Ecology and Evolution of Phytotelm-Breeding Anurans

8/11/2019 Ecology and Evolution of Phytotelm-Breeding Anurans

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ECOLOGY AND EVOLUTION OF

PHYTOTELM-JREEDING ANURANS

Richard M. LehtinenEditor

MISCELLANEOUS PUBLICATIONS

IMUSEUM OF ZOOLOGY UNIVERSITY OF MICHIGAN NO. 193

Ann A h r November 2004


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P U B L I C A T I O N S O F T H EMUSEUM OF ZQOLOGY, UNIVERSITYOF MICHIGAN NO. 192

J B. B U R C I I ,ditot*Ku1.1: SI.EFA NON D J A N I C EAPPAS,ssistant Editoras

The pub lications of the Mu seum of Zoology, The U niversity of Michigan, consist primarily o f two series-theMiscellaneous

P~rhlications nd the Occasional Papers. Both serics were founded by Dr. Bryant Walker, Mr. Bradshaw H. Swales, and Dr. W.W. New comb . Occasionally the Museum publishes contributions o utside of thesc series; beginning in 1990 these are titled S pecialPublications and arenumbered.All s~tbmitledmanuscripts to an y of the Museum s p ublications receive external review.

The Occasiontrl Papers, begun in 1913, sellie as a mcdium for original studies based prii~ci pall y pon the collections in theMuseum . They are issued separately. Wh en a sufficient number o f pages has been printed to mak e a volume, a title page, table ofcontents, and an index are supplied to libraries and individuals on the m ailing list for the series.

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A complete list of publications o n Mam mals, Birds, Reptiles and Amphibians, Fishes, Insects, Mollusks, and other topics is avail-able. Address inquiries to Publications, Museum of Zoology, The University o f Michigan, Ann Arbor, Michigan 4 8 109-1079.

RECENT MISCELLANEOUS PUBLICATIONS

Bailey, R.M., W.C. Latta, G.R. Smith. 2004 . An atlas of Michigan fishes with keys and illustrations for their idcntification.Mix, .Publ. Mus. Zool., Univ. Michigan,No. 192, pp. i-iv, 1-2 15 ,219 figs., 4 tab les.

Storer, R.W. 2002. The metazoan parasite fauna of loons (Aves: Gaviiformes), its relationship to the birds evolutionary historyand biology, and a comparison w ith the parasite fauna of grebes.Misc. Puhl. Mzrs. Zool., Univ. Michig an,No. 19 1, pp . i-iv, 1-44,3 figs., 7 tables.

Albert, J.S. 2001. Species diversity and phylogenetic systematics ofAm erican knifefishes (Gym notifom es, Teleostei).Misc. Puhl.Mzrs. Zo ol., Univ. Michigan ,No. 190, pp, i-vi, 1-127, 50 figs.

Nussbaun~, .A. C.J.Raxwosthy. 200 0. Systematic revision of the genusPar-oedura Giinther (Reptilia: Sq uam ata: Gekkonidae),with the description o f five new species.Mist Ptrbl. MU S.Zool., Univ. Michigan, No. 189, pp. i-iv, 1-26, 12 figs., 7 tables.

Stores, R.W. 2000 . The metazoan parasite fauna of grebes (Aves: Podic ipedifo nnes) and its relationship to the birds biology.Misc.PuOl. Mus. Zoo l., Univ. Michigan,No. 188, pp, i-iv, 1-90, 9 figs., 7 tables.

Nussbaum, R.A . M.E. Pfrender. 1998. Revision of the African caecilian genu sSchisrornetopun7 Parkcr (Amphibia: Gymn ophi-ona: Ca eciliidac). M ix . Publ. Mus. Zool., Un iv Michigan,No. 167, pp. i-iv, 1-32, 15 figs., 15 tables, 4 color plates.

RECENT OCCASIONAL PAPERS

Garrison, R.W., N . von Ellenriedcr M.F. O Bricn. 2003. An annotated list of the name-bearing types of species-group nam es inOdonata preservcd in thc University of Michigan Museum of Zoology.Occ. Pap. Mu.c. Zoo l., Univ. Michigun, No. 736, 73 pp.

Ng, H.H. J.S. Sparks. 2003. The ariid catfishes (Telcostei: Siluriformes: Ariidac) of Madagascar, with the description of twonew species. Occ. Pap. Mzis. Zool., Univ. Michigan, No. 735, 21 pp., figs., 1 table.

Ng, H.H. 2003. At-ius verrucos us, a ncw spe cies of frcshwater ariid catfish (Teleostci: Ariidae) from thc M ekon g River.Occ. Pap.Mtn. Zool., Univ. Michigun,No. 734, 14 pp., 6 figs., 1 table.

Norris, S.M. 2001 Osleology o f the southwestern darters,Etheostoma Oli~ocephalus)Teleostci, Percidae)-with colnparison toother Nosth American p ercid fishes.Occ.. Pup. Mtis. Zoo /., Univ. Michigun,NO. 73 3,4 4 pp., 18 figs.

Ng, H.H. W.J. Rainboth. 2001. A review of thc sisorid catfish genu sOreoglanis (Silur-iforn~cs: Sisorida c) with descriptions offour new species. Occ. Pup. Mus. Zool., Univ. Michigan, No. 732, 34 pp., 13 figs., 3 tables.

Collette, B.B. 2001 . Opsunzrs dichro.stomzrs,a new toadfish (Teleostei: Batrachoididac) from the western Caribbean Sea andsouthern Gulfof Mexico. Occ. Pap. Mus. Zool., Univ. Michigan, No. 731, 16 pp.,5 figs.

Fink, W.L. A Machado-Allison. 2001. Serra.strlrnus has tatus , a new species of piranha from Brazil, with colnlnents onSer-~~a.snlrnus/tzivei and Sert-usaln~us onzpt-essus(Teleostci: Characiformes). Occ. Pap. A41i.c. Zool., Univ Michigan,No. 730, 8pp., 16 figs.

THE REGENTS OF THE UNIVERSITY

David A Brandon, Allti Arbor Rcbecca McGowan, Ann Arbor S Martin Taylor, Crossc Pointe Fal-msLaurcncc B. Dcitch, Bloolnfield Mills Andrca Fischer Ncwm an, Ann Arbor Katherine E. Whit e, Ann ArborOlivia P. Maynard, Goodrich AndrewC. Richncr Mary Sue Coleman, e . ~J f i c io

Cover illustration by John Megahan


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MISCELLANEOUS PUBLICATIONS

MUSEUM OF ZOOLOGY UNIVERSITY OF MICHIGAN NO. 193

E c o l o g y a n d E v o l u t i o n o fP h y t o t e l m - B r e e d i n g A n u r a n s

Richard M. Lehtinen Editor

Herpetology DivisionM useum of Zoology

The University of M ichigan

Ann Arbor Michigan 48109-1079 USA

Departm ent of BiologyThe College of Wooster

Wooster Ohio 44691 USA

Ann Arbor November 2004


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PAGES

Richard M. Lehtinen, MichaelJ. Lannoo, Richard J. WassersugPhytotelin-breeding anurans: past, present, and future research................................................ 1

Janalee P. Caldwell Maria Carm ozina de AraGjoHistorical and ecological factors influence survivorship in twoclades of phytotelm-breeding frog s Anura: Bufonidae, Dendrobatidae).................................. 11

Heather HeyingReproductive limitation by oviposition site in a treehole breedingMadagascan poison frog Man tella laevigata) ......................................................................... 23

Mark-Oliver Rodel, Volker H.W. Rudolf, Sabine Frohschammer, K. Eduard LinsenmairLife history of a w est African tree-hole breeding frog,Phiynobatrachusgzrineensis, GuibC Lamotte, 96 Am phibia: Anura: Petropedetidae). 3 1

Richard M. Lehtinen, Christina M. Richards, Ronald A. Nussbaum

Origin of a com plex reproductive trait: phytotelm breeding in inantelline frogs 5Kyle Summ ers C. Sea McKeonThe evolutionary ecology o f phytotelmata use in neotropical poison frogs............................. 55


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Mi.7~. zrbl. Mtis. Zool., Univ. Mich., 2004, 193: 1-9

PHYTOTELM-BREEDING AN URAN S: PAST, PRESENT AND FUTURE R ESEARCH

Richard M . Lehtinenl*,Michael J. Lannoo2 and RichardJ. Wassersug3

University ofM ichi gan Museum ofZo ology , Division ofRe ptil es andAmph ibians, 1109 Geddes Avenue, Ann Arbol; Michigan 48 109-1079, U.S.A.*

lridiana University School of M edicine, Mzmcie Center for Medical Education,MT201, Muncie, Indiana 47306 USA

' Department ofAnaton~yrid Neurobiology, Sir Charles flipper Medical Building, 58 50 Co llege Street, Dalhousie University, Halifau, Nova Scotia B3H1x 5 Canada

INTRODUCTION

As they hatch, they wriggle violently on the moist andp olishedsurface o the banana stem and go sliding down it until theyreach the water retained between stem and lea Doub tlesstheir progress is often assisted by the frequent show ers ofrain. They undergo their metamorphoses in the seclusionothis private sw imming pool, nourished by the remains of manysmall insects that are drowned in theflui d.

Barbour Loveridge (1928, p. 257)

This description of the life history of the east Africanmicrohylid Hoplophryne uluguruensiswas one of the firstdetailed accounts of a phytotelm-breeding frog. Long thoughtto be a mere oddity or aberration, egg deposition and tadpoledevelopment in water-holding plants is now known to be asomewhat common reproductive mode (found in at least 102species; Table 1). A phytotelm (from G reek phytos = plant;telm = pond; plural phytotelmata) is defined as a water bodycontained within som e part of a plant. Examples include water-filled tree holes, bamboo shunps, bromeliad tanks, nut husks,leaf axils, tree buttresses and other su ch habitats. These micr o-aquatic environments range from being relatively sizeable(tens to hundreds of liters in volume; Schiesariet al.,2003) toextremely small (a few milliliters; Rode1et al., this volume).Phytotelm ata are thought to be relatively safe habitats for frogetnbryos and larvae, compared to ponds or streams whereco~ npet itors and predators are often abundant. However,predators and competitors can also be found in phytotelmataand these habitats offer inany additional challenges such aslow dissolved oxygen concentrations, high risk of desiccationand unpredictable food availability.

Anurans that are obligate breeders in phytotelmata havecvolvedaw idevariety ofstrategies to deal with theseconstraints.

A few of these modifications include: obligatory oophagy(e.g., Hoplophryne, Noble, 1929), terrestrial locom otion(e .g. ,some Mantidactyl~is,Lehtinen, 2004), carnivory (e.g.,some Dendrobates, Caldwell, 1993), and an array of derivedparental care behaviors (Lehtinen and Nussbaum, 2003).These lnodifications are particularly conspicuous in the larvalstage and, in 1987, two of us (MJL and RJW) co-authoredwith Daniel Townsend a review of what was then known of

Co r~ spo nd itl g uthor: Present address: Biology Departnlent, 931 CollegeMall, The Co llege o f ' Woo.vte1; Woostec O hio 446 91 USA. E-mail:rlehti~ien@~vooste~edzi

the tadpoles of these frogs. In the intervening years, much newdata have been p ublished and on July 5Ih 2002, a sympo siumentitled Ecology and Evolution of Phytotelm ic Anurans washeld at the 50th annual meeting of the Herpetologist's Leaguein Kansas City, Missouri. This symposium gathered twelvespeakers to discuss their research on phytotelm-breedingfrogs, and is represented here by the papers of Caldwell andde Araujo, Heying, Lehtinenet al., Rode1 et al. and Summersand McKeon. As a prelude to these papers, we herein reviewpast research, discuss current work and suggest future areasfor research on these fascinating frogs.

PAST RESEARCH

Anumber ofearly papers briefly m entionphytotelm-breedinganurans, usually in the context of other topics. Noble (1927,1929) was among the first to provide a detailed descriptionand discussion of phytotelm-breeding frogs. Other importantpapers appeared periodically such as Dunn (1937), Taylor(1954), S che el(19 70) and Wassersuget al. (1981). Lannoo etal. (1987) published the first summary of this information. Intheir paper, the authors sought to do two things: 1) explain theunusua l morphology of the tadpole of the Jamaican bromeliad-dwelling hylid, Osteopilus brunneus,and 2) summarize whatwas then known about the world's free-living arboreal anuranlarvae. This summary resulted in a classification scheme forarboreal tadpoles. Below we review the Lannooet al. paper inorder to highlight some of the common themes addressed bythe past research of other authors.

Osteopilus brunneus tadpoles live in the tanks of largebromeliads. The morphology of the 0 . b runneus tadpoleincludes an elongate tail but reduced dorsal and ventral tailfins, a large stomach but reduced intestinal mass, a reducedbranchial apparatus including gill filters and gill filaments,

enlarged muscles fo r depressing the jaws and buccal floor butreduced denticles and denticle rows, a v-shaped lower beak,and a reduced lateral line system.

The first goal of Lannoo et al. (1987) was to explain theunusual morphology of the 0 brunneustadpole, and so theyfirst asked: why the long tail? The tail to body ratio in0 .brtlnneus tadpoles is 3.9 and we see similar body elongationin other phytotelm- dwelling larvae. Unlike most tadpoles,0 . b runneustadpoles do not grow isometrically, instead tail-length exhibits a positive alloinetry between Gosner (1960)stages 25 and 3 1. Three functions have been proposed for the


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long tail.1) Dunn (1 926) proposed a cutaneous respiration func tion,

which Lannoo et al. (1987) rejected. The muscular portion ofthe tail is elongated, but the dorsal and ventral tail fins, whichmight help to provide respiratory surface area, are reduced.

2) Laessle (1961) proposed that agitation of the elongated

tail aerates tlie water, which Lan nooet a / . 1987) a lso rejected,since these tadpoles are typically quiescent.

3) Noble (1929) and Jones (1967) hypothesized that theelongated tail aided locomotion through a viscous medium.Lallnoo et 01 (1987 ) felt this argument has merit. The sebrolneliad tanks co ntain the remains of gelatilious egg capsulesand this gelatin-water mixture is viscous. Th e idea here is thatin bromeliad tanks, 0 hrzinneus tadpoles inay not so muchbe swimm ing as they are burrowing. As Cans (1975) haspointed out, elongation is a common evolutionary response toburrowing.

The tail may also fil~lctionas a postural organ. In the

laboratory, Lannoo et 01. (1987) noted that quiescent 0brunnezrs tadpoles orient vertically. This posture has alsobeen seen inAcanthixalis sonjae by Rodel et a/ . (2003) and inbromeliad-dw elling microhylids by Kriigel Richter (1995 )and may fun ction to position the head nearer to sources of foodand oxygen.

The second question La m ooet a / . (1 987) asked about theunus~ialmorphology of the 0 brunnells tadpole regarded thefeeding apparatus. In particular, why do0 hrunneus tadpoleshave a shearing beak, reduced denticles and denticle rows,reduced intestinal mass, and an enlarged stornach? Many ofthcse unusual characteristics are also found in other phytotelm

dwelling tadpoles. Lannoo et01

(1987) found a range of3-3 tadpo les in occupied bronleliad tanks, in a volume ofperhaps half a liter. At densities this high, the question ofwhat to eat becomes important. These authors found that thes t o ~ i ~ a c h sf Gosner (1960) stage 25 to 41 tadpoles containedpredominantly whole 0 brunneza eggs, with tlie number ofeggs l l 10 stom achs ranging froill 5 to 184. Sinc e these eggsshowed few signs of developing, Lanno oel ul. (1 987) prop osedthat these were unfertilized trophic eggs, laid by f'ernalcs asfood for their tadpoles. [Thompson (1996) has since shownthat eggs laid later in the reproductive season are true trophiceggs, but egg s laid earlier are fertilized and w ill develo p if notingested.] La nnoo et al. (1987) asserted that collectively thismorphology reflects a dietary shift from omnivoryldetritivoryto oopllagy. Other phytotelm breeding specics have also beenshown to have oophagous tadpoles with sinlilar characteristics(Table 1).

The third question Lann ooet 01. (1987 ) asked concellled thereduced gill filters and filaments and lack of buccal pump ing in0 brzmneustadpoles. N oble 1927) suggested that in an aquaticenvironment that is severely hypoxic (such as bromeliads;Laessle, 196 I), increased respiratory surface area is requiredto obtain sufficient oxygen. However, Lannooel 01. (1987)observed that at low dissolved oxygen levels,0 hrunnezrs

tadpoles surface to gulp air. Lannooet a/ . (1987) proposedthat reduced surface area in gill elements and tail fins reducesthe amount o f oxygenlost to the water in tlie bromeliad tank.A tadpole that gulps air and lives in an aquatic environmentthat is severely hypoxic likely has more oxygen in its bloodthan there is in the surroundi ng water, and therefore diffus io~ l

gradients favor the loss of oxygen to the environment. In orderfor 0 ~ I , U I ~ M ~ Z . Gadpoles to retain oxygen acquired throughair gulping, aquatic gas exchange surfaces are reduced. Giventhe small size of most phytotelmata, many phytotelm-dwellinglarvaeprobably routinely encounter sinlilar hypoxic conditions.These environmental conditions may account for many of theunusual characteristics of phytotelm-dwelling tadpoles.

The second goal of Lannoo et a/ . (1987) was to modifyOrton's (1953 ) description of arboreal tadpoles as thin,flattened, larvae to enco mpa ss the variety of arboreal tadpolemorphologies described since her early paper. Towa rds thisend, Lannoo et al. constructed a table describing denticle

pattern, body fo nn , taillbody ratio, diet and habitat-for theroughly 42 species with arboreal tadpoles that were known atthe t i~ne.From this table, they described a variety of arborealtadpole types, as follows:

Group - Elongate tadpoles with attenuate bodies, taillbodyratios >2, denticle fo ~l ~ lu la213 usually reduced to 111 or less;highly reduced gill filters and gill filaments, ~nusculoskeletalspecializations for macrophagy oroo phagy , little or no pigment.Osteopilzrs brzlnneustadpoles and the othe r Jamaican hylids fitinto this group. Arboreal I-ioplophr:y~~e,hilautzrs, and someDendrohates larvae also fit here. Gro upI tadpoles are primarilyassociated with leaf axils rather than tree holes. They oc cur in

relatively small vo lun ~e s f water that have little or no primaryproductivity as food. All appear to be obligately oophagous,relying on trophic eggs, which are usually unfertilized, butmay be fertilized in some spec ies at sonle times.

Group - Sho rtertadp oles with stout bodies; taillbody ratios> 2; denticle fonnula reduced to 212 or less; highly reducedgill filters and gill filaments little or no pigment. Am ong thetadpoles that fit this group are W l a zetecki, Hyla p icudoi,Anotheca spinosa, and thc aggressive omnivorous larvae ofDendrohates quinquevittaus. These tadpoles are carnivorousand ~nacrophagousand are associated with broineliads thathave little free water. Conspecific frog eggs may form a majorportion o f their diet, but the evidence for obligate oopha gy andtrophic egg production is not well documented.

Group I Elongate tadpoles with attenuate bodies; tail1body ratio > I .7; denticle forlnula >213; little or noreductionof the internal oral features - i.e., these tadpoles have well-developed gill filters; no cranialmusculoskeletalspecializationsfor macrophagy. Phj~lloc/ytesand M~rntidactj~/u.speciesbelong in this group, as does Hvla br*o~neliacicr nd Hyladenu l-oscarta. The New World Hvla increase lower denticlerows, the Old WorldPhyllodytes and M a n / i d a c ~ ~ l z ~ . sdd upperdenticle rows.

Group IV - Shorter tadpoles with stout bodies; taillbody


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Table 1. Summary of known obligate phytotelm breeding anurans with free-living larvae. Expanded from Lannooet al. 1987. Does not include direct developers that lay eggs in phytotelmatae.g. someEleutherodactylus, Platymantis and Philazrt~rs).

Species Larval Dlet Larval Habitat References

BufonidaeBtfo castaneotic~rsDendroph~ynisc~rsrevipollicatztsFrostizrs p ernambzrcensisMertensophqne micranotisNectophryne afraPelophryne brevipesStephopaedes anotis

DendrobatidaeColostethzrs beebeiColostethus brornelicolaDendrobates arbore~wDendrobates azrratusDendrobntes azureusDendrobates biolatDendrobates castaneoticusDendrobates fantastic2rsDendrobates gran~iliferu sDendrobates histrionicusDendrobates lamasiDendrobates lehmanniDendrobates lezicomelasDendrobates minutusDendrobates mysteriostrsDendrobates pumilioDendrobates reticzilatusDendrobates specioszrsDendrobates tinctori~rsDendrobates truncattisDendrobates vanzoliniiDendrobates variabilisDendrobates ventrimaculat~rsPhyllobates lugzibrisPhyllobates vittatus

HylidaeAgalychnis craspedopusAnotheca spinosaCalyptahyla cr~icia lisFlectonotlrs issilisFlectonotzrs itzgerdd iFlectonotus goeldiiFlectonotus ohausiFlectonotus pygmaeusHyla bromeliaciaHyla dendroscartaHyla m arianaeHyla picadoiHyla wilderiHyla zetecki

detritusnon feedingnon feedingmacrophagy suspectedunknownnon feedingunknown

omnivorous and oophagousunknownunknownomnivorous

unknownpredatory, including cannibalismunknownconspecific eggsconspecific eggsunknownconspecific eggsdetritus possibly cannibalistic in lab)detritus, cannibalisticunknownconspecific eggsomnivorous cannib alistic and oophagous in lab)conspecific eggs

conspecific eggsdetritus, mosquito larvae, conspecific eggs, cannibalisticdetritus, mosquito larvae, conspecific eggs, cannibalisticomnivorous in laboratoryomnivorous in laboratory

unknownconspecific frog eggs, insect matterfrog eggs conspecific?)non feedingnon feedingnon feeding but see Weygoldt and Silva 199 1)non feedingnon feedingplant matter and detritusplant matter and detritusfrog eggs conspecific?)unknownfrog eggs conspecific?)frog eggs conspecific?)

Brazil nut capsulesbromeliadsbromeliadstree holes, snail shellstree holesleaf axils ofPandantis, tree holestree buttresses

giant bromeliadsbromeliadsbromeliadstree holes, bromeliads, stagnant potree holesbambooBrazil nut capsulesbromeliads, leaf axilsbromeliads, leaf axilsbromeliadsunknownbromeliadstree holes and trunks, bromeliadsbromeliadsbromeliadsbromeliads, terrestrial aroidsbromeliadsbromeliadstree holestree holestree holesbromeliads, tree holesbromeliads, Heliconia leaf axilstree holes and bromeliadstree holes and bromeliads

tree holes and buttressesbromeliads, tree holesbromeliadsbromeliadsbromeliads, aroidsbromeliadsgiant bamboobromeliads andHeliconia axilsbromeliadsbromeliadsbromeliadsbromeliadsbromeliadsbromeliads

Caldwell 1993; Caldwell de Araujo, this volumeCarvalho 1949Cannatella 1986Grandison Ashe 1983Scheel 1970Inger 1954; Denzer 1994Channing 1978

Bourne et al. 2001Dixon Rivero-Blanco 1985Myers et al. 1984

01s Silverstone 1975 ; McD iarmid Foster 1975Summers et al. 1999Morales 1992;K. Summers, pers. comm.Caldwell de Araujo 1998, this volumeK. Summers, pers. comm.van Wijngaarden Bolanos 1992Zimmermann Zimmermann 1985; Silverstone 1975Morales 1992; Schulte, 1999; K. Summers, pers. comm.Zimmermann Zimmermann 1985; Silverstone 1975Zimmermann Zimmermann 1980Summers et al. 2000Schulte 1986; K. Summers, pers. comm.Weygoldt 1980; Starrett 1960Zimmermann Zimmermann 1984Jungfer 1985Summers et al. 1999Summers et al. 1999Caldwell 1997K. Summers, pers. comm.Zimmermann and Zimmermann 1984; Summers 1999Silverstone 1976; Zimmermann 1982Silverstone 1976; Zimmermann 1982

Block et al. 2003Taylor 1954; Duellman 1970; Jungfer 1996Dunn 1926Duellman Gray 1983Kenny 1969Duellman Gray 1983Lutz 1954; Duellman Gray 1983Duellman Maness 1980Stuart 1948; Duellman 1970Taylor 1940; Duellman 1970Dunn 1926Robinson 1977; Duellman 2001Dunn 1926Dunn 1937; Duellman 2001


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ratios


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also exhibit a wide variety of parental care types. Of the tentypes defined by Lehtinen and Nussbaum (2003), phytotelmbreeders exhibit at least six (nest construction, egg attendanc e,egg transport, tadpole attendance, tadpole transport, andtadpole feeding).

The preponderance of parental care in pliytotelm-breeders

clearly relates to tlie constraints of these environments.Tadpole feeding, for example, has evolved numerous timesin several different lineages, probably in response to foodlimitation. Provisioning of tadpoles with eggs is known fromnutlieroils species of Dendrobates and, in a wide-rangingreview, Summ ers McK eon surninarize the work that hasbeen done on phytotelm-breeding dendrobatids. SurntnersMc Keo n also present original data on developmental plasticity,larval ecology, and the factors influencing egg, tadpole andclutch size in this lineage. Tadpole feeding also occurs in theOld World equivalent of dendrobatids, the Mantella fromMadagascar. In her paper, He yi~ ig xperimentallydemonstr tes

that oviposition sites (tree holes or bamboo stumps, in thiscase) are a limiting resource for Alantella l~~eviguta.ecauseof th e unique resource that pliytotelmata provide to phytotclm-breeding anurans, tlie denionstrated limitation of populationsize by oviposition site availability may bea general result inmany systems.

A question that has long intrigued he~ petolo gists s howpliytotelm breeding evolved in the first place. That is, whatwas the origin of this trait ? Phylogenetic information indicatesthat the ancestors of pliytotelm-breeding dendrobatids werelikely str ca ~n reeders (see Caldwell de Ar ai~ jo; umtilcrs

McKeon, tliis volumc). The pliylogcny of Lehtincn et 01.suggests tliat in the mantelline h og s of Madagascar; phytotelmbreeding evolved twice independently, but botli times frompond-breeding ancestors. This analysis also suggests tliatfacultative phytotclm dwelling was a precursor to obligatephytotclm breed ing in one lineage. A sinlilar transitional stepto obligate phytotelm breeding is hinted at by Caldwell and deArai~jo, ho observed facultative egg deposition in Brazil nutc a p s ~ ~ l c sy two basal, st[-eam-breedingdcndrobatids.

Tlicse studies (and others, see especially Kriigel Richter(1995); Jungfer (1996); K a ~ n / a/ . (2001); Lardner binLakim (2002), and Prochl (2002)) have used observational,experi~iiental nd ph yloge~ ietic pproaches to address a widevariety of questions. The research presented in this collectionof papers has contributed to an improved understanding ofthe ecological and evolutionary forces acting on phytotelm-brecding anurans and exemplifies the variety of research tliatis currently underway on anurans that brccd in these habitats.Of course, many questions remain unanswered. In tlie nextsection, we discuss the prospect of future research to addresssonie of tliesc reniainingproblems.

FUTURE RESEARCH DIRECTIONS

Given the nature of these micro-aquatic habitats, we expect

increased use of phytotelm systems to study the ecologyand evolutionary biology of anurans. An obvious advantageof working in pliytotelmata is that each phytotelm is a self-contained microcosm whose parameters (biotic, physico-chemical) can be precisely detennined. This is particularlyadvantageous in studies of tadpoles.

Phytotelmata are the simplest aquatic ecosystem used byvertebrates. Yet paradoxically, the diversity of tadpoles froiiithese small aquatic habitats rivals, if not exce eds, the diversityof all tadpoles found in larger pools and ponds. Considerthe following. Even within the same genus, phytotelm-dwelling tadpoles can be unusually long and thin (e.g.,Hy la de~~drosca r t a ,yla 61-omeliucia), or fat and wid e (e. g.,Hyla yicadoi, H yla zetecki). They can have no keratinizedlnouthparts (e.g., microhylids, such as Ratnanella triangu larisand Hoyloyhryne rogersi, and several Hyla). They can havethe typical denticle pattern of pond tadpoles, namely twodenticle rows above and three below tlic opening of the mouth

(e.g., Cro.s.sou actylodes hol cer *~~ ~an ni,olostethus h~*om elicola,Phl-)itmhyrn I-e.sin;fjcfi-ix). But they can also have mor e exoticdental formulas, with botli supernunlerary (such as 513 incertain Nyc,tixalzn spp.) or abbreviated rows (sucli as I11 inva riou s D e n ~ h h a t e spp.).

Because of tlie relativc simplicity of the environments inwhich thesc tadpoles live, we predict that our understandi~igof the functional (eco)morpliology of tlicsc tadpolcs willadvance faster tlian for pond larvae. Functionalmorphologistsunderstand the design of an organist11 when they can cossectlypredict its morphology froni its ecology, or vice versa. Wealready know, for exa ~ii pl c, nore about oral adaptations forpredation and oophagy in phytotelm tadpoles, such as thoseof Anothecrr and 0,steopilus hr-z~nt~cz/sWassersug I-loff,1979; Lannoo et a/., 1987), than about food processing andingestion in classical, pond-dwelling carnivorous tadpoles,such as those of S11ea and Ceruto~?hrj~.r.e also know tliattlic more ttenu te pliytotel111-dwelling tadpoles are designedfor insinuating tlicmselves in narrow clefts of leaf axils. Incontrast, more robust phytotelm-dwelling tadpoles are moreoften found in open trcc holes and other singlc arboreal tanks.

Phytotclm tadpoles that live in tanks (as opposed to leafaxils) can, in theory, bc observed easier tlian many tadpolesthat live in ponds. Thus, despite tlic fact that many phytotelmsitcs may be initially difficult to locate, once found, they canprovide excellent observatoriesfor tadpole behavior. It is thusnot su ~p ris ing hat some of the rnost complex and elegantbehaviors that any tadpoles have shown in relation to botli theirparents and predators have been documented in pliytotelmata.P h y t o t e l ~ i ~ystems are likely to continue to be exceptional inadvancing our knowledge of tadpole behavior.

The proliiise of pliytotelm systems to contributedisproportionately to our understanding of anuran behavioralecology extends to adults as well. Many adult frogs tliat usephytotelms are conspicuous and diurnal, particularly thosein the families Dendrobatidae and Mantellidae. Because of


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tlieir conspicuousness, herpetologists have a better chance oftracking their moveinellts and activities.

With intense direct field obselvation, w e may soon find outhow these frogs locatc phytotelmata in the first place. Do theyhunt for thein randomly, or do they have a Inore structuredsearch pattern? Is vision the primary sensory modality used,

or do they employ othcr sensory systerns, such as olfaction?Can thcy sense a humidity gradient with enough p recision thatthey can use it to locate a suitable phytotelm? If the frogs havehyper-sensitive humidity receptors, where are they located onthc hog s body? These are all tractable questions for which itis reasonable to expect answers in the near future. Whateverinforn~ationwe glean on how phytotelin-dependent speciesfind their brccding sitcs, we suspect it will be applicable toinore gcneralizcd aquatic breeding frogs. S imply because of thevisibility of thc adults and the discrete nature of phytotelmata,phytotclm-breeding species arc a choice model systein foraddressing tlicsc questions in tllc field.

In a similar vein, wc know very little about chemicalcornmimica tion in anurans, o ther than that it docs occur. The reis, lioweve~;good evid ence of intraspecific chemical signalingbctween pliytotelnl tadpoles and their inothcrs in at least onespecics that actively fccds its tadpoles (Ka m Che n,2002).Once again, because of the discrete nature and small size ofphytotclmata, phytotelm anurans are good ~ iio dc l rganisnlsfor identifying the inolec~~lcsnvolved. We expcct thesc~ i io lec i~ lcso be identified in the near future. This would thenopen tlie way to more reductionist questions about, amongother things, thc neurobiology of parent-offspring recognitionsystcms and thc evolution of thc signaling molecules.

Similarly, as several of the contributors to this collectionof papers have dc~nonstrated, ircct interspecific interactionsof pliytotclm tadpoles-both those that pertain to compctition,as wcll as prcdation-are accessible in inany phytotelmata.Sincc phytotcl~nataarc inesocosln systems that are naturaland complete, thcy can inform us about tadpole coinrnunityecology with far greater realism than what can be achievedwith tlic cattlc tanks colnnionly used in einpirical studies onanuran coinlnunity ecology.

Because of slnall clutch sizes, and the limited numberof adults in inany phytotelin systerns, a plcthora of classicqi~cslionsn population biology inay be more easily answeredwith anurans that use phytotelmata than more typical pond-

brecding frogs. For cxamplc, what li~ iii ts ispersal and gencflow in these anurans? Several of thc papers in the presentcollcction demonstrate thc potential of phytotelm-breedingspccics to answer these questions. Despite their largelytropical occurrence, inany phytotelin-using anurans are inoreamcnable to direct studies on population structure and geneflow than common pond specics. Indeed such studies arcalready underway.

In trying to map out future directions for phytotelln research,we are neither prescribing to others what research they shoulddo nor attempting to prognosticatc much beyond the obvious.

What is obvious to us is that interest in these anurans h as beenand will continue to be far greater than one would expe ct frointhe relatively limited numb er of spccies with arboreal tadpoles.Simply stated, thesc frogs are not just fascinating in their ownright; they are ideal for answering a multitude of questionsapplicable to the multitude of more generalized anurans.

ACKNOWLEDGMENTS

We thank numerous anonymous rcfcrccs for reviewing the syrnposiu~nmanuscripts and D. Frost for examining Table1 for nomenclatural problems.We thank the Ilcrpcto logist s League fo r gcnerously s upporting thissymposium. We particularly thankH. Ncying for her help in organizing thesympos i~ l lnn Kausas City and to J. Burch and the University of MichiganMuseum of Zoology Ibr facilitating the publication of this volume. We alsowould like to express our gratitude to W. Ducllman,K.-H. Jungfcl-, Y.C. Ka m,M. Maple s and 11. PI-ochl, for thcir enthu siasm for and participa tion in the2002 symp osium. Wasscrsug s res carch on anurans is supporte d by the NaturalSciences and Engineering Research Council of Canada.

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Misc. Puhl. M11.s. Zool., Univ. Mich., 2004, 193: 11-21

HISTORICAL AND ECOLOGICAL FACTORS INFLUENCE SURVIVORSHIPINTWO CLADES OF PHYTOTELM -BREEDING FROGS ANURA : BUFONIDAE,

DENDROBATIDAE)

Janalee P. ~aldwelll nd Maria Carmodna de ~rau jo

Sum Noble Oklahonicr Muselrn~ f Natfrval Hi st o~ y rnd Department of Zoology, Univet*.si~ f Oklui~oma, orman, Oklahomcr 73072 USA,E-mail:[email protected]

2~tl.stitLrto aeio~ral e P es q~ ~i su s a Amazcinia, Alumeda, Costne Ferreiva 1756, AAleho 69083. Manazrs, Bvasil

ABSTRACT

Tl~roughoutAmazonia, Brazil nut trccs Lccythidaccac,BerthoNetia excel.sa) produce a grapefruit-sized fruit with a thick, woodypcricarp that is f~~nctionallyndchiscent; each fruit contains25 or more seeds Brazil nuts). After falling to the ground, the fruit capsulcsarc chcwcd open and emptied of their seeds by agoutis genusDasypr-octu). The empty capsules rc~nain n the forest floor and fill withrainwater. Five Amazonian frog species in two cladcs, Dendrobatidae and B ufonidac, and two illsects with predaceous larvac use Brazilnut capsulcs for some aspects of reproduction. Thcse small microl~ab itats ack some kinds of prcdators fish) but have othcrs insects) andcan have limited food and low oxyg cll levels. Interactio ~ls mong tadpolcs and insect larvac and the possible effects of Sood limitation andanoxia wcrc studicd at thrcc sitcs in Brazil.Bufo cct.stmeoticrr.s deposits clutches of eggs that are small compared to most oth er species inthc g c ~ n ~ smean number o f cggs: 1 78 at one locality and 234 at another locality). Survivorship of eggs ofBr~fo astuneoticr~.~ t all sitcswas low. Mean volume oSwatcr in the capsules at two localities was 110.9 ml and 132.4 ml; thus, cggs and larvae arc crowd ed, presu~llablyleading to anoxia, cspccially in the absence of rainfall. AII experiment in which tadpoles werc raised with and w ithout Sood revealed thatnlchm orphosi s d ocs 1101 occur in unfed tadpolcs; thus, b o d li ~nitationmay decrease growth and survivorship. Damselfly la ~v ae ccursignilica ntly inore Srcclucnlly with tadpolcs o fBz~li, han in all capsulcs in the sample s. These factors appcar to providc a cornpctitivcrclcasc forBrrfi, tadpolcs; reduction of tadpole density may increase the probability that some individuals will survivc. If they are the firstcolonizers, thc predaceous tadpolcs ofDendrohates can elin~ ina tc redators from the capsulcs. More basal cladcs of dcndrobalids havedctritivo rous Vadpolcs that arc not capable of eliminating prcdato rs from the capsules. Although Lhcy primar ily use small forest poolsand strcaln cdgcs for tadpolc dcposition, tadpolcsof Allohrrles fi.movulis and Colo.stetl~~~,sp. were transported occasionally to Brazil nutcapsules, where their survivorship was low compared toDeridrohnte.~. The propensity of individuals in basal cladcs for depositing som etadpolcs in phylotcl~llata nay have Icd in p a ~ to the evolution of use ofphyto tclmata by the derivedL)cndrohates once a predaceous tadpolecvolved. Occasiotlal dcposition of tadpolcs in phytotelmata by basal dendrobatids may representa transitional step from obligatc tadpolcdeposition in forest stl-cams or pools to Sacultativc phytotclm tadpolc dcposition to obligatc phytotclm deposition(Dendr-ohutes).

Key words: Ruh nid ac,Br fi~, ccrslcrr?eotic~~r.s, cndrohatidac Allohcrle.s A. fernovtrli.~, lc~t~dr-ohotrs, ca.stcrneotir.rrs, D. q1rir7q~1e1~ifttrt1rs,E/)i/)e~lohnte.s, olo.stc~tl~r~.s,hytotclmata, Brazil nut capsulcs

INTRODUCTION

Thc carliest frogs utilized pond-type bodies of watcr Sorbrecding Ducllm an Trueb, 1986). As is typical today,these sites may havecontained large numbers of prcdators thatIcd in 13x1 to the evolution of tcrrestrial inodcs of breedingto avoid preda tion of cggs and larvae. Evidence for the roleof predation as a majorselective force for deposition of eggson land was provided by Mag nusson He ro 1991). In theprcsent-day temperate zone, most frogs still breed in ponds,but scasotiality buffe rs prcdation to some extent. Tem porary

ponds dry out, and many species of frogs breed early inadvance of insects, thus avoiding larval insect predationSkclly, 1996). In the tropics, a more equitable climate may

havc contributed to diversification of frogs by allowing use ofwater bodies other than ponds. Tropical species within manycladcs use various types of phytotelmata, or plant-held watersFish, 1983; Schiesariel nl., 1996; Jung fer Weygoldt, 1999).

Exatnples of these mic rohabitats includ e tree holes, vine holes,bromcliad tanks, leaf axils of various herbaceous plants, andhusks of various types of fruit that fall to the ground and holdwater.

Thcse phytotelmata, while generally providing safety Fromsomc kinds of predators such as fish, present other kinds ofchallenges. For exam ple, certain insects with predaceou slarvae have evolved to use thcse contail~er abitats for eggdeposition; thcse larvac readily capture small tadpoles. Foodresources are limited in these small microha bitats. In some,especially s~ na ll ine and tree holes and fallen fruit husks,the absence of light precludes algal growth and detritus maybe limited or lacking in nutrients. In addition, the amou nt ofwater hcld in som e types of phytoteltnata is generally small, sooxygen depletion can be a problcm or desiccation can occur ifrainfall is insufficient.

Brazil nut capsules provide acommon type of phytotelmatathroughout most of Amazonia Mori, 1992). Brazil nut treesLecythidaceae,Bertholletia excelsa occ ur in stands of 1 or

more trees in terra firme forest throughout the region MoriPrance, 1990). The capsular fruit has a thick, woody pericarpthat is functionally indehiscent; each fruit contains 25 or moreseed s Brazil nuts). After falling to the ground, capsules arechewed open by agoutis genus Dasypro cta); the seeds are eatenor cached by these large rodents. The em pty capsules remainon the forest floor and fill with rainwater, where they are used


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during som e phases of reproduction b y scveral species of frogs biotic and abiotic factors that affect survivorship of eggs andin the clade Dend robatidae and one species in Bufonidac.In tadpoles of Bufo castaneoticus and survivorship of tadpolesaddition, a giant damselfly (Pseudostigmatidae, Microstigma of D quinque vittatus and Allohates ,femorali.s. Specificallyat?omalzim) and a m osquito in the genu s T oxorhynchites we examined the effects of anoxia, desiccation, availability ofdeposit cggs in the Brazil nut capsules and have predaceous food, and predation on survivorship of these species.larvac (Steffan Evenhuis, 198 ; Corbet, 1983; Lounibos et

a/. , 1987; Caldwell, 1993). MATERIALS AND METH ODSWithin Dendrobatidac, nearly all species are diurnal,

deposit terrestrial eggs, and transport tadpoles on the parent'sback to a suitable aquatic site for the rcrnainder of thetadpoles' development (Zug et a]., 2001). Within the mostderived dendrobatids (the genus D endrobates), all species usesome type of phytotelrnata for tadpole deposition (Caldwell

Ara i~ jo ,1998). Some exam ples of types of phytotelrnataused include relatively large tree holes ( D e n h b a t e s auur-atus,Suniiiicrs, 19 89), tiny tree or vinc holes (De ndroba tesvanzolinii, Caldw ell, 1997; Caldw ell Oliveira, 1999), andplant axils or bromeliad tanks (Dend~*obate~~tanilio, Bri~st,

1993; D . ventrirnactrlattis, Sum mers Amo s, 1997).Two specics, Dmdi-obates crrstaneoticzis and Dqtiinqzievittutu.~, are known to use Brazil n ut capsules astadpole development sitcs (Caldwell, 1993; this study). D.crist~meoticzi.~s restricted in distribution to a s~ n al l rea in tliestate of Pa ra, Bra zil, and D. quinqzievittatzis occurs in e asternRondania (Caldwell Myers, 1990) and wcstern Am azonas,Brazil (JPC , unpubl. data). Brazil nut capsules appear to betlie primary microhabitat uscd by D. castaneoticus. A fcwtadpoles of this species were found in fallen water-filled palmpetioles, but these m icrohabitats were not common. Tadpolesof D qz~ingzievittatzis ave been found in various kinds ofpliytotehiiata (Caldw ell My ers, 1990). Tadpoles of bothspecies attain a ~i iaxill iurn otal length o f about 30 lnln and~iietamo rphose n about two months.

Within Bufonidae, most species deposit large clutchesof eggs in s~ iia ll ools, tempo rary ponds, or stream edges(Cru mp , 19 89). In contrast , Bzlfi, caLstaneoticzrLss a phytotelm-breeder, depositing cggs primarily in Brazil nut capsules butoccasiona lly in fallen palm petioles. Bz~foca.rtaneoticza s a leaflitter frog and docs not use arboreal pliytotelmata. Tadpoles ofthis species are small (ma ximu m total Icngth, 12 mm ) and timeto metamorp hosis is relatively brief, about 16-20 d ays. Ascurrently recognized, this species is widespread from easternAm azonia in Brazil to Am azonian regions in Peru and Bolivia(de la Riva et crl., 2000). Future taxonom ic work is necded todetermine whether more than one species is involved.

We investigated colonization rates and tadpole-insectinteractions in Brazil nut capsules at three localities, two ineastern Brazil and one in western Brazil (Caldwell, 1993;Caldwell A rai ~jo , 998). Priority ofcolonization determinedthe outcome of interactiolis between the predaceous tadpolesof D endrobate s castnneo ticu.~ and predatory insect larvae(Caldwell, 1993), although cannibalism was the primarysource of mortality of tadpoles of D. ca.stuneoticus (Caldwell

Ar ai~ jo, 998). T he purpose of this study was to investigate

Colonization by and interactions among anurans andinsects in Brazil nut capsules were studied in two ways:ICapsules were located throughout the forest and organisnisinhabiting them were examined and identified. No capsulewas examined more than once. This procedure was carriedout at all tliree sites and provided a snapshot of co-occurringorganism s. 2) At the two eastern sites, tlie Rio Xingu a nd RioCurua -Una, grids of capsules we rc established in tlie forest andorganisms were allowcd to colonizc naturally; capsules wereexamined every other day for several months. A variation onthis method was used at the western site in Rond8nia; insteadof establishing a grid, capsules were located in the forest,flagged, and examined every four days to study colonization,survivorship , and interactions of tlie organisms. Datacollectedon the first day after these capsules wcre flagged allowed asnapshot comparison with the field-sampled capsules from thetwo eastern localities.

Organisms in the capsules werc examined by pouring thecontents of a capsule into a white enamel tray. Tadpolcs ofDendrobates, Bufi castaneoticus, and Allobates,femorali.s inthe capsules were counted. In the field-sam pled capsules thatwere examined only once, tadpoles were preserved in 10%formalin and were later measured and staged according toGosne r (1 960). Tadpoles in capsules followed ove r time werecounted and measured nearly each time the capsules wereexamined. In some cases, newly deposited eggs or developingembryos of B custuneoticus were not disturbed but werecounted at a later time to avoid inadvertent mortality. Larvaeof the two species of insects werecountcd and measured inall capsules. A flashlight was uscd to carefully search forsmall insects, particularly damselfly larvae that solnetimesclung to the inside walls of the capsule. Most o f the followingmeasurements were taken on each capsule at all sites: outercircumference at the greatest width of the capsulc; m ajor andminor orthogonal axes of the opening; depth of watcr inside

the capsule; volume of water; and pH .Study areas. We examined Brazil nut capsule systems

at tliree study areas, all lowland tropical forest sites. Thchydroperiod for capsules in all three regions is approximately5 mon ths (length of the rainy season). Rio Xingu (hereafterRX), located in the statc o f Para at 3 22'S, 5151 'W, wasstudied in 198 7; Rio Curua-U na (RC U), also in the stateof Para, located 101 km south and 18km east of SantarCm(3 8'44.3 S, 54 50'32.9 W ), w as studied in 1995; and ParqueEstadual Guajari-Mirim (PEG-M), located at 1O 19' 17.2 S,64'33'47.9 W in the state of Ro nda nia was studied in 1998.


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At RX and PEG-M, forests were undisturbed. At RCU,sections of the forest were selectively logged about 8 yearsprcvious to the study; however, thc actual study site had nocvidencc of recent logging. Caldwell and Araujo 1998)providcd additional details concerning RCU, and Caldwell1993) providcd details of the RX slte.

At RX, interactionsamong Dendrobates castaneoticus Bufocastaneoticus and the two larval insect predators were studiedby cstablishing a grid of 40 capsules and following them everyothcr day for 52 days from 18 January to 10 March Caldw ell,1993). On e hundred thirty-five field-sampled capsules werelocated in the forest horn 7 Fcb to 7 M ar and examined once.Solnc tadpolcs of Co1osteth~l.s were obscrved in the capsules,but data on this species wcrc not recorded.

At R CU, the same four specles co-occurred. A grid of 40capsules was established and followed every other day for 55days from 26 February to 21 April. Thc grid was arranged infive lines, each with eight capsules; the lines were irregular

to miniic their natural distribution and also to prevent insectsfrom flying in a straight line and ovipositing in each capsule.Additional details pertaining to the establishment of the R CUgrid arc given in Caldw ell Araujo 1 998). A sample of 101capsules located at random in the forest was exanlined from 16Fcb to 15 Apr at this site.

At RCU, we also investigated whether tadpoles of u f icastaneoticus could complete m etamorphosis without feeding.The ability to do this would negate the idea that competitionfor li~ nit ed ood in the capsules was influencing survivo rship.We established an experiment in which tadpoles were raisedunder identical conditions, but some were fed and some were

not. Wc obtained a clutch of 189 cggs deposited the morningof 9 Mar. When the eggs hatched the following evening, weselected 60 that wcre appro ximately the same size. Wet Inassof 10 of these was obtained by w eighing them together; thesewerc not uscd in the expe ri~n ents.The remaining 50 tadpoleswere established individu ally in 20 1n1 of rainw ater placedin 30-1111 vials; a random numbers table was used to assigntadpolcs to the two treatments. Tadpoles were fed and thewater was changed every three days; for the first two feedingpcriods, they wcrc fed Tetra Pelleted Food fo r Goldfish 0.20 gpellctlvial) and thereafter they werc fed with eq ual amoun ts ofenough leaf litter debris from a nearby pond to cov er the bottom

of the vial. Meta~ norphosiswas defined as the presence of atail stub; metamorphs w ere weighed to the nearest 0.002 g.At PEG-M, work on the Brazil nut system was carried

out for 75 days, from 25 January to 9 April; capsules wereexanlined evcry fourth day. Dendrobates quinquevittatuswas moderately common in this area and was the primaryanuran that used Brazil nut capsules. Bufo castaneotic~~soccurred within 10-20 km G.R. Colli and A.A. Garda, pers.conim.) but was not found in the immediate vicinity of thestudy site. Allobates jemoralis vocalized in the study area,but only two tadpoles were found in Brazil nut capsules. Asinglc Colostethus tadpole another dendrobatid) was found in

a capsule at this site. A s at the two sites in eastern Brazil, giantdamselfly larvae in thc genusMicrostigma and larvae of themosquito Toxovhynchites were foun d in Brazil nut capsules.

Seventy-one field-sampled capsules were located in theforest at PEG-M over a period of 13 days from 25 Jan to6Feb. Data recorded for these capsules on the first day each

capsulc was flagged were used as a snapshot to compare withdata from the field-sampled capsules at the two eastern sites.Tlic 7 1 flagged capsu les wcre su bsequently ex amined evcryfourth day.

Statistical analyses were carried out using Statview AbacusConc epts, 1992). All means are SD. Tadpole size refers tototal length measured from tip of snout to tip of tail).

RESULTS

Water volume in field-sampled capsules was significantlydifferent amo ng thc three sites ANOV A, F,,,,, 20.0,p

Documents

Ecology and Evolution of Phytotelm-Breeding Anurans