Wake 1987

Adaptive Radiation of Salamanders in Middle American Cloud Forests
Author(s): David B. Wake

Source: Annals of the Missouri Botanical Garden, Vol. 74, No. 2 (1987), pp. 242-264
Published by: Missouri Botanical Garden Press
Stable URL: http://www.jstor.org/stable/2399397 .
Accessed: 27/05/2014 14:42
Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at .
http://www.jstor.org/page/info/about/policies/terms.jsp
.
JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of
content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms
of scholarship. For more information about JSTOR, please contact support@jstor.org.
Missouri Botanical Garden Press is collaborating with JSTOR to digitize, preserve and extend access to
Annals of the Missouri Botanical Garden.
http://www.jstor.org
This content downloaded from 91.155.186.71 on Tue, 27 May 2014 14:42:15 PM

All use subject to JSTOR Terms and Conditions
ADAPTIVE RADIATION OF SALAMANDERS IN
MIDDLE AMERICAN CLOUD FORESTS'
DAVID B. WAKE2
ABSTRACT
Tailed amphibians, or salamanders, occur in the tropics only in the New World, where theyare
concentratedprimarilyin Middle America and northwestern South America. All are membersof the
familyPlethodontidae,the lungless salamanders. As recentlyas 1926 only 30 species of tropical
salamanderswere known,and all were placed in a singlegenus. Today 11 generaare recognized.All
occur in Middle America,and over 140 species have been described.Many local tropicalregionsare
veryrich in numbersof species, and as many as 21 species may be presentalong a singlealtitudinal
gradient.Communityorganizationof species of salamanders in the tropicsdiffersfromthat in tem-
perate regionsin that species of tropical salamanders tend to be segregatedinto discreteelevational
zones, withanygivenspecies restrictedto a narrowelevationalband. Withinelevationalzones, species
are segregatedbymajor habitattype,thenbymicrohabitat,body size, and finallytrophicand behavioral
features.Cloud forestsat middle elevations, fromabout 750 m to 2,500 m, are especially rich in
salamanders, in both diversityand density. In Nuclear Central America nearly 50% of arboreal
bromeliads in a local sample (N = 903) contained salamanders. Some species are found almost
exclusivelyin bromeliads, and over 30 salamanders have been encounteredin a single bromeliad.
Farthersouth,in Costa Rica, cloud forestsharbor salamanders in bromeliads as well as in arboreal
and terrestrialmoss mats. Extrememicrohabitatspecializationenrichesthe Costa Rican fauna to the
maximum numberof species presentlocally anywherein the tropics.In the relativelylower latitudes
(e.g., Costa Rica and Panama) the proportionof species occurringat lower elevations increasescom-
pared withMexican and Guatemalan transects.
Bromeliads and moss mats in the mid-elevationalwet and rain forestsare ideal microhabitatsfor
these insectivorous,direct developing amphibians. Bromeliads offerabundant food resources,egg
deposition sites, protectionfrom predation,and microenvironmentsbufferedagainst temperature
extremesand low humidity.Salamanders are top carnivoresin the bromeliad microhabitat.
The extensiveadaptive radiationof plethodontidsalamandersin Middle America has featuredboth
convergentand parallel evolution.The mid-elevationalcloud forests,withtheirrichepiphyticassem-
blages and highlydissectedtopography,have been of greatsignificancein speciation,morphological
and behavioral diversification,geographicalecology,and historicalbiogeographyof tropicalpletho-
dontid salamanders.
The cloud forestsofMiddle Americaare home general,cloud forestsformbetweenelevationsof

to a unique group of vertebrates-lungless, about 800 and 2,700 m. Both upper and lower
climbingsalamanders thatbelong to the family boundaries shiftwithclimaticchanges,withthe
Plethodontidae.By "cloud forest"I referrather lowest occurringalong humid slopes in the low
loosely to those forestassemblages which form latitudes and the highest being found in the
in the presenceof fog.Clouds condense at vary- northerntropicsalong the Pacificslopes.
ing elevational levels in Middle America, de- Cloud forestsofferideal conditionsfortropical
pendingon manylocal and regionalfactorssuch salamanders,all of which are nonaquatic, direct
as temperatureof thewaterof the nearestocean, developingspecies. Althoughtheydo not breed
topography,rainfallpatterns,and wind direction in water, these organisms neverthelessrequire
(Grubb & Whitmore, 1966; Myers, 1969). In moistconditionsforactivity,and thecloud forest
involvingmanyindividuals,especiallyJames
I Research reportedin thispaper has been a collaborativeeffort
F. Lynchand Theodore J. Papenfuss,both of whom have given helpfulcriticismsof the manuscript.Marvalee
H. Wake carefullyreviewedthe manuscriptand David Darda and Nancy Staub also provided usefulcomments.
My researchhas been supportedby the National Science Foundation and the Museum of VertebrateZoology.
I gratefullyacknowledgethe cooperation of governmentalagencies in Mexico, Guatemala, and Costa Rica in
obtainingpermissionto conduct researchin theircountries,and Douglas Robinson and Pedro Leon fortheir
help and cooperationin Costa Rica.
I dedicate thispaper to the memoryof L. C. Stuart,who generouslyofferedhis unparalleledknowledgeof the
Guatemalan herpetofaunato me, and whose published work remains as an inspirationto futurestudentsof
Guatemalan and othertropicalenvironments.
2 Museum of VertebrateZoology and Departmentof Zoology, Universityof California,Berkeley,California
94720, U.S.A. Paper received 7 July1985.
ANN. MISSOURI BOT. GARD. 74: 242-264. 1987.

1987] WAKE-ADAPTIVE RADIATION OF SALAMANDERS 243
environmentsare effectively bufferedfromdes-

iccatingconditions as well as fromextremesof
5,6
temperature.In addition,these foreststypically 8,13
supportabundantepiphytesthatare used exten- .40'
10,27
14,589
sivelyby salamanders. 14,41
There are more than 140 species of pletho- 6,15
dontid salamanders in the New World tropics; 2? 20

2,14
11,85
about 80% occur in Middle America (Wake & 5,41
Lynch, 1976; Frost, 1985). What makes them 343
unusual is theirgreatdiversityin theNew World 1,6

tropicsand theirtotalabsencefromtheOld World PLETHODONTIDAE 1,2
tropics.Middle America has been the settingfor 0 2000/12
an extensive,unique adaptive radiationthathas

remainedverylocalized.
FIGURE 1. Latitudinalgradient andspecies
ofgeneric
The success of these species can be measured inthesalamander family The
Plethodontidae.
diversity
against that of salamanders generally.World- numbersof genera(firstfigure) and species(second
wide, thereare about 350 species ofsalamanders thatoccurin zonesoffivedegreeslatitudeare
figure)
divided among nine families(Frost, 1985). Eight indicated.Data are availablefromtheauthor.Unde-
families are restrictedto North Temperate re- scribedspeciesforwhichdescriptions are beingpre-
paredhavebeenincluded.
gions. Over 200 of the species are members of
thefamilyPlethodontidae,the onlygroupof sal-
amandersto radiatein tropicalregions.All trop- use a highlyspecialized, extremelyfast tongue
ical species of salamanders are members of the projection mechanism to capture moving prey
supergenus Bolitoglossa (Wake, 1966), which at a considerabledistance,and thustheyare able
contains 11 generaand about 40% of the species to feed on a wide arrayof invertebrateanimals.
of salamanders in the world. The supergenusis We stillknowrelativelylittleabout thetropical
exclusivelyNew World in distributionand does plethodontids.The authoritativework of Dunn
not occur northof Mexico. (1926) listed but 30 species and placed them all
The plethodontidshave a curiousdistribution, in a single genus. Taylor (1944) recognizedthe
with two primaryareas of evolutionarydiver-
genericdiversityofthegroup(seven genera),but
sification:NorthAmerica withconcentrationin fouradditionalgeneraweredescribedas recently
the Appalachian region, and Middle America as 1983 (Elias & Wake, 1983; Wake & Elias,
(Fig. 1). In easternNorthAmericaare foundthree 1983), and about one-halfofthe 140 specieshave
majorgroupsofplethodontids, twoofwhichhave most
been describedsince 1950. Not surprisingly,
life historiesinvolving an aquatic larval stage.
published work has dealt with taxonomy and
The Middle Americanregioncontainsmembers
systematics,although there has been some re-
of a fourthmajor group,the tribeBolitoglossini,
searchon lifehistory(Vial, 1968; Houck, 1977a,
membersof which have a uniphasic lifehistory
1977b) and geographical ecology (Schmidt,
featuringdirect development without a larval 1936a; Martin,1958; Wake & Lynch,1976; Wake
stage (Wake, 1966). The othertwo supergenera et al., 1987).
in the Bolitoglossinioccur in Californiaand Or-
The presentpaperattemptsto evaluate therole
egon (and possibly in Alaska and Mexico), and of epiphyticcommunitiesin theevolutionof the
on Sardinia, the Italian mainland, and a tiny
neotropical salamanders. I summarize infor-
portionof southeasternFrance. mationthatmyresearchcollaboratorsand I have
I have arguedelsewherethatthe absence of an
gatheredover the past 15 years. In particular,I
aquatic larval stage facilitatedoccupancy of the examinetheresultsoftransectstudiesfromMex-
relativelydenselycrowded,predator-rich tropics
ico to Costa Rica and concentrateon an area that
(Wake, 1966; Hanken et al., 1980). A unique
appears to have been of criticalimportancefor
feedingmechanismand an associated behavioral
salamanders,the mid-elevationcloud forests.
repertoire(Lombard & Wake, 1977, 1986; Roth
& Wake, 1985a, 1985b), which could evolve its GEOGRAPHY AND SYSTEMATICS
ECOLOGICAL
particularcharacteristicsonly in a grouplacking
aquatic larvae, may have aided in the successful Salamanders in the tropicshave diversifiedin
radiationof the tropical species. Those animals threemajor regions,each characterizedby a rel-

244 ANNALS OF THE MISSOURI BOTANICAL GARDEN [VoL 74
OLD
NEW
0 I. 2- 36~ s
FIGuRE 3. Chiropterotriton a bromeliad-

arboreus,
dwellingsalamander fromnear Zacualtipfin,Hidalgo,
ACTWE Mexico. This species has the typicalfeaturesof a bro-
meliad specialist:a long prehensiletail, relativelylong
legs,largehands and feetwithwidelyspreaddigits,and
frontallydirectedeyes. The finedivisions on the scale
are mm.
gion 3, and onlyone species extendsas farnorth

FIGURE2. Generalized map illustratingregionsof as Chiapas. The alpha assemblageofBolitoglossa
major evolutionarydiversificationwithin the family
is centeredin region 3 and areas to the south,
Plethodontidaeduring Cenozoic times. Some major
but a distinctspecies group extends northwest-
faultsystemsare indicated. The familyis thoughtto
ward to the othertwo regions.The genus Noto-
have originatedin the old and tectonicallyrelatively
tritonis somethingof a puzzle (see below). It has
stableAppalachian region.For much of the Cenozoic,
representatives of the familyhave been undergoingan
species in all threeregions.
adaptive radiation in what is today Middle America, Earlyzoogeographicbiases combined within-
withdiversification concentratedespeciallyin thethree
adequate collectingled to the perceptionoftrop-
core regionsindicated:the southeasternmarginof the
Mexican Plateau, Nuclear Central America, and Ta-ical salamanders as northerninvaders that had
lamancan CentralAmerica. Two supergenerawithaf- "trickled" down into the tropics. Dunn (1926)
finitiesto thetropicalsupergenusBolitoglossamayhave
placed all 30 species thenrecognizedin a single
been involved in a reinvasion of temperate North
Americathroughassociationwithland movementsand
genus, and several of his species groups later
provedto be polyphyletic.
tectonicactivityin the extendedSan Andreas faultsys- For example,he united
all elongateanimals intoone group,and all small,
tem. For more detailed analysis of geological history
in relationto salamanderdistributionsee Hendrickson
bromeliad dwellers into another, thereby ob-
(1986). scuring the extensive parallelism and conver-
gence that have occurred. Even afterTaylor's
atively ancient tectonic core, high topographic (1 944) generallyprogressivedivisionofthegenus
diversity,and hightectonicactivityalong some Oedipus into several genera, the bias of recent
borders.From northto south,these regionsare:
1) the southeasternmarginsof the Mexican Pla-
teau and the highlandsof northernOaxaca, 2)
Nuclear Central America, and 3) Talamancan
CentralAmerica (Wake & Lynch, 1976; Fig. 2).
Each regionis characterizedby species richness
and a highdegreeof endemism (Savage, 1982).
For example, Chiropterotriton,Lineatriton,
Thorius,and Parvimolgeare endemic to region
1, and Pseudoeuryceaoccurs mainlyin region 1
withonlya fewspecies in region2. Dendrotriton,
Bradytriton, and Nyctanolisare endemic to re-
gion 2, and the greatmajorityof the species of
the beta assemblage of the large genus Bolito- FiGuRE 4. Dendrotriton xolocalcae,a bromeliad-
glossa occur there. The few species of Bolito- dwelling salamander fiom the upper slopes of Cerro
Ovando, Chiapas, Mexico. This bromeliad specialist
glossa beta which occur in regions 1 and 3 are shares many gross stnrcturalsimilaritieswith species
membersof distinctsubgroups(see Papenfusset thatoccupysimilar microhabitats(Figs. 3, 5). The scale
aL, 1983). The genus Oedipina is centeredin re- bar is 25 mm.

915*
20'
/M
L.
* M
4E 1
Dendrotr'1cV.
FIGURE 5. Nototriton veraepacis, a bromeliad-
dwellingsalamander from 10.5 km N Santa Cruz. Za-
capa, Guatemala. in the Sierra de las Minas. Compare
thisspecies withunrelatedbromeliadspecialistsin Fig-
ures 3 and 4. The scale bar is 25 mm. 0 4,00 so
penetrationfromthe northpersisted.The genus FIGURE 7. Distributionof the genus Dendrotriton.

Chiropterotriton as recognizedpriorto 1983 pro- Species of thisgenus are bromeliad specialistsrestrict-
ed to cloud forests.All occupysmall geographicranges,
vides an example. Its species mainly are bro- and only D. rabbi occurs in more than one of the iso-
meliadspecialistslivingin cloud forests,and they lates indicated here (Elias. 1984).
are superficiallysimilar in externalmorphology
(Figs. 3-5). Both Rabb (1960) and Wake (1966)
recognizedthat members of the genus differed Costa Rica (Figs. 3-5). Based on theirstudyof
substantiallyin osteology,but theychose to in- comparative osteology,Lynch & Wake (1975,
terpretthis as increasing divergence and spe- 1978) recognizedthatthe species below the Isth-
cialization toward the south. This especially in- mus of Tehuantepec formeda cladisticallydis-
structivecase is relevantto the main theme of tinctgroup,which theytermedChiropterotriton
this paper and is developed furtherbelow. beta. The lattergroup was found to include at
Species once assigned to Chiropterotriton are
typicallysmall, slender, long tailed, acrobatic
forms,thatare common inhabitantsofcloud for-
ests in Mexico, Nuclear Central America, and
IS -, w Lss--
."J
N -,<
l fbtoriton l
. K.0 9 I
FIGURE 8. DistributionofthegenusN~ototriton. 1This

genus may not be a monophyletic group. The species
FIGURE 6. Probable distributionof the genus Chi- are all small and resemble one another in many external
ropterotriton.
Most species occur in cloud forests,and morphological and ecological features. All of the species
a numberutilizebromeliadsas microhabitats.The gen- inhabit cloud forests, but the Costa Rican species use
ealized ranges were derived by groupingknown lo- moss mats as a primary microhabitat. while the Gua-
calitiesinto potentiallycontiguousunits.based on for- temalan and Honduran species are bromeliad special-
est distribution.Informationgathered by David M. ists. The Chiapan and Oaxcacan records are based on
Darda and the author. recentlv discovered and as yet undescribed species.

246 ANNALS OF THE MISSOURI BOTANICAL GARDEN [VOL. 74
caz
.
on:- c)-:
N
CerroSon Felipe 0I
C3 1--
3000- (nN CerroPei6n K O
3000 OadByo| l;><U-K Pine < | F~l~s,; |
Hg
| Pine Oak Forest a Ah :ine-Or Forest
F a
n
I .0~~~~~~~~~
flO
2000 we~
lz o et X m
|i
-'
000 Guelatoo ~~~~~Forest

~~~~~~~~~~~~~~~~~~Evergreen
:
I Seasonal X L].
I
?X
a) D | Low Deciduous Forest
+- SW 0I Kms NE
FIGURE9. Distribution
ofplethodontid
salamanders
alongtheNorthern
Oaxacantransect,
about100kmin
length,
extending fromCiudadde Oaxaca,overCerroSan Felipeand theSierrade Juarez
north-northeastward
to thevicinity
ofTuxtepec,Oaxaca, Mexico.The northernslopesoftheSierrade Juarezare occupiedby an
extensivecloudforestwhichoffers
habitatto numerousspeciesof salamanders.
Updatedversionofdiagram
presentedbyWakeet al. (1987).
least two distinctsubgroups,an interpretation and it occurs in regionsof Caribbean drainage.

subsequentlysupportedby molecular biological An undescribedOaxacan species of Nototriton
data (Maxson & Wake, 198 1). The two southern occurs in sympatrywithan undescribedspecies
groups finallywere given genericstatusas Den- of Chiropterotriton, an association that was un-
drotriton and Nototriton by Wake & Elias (1983), expected. Both were discovered as a result of
who noted that Nototritonmight prove to be detailedstudiesofverticalzonation along a tran-
paraphyletic.Some species of each of the three sect (Fig. 9). Our knowledgeof the groupsprob-
generaresultingfromthe subdivisionof Chirop- ablyremainsfarfromcomplete,even at thealpha
terotriton include membersthatare verysimilar taxonomiclevel,buttheyclearlyofferfascinating
in externalmorphology.Because the species are opportunitiesfor the study of convergentevo-
very small (frequently<40 mm in head plus lution.
body length), the critical differencesin mor- Lynch& Wake (1 9 78) showed thatbromeliad-
phologycan be difficult to detect.The species of inhabitingspecies currentlyplaced in the genera
thethreegeneratypicallyhave small ranges,and Dendrotriton and Nototriton resembleeach other
thewidelydisjunctrangesofferlittleopportunity very closely in externalmorphology.The bro-
for sympatry.These salamanders are found meliad-dwellingspecies of Nototritonare more
mainly in isolated cloud forests,and several of similar to bromeliad-dwellingspecies of Den-
them remain rare and poorlyknown. drotritonin externalmorphology(evaluated by
Until recentlywe thoughtthat Chiropterotri- methodsofmultivariatemorphometrics)thanto
ton, Dendrotriton,and Nototritonwere exclu- semi-fossorialcongenersthat live in moss mats
sivelyallopatric(Figs. 6-8). Chiropterotritonoc- on soil banks.These distantlyrelatedspecieshave
curs as 11 or more discretegeographicisolates convergedso thattheysharebody formsthatare
in easternMexico, northof the Isthmus of Te- especiallywell suited forlife in bromeliads. In-
huantepec.Dendrotriton is foundonlyin Nuclear deed, if Nototritonis, as I believe, paraphyletic
Central America, mainly on Pacific slopes, but it is possible that we actually have underesti-
also in some internalregionsofCaribbean drain- mated the trueamount of evolutionaryconver-
age. Nototriton is thesouthernmostofthisgroup, gence.

The three genera discussed above are com- spread Gulf-Caribbeanslope speciesB. rufescens
monly encounteredinhabitantsof cloud forests (Taylor & Smith, 1945), which rangesfromSan
and epiphytes.Othertropicalsalamandergenera Luis Potosi, Mexico, to Honduras. The onlytwo
also contain cloud forestinhabitants,and many species of the beta assemblage that reach Costa
use epiphytesas theirmain microhabitats.Some Rica (B. alvaradoi,B. arborescandens)have been
of these,such as the Nuclear CentralAmerican takenin bromeliads(Taylor,1954; unpubl.data).
Nyctanolisand Bradytriton, are recentlydiscov- Occurrenceof membersof the largealpha as-
eredand theirhabitsare verypoorlyknown(Elias, semblage of Bolitoglossa in bromeliads is less
1984). The monotypic Mexican genera Parvi- well documented.The distributionof thisgroup
molgeand Lineatriton(thelatteran elongatefos- is centered in the Talamancan region and in
sorial formthat utilizes moss mats to some de- northernColombia; only the mexicana group
gree; Fig. 11) are relativelyrare within their (Wake & Lynch,1976) occursas farnorthas the
restrictedranges,which lie at the lower margins easternmarginsof the Mexican Plateau and Nu-
of cloud forests.Some species of the Mexican clear Central America. The mexicana group is
genus Thoriusoccasionally occur in bromeliads; foundmainlyin the lowlands, and thereare no
an undescribedspecies fromthe northernslopes recordsof the species beingfoundin bromeliads
of the Sierrade Juarezin Oaxaca seems to occur in cloud forests.Two membersof the group,B.
primarilyin bromeliads (undescribedspecies E, platydactylaand B. mexicana, have been re-
fig.9 in Hanken, 1983). The remaininggenera corded frombromeliads,mainlyat elevationsof
(Pseudoeurycea,Bolitoglossa,and Oedipina) have < 500 m (Taylor & Smith,1945). There are scat-
numerous species that are inhabitantsof cloud teredreportsofBolitoglossaalpha in cloud forest
forests. bromeliadsin Talamancan CentralAmerica and
Pseudoeuryceais widespread in Mexican and regionsto the south(e.g.,B. borburatanear Ran-
southwestern Guatemalancloud forests,but most cho Grande, Venezuela, Trapido, 1942; B. lig-
species are terrestrial
and are not oftenfoundin nicolor,Dunn, 1937; B. subpalmata, Robinson,
epiphytes.The only described species that are 1977; B. taylori,Wake et al., 1970). But in Costa
bromeliad specialistsare P. firscheini(Werler& Rica, wherethe assemblage is well represented,
Smith, 1952; Shannon & Werler,1955b) and P. thereare surprisinglyfew records of its occur-
nigromaculataof Veracruziancloud forests(un- rencein bromeliads(Robinson, 1977), although
publ. data, contraTaylor, 1941). An undescribed we now know thatsome species are common in
speciesfromour NorthernOaxacan transect(Fig. such microhabitats(see below).
9) uses arborealmicrohabitats,and an additional Several species of the alpha assemblage ofBo-
undescribedspecies fromour San Marcos tran- litoglossaare associated witharborealmicrohab-
sect (Wake & Lynch, 1976: 30) uses bromeliads itats in cloud forests.The only known adult of
consistently. Bolitoglossadiminutawas collected withan egg
Bolitoglossa, with 68 currentlyrecognized mass in a mat of liverworts(Robinson, 1976;
species, has by farthe greatestgeographicrange recentexaminationof the tinyholotype,which
of the tropical salamander genera (from Vera- lacks a sublingualfold,suggeststhatthis species
cruz,Mexico, to Brazil,Bolivia, and Peru). Many should remain in Bolitoglossa, contra Wake &
of the species in Nuclear Central America are Elias, 1983). Otherspecies associated withmoss
cloud forestspecialists,and theyfrequently occur mats coveringtreetrunksand branchesinclude
in bromeliads. Over one-half of the B. engel- B. marmoreaof Panama (Wake et al., 1973) and
hardtiencounteredduringan intensiveinvesti- an undescribedspecies sympatricwithB. dimi-
gation of an elevational transecton the lower nuta.
slopes of Volcdn Tajumulco, western Guate- The final genus, Oedipina, is widespread in
mala, werefoundin bromeliads,and B. franklini cloud foresthabitatsin Costa Rica, the centerof
is also a frequentinhabitantofbromeliads(Wake its diversity(Brame, 1968). These salamanders
& Lynch, 1976). Most records for Bolitoglossa are elongate,mainlyfossorialspeciesthatinclude
in bromeliads referto members of the beta as- some relativelyspecialized arboreal climbersin
semblage(e.g.,Stuart,1943). Some oftheseoccur lowland forests(e.g., 0. parvipes). The species
northof the Isthmusof Tehuantepec (the north- that occur at intermediateelevations in cloud
ernlimitsofNuclear CentralAmerica),including foreststypicallyare foundin moss mats covering
B. hermosa (Papenfuss et al., 1983), from the downed vegetationand soil banks.
Pacificslopes ofGuerrero,Mexico, and thewide- Informationin the above paragraphsmakes

clear that therehas been an extensive adaptive tebrates:frogs(especially Hyla and Eleuthero-
radiationofsalamandersin theNew Worldtrop- dactylus),lizards(especiallyAbronia),and snakes
ics, but the age of this radiation remains un- (e.g., Bothropsschlegeli).However, withthe ex-
known. Since the initial effortof Dunn (1926), ception of a fewspecies of frogswhose tadpoles
subsequent studies have forthe most part sug- are clearlyadapted forlife in the water of tank
gestedprogressively earlierdates forthe entryof bromeliads,only salamanders relyon epiphytic
salamanders into the region(Martin & Harrell, plants as their main microhabitats,and sala-
1957, is a strikingexception),and untilrecently manders are far more common in bromeliads
an Early or Middle Tertiaryoriginof the group than are any othervertebrates.
was accepted (Wake & Lynch, 1976). But bio- The densityof salamanders in bromeliads is
chemical and immunologicalstudies in the last difficultto document. As many as 34 Dendro-
decade have shownthateven withingenerathere tritonxolocalcae have been foundin a singlebro-
has been verygreatgenic differentiation, which meliad in Chiapas, Mexico (Taylor & Smith,
implies relativelygreatage forthe separationof 1945), but untilrecentlywe have had fewquan-
the lineages studied (Hanken, 1983; Hanken & titativedata to indicate the frequencyof occur-
Wake, 1982; Larson, 1983, 1984; Lynch et al., rence of salamanders in bromeliads. Although
1983; Maxson & Wake, 1981; Papenfuss et al., one of the firstreportsof salamanders living in
1983; Wake & Lynch, 1982). Progresshas been bromeliadswas fromCosta Rica (Picado, 1913),
made in definingmonophyleticgroups,but I be- the general impressionhas been that salaman-
lieve thatwe have not yetachieved a robustcla- ders are not common in bromeliads (Robinson,
distic hypothesisfor the group (Wake & Elias, 1977). Bromeliadshave been thoughtto be more
1983), mainlybecause of the extensiveparallel- importantfor salamanders in Mexico, Guate-
ism and convergencethat have obscured pat- mala, and Honduras. In an earlyaccount,Gadow
terns.Nevertheless,Hendrickson(1986) has at- (1908) reportedthata Mexican species of Pseu-
temptedto interpretthe historyof the group by doeurycealeads a "partlyarboreal life,theirfa-
combiningwhat is known about likelycladistic vorite huntingand hiding-placesbeing in the
patternswithknowledgeofthegeologicalhistory clustersof epiphyticplants, such as tillandsias,
oftheregionin a vicariancebiogeographystudy. orchids and the climbing phyllodendrons."
He suggestedthat salamanders which gave rise Schmidt (1936a, 1942) described bromeliad-
to thetropicalradiationfirstseparatedfromthose dwellingsalamanders as relativelyabundant in
in the Appalachia area by riftingof an ancient Guatemala and Honduras, apparentlymore so
Maya terranefromAppalachia or by a post-Mid- than in Costa Rica and Panama (Dunn, 1937).
dle Jurassicto Mid-Cretaceousmarinetransgres- In contrastto the above generalization,sala-
sion. In generalhe argues formuch older times mandersin Costa Rica use moss mats morecom-
of separationthan previous authors,based both monlythan do salamandersfartherto the north
on argumentsfromearth historyand fromhis and west. The genera Nototritonand Oedipina
belief (although he has not studied these sala- use moss mats extensivelyin Costa Rica, but
mandersdirectly)thatthe extensiveradiationof apparently rarely do so in northern Middle
the tropicalsalamandersmusthave takena long America. To the north and west Oedipina is
time. I cannot discuss this provocative studyin mainly fossorial, and Nototritonis associated
detail here,but it is importantto understandthat mainlywithbromeliads (an exceptionmay be a
available evidencesuggeststhatsalamandersand poorlyknown,undescribedspecies fromChiapas
habitats have coevolved in areas that became thathas been taken in a moss-coveredbank).
present-dayMiddle Americafora verylongtime. There is a generalmorphologythatcharacter-
izes mostbromeliad-dwellingsalamanders(Figs.
3-5). They typicallyare small animals (usually
SALAMANDERS AND EPIPHYTES
< 50 mm body length)withlong,prehensiletails,
The epiphyticcomponentof cloud forestsof- long limbs with widely spread digits,and fron-
ferstwo major classes of microhabitatsforsal- tallydirectedeyes. They are acrobatic climbers
amanders-arboreal bromeliads and moss mats and are very adept in a three dimensional en-
(which are complex and contain diverse ferns, vironment.Some larger salamanders use bro-
club mosses, and roots,stems,and entiresmall meliads on occasion, but thetruespecialistsusu-
angiosperms).These microhabitats,particularly ally approximatethe above description.
bromeliads,are used on occasion by otherver- Occupants of moss mats are less characteristic

in morphology.In generaltheyare slenderand ders,includinga lowercloud forest(1,600-2,400

have relativelyshort legs. The Appendix con- m) groupoffourand an uppercloud forest(2,400-
tains a list of species which have been reported 2,800 m) groupofsevenspecies.These tenspecies
to occur in bromeliads and moss mats. It also (one is presentin both elevational belts) are re-
containsa fewspecies knownby me to have such strictednotonlyin elevationalzonation,but also
habits,but which as yet are not reportedin the in geographicdistribution;none of the species
between
literature.This listdoes notdifferentiate occurs beyond the limits of the southwestern
speciesthatspecializeon thesemicrohabitatsand Guatemalan volcanoes and the adjacent Sierra
those thatare but casual occupants. Madre of Chiapas, Mexico. The regionbetween
1,600 m and 2,800 m is occupied by Evergreen
Cloud Forest (above about 1,900 m) and Mon-
COMMUNITY ORGANIZATION
taneRain Forest,usingtheterminology ofBreed-
For nearly 15 years my colleagues (James F. love (1981), who also has characterizedthese
Lynch and Theodore J. Papenfuss) and I have formationsfloristically.
been engagedin a broadlybased surveyof geo- Withinelevational zones we examined differ-
graphical ecology and communityorganization ential use of major habitat types.For example,
of the salamanders of Mesoamerica (Wake & some species are more common in edge situa-
Lynch, 1976; Wake et al., 1987). We established tions,and some favor small clearingsand open
a series of line transectsin Mexico, Guatemala, spaces, while others are found throughoutthe
and Costa Rica and conducted intensive sam- dense forest.Within a major habitat we exam-
plingovera multi-year periodalongeach ofthem. ined the use of specificmicrohabitats.We rec-
By far the most intensivelystudied of these ognized four categories: ground-dwelling(be-
transects is located in extreme southwestern neath logs, rocks, and other surface objects),
Guatemala and adjacent Mexico, between San log-dwelling(withinand under the bark of logs
Marcos, Guatemala, and Tapachula, Chiapas, and stumps),arboreal (withina leaf-axilmicro-
Mexico. Our San Marcos transectextendsfrom habitat, including bromeliads), and fossorial
the continentaldivide, down the Pacific slopes (withinsubterraneanpassageways).We foundno
ofVolcdnTajumulco, to thePacificcoastal plain. moss mat specialistsand thereforedid not rec-
Here we have documentedthe presenceof a rich ognize this microhabitatcategory.Within mi-
salamanderfaunacomprisedof 15 species,rang- crohabitatswe paid special attentionto differ-
ing fromnear sea level to nearly4,000 m. This ences in body size and in trophicspecializations
transecthas provided an opportunityto study (morphologyofthejaws and teeth).The primary
the ecological organization of this group of modes of ecological segregationof the 15 species
species, relative to each other and to various are indicatedin Table 1. Here a one-sidedmatrix
physicaland bioticfactors.An earlierstudy(Wake of potentialco-occurrenceof the species records
& Lynch, 1976) presenteda generaloverview of our assessment of primarysegregationordered
our results,and a recentreport(Wake et al., 1987) accordingto decreasingspatial proximityof the
updates the main patterns of distribution.A segregatedspecies: elevation,habitat,microhab-
summaryof our primaryresultsand data rele- itat,size,and trophicspecialization.Nearlythree-
vant to the use of epiphytesby salamanders is fourthsof the potential sympatricassociations
presentedhere. of the 15 species are precludedby differences in
Schmidt(1 936a) collectedseven species ofsal- elevational distribution,and habitat or micro-
amanders on the slopes of Volcdn Tajumulco habitat differencesseparate all but nine of the
and inferredthe presence of two additional remainingpaired associations. Of the nine pairs
species. He outlinedtheirmain patternsof ver- of species which show elevational, habitat,and
ticaldistribution and presentedcomparisonswith microhabitatsympatry,eightdifferimportantly
the nine species then known from Veracruz, bysize. The ninthcase involvescongenericspecies
Mexico. His basic conclusion was thatzonation similarin size and morphology,except thatone
was sharperin Guatemala than in Mexico. species has about halfas manysubstantiallylarg-
We (Wake & Lynch, 1976; Wake et al., 1987) er maxillaryteethand enlargedjaw muscles.
found eight additional species on the Guate- Six species on the transectcommonlyoccur in
malan transectand confirmedthemain elements arborealmicrohabitats(in orderof frequencyin
of Schmidt's preliminaryanalysis. We recog- such microhabitats,frommostfrequentto least):
nized fourelevational assemblages of salaman- Bolitoglossaoccidentalis,Dendrotriton bromelia-

12
e,1
10
c- 0 / / X
/. 8...
cQ a
00
61W~~~~~~~~~
FIGURE 10. Proportional useof
diagramindicating
microhabitats by 12 specieson theSan Marcostran-
sect.The dashedlinesareisodiversitycontoursbased
0 CZ on occurrences of approximately 1,100salamanders.
Microhabitats werescoredas follows:A = arboreal
bromeliads; T = underrocks,logsand debris,on the
surfaceofthesoil;I = underbarkofstumpsandstand-
0 0~~~~~~~~~~~~~~~0
C0 sC c ingtrees,and insidefallenlogs.Opensymbol= Pseu-
doeurycea;half-closed symbol= Dendrotriton;closed
symbol= Bolitoglossa. 1, P. rex; 2, P. brunnata;3, P.
to 0 goebeli; 4, P. sp.; 5, B. morio; 6, B. flavimembris;7,
B. rostrata;8, B. resplendens;9, B. franklini; 10, B.
engelhardti;11, B. occidentalis; 12, D. bromeliacia.
Numbers2 through10, and 12, are cloud forestin-
habitants.
FigurefromWake& Lynch(1976).
CZ,E cia, B. engelhardti,B. franklini,Pseudoeurycea

sp., and B. resplendens(Fig. 10). All but thefirst,
~
c~~~~~c ~ ~ c which occurs at relativelylow elevations, are
presentin the cloud forestand make extensive
use of bromeliads. Bolitoglossa occidentalisis a
small,mainlylowland species thatoccursin bro-
meliads, but it is most commonly found now
withinthe so-called "coffeezone," where it oc-
curs in agriculturalplantingsof bananas.
JamesF. Lynchand I are preparinga detailed
ecological account of our work in this transect,
;?> ;Q = v ;; ; ;
and withhis permissionI presenthere some of
our data concerninguse of bromeliads in cloud
forestsby theabove listedspecies. When we first
visitedthisarea in 1969 primaryforestextended
to roadsideand bromeliadswereabundant.When
we last visited the cloud forestregion in 1980
the foresthad been removed and pasture occu-
pied nearlythe entirearea between 1,500 m and
2,700 m. Below 1,500 m traditionalcoffeeplan-
tations,which featurelarge shade treesand ex-
<< << 44 ? o ? tensive plantingsof bananas, had given way to
4 vi 11
4~~~~~~~r 06 o C; r- rl 4
CZ (A _- o _( -- -- -- - a nearmonocultureofcoffeegrownin hedgerows
withoutany suitablecover forarborealsalaman-
ders.

TABLE 2. Relative abundance of salamanders in bromeliads,San Marcos transect.
Elevation Wet Season' Dry Season2 Combined

Below 1,750 m - 3/25 = 0.123 3/25 = 0.12
1,750-2,000 m 6/39 = 0.15 41/75 = 0.55 47/114 = 0.41
2,000-2,250 m 48/239 = 0.20 29/64 = 0.45 77/303 = 0.25
2,250-2,500 m 89/121 = 0.74 140/191 = 0.73 229/312 = 0.73
2,500-2,750 m 81/25 = 0.72 27/30 = 0.90 45/55 = 0.82
Above 2,750 m 14/73 = 0.19 13/21 = 0.62 27/94 = 0.29
May-September.
2November-February.
of bromeliads.
3Number of salamanders/number
Salamanders are common inhabitantsof bro- Martin Feder accompanied us on one tripto
meliads along the San Marcos transect(Table 2). our transectand studied the thermalecology of
We found salamanders in approximatelyevery some of the cloud forestsalamanders (Feder,
second bromeliadwe opened. These bromeliads, 1982). He found that bromeliads, even in the
primarilymembersof the genera Tillandsia and cloud forest,affordcooler and more stable tem-
Vriesia,were located relativelylow in the trees. peratures than microhabitats in immediately
Salamanders in southwesternGuatemala are surrounding areas. Bromeliad-dwellingsalaman-
most abundant in bromeliads at elevations be- ders appear not to thermoregulatebehaviorally
tween2,250 and 2,750 m. From theseelevations or physiologically,because thermaldiversityin
down to approximately1,700 m, bromeliadsre- their microhabitatsis so low as to offerlittle
main relativelycommon, and thereare brome- opportunityfor such behavior. As is usual for
liads presentat elevations up to approximately salamanders,thereis a highcorrelationbetween
3,000 m. All of the bromeliad specialists occur body temperaturesof salamanders and prevail-
in thecloud forest(roughly1,500-2,750 in), even ing microenvironmentalconditions (Feder &
though bromeliads are found both above and Lynch, 1982), so the more stable the microen-
below that formation.Above the cloud forest vironment,the less variable will be the temper-
those species that use bromeliads at lower ele- ature of the salamander. The tropical salaman-
vations (e.g., Bolitoglossa rostrata,Pseudoeury- ders contrast sharply with more northern
cea rex) shiftalmost entirelyto terrestrialmi- plethodontidsin having very limited abilityto
crohabitats.Salamanders are consistentlymore undergothermalacclimation(Feder, 1978, 1982).
abundant in bromeliads duringthe dry season This may be eitherthe cause or the effectof the
than duringthe wet season, except in the heart highfidelityto elevationalzone and microhabitat
of the cloud forest(2,250-2,500 in), wherethere displayedbymanyofthesespecies(Feder, 1983).
is less seasonalitythan elsewhere. The data and analyses in Tables 3-5 indicate
that the distributionof salamanders per bro-
TABLE 3. Distributionof salamanders in brome-

liads, San Marcos transect,16 January1972, 2,400 m
elevation.i of salamandersin brome-
TABLE 4. Distribution
18 January1972,2,300-
liads,San Marcostransect,
Number of Salamanders 2,350 m.'
per Bromeliad Frequency
NumberofSalamanders
0 15 Frequency
perBromeliad
1 10
2 8 0 12
3 3 1 8
4 1 2 10
5 1 3 7
6 1 4 1
8 1 5 2
'These data are for55 Dendrotritonbromeliaciaand 'These dataarefor59 Dendrotritonbromeliaciaand

threeBolitoglossafranklinitaken froma sample of 40 fourBolitoglossafranklinicollected in a sample of 40
bromeliads (x = 1.45 salamanders per bromeliad). (x = 1.58 salamanders
bromeliads perbromeliad).

TABLE 5. Test forrandomness,combineddata from

Tables 3 and 4.'
4?
Number of
Salamanders Expected
per Observed Frequency
Bromeliad Frequency (Poisson)
0 27 17.5
1 18 26.6
2 18 20.2 Imm
3 10 10.3
4 2 3.9
5 3 1.21 FIGURE 11. Outlines of the lefthind foot of two
6 1 > 7 0.3 5.5 lowland species of Bolitoglossa from Pacific coastal
7 _ 1 0.11 Guatemala. The digits and bony phalanges are indi-
8 1J 0.0J cated in each. Bolitoglossa salvinil is a large species
(this specimen is 67.5 mm, snout-ventlength)with
Chi-square (goodness of fit)= 8.50 with4 df extensivewebbingand is capable of generatingsuction
0.05 > P > 0.1 in arborealsituations.Bolitoglossaoccidentalisis a di-
iData for 121 salamanders collected from80 bro-
minutive species (this specimen is 38.7 mm, snout-
vent length)with feet that superficiallyappear to be
meliads (X = 1.52 salamanders per bromeliad).
webbed,but in realityare just incompletelydeveloped
(paedomorphic)as suggestedby the stronggradientin
phalangeal structurewithineach digit.
meliad is notsignificantlydifferentfromrandom.
However, thereis at least a suggestionthatthere
mightbe an excess of bromeliads that lack sal- boreal lowland species B. occidentalis). Although
amanders,as well as a deficiencyof bromeliads exposure to predation may be a relative cost for
containingsinglesalamanders.Thus, theremight living in bromeliads, the cost is apparently out-
be a tendencytowardclumpingunderconditions weighed by other advantages, such as those men-
of highsalamander abundance. tioned above.
Bromeliads mightseem to be a near perfect Although bromeliad dwellers in cloud forest
microhabitatforsalamanders,in termsof food habitats differ greatly in morphology, ecology,
availability,thermalstability,and constancyof and behavior from even the most arboreal North
humidity.But concentrationof salamanders in American plethodontids (e.g., Aneides), they are
bromeliadsmightattractpredators.Spiders and not the most extremely specialized species on the
salamandersare thetop residentcarnivoreswith- San Marcos transect. At elevations below about
in bromeliads,and theydo notpreyon each other 1,400 m the cloud forests, and the lower cloud
very extensively.Some arboreal snakes forage forest salamander fauna, are absent. A new sal-
widely and may be important,although infre- amander community appears at about 1,000 m,
quent, predatoryvisitors to bromeliads; birds composed of three extreme morphological and
mightalso be importantpredators.All tropical ecological specialists. This community includes
salamanders have a specialized autotomyzone a relatively large and a relatively small arboreal
at the base of the tail, and Shaffer(1978) ex- species of the genus Bolitoglossa and an elongate
amined tail loss frequencyas a rough index of fossorial species of the genus Oedipina.
relativepredationpressureon 10 species of sal- Bolitoglossa salvinil, a large species, is an ac-
amanders fromthe San Marcos transect(parts tive, climbing animal with a long prehensile tail
of tails may be lost in intraspecificaggressive and large hands and feet with extensive inter-
encounters,but these species are not known to digital webbing (Fig. 11). These animals, which
be veryaggressive).He found an inverse corre- frequent surfaces of Heliconia and other large-
lation between rates of tail loss and elevation, leafed plants on moist evenings, are capable of
and we know that snake densitiesalso decrease producing suction with their large hands and feet
with elevation. Two of the three cloud forest (Alberch, 1981).
species commonly found in bromeliads (Den- Bolitoglossa occidentalis, the small species, has
drotritonbromeliacia,Bolitoglossafranklini) had small hands and feet that appear to be fully
thesecond and thirdhighesttail loss percentages webbed. In reality the hands and feet manifest
of the species studied (the highestwas the ar- incomplete development, a phenomenon known

19871 wAKE-ADAPTivE RADIATION OF SALAMANDERS 253
as paedomorphosisthataffectsa numberof fea-

tures of the organism (Wake, 1966; Wake &
Brame, 1969; Alberch et al., 1979; Alberch &
Alberch,1981). Such similarlyaffectedfeatures
include a relativelyshort and stronglytapered
tail, as well as a reductionin skull ossification.
The hands and feetare essentially"embryonic,"
withdigitsthatshow a stronggradientof devel-
opment(Fig. 11). Althoughtheseanimals do not
generatesuction with theirhands and feet(Al-
berch,1981), theyare veryagile,partlyas a result
of theirsmall size. They have an extensiveven-
tralsurfacearea (body, limb,and tail) relativeto FiGuRE 12. Lineatriton lineola (top), from near
Fortinde las Flores, Veracruz,Mexico, and Oedipina
theirmass, so they"stick" to moistplantsurfaces ignea(bottom),fromFmcaSantaJulia,nearSanRafael
by surface tension. Apparentlythese salaman- Pie de la Cuesta,San Marcos,GuatemalaThe scale
ders are virtuallyrestrictedto leaf axil retreats. bar is 25 mm.Theseextremely elongatedspeciesare
They especially favorHeliconia and both culti- semi-fossorial in habit,and haveevolved
to fossorial
vatedand feralbanana plants(Musa spp.). Smith convergently.
(1945) reported findingBolitoglossa rufescens
(very similar in morphologyand ecology to its 3,700 m) towersover the Plateau, to which it is
close relativeB. occidentalis)to be abundant in attached along only its northernflankat a low
red bananas (he foundabout 250 per hour) at a elevation (about 1,000 in). The contrastin sal-
Veracruzian site. These animals are adept at amander faunasbetweenVolcin Tajumulco and
climbing small tendrils,stems, and strands of Volcin Agua is great. Only three species have
moss. been collected on the slopes of Agua. There is a
Members of the small species of Bolitoglossa singlehighelevation memberof thegenus Pseu-
are encounteredonly rarelyin terrestrialsites, doeurycea(P. goebelt),one low elevation species
and the large species, while occasionally found ofthegenusBolitoglossa(B. salvindi,a large,fully
on the ground (e.g., crossing roads on rainy webbed species), and a middle elevation gener-
nights),also are basicallyarboreal.(An exception alized species of the genus Bolitoglossa (B. mo-
may be the verylarge species B. dofleini,which rio). All threeof thesespecies also are presenton
can be very common in terrestrialsituations.) the San Marcos transect There is a well-devel-
But anothergroup of lowland species, the very oped cloud forestwithabundant bromeliads on
elongate,short-leggedgenus Oedipina, is found Volcin Agua, but the forestis localized and it is
only at and beneath the surfaceof the ground. isolated fromsimilar habitats to the northand
Species of Oedipina are elongated as a resultof west by low elevations covered by drier vege-
the addition of trunkand especially tail verte- tationtypes.In 1969 we opened about 600 bro-
brae, and theyhave bizarre long tails (Fig. 12). meliads on Volcan Agua, but found only two
In addition to theirextremelyshortlegs and tiny slamanders! This contrastssharplywiththedata
hands and feet,they have heads and bodies of presentedearlier for the San Marcos transect.
verysmall diameters;all of these featuresfacil- Bolitoglossa morio,the species we encountered,
itateuse of root channels and undergroundbur- is a widespread and relativelycommon inhab-
rows. itantof groundand log microhabitatsin forested
The San Marcos transectis special because areas of the Guatemalan Plateau. On the San
more species of salamandersoccur therethan in Marcos transectit is foundonly at the top of the
any otherarea of the Pacific Versant in Middle cloud forestand in drierbroadleafforestabove,
America. Volcin Tajumulco (4,200 m) is at- where the edge of the Plateau contacts Volcin
tached to the Guatemalan Plateau at about the Tajumulco. Here the species occurs occasionally
3,000 m level, so on both sides of the volcano in bromeliads (Fig. 10). On Volcin Agua, al-
thereare substantialareas of moderateelevation though B. morio remains uncommon in bro-
whichtrapmoistureand therebycreatefavorable meliads and apparentlyhas not modifiedits mi-
salamander habitat. To the south and east the crohabitatutilization patternsin any dramatic
Plateau graduallylowersand rainfalldeclines. In way, its elevational range is 1,300-2,500 m. At
thevicinityofGuatemala City,Volcin Agua (over this site,whereB. moriois the only salamander

Costa Rica seven species are known fromele-

vationsbelow 1,000 m, butnot in local sympatry
(see below). The proportionof the total sala-
mander fauna presentin the lowlands increases
at lower latitudes within Middle America (see
Table 5 in Wake & Lynch, 1976). There is evi-
dence ofincreased"tropicality"(thatis, ofcloser
packingof species in communitiesand increased
numbersof species presentlocally)as one moves
intothedeep tropics.Finally,however,in north-
westernSouth America thistrendstops,perhaps
because plethodontidsare not thoughtto have
dispersedinto South America untillate Pliocene
times (Wake & Lynch, 1976; Hanken & Wake,
1982). Except in the Choc6 and the flanksof the
COSTA RICAN TRANSECTS
!0U25 50 Km 100 150 1 1 8 8
northernCordilleran regions of Colombia, the
numberofsalamanderspeciespresentin lowland
sites in South America is not known to exceed
FIGURE 13. Map of Costa Rica indicatingthe lo-
cation of the Irazfiand Tapanti transectsillustratedin two, even in such bioticallyrichforestsas those
Figures 14 and 15. of the Rio Palenque area of Ecuador.
ThroughoutMiddle America,salamandersare
foundin cloud forests.In Mexico and in Nuclear
present,it occupies an elevational range that
CentralAmerica,cloud forestsalamandersmake
accommodates ten species on the San Marcos
extensive use of bromeliads as microhabitats,
transect.The patternsof species distributionin
even at the extremenortheasternlimits of the
the tropics(thisexample,but see below also) are
rangeof the supergenusBolitoglossa in the G6-
probably determined by combinations of
mez Farias region of Tamaulipas (where cloud
physiologicalconstraints(in relationto physical
forestsalso reach theirnorthernlimit; Martin,
factorsin the environment)as well as such in-
1958). But the mannerin whichcloud forestmi-
terspecificinteractionsas predation and com-
crohabitatsare utilized changes in Costa Rica.
petition.
The Costa Rican salamander fauna justifiably
has been considered one of the best known in
COMPARATIVE ASPECTS OF
the tropics,thanksprimarilyto the workof Tay-
COMMUNITY ORGANIZATION
lor (1952, 1954). However, very littlehas been
Until recentlymostfieldworkby mygrouphas reportedconcerningmicrohabitatutilizationand
been in Mexico and Guatemala (forgeneralsum- patternsofco-occurrenceofCosta Rican species.
maries see Wake & Lynch, 1976; Wake et al., Only fourspecies are reportedto occur in bro-
1987). In general,theresultsofour detailedstud- meliads (Robinson, 1977), althoughmany more
ies of the San Marcos transecthave been mir- species are knownto inhabitcloud forests.
rored in otherareas (cf. Fig. 9). Typically only RecentlyI have been investigatingthe system-
one ortwospeciesoccurat elevationsabove 3,500 atics and distributionof Costa Rican salaman-
m; as one moves lower the number of species ders in some detail. I have focusedattentionon
presentin a givenhabitatincreasesdramatically two general transects(Figs. 13-15). Results for
at about 3,000 m and continuesto be relatively Costa Rica are preliminary,because major sec-
high untilthe lower limit of the cloud forestis tions of these generalizedtransectshave yet to
reached. At elevations below 1,000 m the num- be searched thoroughly.Nevertheless, certain
ber of species presenttypicallydeclines, and at marked contrastswith more northerlytransects
sea level the largestnumberof species definitely are apparent.
knownto be presentis fouron theOsa Peninsula A dominantthemein the historyof studiesof
of Costa Rica, where there are two species of tropical salamanders has been that the species
Bolitoglossa and two species of Oedipina. Pos- whichare themostconservativeecologicallyand
sibly five species occur togetherat sea level in the most primitive phylogeneticallyoccur in
the regionof Bocas del Toro, Panama (Wake et Mexico, and that there is both increased spe-
al., 1973 and unpubl. data), and in northeastern cializationand a decline in thenumberofspecies

Volcan Irazd ?
Montane
3000 WetForest
2 Montane
Rain
2 W X Forest Forest
_N~~~~~~~~~C
2000 0
~Lwer
0 0
W Montane
Rain
Forest
Li
L
1000-
X ~~~~~~~Premontane
Rain
Forest
500-
H Wet and
~~~~~~~~~~Tropical
u~~s~~Finca
~~~~~ ~ ~ ~ ~ ~Premontane
La Selva
WetForestII
0 20 40
Km
FIGURE14. Verticaldistributionof plethodontidsalamanders along the Irazi transect,extendingabout 55
km fromFinca La Selva to Volcdn Irazu, Costa Rica.
to the south (Dunn, 1926; Taylor, 1944, 1952; ternsof microhabitatutilizationdifferdramati-

Brame & Wake, 1963; Wake, 1966; Wake & cally between Mexico and Nuclear Central
Lynch,1976). Even thoughWake & Lynch(1976) America on one hand, and Talamancan Central
documented the presence of a large number of America on the other.
species below 100 latitude,we continued to es- Perhaps the most strikingdifferencebetween
pouse the traditionalview of relics in the north the above regionsis the presenceof a richfauna
(e.g., Chiropterotritonpriscus of Coahuila and associated with moss mats in the cloud forests
Nuevo Le6n, Mexico) and increasinglyderived of Talamancan CentralAmerica. As noted ear-
formsto the south. The recentdiscoveryof the lier (Table 2), salamanders are sometimes very
most primitiveknowngenus of tropicalpletho- abundant in cloud forestsof northernMiddle
dontid in Guatemala (Elias & Wake, 1983) and America,wheremanyspecies utilizebromeliads
a freshanalysis of relationshipsof new and ex- (Wake & Lynch,1976). In Veracruz,Mexico, and
istinggroups(Wake & Elias, 1983) have forced in Nuclear Central America, elongate,fossorial
me to re-evaluatemyearlierviews. It now seems species of Lineatritonand Oedipina occur only
likelythatsalamandershave been in the tropics at elevations below the lower limit of cloud for-
of present-dayMiddle America fora very long est. In contrast,elongate membersof the genus
time,possiblythroughouttheTertiary(see above Oedipina are wellrepresentedin Costa Rican and
section on Ecological Geography and System- Panamanian cloud forests,extendingupwardsto
atics). Middle elevations doubtless have been elevations in excess of 2,000 m (Figs. 14, 15).
importantareas of both survival and radiation Here theyutilizemoss mats coveringsoil banks,
in the group,and we have discovered that pat- downed logs, and stumps. Furthermore,living

: ()
i Cerro de
la Muerte
3000A
~~ ~~~ Montane~
fl Rain
E | 't o 0 Forest
Li
wer
Lower
Qi
2000-
2r) ?| g 0 W0 < Op6X
q
&Montone i;
Rain
> ~~~~~Forest
0000 [1 .
40r
( IPremontane
60
P remonTane?
0 ~~~~Rain
Forest PremontaneWetForestRanFrs
FIGURE15.Verticaldistributionrofpal n salamanders
alonaenealizdtrnsethTropical
I~~.~~ Qi,~ ~ Forest
Wet ~ ~ ~ ~ ~MitFrs
~ K
200- ~ U ??-
o3 Siquirres Tropical Moist and PremontaneWet Forest
Km
FIGURE 15. Verticaldistributionof plethodontidsalamanders along a generalizedTapanti transect,which
extendsbetweenSiquirresand Cerro de la Muerte,Costa Rica. This region,about 60 km long, contains more
species of plethodontidsalamandersthan any known area in tropicalAmerica.
in moss mats in these cloud forestsare species ently11 species of salamanders(in threegenera)
of Nototriton, a genus thatis mainlyconfinedto known from this transect.As with the more
bromeliads in Nuclear Central America. There northerly transects,onlyone species (Bolitoglos-
is even an undescribedCosta Rican species of sa subpalmata) is likelyto occur at elevations of
Bolitoglossa that has been taken only in moss > 3,000 m (and I cannot document its presence
surroundingtwigson treesand shrubsin cloud at thatelevation as yet,althoughI expectit may
forests.This substantialfaunarepresentsan eco- be found). However, in contrast with more
logical componentthatis rare(e.g.,Dendrotriton northerlytransects(cf. Wake et al., 1987), there
cuchumatanus occurs in moss mats in Guate- are at least five species presentat elevations of
mala, Lynch & Wake, 1975) or is missing in <500 m. Eightspecies occur in cloud forestbe-
cloud forestsof Nuclear CentralAmerica. tween 750 and 2,000 m, includingtwo species
The two Costa Rican transectsoffersome in- that specialize on moss mat microhabitats(the
teresting contrasts.Bothextendup theCaribbean two species of Nototriton;see also commentsin
slopesfromnearsea levelto elevationswellabove Taylor, 1954), two othersthatutilizemoss mats
3,000 m. The first(Fig. 14), the Irazuitransect, extensivelybut also use burrowsin soil (the two
extendsfromthe vicinityof Finca La Selva for species of Oedipina), and two Bolitoglossa (B.
about 55 km to the peak of Volcdn Iraz6. Sala- subpalmata,B. robusta)thatI have foundin moss
mander distributionsalong this transect are mats,althoughothermicrohabitatsare used more
poorlyknownexceptfortheregionbetween1,000 frequently. BothB. subpalmata(at thiselevation)
and 2,500 m. For example, Scott et al. (1983) and B. alvaradoi use bromeliads.
listed two species of Oedipina from Finca La I expectthatmore species willbe foundon the
Selva, but studyof specimensfromthe area sug- Irazi transect,in part because of the unusually
geststhatthreeoccurthere.The taxonomyofthe highnumbersof species presenton the Tapanti
groupis difficult,but it may be thatnone of the transect(Fig. 15). The lattertransectis farmore
threeare the species listed. (Note that only two generalizedin its boundaries than the first,and
species are indicatedon Fig. 14.) There are pres- is essentiallya broad (ca. 20 km) swath of ter-

ritoryextendingabout 60 km fromthe vicinity Tapanti thereis an especiallyrichepiphytefau-

ofSiquirresto thesummitofCerrode la Muerte. na, and thisis thelocalitywherethelargestnum-
The Tapanti transectis not a straightline, but ber of species are found. However, in marked
twistssomewhatto encompass siteswheresome contrastto the situationin the cloud foreston
of the rarerspecies are knownto occur. There is our San Marcos transect,the densityof individ-
extensivehabitatdisturbancealong thistransect ual speciesis uniformly low on thistransect.This
(forexample, in the vicinityof Turrialba),and I situationof high species diversityand low den-
justifyweaving togetheran indirecttransectas sityof individual species is one more indication
an attemptto demonstratethe potentialnumber of theincreased"tropicality"of the Costa Rican
of species one mightreasonably expect to find salamander fauna.
on a continuousaltitudinaltransectunder pris- The contrastbetweenthe cloud forestthatoc-
tineconditions.The Tapanti transectthusoffers curs at around 1,000 m and the forestaround
a greaterdiversityofhabitatsthandoes theIrazi 3,000 m on this transectis sharp. At high ele-
transectand one mightexpect more species to vations the densityof Bolitoglossa subpalmata
be present.To my surprise,the Tapanti transect is extraordinarilygreat,on the orderof 9,000/ha
is the richestthat I have found in the tropics, (Vial, 1968). Four species occur in sympatryat
with 21 species. There are only 26 species of around2,500 m; in myexperienceB. subpalmata
plethodontidsknown fromCosta Rica (Scott et is about 100 times more common than B. cer-
al., 1983; theirlist and mine differslightlybut roensis,about 1,000 times more common than
we obtain thesame totalnumberof species),and B. sooyorum,and about 10,000 timesmorecom-
thatabout 80% of themoccur along thistransect mon thanB. nigrescens!Doubtless thereis a col-
atteststo its richness. lectingartifactinvolved, but the firstspecies is
The Tapanti transecthas a highernumber of remarkablyabundant and the last has been, at
species (seven) occurringbelow 500 m thandoes the veryleast,elusive. The highdensityof a sin-
the Irazittransect,and in both Panama and Nic- gle species at highelevation is a common theme
aragua anotherspecies (Oedipina collaris)occurs in tropicalsalamander biology.
at elevationsof <500 m (Brame, 1968), so there Bolitoglossa subpalmata, which can be ex-
is thelikelihoodthatan eighthspecies eventually ceedinglyabundant at high elevations in Costa
will be found.Bolitoglossa alvaradoi apparently Rica, displays a marked shiftin microhabitat
occursat elevationsof < 500 m elsewherein Cos- utilizationand a reductionin abundance at lower
ta Rica. Thus, as many as nine species mightbe elevations. The species is primarily ground-
expected in the lowlands in the area crossed by dwellingat highelevation,althoughit also uses
this transect. bromeliads.I have collectedB. subpalmata from
Thirteen species occur in the cloud forestof bromeliads 30 m above groundlevel in an oak
the Tapanti transect,if we accept 750-2,000 m treeat 3,000 m elevation.At elevationsof < 2,000
as its elevational bounds. In fact,cloud forest m the species becomes increasinglycommon in
conditionsexist almost to 3,000 m, althoughin bromeliadsand is encounteredonlyinfrequently
generalcloud forestsare less welldefinedin Costa in terrestrialsituations.This species can be ex-
Rica and Panama than fartherto the north traordinarily persistentin thefaceofeven drastic
(Myers, 1969). This transectcontainsthe richest habitat change, so long as bromeliads remain.
cloud forestsalamander fauna found anywhere An anecdote illustratesthis point. An old col-
in the tropics.Here, too, I have probablyunder- lectinglocalityin the Montes de Aguacate, west
estimatedthenumberofspecies present.At least of San Jose,was visitedrecently.Only tinyfrag-
one more species ofBolitoglossamay be present, mentsofforestremainat thissite,at about 1,500
and the two poorly known highland species of m. Salamanders were common residentsof bro-
Oedipina may well extend to lower elevations, meliads in one forestfragmentwheretreeswere
since the genus as a whole is stronglyconcen- being felled. We opened 130 bromeliads and
tratedat lower elevations. Two species of Boli- found 55 salamanders,including 14 adults and
toglossa (an undescribed species and B. dimi- a subadult in a single bromeliad. As many as
nuta, Robinson, 1976) use mats of vegetation threeadults were found in the axil of a single
includingmosses and liverwortsthat surround leaf.This is a graphicdemonstrationof the suit-
twigsand branchesoftrees.Several otherspecies ability of bromeliads as microhabitatfor sala-
use bromeliads and moss mats, but no quanti- manders, especially under conditions of great
tativedata are available. In theforestsofRefugio habitat modification.I have had similar expe-

rienceswith Chiropterotriton lavae in fragments chains. These postulatedcyclesofexpansion and

of cloud forestabove Jalapa, Veracruz,Mexico, contractionofgeographicrangesand population
and with Bolitoglossa morio in an area devas- densitieswould establishthe settingforthe kind
tated by volcanic activity on Volcdn Pacaya, ofspeciationalprocessesI envisionhavingtaken
Guatemala. place among the tropicalsalamanders.
It is stilltoo earlyto generalizeveryextensively The two primaryfactorsin the historyof the
fromour comparativetransectstudies.We have tropical salamander fauna probably have been
come to be suspicious of species with broad el- thecombinationofadaptationofspecies to cloud
evational ranges(such as 0. uniformis, Figs. 14, forestenvironmentsand the long, complex his-
15),and thesedeservecarefultaxonomicre-eval- toryoftectonicactivityin Middle America.There
uation,formost species occurwithinrathernar- are some relativelystable areas, such as the an-
row elevational limits. We also have come to cientcore ofNuclear CentralAmerica,wherethe
expectfewextremehighlandor lowland species, upper and lower boundaries of the cloud forest
but thereare more lowland species at low lati- have shifted,but where cloud forestin a broad
tudes. Cloud forestsand salamanders are most sense probablyhas been presentformuch of the
abundant at mid-elevations. Tertiaryand Quaternaryperiods (see discussion
in Wake & Lynch, 1976). However, there are
FACTORS INFLUENCING SALAMANDER manyotherareas wheretectonicmovementsand
SPECIATION AND RADIATION associated volcanic activityhave been so great
and so persistentthat cloud forestshave been
Species of plethodontidsalamanders charac- onlyan ephemeralpresence,shifting almostcon-
teristicallydisplay a highdegreeof geneticfrag- stantly.
mentation(Larson et al., 1984; Larson, 1984). The threefociforsalamander radiationin the
Larson (1984) has argued that a generalpattern tropics(Fig. 2) all have stable, ancient tectonic
forthe historyof population structurein pleth- coreareas surroundedbyregionsofgreattectonic
odontids is that followingoriginationthey ex- activity.(For summaryof tectonichistory,see
pand graduallyand contiguouslyinto regionsto Hendrickson,1986.) These areas have been cited
which they have ecological access. Later, as a by otherworkersas havingphylogenetically dis-
resultof climaticchange which may resultfrom tinctivefaunal components. For example, Sav-
manyproximalcauses, theirpopulationsbecome age (1982) stated:
fragmentedinto islands among which there is
littleor no geneticexchange.Subsequentclimatic I nowbelievethatthedistinctivemontaneher-
changesmay lead to re-establishment of ecolog- petofaunasofthesouthern SierrasofMexico,Nu-
clearCentralAmerica,and theTalamancaarea
ical access to areas separatingisolated popula- developedmoreorlessin situfromancestors that
tions. This may lead eitherto renewed genetic "rode"theuplifted areasandevolvedwiththem.
exchange or, depending on the level of genetic Each endemicmontanearea thenrepresents an
divergenceand itseffect on isolatingmechanisms uplifted
islandbiota vicariatedfroma moreor
lesssimilarsea ofwidelydistributed
ancestors.
or mate recognitionsystems,to a varietyof in-
teractions.There may be a hybridswarm,a nar- Nuclear Central America (Fig. 16) illustrates
row hybridzone, a narrowzone of overlap with the ideas outlined above. That regionhas as its
occasional hybridization,partial sympatrywith core the ancientSierrade los Cuchumatanes,lo-
boundariessetby competitiveinteractions, or co- cated on thesouthernpartoftheNorthAmerican
existencewithdifferent ecological requirements. plate. The area has been characterizedas the
All of these interactionshave been documented Middle AmericanMegathrustby Plafker(1976),
among plethodontids.The many studiesof pop- because itis theconjunctionofthreemajorplates.
ulation structurebased on electrophoreticanal- The Cocos plate, to the southwest,is being sub-
ysis of proteins,togetherwith studies of distri- ducted near the intersectionof the NorthAmer-
bution, phylogenetichistory,and biogeography ican and Caribbean plates (for evidence of the
(reviewed by Larson, 1984), suggestthat geo- widespread influenceof this phenomenon see
graphicor allopatricspeciationby subdivisionis Singh et al., 1985). The latter is being forced
the common mode in plethodontids.There are eastwardbythecombinedplate movements,and
similaritieswith the concept of "taxon cycles" a small western tip of the plate is effectively
(Wilson, 1961; Ricklefs & Cox, 1972), which "caught" between the North American and the
usually have involved examples from island Cocos plates. The zone between the Caribbean

94' 92 .'.
of ~
Te/uonepc
continental
180 -.~~~~~~~~~~~~~~~.
~~~~Mo/agua crust
Pacific \ I
IsthmusOcn
CaribbeanP/ate
Tehuantepec
'''''''''"''"'.)<~~~~Ishmu I
MEXICO
'160
/Sierra els -
/Cuchumatanes
PacifPolchi
Pacific - Ma t\
-_-- /
7 1~~~~~~~~~:
Ocean
140 ...
!
0 50 Km 100 150 EL SALVADOR
920 9 8
FIGURE 16. Nuclear Central America. A generalized diagram illustratingrelationshipof the core region,
northof the Polochic Fault, to the intersectionof threecrustalplates. The marginsof the core regionare areas
of intensetectonicactivitybecause of the complex geologyof the region.Nuclear CentralAmerica has been an
area both of preservationof apparentlyancient lineages,because of the continued stabilityof the core, and of
speciationof cloud forestforms,due in largepartto the fragmentation and reassemblyof areas of cloud forest.
Inspiredby and based largelyon Plafker(1976).
and North American plates is outlined by the occurring species of salamanders in Middle
Motagua and Polochic faultzone. This has been Americais found,along our San Marcos transect.
an area of intensetectonicactivityformillions The relativelystable upland of the Sierra de
of yearsand Plafker(1976) has estimatedthatat los Cuchumatanesis in manywaysan even more
least 200 km oflateralmovementofplates along interestingarea thanthePacificvolcanic belt.We
this faultzone has occurredsince the Miocene. began fieldworkin this area in 1974, at a time
The westerntip of the Caribbean plate, trapped when only two species of salamanders were
betweenthe otherplates, is being ripped,or de- knownfromthe Caribbean slopes of the Cuchu-
coupled (Plafker,1976). Grabens have formed, matanes,despitea numberofbriefcollectingtrips
with small volcanic cones risingwithin them. by different herpetologists.Results of our inves-
Parallel to the Pacific versant,above the zone tigationshave been summarizedby Elias ( 1984),
wherethe earth'smantleis being pierced by the who found 13 species of salamanders in this re-
subductedCocos plate, the famous Guatemalan gion (see also Wake et al., 1987). As elsewhere
volcanoes are lined up. Volcdn Tajumulco and in Middle America,the cloud forestis of special
VolcainTacanai lie at the northwesterncornerof interest,forsix species with narrowelevational
theCaribbean plate,wherethethreeplates meet. rangesoccur just above the cloud line, here lo-
In thistopographicallycomplexzone ofmaximal cated at about 1,300 m. Two new generaof sal-
geologicalturbulence,the largestnumberof co- amanders were discovered in this cloud forest

(Elias & Wake, 1983; Wake & Elias, 1983), in- parallel(Wake, 1966; Wake & Brame, 1969; Lar-
cluding the exceptional Nyctanolis,a morpho- son, 1983; Elias, 1984). These phenomena have
logicallyprimitivegenuswhichappears to be the made phylogeneticanalysisverydifficult, forany
sister group of all other tropical salamanders. phylogenetichypothesisrequiresextensivecon-
Thus, on the one hand, the ephemeralcloud for- vergence,parallelism, or evolutionaryreversal
estsofthetectonicallyactiveand topographically (Wake & Elias, 1983).
complex margins of the Cuchumatan uplands Epiphytesappear to have been significant fac-
have contributedto speciation and led to the torsin theevolutionoftropicalsalamanders.The
highlydisjunctdistributionalpatternsillustrated convergence in morphology and behavior of
previouslyforDendrotriton and Nototriton(Figs. bromeliad-dwellingsalamanders is one indica-
7, 8). On the otherhand, the more stable cloud tion of thisimportance,and the extentto which
forestson the northeasternslopes of the core of bromeliads and moss mats are utilized as mi-
the Cuchumatan region have served as refugia crohabitatsis another.It is also significantthat
forwhat must be extremelyancientlineages. salamanderspersistin the face of greatenviron-
mentalchangeso longas fragments offorestwith
CONCLUSIONS the preferredmicrohabitatsremain.
We still have much to learn about the sala- The tropical salamanders, which originated
mandersoftheNew World and
tropics, even the from a Laurasian ancestralgroup(Savage, 1973),
best knownareas of Middle America have yield- are a markedexceptionto a common patternof
ed manyrecentsurprises.Earliermisconceptions tropical originand subsequent temperateinva-
concerningthe probable historyand ecology of sion.Late in thehistoryofsalamandersas a group,
tropicalsalamandershave led to underestimates but neverthelessa very long time ago (perhaps
of the age and diversityof the group and have at the beginningof Tertiary),theyinvaded the
contributedto our relativeignoranceoftheecol- area that has become modern Middle America.
ogy of the cloud forestand lowland species, es- Compared withsalamandersgenerally,thetrop-
pecially the arboreal and fossorialforms.New ical salamanders have been phenomenallysuc-
species are being discovered more rapidlythan cessful.But now theirsurvival and, indeed, the
theycan be described,formanyspeciesare known survivalof much of thediversityof tropicaleco-
fromsmall series. Our knowledge of the com- systemsis at risk,forthelowland forestsand the
parativeosteologyand of molecularevolutionof middle elevation cloud foreststhatharbormost
this group, while still fragmentary, is sufficient tropical salamanders are being cleared at rates
to demonstratethatparallelismand convergence that almost defybelief. Not a tree is standing
are rampant. over extensivepartsof our San Marcos transect,
This, in turn,implies both that theremay be whichwas in an almost pristinestateas recently
only a limitednumberof ecological roles avail- as 1969. In a single human lifetimethe results
able to tropicalsalamanders,and thattheremay of perhapsa hundredmillion yearsof evolution
be functionaland developmental-historical con- will have been dramaticallychanged,if not ex-
straintswhichimpose limitson theevolutionary tinguished.
potentialof the group. An especially clear case
LITERATURE CITED
of convergenceis the elongationassociated with
fossoriallifein the generaOedipina (fromsouth ALBERCH, P. 1981. Convergenceand parallelism in
foot morphologyin the neotropical salamander
and east of the Isthmusof Tehuantepec) and Li- genusBolitoglossa.I. Function.Evolution 35: 84-
neatriton(fromnorthof the Isthmus) (Fig. 12). 100.
The formerhas become elongate by increasing & J. ALBERCH. 1981. Heterochronicmecha-
thenumbersofvertebrae;thelatterby increasing nisms of morphologicaldiversificationand evo-
lutionarychange in the neotropical salamander,
the lengthof the individual vertebrae,whichare
Bolitoglossa occidentalis (Amphibia: Plethodon-
identicalin number(in the trunk)to all tropical tidae). J. Morphol. 167: 249-264.
generaexcept Oedipina (Tanner, 1950; Wake & ,S. J.GOULD,G. F. OSTER& D. B. WAKE, 1979.
Lynch, 1976). Earlierin this paper I highlighted Size and shape in ontogenyand phylogeny.Paleo-
the convergencein the Chiropterotriton-Dendro- biology 5: 296-317.
BRAME, A. H., JR. 1963. A new Costa Rican sala-
triton-Nototriton assemblage. WithinBolitoglos- mander (genus Oedipina) with a re-examination
sa webbingof hands and feethas evolved both of 0. collarisand 0. serpens.Nat. Hist. Mus. Los
convergently(Alberch & Alberch, 1981) and in Angeles Co., Contrib.Sci. 65: 3-12.

* 1968. Systematicsand evolutionoftheMeso- , J.F. LYNCH & D. B. WAKE. 1980. Salamander

americansalamandergenusOedipina. J.Herpetol. invasion of the tropics.Nat. Hist. 89(12): 46-53.
2: 2-64. HENDRICKSON, D. A. 1986. Congruence of bolito-
& D. B. WAKE. 1963. The salamanders of glossinebiogeographyand phylogenywithgeolog-
South America. Nat. Hist Mus. Los Angeles Co., ic history:paleotransporton displaced suspectter-
Contrib.Sci. 69: 1-72. ranes?Cladistics 2: 113-129.
& . 1972. New species of salamanders HOUCK, L. D. 1977a. Reproductivebiologyof a neo-
(genusBolitoglossa) fromColombia, Ecuador and tropicalsalamander,Bolitoglossarostrata.Copeia
Panama. Nat. Hist. Mus. Los Angeles Co., Con- 1977: 70-83.
trib.Sci. 219: 1-34. 1977b. Lifehistorypatternsand reproductive
BREEDLOVE, D. E. 1981. Introductionto the floraof biologyof neotropicalsalamanders. Pp. 43-72 in
Chiapas. Pp. 1-35 in Part I, Flora of Chiapas. D. H. Taylor & S. I. Guttman (editors),The Re-
CaliforniaAcademy of Sciences, San Francisco. productiveBiologyofAmphibians.Plenum Press,
DUNN, E. R. 1926. The Salamanders of the Family New York.
Plethodontidae. Smith College, Northampton, LARSON, A. 1983. A molecular phylogeneticper-
Massachusetts. spective on the originsof a lowland tropical sal-
1937. The amphibian and reptilianfauna of amander fauna. I. Phylogeneticinferencesfrom
bromeliads in Costa Rica and Panama. Copeia proteincomparisons. Herpetologica39: 85-99.
1937: 163-167. 1984. Neontologicalinferencesof evolution-
ELIAS, P. 1984. Salamanders of the northwestern ary patternand process in the salamander family
highlandsof Guatemala. Nat. Hist. Mus. Los An- Plethodontidae.Pp. 119-217 in M. K. Hecht, B.
geles Co., Contrib.Sci. 348: 1-20. Wallace & G. T. Prance (editors), Evolutionary
& D. B. WAKE. 1983. Nyctanolispernix, a Biology,Volume 17. PlenumPubl. Co., New York.
new genusand species ofplethodontidsalamander , D. B. WAKE & K. P. YANEV. 1984. Measuring
fromnorthwestern Guatemala and Chiapas, Mex- gene flowamong populations having high levels
ico. Pp. 1-12 in A. G. J. Rhodin & K. Miyata of geneticfragmentation. Genetics 106: 293-308.
(editors), Advances in Herpetologyand Evolu- LOMBARD, R. E. & D. B. WAKE. 1977. Tongue evo-
tionaryBiology:Essays in Honor of ErnestE. Wil- lution in the lunglesssalamanders, familyPleth-
liams. Mus. Comp. Zool., Cambridge,Massachu- odontidae. II. Function and evolutionarydiver-
setts. sity.J. Morphol. 153: 39-80.
FEDER, M. E. 1978. Environmentalvariabilityand & . 1986. Tongue evolutionin thelung-
thermalacclimationof metabolismin neotropical less salamanders,familyPlethodontidae.IV. Phy-
and temperatezone salamanders. Physiol. Zool. logenyof plethodontidsalamanders and the evo-
51: 7-16. lution of feedingdynamics. Syst. Zool. 35: 532-
1982. Thermal ecology of neotropicallung- 551.
less salamanders(Amphibia: Plethodontidae):en- LYNCH, J. F. & D. B. WAKE. 1975. The systematics
vironmental temperatures and behavioral re- of the Chiropterotriton bromeliacia group (Am-
sponses. Ecology 63: 1665-1674. phibia: Caudata), with a descriptionof two new
1983. Integratingtheecologyand physiology species fromGuatemala. Nat. Hist. Mus. Los An-
of plethodontidsalamanders. Herpetologica 39: geles Co., Contrib.Sci. 265: 1-45.
291-300. & . 1978. A new species of Chiropter-
& J. F. LYNCH. 1982. Effectsof latitude,sea- otriton(Amphibia: Caudata) fromBaja Verapaz,
son, elevation, and microhabitaton field body Guatemala,withcommentson relationships among
temperaturesof neotropicaland temperatezone CentralAmericanmembersofthegenus.Nat. Hist.
salamanders. Ecology 63: 1657-1664. Mus. Los Angeles Co., Contrib.Sci. 294: 1-22.
FROST, D. R. (editor). 1985. Amphibian Species of & S. Y. YANG. 1983. Genic and mor-
theWorld. Allen Press,Inc. & Assoc. Syst.Collec., phologicaldifferentiation in populationsofthesal-
Lawrence,Kansas. amander genus Pseudoeurycea inhabiting the
GADOW, H. 1908. ThroughSouthernMexico. With- transversevolcanic rangeof Mexico, withdescrip-
erby& Co., London. tion of a new species. Copeia 1983: 884-894.
GRUBB, P. J. & T. C. WHITMORE. 1966. A comparison MARTIN, P. S. 1958. A biogeographyof reptilesand
of montane and lowland rain forestin Ecuador. amphibians in the G6mez Farias region,Tamau-
II. The climate and its effectson the distribution lipas, Mexico. Misc. Publ. Mus. Zool. Univ. Mich-
and physiognomyof the forests.J. Ecol. 54: 303- igan 101: 1-102.
330. & B. E. HARRELL. 1957. The Pleistocenehis-
HANKEN, J. 1983. Genetic variation in a dwarfed tory of temperatebiotas in Mexico and eastern
lineage, the Mexican salamander genus Thorius United States. Ecology 38: 468-480.
(Amphibia: Plethodontidae):taxonomic,ecologic MAXSON, L. & D. B. WAKE. 1981. Albuminevolution
and evolutionaryimplications.Copeia 1983: 1051- and its phylogeneticimplications in the pletho-
1073. dontidsalamandergeneraPseudoeuryceaand Chi-
& D. B. WAKE. 1982. Genetic differentiation ropterotriton. Herpetologica37: 109-117.
among plethodontidsalamanders (genus Bolito- MYERS, C. W. 1969. The ecologicalgeographyofcloud
glossa) in Central and South America: implica- forestin Panama. Amer. Mus. Novit. 2396: 1-52.
tions forthe South American invasion. Herpeto- PAPENFUSS, T. J., D. B. WAKE & K. ADLER. 1983.
logica 38: 272-287. Salamanders of the genus Bolitoglossa fromthe

Sierra Madre del Sur of southernMexico. J. Her- & . 1955b. Reporton a small collection
petol. 17: 295-307. of amphibians fromVeracruz,witha description
PICADO, C. 1913. Les bromeliacees epiphytescon- of a new species of Pseudoeurycea.Herpetologica
sidereescommemilieubiologique.Bull. Sci. France 11: 81-85.
Belg. 7: 215-360. SINGH, S. K., G. SUAREZ & T. DOMINGUEZ. 1985. The
PLAFKER, G. 1976. Tectonic aspects of the Guate- Oaxaca, Mexico, earthquakeof 1931: lithospheric
malan earthquake of 4 February 1976. Science normalfaultingin the subductedCocos Plate. Na-
193: 1201-1208. ture 317: 56-58.
RABB, G. B. 1955. On certainMexican salamanders SMITH, H. M. 1945. Herpetologicalcollectingin ba-
of the plethodontidgenus Chiropterotriton. Occ. nana fieldsofMexico. Ward's NaturalScience Bull.
Pap. Mus. Zool. Univ. Michigan 587: 1-37, pls. 1945: 3-7.
I-III. STUART, L. C. 1943. Taxonomic and geographiccom-
1960. A new salamander of the genus Chi- ments on Guatemalan salamanders of the genus
ropterotriton fromChiapas, Mexico, withnoteson Oedipus. Misc. Publ. Mus. Zool. Univ. Michigan
relatedspecies. Copeia 1960: 304-311. 56: 1-33, pls. I-II.
RICKLEFS, R. E. & G. W. Cox. 1972. Taxon cycles 1948. The amphibians and reptilesof Alta
in the West Indian avifauna. Am. Nat. 106: 195- Verapaz,Guatemala. Misc. Publ. Mus. Zool. Univ.
219. Michigan 69: 5-107.
ROBINSON, D. C. 1976. A new dwarfsalamander of 1954. Descriptionsof some new amphibians
thegenusBolitoglossa(Plethodontidae)fromCos- and reptiles from Guatemala. Proc. Biol. Soc.
ta Rica. Proc. Biol. Soc. Washington89: 289-294. Washington67: 159-178.
1977. Herpetofauna bromelicola costarri- TANNER, W. W. 1950. A new genus of plethodontid
cense y renacuajos de Hyla picadoi Dunn. Pp. 31- salamander from Mexico. Great Basin Nat. 10:
43 in L. D. G6mez (editor),Historia Natural de 37-44.
Costa Rica, Volume 1. Biologia de las Bromeli- TAYLOR, E. H. 1941. New amphibians fromthe Ho-
aceas. Museo Nacional de Costa Rica, San Jose. bartM. Smith Mexican collections.Univ. Kansas
ROTH, G. & D. B. WAKE. 1985a. Trends in the func- Sci. Bull. 27: 141-167.
tional morphologyand sensorimotorcontrol of 1942. New caudata and salientia fromMex-
feedingbehavior in salamanders: an example of ico. Univ. Kansas Sci. Bull. 28: 295-323.
the role of internaldynamics in evolution. Acta 1944. The generaof plethodontsalamanders
Biotheoretica34: 175-192. in Mexico, Pt. 1. Univ. Kansas Sci. Bull. 30: 189-
& . 1985b. The structureof the brain- 232.
stemand cervicalspinal cord in relationto feeding 1952. The salamandersand caecilians ofCos-
oflunglesssalamanders,familyPlethodontidae.J. ta Rica. Univ. Kansas Sci. Bull. 34: 695-791.
Comp. Neurol. 241: 99-1 10. 1954. Additionsto the knownherpetological
RUTHVEN, A. G. 1922. The amphibians and reptiles fauna of Costa Rica with comments on other
of the Sierra Nevada de Santa Marta, Colombia. species. No. 1. Univ. Kansas Sci. Bull. 36: 597--
Misc. Publ. Mus. Zool. Univ. Michigan 8: 5-69, 639.
pls. 1-12. & H. M. SMITH. 1945. Summaryof the col-
SAVAGE, J. M. 1973. The geographicdistributionof lectionof amphibians made in Mexico underthe
frogs:patternsand predictions.Pp. 349-445 in J. Walter Rathbone Bacon Traveling Scholarship.
L. Vial (editor),EvolutionaryBiology of the An- Proc. U.S. Natl. Mus. 95: 521-613.
ura. Univ. Missouri Press, Columbia, Missouri. TRAPIDO, H. 1942. A new salamander fromVene-
1982. The enigma of the Central American zuela. Bol. Soc. Venezolana Cien. Nat. 8: 297-301 .
herpetofauna:dispersalsor vicariance?Ann. Mis- VIAL, J. L. 1968. The ecology of the tropical sala-
souri Bot. Gard. 69: 464-547. mander,Bolitoglossa subpalmata, in Costa Rica.
SCHMIDT, K. P. 1936a. Guatemalan salamanders of Rev. Biol. Trop. 15: 13-115.
thegenusOedipus.Zool. Ser. Field Mus. Nat. Hist. WAKE, D. B. 1966. Comparative osteologyand evo-
20: 135-166. lution of the lunglesssalamanders, familyPleth-
1936b. New amphibians and reptilesfrom odontidae. Mem. So. Calif. Acad. Sci. 4: 1-111.
Honduras in the Museum of Comparative Zool- & A. H. BRAME, JR. 1969. Systematicsand
ogy. Proc. Biol. Soc. Washington49: 43-50. evolution of neotropical salamanders of the Bo-
1942. A cloud forestcamp in Honduras. Chi- litoglossa helmrichigroup. Nat. Hist. Mus. Los
cago Nat. 5: 23-30. Angeles Co., Contrib.Sci. 175: 1-40.
SCOTT, N. J.,J. M. SAVAGE & D. C. ROBINSON. 1983. & P. ELIAS. 1983. New genera and a new
Checklistofreptilesand amphibians.Pp. 367-374 species of CentralAmerican salamanders,with a
in D. H. Janzen(editor),Costa Rican Natural His- reviewof thetropicalgenera(Amphibia,Caudata,
tory.Univ. Chicago Press, Chicago. Plethodontidae).Nat. Hist. Mus. Los AngelesCo.,
SHAFFER, H. B. 1978. Relative predationpressureon Contrib.Sci. 345: 1-19.
salamanders (Caudata: Plethodontidae)along an & J. F. LYNCH. 1976. The distribution,ecol-
altitudinaltransectin Guatemala. Copeia 1978: ogy,and evolutionaryhistoryof plethodontidsal-
268-272. amandersin tropicalAmerica.Nat. Hist. Mus. Los
SHANNON, F. A. & J. E. WERLER. 1955a. Notes on Angeles Co., Sci. Bull. 25: 1-65.
amphibiansofthe Los Tuxtlas Range of Veracruz, & . 1982. Evolutionaryrelationships
Mexico. Trans. Kans. Acad. Sci. 58: 360-386. among CentralAmerican salamanders of the Bo-

litoglossafranklinigroup,with a descriptionof a tributionof salamanders along elevational tran-

new species fromGuatemala. Herpetologica 38: sectsin Mexico and Guatemala. Brenesia (Suppl.)
257-272. (in press).
, A. H. BRAME & W. E. DUELLMAN. 1973. New WALKER,C.F. 1955. Anewsalamanderofthegenus
species of salamanders,genus Bolitoglossa, from PseudoeuryceafromTamaulipas. Occ. Pap. Mus.
Panama. Nat. Hist. Mus. Los Angeles Co., Con- Zool. Univ. Michigan 567: 1-8, pl. I.
trib.Sci. 248: 1-19. WERLER, J. E. & H. M. SMITH. 1952. Notes on a
5 & C. W. MYERS. 1970. Bolitoglossa collectionof reptilesand amphibians fromMex-
taylori,a new salamanderfromcloud forestof the ico, 1951-1952. Texas J. Sci. 4: 551-573.
Serrania de Pirre,eastern Panama. Amer. Mus. WILSON, E. 0. 1961. The nature of the taxon cycle
Novit. 2430: 1-18. in the Melanesian ant fauna.Amer. Nat. 95: 169-
, T. J. PAPENFUSS & J. F. LYNCH. 1987. Dis- 193.
APPENDIX I
Use of bromeliadsand moss mats by neotropicalsalamanders.All species knownto occur in either
of these microhabitatsare listed below. Literaturereferencesdo not include all observations for a
given species, but eitherthe firstor the best documentedexample. Where no publicationexists field
notes or notes frommuseum collectionsmade by the authorare cited.
Bromeliad Occurrence:
Bolitoglossaalvaradol DBW notes
B. arborescandens Taylor (1954)
B. borburata Trapido (1942)
B. cuchumatana Stuart(1943), Elias (1984)
B. dunni Schmidt (1942)
B. engelhardti Schmidt (1936a), Wake & Lynch (1976)
B. flavimembris DBW notes
B. franklini Taylor (1941), Wake & Lynch (1976)
B. hartwegi Wake & Brame (1969), Elias (1984)
B. helmrichi Schmidt (1936a)
B. hermosa Papenfusset al. (1983)
B. jacksoni Elias (1984)
B. /ignicolor Dunn (1926)
B. /incolni Wake & Lynch (1976), Elias (1984)
B. meliana Wake & Lynch (1982)
B. mexicana Taylor & Smith (1945)
B. minutula Wake et al. (1973)
B. morio Wake & Lynch (1976), Elias (1984)
B. mulleri Stuart(1943)
B. nicefori Brame & Wake (1963)
B. occidentalis Shannon & Werler(1955a)
B. odonnelli Stuart("probably," 1948)
B. platydactyla Taylor & Smith (1945)
B. ramosi Brame & Wake (1972)
B. resplendens Wake & Lynch (1976)
B. rostrata Wake & Lynch (1976)
B. rufescens Schmidt(1936a), Taylor & Smith (1945)
B. savagei Ruthven (1922)
B. subpalmata Dunn (1937)
B. taylori Wake et al. (1970)
B. vallecula Brame & Wake (1963)
B. walkeri Brame & Wake (1972)
B. yucatana DBW notes
Chiropterotritonarboreus Rabb (1955)
C. chiropterus DBW notes
C. chondrostega Martin (1958)
C. /avae Taylor (1942)
C. multidentatus Martin (1958)
Dendrotritonbromeliacia Schmidt(1 936a), Wake & Lynch (1976)
D. megarhinus Rabb (1960)
D. rabbi Lynch & Wake (1975), Elias (1984)
D. xolocalcae Taylor (1941)
Nototritonbarbouri Schmidt(1936b)

APPENDIX I. Continued
N. nasalis Dunn (1926), Schmidt(1942)

N. picadol Picado (1913)
N. veraepacis Lynch & Wake (1978)
Pseudoeuryceabell/i DBW notes fromT. J. Papenfuss
P. brunnata Wake & Lynch (1976), and DBW notes
P. exspectata Stuart(1954)
P. firscheini Werler& Smith (1952), Shannon & Werler
(1955b)
P. goebeli Schmidt(1936a), and DBW notes
P. leprosa DBW notes
P. nigromaculata DBW notes
P. scandens Walker (1955), Martin (1958)
P. smithi DBW notes fromT. J. Papenfuss
Thoriusdubitus DBW notes
Moss Mat Occurrence:
Bolitoglossadiminuta Robinson (1976-in a liverwortmat)
B. marmorea Wake et al. (1973)
B. subpalmata Taylor (1952)
Dendrotritoncuchumatanus Lynch & Wake (1975)
Nototritonpicadoi Taylor (1954)
N. richardi DBW notes
Nyctanolispernix Elias & Wake (1983)
Oedipina poelzi Brame (1963)
0. pseudouniformis Brame (1968)
0. uniformis Brame (1968)
Pseudoeurycearex Elias (1984)
P. scandens Martin (1958)
P. werleri Shannon & Werler(1955a)
Thoriusdubitus Taylor (1941)


Wake 1987

Uploaded by

Document Information

Original Description:

Copyright

Available Formats

Share this document

Share or Embed Document

Sharing Options

Did you find this document useful?

Is this content inappropriate?

Copyright:

Available Formats

Wake 1987

Uploaded by

Copyright:

Available Formats

Adaptive Radiation of Salamanders in Middle American Cloud Forests

Author(s): David B. Wake

This content downloaded from 91.155.186.71 on Tue, 27 May 2014 14:42:15 PM

The cloud forestsofMiddle Americaare home general,cloud forestsformbetweenelevationsof

94720, U.S.A. Paper received 7 July1985.

ANN. MISSOURI BOT. GARD. 74: 242-264. 1987.

This content downloaded from 91.155.186.71 on Tue, 27 May 2014 14:42:15 PM

environmentsare effectively bufferedfromdes-

dontid salamanders in the New World tropics; 2? 20

unusual is theirgreatdiversityin theNew World 1,6

tropics.Middle America has been the settingfor 0 2000/12

an extensive,unique adaptive radiationthathas

This content downloaded from 91.155.186.71 on Tue, 27 May 2014 14:42:15 PM

FIGuRE 3. Chiropterotriton a bromeliad-

gion 3, and onlyone species extendsas farnorth

This content downloaded from 91.155.186.71 on Tue, 27 May 2014 14:42:15 PM

penetrationfromthe northpersisted.The genus FIGURE 7. Distributionof the genus Dendrotriton.

FIGURE 8. DistributionofthegenusN~ototriton. 1This

This content downloaded from 91.155.186.71 on Tue, 27 May 2014 14:42:15 PM

000 Guelatoo ~~~~~Forest

least two distinctsubgroups,an interpretation and it occurs in regionsof Caribbean drainage.

This content downloaded from 91.155.186.71 on Tue, 27 May 2014 14:42:15 PM

This content downloaded from 91.155.186.71 on Tue, 27 May 2014 14:42:15 PM

This content downloaded from 91.155.186.71 on Tue, 27 May 2014 14:42:15 PM

in morphology.In generaltheyare slenderand ders,includinga lowercloud forest(1,600-2,400

This content downloaded from 91.155.186.71 on Tue, 27 May 2014 14:42:15 PM

CZ,E cia, B. engelhardti,B. franklini,Pseudoeurycea

This content downloaded from 91.155.186.71 on Tue, 27 May 2014 14:42:15 PM

TABLE 2. Relative abundance of salamanders in bromeliads,San Marcos transect.

Elevation Wet Season' Dry Season2 Combined

TABLE 3. Distributionof salamanders in brome-

'These data are for55 Dendrotritonbromeliaciaand 'These dataarefor59 Dendrotritonbromeliaciaand

This content downloaded from 91.155.186.71 on Tue, 27 May 2014 14:42:15 PM

TABLE 5. Test forrandomness,combineddata from

This content downloaded from 91.155.186.71 on Tue, 27 May 2014 14:42:15 PM

as paedomorphosisthataffectsa numberof fea-

This content downloaded from 91.155.186.71 on Tue, 27 May 2014 14:42:15 PM

Costa Rica seven species are known fromele-

This content downloaded from 91.155.186.71 on Tue, 27 May 2014 14:42:15 PM

to the south (Dunn, 1926; Taylor, 1944, 1952; ternsof microhabitatutilizationdifferdramati-

This content downloaded from 91.155.186.71 on Tue, 27 May 2014 14:42:15 PM

This content downloaded from 91.155.186.71 on Tue, 27 May 2014 14:42:15 PM

ritoryextendingabout 60 km fromthe vicinity Tapanti thereis an especiallyrichepiphytefau-

This content downloaded from 91.155.186.71 on Tue, 27 May 2014 14:42:15 PM

rienceswith Chiropterotriton lavae in fragments chains. These postulatedcyclesofexpansion and

This content downloaded from 91.155.186.71 on Tue, 27 May 2014 14:42:15 PM

This content downloaded from 91.155.186.71 on Tue, 27 May 2014 14:42:15 PM

This content downloaded from 91.155.186.71 on Tue, 27 May 2014 14:42:15 PM

* 1968. Systematicsand evolutionoftheMeso- , J.F. LYNCH & D. B. WAKE. 1980. Salamander

This content downloaded from 91.155.186.71 on Tue, 27 May 2014 14:42:15 PM

This content downloaded from 91.155.186.71 on Tue, 27 May 2014 14:42:15 PM

litoglossafranklinigroup,with a descriptionof a tributionof salamanders along elevational tran-

This content downloaded from 91.155.186.71 on Tue, 27 May 2014 14:42:15 PM

N. nasalis Dunn (1926), Schmidt(1942)

This content downloaded from 91.155.186.71 on Tue, 27 May 2014 14:42:15 PM

You might also like