes in thehabitat (Blaustein 1994; Blaustein et al. 1994

b

; Pech-mann & Wilbur 1994), nor is there agreement as to

whether these concurrent declines around the world areisolated incidents or whether global changes are respon-sible. The long-term population and climatic data neces-sary for statistical and biological proof is lacking in manycases, particularly for tropical montane sites wheremany declines have been reported (Laurance et al.1996). Rather than long-term data from a particular site,we must resort to comparisons among sites. Even moreproblematic, the natural history (e.g., breeding site, lar-val characteristics, reproductive phenology) of manytropical montane amphibians is unknown.

Regardless, certain amphibian species have not beenseen for several years (Crump et al. 1992; Carey 1993),and certain sites have shown sudden multiple declinesof several amphibian species (Weygoldt 1989; Pounds &

*

Current address: Department of Biology, St. Lawrence University,Canton, NY 13617, U.S.A., email [email protected] submitted October 11, 1996; revised manuscript acceptedApril 7, 1997.

Conservation BiologyVolume 12, No. 1, February 1998

Lips Amphibian Decline in Costa Rica

107

Crump 1994; Drost & Fellers 1996; Laurance et al.1996). In general, unexplained declines tend to occur inmontane sites over a 2- to 5-year period, to affect aquaticspecies more than terrestrial species, and to occur amonga variety of species, reproductive modes, and life histo-ries. Sudden coincidental declines of several species overa large area are suggestive of atypical population de-creases (Drost & Fellers 1996; Laurance et al. 1996).Known causes of declines (reviewed in Pounds & Crump1994; Laurance et al. 1996) include ultraviolet radiation,acidification, introduction of predators, and environ-mental contaminants. Some investigators (Carey 1993;Pounds & Crump 1994; Laurance et al. 1996) posit acombination of factors as the cause of declines, withstrong suggestion that changes in the environment havecompromised the immunology of amphibians. This meansthat amphibians may succumb to infections that are notusually fatal or may be killed by pathogens that do notnormally cause mortality.

Three aspects of their biology make amphibians par-ticularly susceptible to environmental perturbation andmay provide insights into understanding population de-clines: (1) possession of a complex life cycle, whereinthe embryo or larva requires a different habitat and in-gests different food items than the adult; (2) diversity ofreproductive modes (location of embryonic and larvalstages; Crump 1974) among the amphibians at a particu-lar site; and (3) permeable skin. Understanding themechanisms of these declines requires investigation ofall stages in the life history of amphibians and examina-tion of all habitats experienced by the amphibians at asite.

In 1991 I began research on the population biology of

Hyla calypsa

, a stream-breeding tree frog at Las Tablas, aremote, high-elevation cloud forest in Costa Rica previ-ously renowned for its abundance of amphibians (F. Bo-laños, personal communication). Based on my reports,Pounds and Crump (1994) wrote that

Atelopus chiri-quiensis

and

Bufo fastidiosus

appeared to be thriving atLas Tablas, whereas related species,

A. varius

and

B.periglenes

, at Monteverde were declining. Since thattime the populations of many amphibian species at LasTablas have either disappeared or declined to a fractionof pre-1994 levels. I present data on changes in the de-mography and phenology of the amphibian fauna of thishigh-elevation site and discuss possible mechanisms ofthis decline. Las Tablas is now the sixth reported uplandsite in the tropics to suffer unexplained declines of am-phibian populations (Atlantic coast Brazil, Heyer et al.1988 and Weygoldt 1989; Venezuelan Andes, LaMarca &Reinthaler 1991; Costa Rica, Pounds & Crump 1994;Eastern Australia, Laurance et al. 1996). I compareevents at Las Tablas to those at these other sites becausesimilarities in target taxa, habitat characteristics, and/orpatterns of decline may provide direction for researchinto the mechanisms of these declines.

Study Area

All surveys were conducted at Finca Jaguar, approxi-mately 18 km north-northeast of La Lucha, Canton CotoBrus, Puntarenas Province, Costa Rica (8

8

55

9

N, 82

8

44

9

W).This private farm is an isolated human residence within theZona Protectora Las Tablas, a component of the AmistadBiosphere Reserve. This protected area is the source ofthe aqueduct that supplies the entire Canton of CotoBrus with drinking water; Las Tablas was included in theBiosphere Reserve to protect the water supply. This siteis approximately 250 km southeast of Monteverde and issimilar to that site in terms of forest composition, gen-eral climate patterns, and the taxonomic composition ofthe herpetofauna. Las Tablas supports a high-elevation(1900 m) cloud forest (Lower Montane Rainforest in Hold-ridge [1982]) and experiences pronounced wet (May–December) and dry ( January–April) seasons with dailyheavy precipitation during the rainy season. Soils areacidic throughout this area (L. D. Gomez, personal com-munication).

Surveys were centered along a stretch of the head-waters of the Río Cotón, the surrounding forested hillsides,and a small, nearby pasture. The Río Cotón is a swiftlyflowing permanent stream with a rocky bed, deep pools,and numerous mossy rocks and boulders along thebanks. Dense vegetation overhangs the stream. Streamwidth ranges from 1 to 15 m, and maximum depthreaches 97 cm. Water is cool (about 15

8

C) and acidic(pH

5

5.0–5.5), and its clarity probably indicates nutri-ent-poor conditions; there are no aquatic plants.

Methods

Precipitation was measured daily with a standard raingauge located in a pasture between two stream transects.These data overestimate the amount of rainfall receivedby the stream but underestimate the amount of moisturederived from cloud water deposition. A maximum-mini-mum thermometer was placed next to the rain gauge,and temperatures were measured daily. Because of un-equal sampling effort during the study, climatic datawere combined into 24 2-week periods (Appendix 1).

In July 1991 I began research at Las Tablas on

Hyla ca-lypsa

. In addition to collecting mark-recapture data onadults of this species, I noted the phenology of the otheramphibian species at this site and, where possible, mea-sured and marked adults for population estimates. Theextent of research on these other species varied withavailable time and accessibility during this 5-year period.Except where noted, censuses were conducted alongtwo 400-m transects along the headwaters of the RíoCotón. The two stream transects were separated by 50 mand were located about 1.5 km north (upwind and up-stream) from the apple orchards, aqueduct, and finca

108

Amphibian Decline in Costa Rica Lips


proper. I walked 117 nocturnal and 352 diurnal cen-suses during this period, using a combination of visualand audio cues to locate amphibians and their life stages(eggs and larvae). Upon capturing a frog or toad, I toe-clipped new individuals, measured snout-vent lengthand mass, and determined sex and age. I collected ex-tensive mark-recapture data from

Hyla calypsa

and

Ate-lopus chiriquiensis

, the most abundant diurnal amphib-ian at the site. The data I collected on other species ofthe amphibian fauna are less detailed.

Results

The cumulative rainfall during the study varied among2-week periods (Fig. 1). In 1992 the rainy season beganin mid-April, but in 1994 rains were delayed until June.Rainfall distribution also varied by year; I combined therainfall data from 1991–1996 to derive the average cu-mulative rainfall per 2-week period (Fig. 2). Distinct wet(April-December) and dry ( January-March) seasons weredistinguished. Even during the height of the rainy sea-son, however, average cumulative rainfall varied among

periods, and some rain fell during the dry season. Aver-age daily temperature was affected by time of day, cloudcover, and rainfall, and it varied considerably, but the5-year average maximum and minimum temperaturesare relatively constant throughout the year (Fig. 3).

Other than obvious reductions in species abundance, Idescribe three phenomena that may be related to am-phibian declines at this site. Before I noticed actual de-creases in abundances, I found dead or dying individualson the transects in September 1992 and between Juneand August 1993. Six dead animals were found in thestream or on rocks in the stream; they were not obvi-ously damaged or emaciated. One glass frog, a gravid

Hy-alinobatrachium fleischmanni

, was dying upon cap-ture and exhibited a trembling of the limbs, a fadeddorsal color, and a damaged left foot. The other individu-als included two female

Eleutherodactylus melanostic-tus

, an

Atelopus chiriquiensis

female, an

Oedipina gran-dis

gravid female, and a

Hyla calypsa

gravid female. Thedead animals and some live representatives of these spe-

Figure 1. Average cumulative rainfall during each 2-week period for the duration of the study each year. Timing and intensity of rainfall varies by period and year.

Figure 2. Average cumulative rainfall for each 2-week period for the entire year based on averages from 1991 to 1996.

Figure 3. Average minimum and maximum tempera-tures (8C) for each 2-week period based on data col-lected during 1991–1996. For exact dates of periods, see Appendix 1.



109

cies were preserved in 90% ethanol or 10% formalin andsent to the University of Florida School of VeterinaryMedicine for pathological examination. Some specimenshad enlarged fat bodies, suggesting a rapid rather than agradual demise. No evidence of either a viral or bacterialsystemic infection was found, although the superficialdegeneration and necrosis of the skin of several individ-uals of different species (

Atelopus

,

E. melanostictus

,

Oe-dipina

) suggests the possibility of a common factor suchas an external toxin or unfavorable environmental condi-tion. Alternatively, this change may represent a commonnonspecific response to various insults, whether infec-tious or environmental. The possibility of a protozoanparasite in some of the epidermal lesions cannot be fur-ther substantiated without electron microscopy or ex-amination of skin scrapings from affected animals priorto formalin fixation (R. Papendick, personal communi-cation).

In 1994 I noticed that tadpoles of

Hyla calypsa

lackedkeratinized mouthparts. Many tadpoles have keratinizedbeaks surrounding the mouth and from 1 to 38 elongate,parallel rows of small, keratinized teeth anterior and pos-terior to the beaks. It has traditionally been assumed (Al-tig & Johnston 1989) that these hard structures scrapethe microscopic animal and plant material off leaves,rocks, and other submerged structures. In 1994 I mea-sured over 100 tadpoles of

H. calypsa

; none of these in-dividuals had the usual dark keratin covering the fivefleshy pads and ridges of the oral disc (Lips 1996). Thesetadpoles included very early stages (Gosner [1960] stages25–30) as well as those ready to complete metamorpho-sis (Gosner stage 42), yet all of the hatchling tadpolescollected from eggs in 1993 (the same cohort of tad-poles) had keratinized mouthparts. All of the tadpolesthat hatched from eggs in 1996 also had a complete setof keratinized tooth rows and beaks. In 1996 I netted 50tadpoles; of those, 3 tadpoles (Gosner stages 25–28) hada few teeth on one tooth row, 4 other tadpoles had kera-tinized beaks but no tooth rows (Gosner stages 25–27,36), and the remaining 43 completely lacked keratinizedmouthparts. This phenomenon, repeated over a 2-year pe-riod strongly suggests that development of the mouthpartsis normal but that degradation of the keratinized por-tions of the mouthparts occurs after the tadpoles have en-tered the stream. Both bacteria (Friedrich & Antranikian1996) and fungi (Malvia et al. 1991) can degrade keratin.

The third phenomenon involved leaf-litter plots, astandard technique (Scott 1976; Jaeger & Inger 1994) forquantifying the herpetofauna of the forest floor. In July1991 a field assistant and I cleared two plots 8

3

8 m

2

ofall the vegetative material and collected the amphibiansand reptiles. In July 1996 we cleared two plots 5

3

5 m

2

in the same manner within 100 m of the original plots.In 1991 we found 15

Bufo fastidiosus

, 3

Atelopus chiri-quiensis

, 5

Eleutherodactylus podiciferus

, 1

E. mel-anostictus

, and 4

Oedipina grandis

from the two plots,

for a total of 29 individuals in the 128 m

2

we searched.In 1996 we found no animals in the 50 m

2

searched. Our1991 density of 22.7 individuals/100 m

2

is surpassed bya value of 58.7 reported for San Vito (actually LasCruces), a mid-elevation site within 40 km of Las Tablas,and by a value of 45.1 individuals/100 m

2

for a lowlandsite in Silugandí, Panama (Scott 1976). Scott found that,throughout the wet tropics, mid-elevation sites had thehighest densities of leaf-litter herpetofauna, so the re-duction from 22.7 to 0 individuals/100 m

2

over a 5-yearperiod is unexpected.

Individual Species Accounts


Most

Atelopus

species are brightly colored, diurnal bu-fonids ubiquitous along streams in the foothills andmountain ranges from Costa Rica southward throughoutthe Andes (Savage 1972).


isclosely related to

A. varius

, the harlequin frog fromMonteverde, but

A. chiriquiensis

occurs at higher eleva-tions (Savage 1972). Like other members of this genus,males of

A. chiriquiensis

are abundant along mountainstreams and riverine forests; females are less abundantthan males and are often found in amplexus when en-countered.


has a long reproduc-tive season and deposits strands of eggs on vegetationand mossy rocks in the fast-moving segments of streams(personal observation). Upon hatching, the small tad-poles use ventral adhesive disks to attach to rocks in thecurrent. When I first visited Las Tablas in June-August1990, males of this species were abundant enough tocarpet the forest floor. I surveyed a trail parallel to astream transect three times in July 1991. I encountered 7

A. chiriquiensis

in 30 minutes along 300 m, 20 individu-als in 100 m and 30 minutes, and 29 individuals in 250 mand 25 minutes. Considerably fewer individuals wereseen along this trail in 1992, very few in 1993, and nonein either 1994 or 1996.

Beginning in 1991 I surveyed all individuals of thisspecies during regular stream transect surveys. In 1991

A. chiriquiensis

was the most abundant species at thissite; I observed amplectic pairs laying eggs throughoutthe wet season, and the abundance of tadpoles was sogreat that small submerged rocks appeared black. Inever encountered juveniles. I measured 348 adult

A.chiriquiensis

and recaptured 21 individuals between1991 and 1993. The low recapture rate may indicate ei-ther a very large population or extensive individualmovement. When adult captures decreased substantiallyin 1994 I ceased toe-clipping and measured only snout-vent length and mass.

To compare changes among years when field workvaried in time and duration, I combined survey data into

110



the same 2-week periods as the climatic data (Appendix1). I combined surveys from both transects and presentthe cumulative number of surveys and cumulative num-ber of

A. chiriquiensis

adults found (Fig. 4). This speciesshows a step-wise pattern of decline (Fig. 4), from veryhigh (1991) to moderate (1992–1993) to very low abun-dance (1994–1996). I captured this species all year longbut captured more individuals during the rainy season.The sex ratio (proportion of males among all captures)was consistently male-biased during this time, withyearly averages of 0.70 (1991) and 0.58 (1992). In 1993the situation changed to slightly female-biased sex ratios(0.30), although both the average and maximum num-ber of captures were similar to those of 1991–1992. By1994 I noticed a major decrease in the number of adultcaptures: the maximum number of individuals droppedto 1 or 2 per survey, for an average of 0.1–0.2 toads persurvey, and the average sex ratio was 0.33. By 1996 Isaw no animals in any of 64 surveys and only one indi-vidual in six surveys, for a total of five individuals (twomales, three females, one recapture). No tadpoles or eggmasses were noted during surveys in 1994, and I foundneither eggs nor tadpoles during specific searches in1996.

Rana vibicaria

Rana vibicaria

, a large ranid, is restricted to montaneareas of Costa Rica and Panama (Hillis & de Sa 1988) andbreeds in pools of slowly moving streams or temporarypools formed in seepage areas. At Las Tablas I foundeggs from November through May. In 1991–1992 I sawtadpoles of all sizes in the temporary and permanentpools in the pasture, suggesting a long larval period. Ilast saw tadpoles and adults at this site in June-July 1993.

In 1996 I searched and dip-netted intensively in the pas-ture pools and encountered no tadpoles. I limited ma-nipulations on this species to measuring and toe-clip-ping 44 adults in 1991.

Hyla calypsa

Hyla calypsa

is found along streams above 1800 m ele-vation in the Cordillera de Talamanca of southern CostaRica and western Panama (Lips 1996). Males are territo-rial and call from leafy perches to attract females, whichlay clutches of 10–30 eggs on vegetation overhangingthe stream (Lips 1996). This is a moderately-lived spe-cies: adults may live up to 3 years, eggs require 1 or 2months to hatch, tadpoles may take 8 or 9 months toreach metamorphosis, and juveniles may require an ad-ditional year to reach sexual maturity (Lips 1995). Malesand females are site-faithful and have an average homerange of 10–20 m

2

, although females return to thestream only to oviposit. For these reasons, it is unlikelythat the disappearance of individuals is due to emigra-tion or, even if healthy populations were nearby, thatimmigration would replenish populations (Blaustein etal. 1994

b

).I studied this species from 1991–1994 and in the pro-

cess handled, measured, and toe-clipped 325 adults andmeasured both eggs and tadpoles. The total number ofcaptures varied among nightly surveys during the study(Fig. 5). On many survey nights I found unmarked ani-mals, suggesting that recruitment occurred throughoutthe year. Emigration is a less likely possibility given thehigh site fidelity of adults. On average, recaptures com-prised 67% of nightly captures between 1991 and 1994(Lips 1995). In 1994 the rainy season was delayed untilafter I left in June, so I was unable to determine how

Figure 4. Cumulative adult captures of A. chiriquiensis from 1991 to 1996. Transects were surveyed at different times of the year, but, except for 3 months in 1992, all sur-veys were conducted during the normal breeding season of this frog. For dates of each survey, see Appendix 1.



111

many individuals were present that year. In 1996 thesame seven males were present for the 2 months of thestudy (100% recaptures, no recruitment, and no emigra-tion). One of those males was first captured in 1993, sothey were not all recent metamorphs. I rarely found fe-males; however, because they lay one clutch of eggs pervisit (Lips 1995) I assumed that the 20 clutches found in1996 were laid by 20 different females. This female-biased sex ratio (6 males, 20 females

5

0.23) differsfrom the equal male-to-female sex ratio found amongmarked individuals between 1991 and 1993. Despite re-ceiving the greatest amount and intensity of manipula-tion,

H. calypsa

currently has the largest population ofany stream-breeding anuran at this site.

Hyla rivularis

Hyla rivularis

, a small brown tree frog, was an abun-dant member of the nocturnal stream community; dur-ing 1991–1992 I captured and toe-clipped both callingmales and gravid females along the stream transects dur-ing every month of the year. In 34 nocturnal surveys Ifound 7.8 adults on average (range

5

0–28). The eggdeposition site of this species is unknown but is pre-sumed to be in the stream, perhaps under rocks or sub-merged vegetation. Tadpoles were abundant year-roundand easily distinguished by their large oral disc with ex-tensive tooth rows. Recaptures were always low, com-prising fewer than five individuals per night (

5

1.15).In 1993 this species was present during research con-ducted between June and August, although by 1994 Isaw a few calling males in April and netted some tad-poles (Fig. 6). I found no adults and only one tadpole in1996, despite extensive searches, and that tadpole (Gos-ner stage 31) had a complete set of keratinized mouth-parts. Like the few tadpoles of

Hyla calypsa

found with

x

some mouthparts in 1996, the tadpole was at an earlydevelopmental stage and may not have been exposedlong enough for the mouthparts to lose their keratin.

Hyla picadoi

Hyla picadoi

is a treefrog that spends its entire life in ar-boreal bromeliads. I often found two or three adult frogsin the leaf axils of a bromeliad, and I collected tadpolesand metamorphosing juveniles from a water-filled bro-meliad in December 1991. Adult males can be heard call-ing throughout the year but increase calling during therainy season (personal observation), when breeding prob-ably occurs. I performed no manipulations of this spe-cies and did not quantify calling males. I did not noticeany obvious change in the amount of vocalizing by males,and I estimated that during the study perhaps half of thebromeliads contained calling males of

H. picadoi

.

Bufo fastidiosus

Bufo fastidiosus

is related to

B. periglenes

, the goldentoad of Monteverde, and

B. holdridgei

of the CordilleraCentral (Savage & Donnelly 1992), and it shows similari-ties in reproductive behavior with those species (Lips &Krempels 1995). Neither

B. holdridgei

nor

B. periglenes

has been seen in years (Pounds & Crump 1994). Adult

B.fastidiosus

bred in pools formed by pasture seeps be-tween April and May 1992, although I occasionally sawadults and small juveniles along stream transects duringthe wet season (Lips & Krempels 1995). I measured andtoe-clipped 163 adults and juveniles between 1991 and1993 but saw none in either 1994 or 1996. I was presentin March-April 1994 to study these toads; unfortunately,the rainy season was delayed and I left before toads be-gan breeding. We found no toads in litter plots or duringhaphazard raking of the leaf litter between tree but-

Figure 5. Total number of captures of Hyla calypsa for each survey from 1991 to 1996. Except for the dry sea-son from November 1991 to March 1992, all surveys were conducted during the normal breeding season of this frog.

Figure 6. Total number of captures of Hyla rivularis for each survey from 1991 to 1996.

112



tresses in 1996, although these frogs were abundant inthe leaf litter between 1991 and 1993.

Stream-Breeding

Eleutherodactylus

During nocturnal and diurnal censuses along the streamI occasionally encountered adults of

E. punctariolus

and

E. melanostictus

. Like

E. angelicus

(Hayes 1985), thesetwo large, stream-dwelling species may deposit eggclutches in sandy banks or sand bars along the stream,and both species probably have direct development andlack tadpole stages. During 1991–1992 I captured 9adults of

E. punctariolus during stream censuses, but Isaw no frogs after November 1992. Adults of E. mel-anostictus were more common. I marked 23 individualsduring 24 of the 77 surveys between July 1991 and No-vember 1992, but I saw only 1 individual in each of thefollowing years.

Forest-Breeding Eleutherodactylus

Eleutherodactylus podiciferus, E. hylaeformis, and E.cruentus are the common leaf-litter frogs of the forestunderstory at this site. All three species probably layclutches of eggs in the leaf litter of the forest and, likeother Eleutherodactylus species, have direct develop-ment. All three species were present in 1996, although Ihave never determined population densities.

Salamanders

Six species of salamanders are known from this site: Oe-dipina grandis, Bolitoglossa minutula, B. compacta,B. marmorea, B. nigrescens, and B. “red tail” (D. Wake,personal communication). Bolitoglossa compacta, B.“red tail,” and B. marmorea occur at such low densitiesthat I cannot quantify their past or current status, andB. nigrescens was never found in the immediate studyarea. Like species of Eleutherodactylus, tropical pleth-odontid salamanders have direct development. Oedi-pina grandis is an elongate, fossorial salamander that“swims” through the soil. Between 1991 and 1993 thisspecies was easily located in the leaf litter between treebuttresses or under rotting logs in the riverine forest.The forested ridge where I sampled leaf litter plots wasan especially good location: 5–10 individuals could becollected in an hour. In 1996 I found no Oedipina in thetwo leaf litter plots nor in cursory raking of the leaf litterbetween tree buttresses along this ridge. One adult fe-male O. grandis was found dead and floating in thestream; this is the only salamander that seems to havedecreased in abundance. Throughout this study I foundadults of B. minutula on low vegetation during nightlywalks through the forest. During three nocturnal sur-veys in 1996 along a riverine forest trail, I found 7 adults

in 100 minutes and 500 m, 6 adults in 90 minutes and400 m, and 3 adults in 45 minutes and 250 m.

Possible Causes of Decline

Because biologists rarely intend to study declining popu-lations, it is unusual to have demographic data for all am-phibians at a site; therefore, it is difficult with haphaz-ardly collected data to demonstrate conclusively that theamphibian fauna has declined. Once a decline is suspected,it is often too late to collect enough amphibians for patho-logical examination or to design experiments to deter-mine the cause of the decline. In such a case one should(1) examine survivorship at each stage in the life historyof affected species (e.g., mortality of aquatic eggs and/ortadpoles might indicate a water-borne vector) and (2)look for differential mortality among reproductive modes(e.g., all stream-breeders or all species with direct devel-opment) or environmental requirements. Because I lackedreliable, long-term climatic data and survey data for theentire amphibian fauna of Las Tablas, I compared my re-sults to patterns of amphibian decline from four othertropical upland sites using these guidelines.

Habitat Destruction

Habitat destruction and/or degradation has probablycaused the extermination of more amphibian popula-tions than any other factor (Blaustein 1994), but it isprobably not a major source of mortality at this protectedsite. The transects do border a pasture, but it is smalland surrounded by unlogged forest, and it was clearedover 15 years ago (M. Sandí, personal communication).About 2 km downhill reside the only other human habi-tants of this Zona Protectora: the Sandí family grows ap-ples and raises cattle, but only cattle occupy the pasturenear the study site. No logging occurs at this site, and ad-ditional forest has not been cleared since this area be-came part of the Amistad Biosphere Reserve in 1982.

Introduced Fishes

Like many of the montane streams of Central and SouthAmerica (LaMarca & Reinthaler 1991), the Río Cotón hasbeen stocked with rainbow trout (Oncorhynchus mykiss)several times over the past 15–20 years, although troutwere last introduced at Las Tablas over 5 years ago (M.Sandí, personal communication). It is likely that intro-duced trout would feed on the aquatic eggs and larvaeof native amphibians, although the few trout stomachs Iexamined between 1991 and 1994 were filled with aquaticinvertebrates. Predation by introduced fish has reducedanuran populations in the western United States (Brad-ford 1989) and may be a factor in Central America, butamphibians that occupy forest pools, bromeliads, and


Lips Amphibian Decline in Costa Rica 113

other isolated bodies of water are safe from trout preda-tion. Because Rana vibicaria (a pool-breeder found inthe pasture and forest) has disappeared, it is unlikely thattrout are the sole cause of site declines. Two species withaquatic eggs and larvae (Hyla rivularis and Atelopuschiriquiensis) have disappeared, however; their disap-pearance might be consistent with trout predation ofeggs or tadpoles.

Researcher Disturbance

Scientists always affect their study species in some way.It is possible that my presence from 1991 to 1994caused the direct mortality of several species. Toe-clip-ping may (Clarke 1972) or may not (Lemckert 1996 andreferences therein) reduce survivorship of anurans. Itoe-clipped many individuals of Hyla calypsa, H. rivu-laris, Atelopus chiriquiensis, and Bufo fastidiosus butvery few or no individuals of the other species. WhereasA. chiriquiensis and B. fastidiosus may soon be extinct,H. calypsa has the largest population of any stream-breeding frog at this site despite the greatest amountand intensity of handling. Blaustein et al. (1994b) re-viewed long-term studies of amphibians; although manyof these populations were fluctuating, none showedsudden declines, despite a variety of marking tech-niques, including toe clips. In Las Tablas I marked fewindividuals of Oedipina grandis, Rana vibicaria, andthe stream-breeding Eleutherodactylus, and these popu-lations should not have declined from this level of re-searcher handling.

Ultraviolet Radiation

Blaustein et al. (1994a) demonstrated that greater expo-sure to UV-B radiation results in increased embryonicmortality of some amphibians. Only a few species fromthe Pacific Northwest have been tested for susceptibilityto UV-B radiation, but increased UV-B radiation shouldhave similar effects on many amphibians because am-phibian eggs lack a hard coating and few species haveprotective egg pigments. While UV-B radiation may havereduced the abundance of some species at Las Tablas(e.g., Rana vibicaria), it cannot be the sole effect be-cause there was no increase in embryonic mortality in1994–1996 compared to 1991–1992 for the arboreal eggclutches of Hyla calypsa (Lips, unpublished data). Eggclutches of this tree frog are laid underneath leaves thatoverhang the stream, but most clutches experiencesome exposure to sunlight and incidental radiation dur-ing the 3– to 8–week developmental period (Lips 1996).

Habitat Acidification

Throughout parts of Europe and North America acid rainhas reduced the biodiversity of many ponds and lakes.

Field and laboratory work has shown that many amphib-ian species are particularly sensitive to low pH. For ex-ample, many temperate amphibians belonging to thefamilies Hylidae, Ranidae, and Bufonidae have reproduc-tive problems below pH 5.0 (reviewed in Sparling 1995).The tropics are renowned for their acidic soils (Mabber-ley 1986); because stream water must percolate throughand across the soil, many tropical montane streams andpools are also acidic. Crump et al. (1992) found that wa-ter from rain and fog has a pH higher than that of thetemporary forest pools. Resident amphibians should beadapted to these acidic conditions, although a reductionin pH of acidic water could have detrimental effects. In1991 I used wide range litmus paper and measured thepH of the Río Cotón as 5.0–5.5. This value is comparableto the pH of forest pools at Monteverde (Crump et al.1992). Other evidence is equivocal for aquatic acidifica-tion at Las Tablas. Luis Diego Gomez, director of theJardín Botanico Wilson of the Organization for TropicalStudies in Las Cruces (about 45 km southwest of Las Ta-blas), periodically tests rain water for acidity and has notnoticed any changes in pH (personal communication).Also, if acid rain were killing animals at Las Tablas, thenmany species would be exposed to acid rain, includingterrestrial Eleutherodactylus and salamanders and thebromeliad frogs (H. picadoi). Likewise, amphibian em-bryos are the most sensitive life stage (Sparling 1995), yetmany tadpoles were seen subsequent to reductions inadult abundances. The skin necroses of the dead animalsis consistent with an acidified environment, however,and these animals included a fossorial salamander. Labo-ratory experiments could determine the pH tolerance ofthese species.

Alteration of Rainfall Patterns

Moisture is a crucial resource for amphibian reproduc-tion regardless of reproductive mode. Reduction orchanges in rainfall patterns could reduce amphibian re-production or recruitment, as could changes in the tim-ing, duration, or source of rainfall (reviewed in Donnelly& Crump in press). Deforestation has been correlatedwith reduced rainfall in the tropics, and Costa Rica hashigh rates of deforestation (Mabberley 1986). Rainfall datafrom Monteverde (Pounds & Crump 1994) and north-eastern Australia (Laurance 1996) reveal significantchanges in rainfall patterns within the past 8 years. TheCosta Rican electric company maintains weather sta-tions throughout the country, but Las Tablas differs fromthe closest stations in both life zone and elevation, so Icannot compare recent weather patterns at Las Tablas tohistorical levels. The decline at Las Tablas did not coin-cide with either a drought or an El Niño–southern oscil-lation event but spanned a period in which such eventsinfluenced the climate and rainfall patterns to varyingdegrees. If changes in rainfall per se are responsible for

114 Amphibian Decline in Costa Rica Lips


population declines, then amphibians that deposit eggsinto this permanent stream should be less affected thanthose species with either direct development or arbo-real eggs. As was also reported for Australia (Laurance1996), just the opposite is the case: species that repro-duce in permanent streams are affected more than thosethat oviposit terrestrially.

Environmental Contamination

Environmental contamination (agrochemicals, industrialpollution, or other human influences) is one of twolikely causes of declines at Las Tablas. Unlike Monte-verde, Las Tablas is far from any industrial center: theclosest is in Villa Neily, 50 km to the south-southwest,where there is an oil palm refinery. Las Tablas is also farfrom any active volcano that could promote acid rainformation. Many agrochemicals persist in the environ-ment for a long time, however, and many chemicals thathave been banned in the United States and Europe are inwidespread use throughout developing countries of thetropics (Colborn et al. 1993). Large numbers and quanti-ties of endocrine-disrupting chemicals have been re-leased into the atmosphere since World War II (Colbornet al. 1993), and many of these chemicals, includingDDT and PCBs, vaporize readily and can be transportedlong distances via the atmosphere (Eisenreich et al.1981; Rapaport et al. 1985). “Pristine” or otherwise le-gally preserved or isolated habitats will not be protectedfrom airborne contaminants. In Monteverde, for exam-ple, clouds deposit on vegetation nitrogen and phospho-rus derived from agrochemicals (Pounds & Crump 1994).

Not only do these chemicals toxify the environment,but many cause reproductive and estrogen-disrupting ef-fects in a variety of organisms (reviewed by Schmidt1994). Known health effects include morphologicalchanges in secondary sex characteristics, changes in thepopulation sex ratio, developmental abnormalities, andeven alteration of immunological function (Erdman 1988in Colborn et al. 1993; Martineaua et al. 1988). I noticedunusual female-biased sex ratios in A. chiriquiensis andH. calypsa in 1996. This bias could indicate reproduc-tive disruption from chemical contamination, or it maybe a result of greater mortality of males because of in-creased exposure to predation or chemicals during terri-tory defense, vocalization, and other reproductive activi-ties. In any case, of the three common chemicals sprayedon the apple orchards at Las Tablas, two (Mancozeb andBelnate) are known to have reproductive and endocrine-disrupting effects (Colborn et al. 1993), and all six deador dying individuals were females. Amphibian speciesexhibit different responses to a variety of pesticides(Berrill et al. 1994); if a site were contaminated by pesti-cides, different species might exhibit different symptomsand susceptibility. Pounds and Crump (1994) proposethat amphibian declines at Monteverde are due to a syn-

ergistic effect between climate change and environmen-tal contamination. I suggest that amphibian declines atLas Tablas are consistent with patterns from Monteverdeand this hypothesis.

Pathogen Outbreak

An outbreak of some pathogen is the second likely causeof declines at Las Tablas, and perhaps for the decline ofmany amphibian faunas. Laurance et al. (1996) reasonthat an exotic and highly virulent pathogen could causesudden declines like those seen in eastern Australia. De-clines in Australia spread at a mean rate of 100 km/year;Laurance et al. (1996) liken these patterns to those de-scribed by Scott (1993) for some sites in the westernUnited States. Scott (1993) described a wave-like spread(south to north), rapid and precipitous mortality, greatereffects at higher elevations, and selective declines (usu-ally adults of particular taxa). Laurance et al. (1996) ar-gue that the long-distance spread of pathogens could befacilitated by fish introductions. If pesticides, herbicides,and other agrochemicals can be spread through the at-mosphere, so can pathogens. Other vectors of long-dis-tance dispersal might include cattle or humans.

The Atlantic coast of Brazil may be another region ex-periencing a wave-like spread of sudden mortality of di-urnal or stream frogs from montane areas (Heyer et al.1988; Weygoldt 1989). Heyer et al. (1988) suggest that aserious frost in 1979 caused the decline, but they couldnot rule out aerial pollution as a factor. The sudden de-cline of closely related frogs to the north (Weygoldt1989) between 1981 and 1986 may be evidence for apathogen moving northward between 150 and 50 km/year depending on whether declines occurred in SantaTeresa in 1981 or 1986. Weygoldt (1989) believes thatthese two extinctions may have a common cause but ar-gues for acid rain. Weygoldt (1989), however, providesevidence for a possible bacterial infection of stream tad-poles. This case argues for a common sampling programso that similar data are collected at every site.

Costa Rica is the third area to experience two widelyseparated declines, at Monteverde (Pounds & Crump1994) and Las Tablas (this study). As in the Brazilian ex-ample, different causes are proposed for the two sites,but the similarity in the climatic conditions, the closephylogenetic relationships between the herpetofauna atthese two sites, and especially the similarity in patternsand timing of declines argue for a common cause. De-clines occurred in Monteverde in 1986–1987 and in LasTablas in 1993–1994; these declines correspond to amovement of about 250 km in 6 years, or about 42 km/year. The rate of spread of declines in Australia (100 km/year), Brazil (150 and 50 km/year), and Costa Rica (42km/year) are strikingly similar.

A similarity among these regional collapses is the largenumber of tadpoles present while adults are dying (Lau-



rance et al. 1996). I saw many tadpoles of several spe-cies at my site during the early decline period, but thetadpoles of at least one species at Las Tablas have mor-phological deformities of the mouthparts, and Weygoldt(1989) saw high mortality in laboratory-reared tadpolesuntil he treated the water with a bactericide for aquar-ium fish. Both bacteria and fungi can degrade keratin(Malvia et al. 1991; Friedrich & Antranikian 1996), so theloss of keratinized mouthparts in tadpoles of H. calypsaat Las Tablas may be an indication of infection by apathogen. Alternatively, this loss could indicate chemi-cal contamination. Normal sloughing of mouthparts oc-curs just prior to metamorphosis and is regulated by thethyroid; thyroid function has been shown to be alteredby exposure to hormone-disrupting chemicals (Mocciaet al. 1981, 1986). Future research should focus on larvalcondition in addition to abundance and should test forlarval responses to agrochemicals. I suggest that de-clines at Las Tablas and Monteverde, Costa Rica (Pounds& Crump 1994), are consistent with patterns seen inAustralia (Laurance et al. 1996) and Brazil (Heyer et al.1988; Weygoldt 1989) and with the hypothesis of apathogen outbreak.

Conclusions

Results from Las Tablas are strikingly similar to thosepatterns described for Australian rainforests (Laurance etal. 1996), Costa Rica (Crump et al. 1992; Pounds &Crump 1994), the Venezuelan Andes (LaMarca & Rein-thaler 1991), and the Atlantic coast of Brazil (Heyer et al.1988; Weygoldt 1989). Similarities among these fivesites argue for a common cause of amphibian declines atthese tropical montane sites; they include: (1) extinctionwaves moving directionally (north to south in CostaRica, south to north in Australia and Brazil); (2) taxo-nomic (bufonids, ranids) and ecological specificity (diur-nal species and stream-breeders); (3) upland tropicalsites with high endemicity; and (4) rapid concurrentcrashes of many species at a site. I found that speciesmost affected were those with both eggs and larvae inaquatic sites (Rana vibicaria, Hyla rivularis, Atelopuschiriquiensis). The abundance of frogs that breed inbromeliads (H. picadoi) and of those amphibians thathave direct development (salamanders) and breed in theleaf litter (Eleutherodactylus spp.) also suggests that thecausative agent is water-borne. Some species in declineshowed a change in the sex ratio from usually male-biased sex ratios to female-biased sex ratios (H. calypsa,A. chiriquiensis); this argues for future investigation intoenvironmental contamination. The sudden nature of de-clines and the presence of dead and dying individualssuggests an epidemic of some bacteria or virus, althoughnovel weather patterns could also deposit unusual typesor quantities of chemicals. Because of the isolated na-

ture of Las Tablas, it seems likely that declines may becaused by or aggravated by long-range atmospheric trans-port. Long-term weather data might indicate whetherweather patterns have recently changed over Las Tablas,and atmospheric testing could determine whether cloudor rain water carries chemical contaminants. Finally, mon-itoring of amphibian populations needs to be continuedat Las Tablas, and pathological surveys need to be initi-ated on the remaining species.

Acknowledgments

I thank M. Sandí C. and family for 5 years of hospitalityand assistance at Las Tablas. I thank the Organization forTropical Studies and the Ministerio del Ambiente and En-ergia for permits. I thank M. Donnelly, J. Savage, R. Altig,F. Bolaños, and S. Rand for general discussions and J. Sav-age, M. Donnelly, S. Rand, and C. Budd for comments onthe manuscript. I thank S. Roselle for assistance with theSpanish translation. Primary financial support for thisproject was provided by the National Geographic Soci-ety, the Organization for Tropical Studies Pew/MellonFellowship, and the University of Miami Tropical BiologyFellowship. Additional funding came from St. LawrenceUniversity, the Explorer’s Club, the American Museumof Natural History, the American Society of Ichthyologistsand Herpetologists Gaige Fund, Society for the Study ofAmphibians and Reptiles Grants-in-Herpetology, andthe National Science Foundation (DEB #9200081 to J.Savage).

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Appendix Dates of climatic (periods 1–24) and amphibian data collection.

Surveys conducted

Period Dates 1991 1992 1993 1994 1996

1 16–30 April X X2 1–15 May X X3 16–31 May X X X4 1–15 June X X X5 16–30 June X X X6 1–15 July X X X7 16–31 July X X X X8 1–15 August X X X9 16–31 August X X X

10 1–15 September X X11 16–30 September X X12 1–15 October X X13 16–31 October X14 1–15 November15 16–30 November X16 1–15 December X17 16–31 December X18 1–15 January X19 16–31 January X20 1–15 February X21 16–28 February X22 1–15 March X23 16–31 March X24 1–15 April X X

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