Biogeographic area relationships of lowland
Neotropical rainforest based on raw
distributions of vertebrate groups
SANTIAGO R. RON*
Hyothesrs of thc historic biogeography of Neotropical anurans inliabitirig lotvland forests
\<crc generated using Parsimony IZnalysis of Endemicity. In ordrr to establish comparisons
\vith the Ihgcographical patterns of other vertebrates, previous cladistic analyses rrportcd
in thr literature (for lizards and primates) \ v e x extended and reanalysed to match the
geographical scope of the aiiuran analysis. Cladistic analysis of the distribution of 33.5 annran
species at I + localities showed two regions that form a basal dicliotoml.: ( I ) Central
i h e r i c a Choco and (2) Amazon Basin Brazilian Atlantic Forest. This rcsult i s interpreted
as tlic first ~icariancrc lit that separated loivland Neotropical rainforcsts into Cis-Andran
(east from the Andes) and Tr a ns- hde a n (\vest from thc Andes) areas. \Vithin the Cis-IZndean
localitics, thc earliest separation occurred Ixtwccn the Amazon Basin and the Brazilian
.Itlantic Forest. \Vitliin the Amazon Basin. thrcc distincti\,e clusters arc defined: (1) B e l h ,
( 2 ) Guianan Region, and (3) Cppcr Amazon Basin. Data sets on the distribution of anurans,
lizards, and mammals hai.c strong cladistic signal. Strong congruencc cxists among the arca
cladograms of anurans, lizards, and primates. All of them hayc, or at least did not conflict
\vith: (1) a basal srparatiori bet\veen Cis- and Trans-Andean regions, (2) a Central American
clad?. (3) thc Choco R r p n is sister to the Central American clade; (4) an Amazon Basin
clade. (5) an Upper Amazon Basin clade: and (6) a Guianan clade. The arca cladograms
are dichotomous and thrrrforc do not support biogeographic theories that Inpothesize
simultancous isolations of biotas in thr Ncotropics.
+
+
0 2000 'I'hr I.itinrari Socictv of' L.onrlon
XDDITIONAL KEY IVORDS: biogeography
anuriins lizards primates Amazonia
cndcmi~m tropical rainforrst.
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Parsimony Analysis of Endemicity
South America Central America arcas of
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(:oNTENI'S
lntroduch n . . . . . . . . . . . . . . . .
Analytical considerations . . . . . . . . .
PAE: theoretical considcrations . . . . . . .
Congruence betlveen cladistic biogeography and PAL
Is PAE applicable to Neotropical aniirans? . . .
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* Current address: ?\Iusco dc Zoologja, Lkpartamento de Ciencias Biolhgicas, Pontificia Universidad
<:atblica dcl Ecuador, Apartado Postal 17-0 1-2 184, Quito, Ecuador. E-mail: [email protected]
0024 -L066/00/ 11037!)
+ 2-1 $3.5.lK)/O
379
0 2000 'I'lic. I h i r a n Socit-t\ nT 1.ondon
I\ I1101)L
c. 1 I O \
1)cy)ite the fact that the Neotropical Realm has the greatest anuran di\.ersit). it1
\Yorld iSO% of tlic total number of species:~,kiioavledgc of the t)iogcographic
histories of Neotropical aiiuraii faunas is limited. ‘llie first attempts to csplaiii
I )iog::cwgrapIiicpatterns of Ncotropical itnuratis folloived a dispcrsalist approach
Sar.agc. 1 982; Vanzoliiii 8r Hcyer, 1985; Ducllman, 1988, 1990). According to
thost. liypothcscs, thc distributions of aiiurari species wcrc influenced greatly 13) tlic
Ioc.ation of thr centres of origin of taxa and subscqucnt dispersal and \.icarianw
t IN.
C’\
cxnti;.
h t a i i t c.onimunitics are believed to be composed of clcnicrits belonging to thrw
dilli-rent historic faunal asscmblages: North American, Central American, arid South
.\inc.rican [Sa\.age, 1982; \‘anzolini 8r Hcycr, 1985; Duellman, 1988, 1990). Thc
c\-idcricc uscd to detcrmiric centres of origin was based mainly 011 patterns of
tli\wsity (i.e. regions with higher diversity equal the centre of origin of t;-is:<j.
Ho\wver, as Vaiizolini 8i Hcycr (1 985) acknowledged, alteriiatc intcrprctatioiis arc
possiihlc. ‘l’lierc arc many other criteria from which centres of origin can lie infci
A\~iioiig
tlicsc are (1) tlie arca of highest dominance and density of clistrihution; (2)
c ~ r ( ~ivhcre
x,
indi\-iduals show morv complex anatomical structures: and (3) areas
\\ I I ~ Y ( . the most ph?-logenetically derived or basal tam occur. Caiii (1 944) listed 1 3
t,ritcLria fix- dctcrmining centres of origin. Unfortunately, cacli can lead t o diffcrctit
c.onclusions (Humphries 8r Parcnti. 1986). Rased on patterns of di\Pcrsit);, lJyiic1i
1 9 i 9 ) dcfiiicd [bur arcas of marked endemism of ampliihians in South .\mcricmi
lo\\ land tropical forests: (1) Choch, (2) Upper A4mazonBasin. (3) Guianas. and ‘4,
.\dantic Forrst of Brazil.
<:omparisom of species asscmh1agc.s based on raw similarity also lia\.e tiecm usccl
to dcri\.c biogeographic h?l)otheses about anurans in the Ncotropic:s. I>ucllman
I !)!)(I) coiisidcrcd community similarity of the 1-ierpcztofaunasat thrccc localitirxs in
rlic. .\mazon Basin and t\vo in Central America. He concluded thai. tlic Central
.liiir.ricaii localitics (i.e. Rarro Colorado, Panama; La Selva, Costa Kicaj are more
\iiiiilar to each other than the); are to any of the localities in the Amazon Basin 1i.c.
ilia, Lcuador; Cocha Cashu, Pcru; hlanaus, Brazil).
k i \ v comparisons of thc numlier of sharcd species among regions (~c.g.
c.oniinriiiit)-
resemblance indices, multivariate clustering techniques) rely on the intuitive assumption that similarities in the composition of biotas can be, at least partially, the
consequcnce of shared geographic history. However, the results derived from these
‘phenetic’ techniques are limited by the fact that they are process neutral and,
therefore, their strict biogeographical meaning can be enigmatic (Rosen, 1992). An
additional problem is that the usc of different algorithms can lead to contradictory
hypotheses for the same historical truth of area relationships (Raxworthy &
Nussbaum, 1996).
Haffer (1969, 1974) postulated through the Pleistocene Refuges Hypothesis that
diminution in temperature and moisture during glacial periods led to reductions
and isolation of forested environments. This resulted in speciation within the isolated
biotas, and therefore, increased diversity and endemicity throughout the Neotropical
lowland forests. Lynch (1979) and Duellman (1982) analysed distribution patterns
of amphibians and outlined congruencies with Haffer’s hypothesis.
Anahtical considerations
In recent years, most attempts to elucidate biogeographic history have been based
on the combination of phylogeny and distribution of taxa. These powerful analytical
techniques, known under the generic names of cladistic, or vicariance, biogeograph) ,
are used in an attempt to detcrmine the history of geographic vicariance based 011
the history of phyletic divergence of taxa (for reviews, see Humphries & Parenti,
1986; Brooks & hlclennan, 1991; Espinosa & Llorente, 1993). The basic assumption
made is that the history of the distribution of taxa covaries with their history of
speciation (Wiley, 1988). Under a scenario in which the distribution patterns
generated by long distance dispersal and extinction are unorganized (no signal) with
respect to those generated by allopatric speciation, phylogenetic relationships are
expected to be a mirror image of the history of geographic vicariance (Wiley, 1988).
A strictly methodological problem in the application of cladistic biogeographic or
dispersal-vicariance analyses (Ronquist, 1997) is that they require knowledge of
phylogeny of taxa distributed allopatrically in the target regions. This is a serious
problem for most vertebrate groups inhabiting Neotropical lowlands, for which there
are few well supported phylogenctic hypotheses.
An alternative technique that uses cladistic parsimony to infer historic relationships
among areas is Parsimony Analysis of Endemicity (PAE). This procedure, proposed
by Rosen (1988) and Rosen & Smith (1988), has been applied increasingly in several
biogeographic studies to a variety of taxa and regions (Roscn & Smith, 1988;
Cracraft, 199 1 ; Morrone, 1994; Avila-Pires, 1995; Fernandes, Da Silva & Silva,
1995; da Silva & Oren, 1996; Posadas, 1996; Raxworthy & Nussbaum, 1996;
Emerson, Wallis & Patrick, 1997; Bates, Hackett & Cracraft, 1998). It is andlogous
to phylogenetic systematic analysis in the use of cladistic parsimony to determine
historical hierarchies among the entities analysed. In PAE, the target localities or
geographic regions are regarded as equivalcnt to taxa in phylogenetic sy stematicy,
whereas the presence or absencc of natural taxa (e.g. genus, species, subspecies) in
the locality or region are regarded as equivalent to characters. Subspecies are
considered natural taxa only if they include all the descendants from a common
ancestor.
R X : tlimeticnl con ridemtion \
,\ccordiiig to Rosen ( 1 988), tlie logical basis that underlies the use of P:\E is th(,
a\s;umption that sites that share taxa are closely related because the). share ;I morc
rvccii~Iiislor). of tiiunistic exchaiigc. Ho\ve\.cr, this assumption, li>- itself: does no1
j i i y t i l ) the use of cladistic parsimon). for area grouping. If community similarity is
m;itc~liccl dirc,ccly 1)- historical relatedness. it ~vould tic equally or ( t ~ m
iiioix~
:tppropriatc to usc 'phenctic' techniques \)ased on r a \ . similarit), (i.c. tlic i i w o f
;iiial)-scs that treat any kind of similarit!. as c\ideiicc of rclatednrss').
(~:racraftf 1 YC) 1 ) offcred a more elithoratc interpretation. He suggested that sliai-ctl
t x i i aniong arcas sen^ a s c\.idencc of historical relatedncss and arc tlie coiisequciicc
o I' f;iilurc. 01' speciation i \ h i the arcas bccamc separatcd. i\ccordirig to C:rac.ratt
1 !)W. il' biotic dispersion is historically constrained. it should he cxpcc-tcd that the
(li,ti-il)utioii of' natural taxit I\ ill csliihit Iiierarchical congruence \\-hen
(.I,< I (1 ISrIc~all).
'.
'
111 c,latli.;tic, hiogcography, tlirce :tssumptions have heen niadc t o interpret the
iiiIi)i.iiiati\-ci~cssof^ \\-idcsprcad taxa. Urictcr I\ssumption 0 (Zandce & Koos. 1 W i :
l\'ilt,>. I W j i I. \\-itlcspread taxa are considered to hc monopliylctic. (thcrcfixcs. the
~ i x ' ; i \\s 1iei.c each one occurs are considered to he 'riioiiophyletic' as ivcll)..\ssuiiiptioiis
I ;tiid 2 (Nelson & Platnick. 1981 ) interpret midespread taxa a s possihl). parapli).lctic.
;tiid possilolJ- pol~phylrtic,rcspccti\.cly (Nelson & Ladigcs. 199 1).
l'.\I< opcratcs iuicier ,\ssumption 0. 1t intcrprets \videspread iiatural taxa c3.g.
moiiol)h).lctic gcncra, species, subspecies) ;is evidence for the clustcring together of
ycographic. regions or localities (i.e. making them 'monopli).letic'). It fi)llo\v~tlir
clcliiiitioii of 's).iiaI)"ii~orphy' in hiogeography proposed by Zandcc & Roos i1987 ,:
"S~ii"Ij~)iiior1Ih!. or hornolo,q is a inonoplij.lctic group of. taxa uniqucl!- sharing ;I
s ;t ci)iiseclLieiicc of shared history. Indicators of nun-shared histor! .
1 aiitl extinction, arc ad-lioc statements and thus arc aiialog~irst o
lioiiioplas) ." For cxaniplc, in the PAE of Neotropical aiiuraiis pcrformcd in tlic
n t study. t ' J l r ' i i t l i ~ ~ ~ d n t .ultniria.yuicii.)
t~~lu,~
Rarhour aiicl Duiin ( lY2 1 ) is intcrprctcd
21s ;I s!.iiapoiiiorptij, Lor the sevcii localities (Upper Amazonian) \\.lierc it occurs. I\
i h (.oiisiclcxd to he a n indication that a t some point in the past, thc t'ppcr .4niazoii
l3:ihiii constituted a single hiogeographic unit.
1-1 itlr r .\ s s u n i p ti on 0. cladis t ic hiogcograph y deri\w co iiiponcii t s for 21 I-ca (,I ii tloqrains Ioascd oil the distribution of extant taxa and the distributioii o f their
~ i i ( ~ s t o r Phylogcnics
s.
arc recpircd a s ;I iiicaiis to infer the distrihution of' tlic
aiic.c\tral t u a (assuming that ancienl distributioiis arc tlie s u m of the disti-il,utioii
( i f ' tlic dcsccndants). PXE focuscs on a suhsrt of the inforiiiatioii rramined 1,)
(.1,a1'istic
.
t)iogeograpliic tcchniqurs under Xssumption 0, bccause it only c()iisitlci.j
rlic. distribution of extant taxa. From an aiial?-tical point of viv\v. this is c.ornplctclJ
Icgi1iiiiatc h.aLisc in cladistic analysis --as in Brooks' iisc of PAIL(\\'ilc>-. 1988I or
in t h c aiial!,sis proposed toy Zandec & Roos (1 987)- transformation
t l a i a niatriccx arc considered independent of one another. Each taxo
<iii(x->traIj
coiitrihutes c c ~ ~ i arelc\-ant
ll~~
infi)miation for the ljuildirig of' the area
c~1;rcloyriuii(l)ut see Y[aydeii. 1988). If' thc suhset of- information considcrd 1)). P.?IF,
i \ Iiirgc, ciiougli, a r m cladograriis that accurately represent the histor)- (.if pograpliic.
\.ic.:iriaiicc should he cxpcctcd. 'Zbesc results arc predicted to lie sirnilar t o t l i o w
tlcri\.cd frurn cladistic biogeographic analyses.
~
'
Coiy ueiice betkteen cladistic biogeogiapb and M E
Some evidence suggests that PAL can gcncrate biogeographic hypothesea that
arc congruent with the results of cladistic biogeographic analyses. Cracraft (1 99 1,
1994) applied PAE to the distribution of genera, species, and subspecies of
,Australian birds through 14 areas of cndemisni and found a 'moderately strong'
congruence with area cladograms derived from cladistic biogeographic techniques.
Da Sil1.a 8r. Oren (1996) applied PAE to Amazonian primate taxa and found
similar area cladograms to those derived from cladistic biogeography applied to
Neotropical bird taxa by Prum (1 988). "henever possible, the performance of PAE
should be evaluated with area cladograms obtained from cladistic biogeographic
techniques.
IJ PAE a/$licabLe to &eotro$cal anuranJ?
PAE should not be applied without at least some empirical evidence that as a
\\.hole, the target organisms meet the restrictions posited by Assumption 0. The
distribution patterns generated by sympatric speciation, long-distance dispersal, and
extinction should be less frequent, or at least unorganized (lack signal), relative to
the distribution patterns generated by vicariance.
Consequently, ideal organisms for the application of PAE (and also cladistic
biogeography techniques) are those that have limited dispersal abilities and speciate
in a Licariant manner. Anurans seem to he a good group for the application of
PAE. They have low vagility and high endemicity mainly because of their limited
physiological tolerances (Duellman, 1982). Moreover, some empirical evidence
suggests that vicariance speciation is the most frequcnt speciation mechanism in
anurans. Lynch (1989) found that 84% of a total of 32 anuran species belonging to
the genera Eleuthemdacbvlus, C'eratophgjs, and Ram appeared to have speciated vicariantly
(\Yiley's, 1981, Allopatric Speciation hIode I). In the same study, Lynch found
evidence that suggests that vicariance also is the most common mode of speciation
among vertebrates (7 1%, n = 66).
Thc present investigation analyses the distributional patterns of Neotropical
lowland forest anurans by using cladistic parsimony techniques. The purpose of this
analysis is to generate hypotheses of the historical biogeography for the group. In
order to establish comparisons with the biogeographies of other vertebrates, previous
PAE applied to lizards (Avila-Pircs, 1995) and primates (da Silva & Oren, 1996) in
this region were extended and reanalysed in an attempt to match the geographical
scope of the anuran analysis.
Anurans
PRE was applied to the distribution of species of anurans at 14 localities of
lowland Neotropical rainforests in Central America, the Chocoan Region, Amazon
384
S. R. RON
Figure I. Localities selected for the Parsimony Analysis of Endemicity of anurans on lowland Neouopical
rainforests.
Basin, and the Brazilian Atlantic Forest (Fig. 1). The analysis was restricted to
rainforests to reduce the effect of differing environmental conditions as a factor in
the composition of the anuran communities. The localities considered are listed
below (main source of data on species occurrence in parentheses; all lists updated
taxonomically).
Central America
- Barro Colorado, Panama (Rand & Myers, 1990)
- La Selva, Costa Rica (Guyer, 1990; Donnelly, 1994)
Western Ecuador (Chocoan)
-Rio Palenque (collection at the Natural History Museum at the University of
Kansas)
Amazonian Ecuador
- Santa Cecilia (Duellman, 1978)
-Yasuni (collections by S. Ron, S. de la Torre, and Morley Read)
ilmazonian Peiu
Cocha Cashu (Rodriguez & Cadle, 1990)
Cuzco-Amazhico (Duellman & Salas, 1991)
Explorama (observations and collections by W.E. Duellman and L.O. Rodriguez)
Northern Loreto (combination of Teniente Lopez and San Jacinto from Duellman & Mendelson, 1995)
Panguana (Toft & Duellman, 1979; Schluter, 1984; Aichinger, 1987; Duellman
& ‘lhomas, 1996)
-
-
-
~
L4magonian Brazil
- Beltm (Grump, 1971; Duellman, 1997)
INPA-WWF Reserves (Zimmerman & Rodrigues, 1990; Zimmcrman & Simberloff, 1996; Duellman, 1997)
-
Atlantic Forest Brazil
Boractia (Heyer et al., 1990)
-
French Guyana
- Trois Sauts (Lescure, 1982; ‘Upper Rivicre Oyapock’ from Duellman, 1997).
The sizes of the areas sampled at each locality were defined by the author(s) of
each survey. At all localities, a variety of habitats was sampled (e.g. terra firme and
flooded forests, open areas).
An additional PAE was performed with localities grouped according to Haffer’e
endemicity regions (Haffer, 1974, fig. 2; Haffer, 1985; Prum, 1988; da Silva & Oren,
1996).
Beltm
Central America (Barro Colorado La Selva)
Choco (Rio Palenque)
Guiana (Trois Sauts INPA-MTYF Resen.es)
- Inambari (Cocha Cashu
C u ~ c oAmaz6nico Panguana)
Napo (Santa Cecilia 1,oreto Yasuni)
-RondAnia (data from de la Riva, 1993 and collcctions at the Natural History
Sluseum at the University of Kansas)
Serra do Mar (Boractia)
-
+
-
-
-
-
+
+
+
+
+
-
Although the RondBnia area is mostly dominated by dry seasonal forests, it was
included in this analysis in order to establish comparisons with the analysis of other
vertebrates (not restricted to lowland rainforests). Explorama was not considered for
this PAE, because it is located at the border of the Napo and Inambari regions.
For the PAE, the presence or absence of species was codcd in a matrix of taxa
x localities (0 for absence, 1 for presence). A hypothetical ‘empty locality’ where
no species occur was used to root area cladograms (Rosen, 1988; Cracraft, 1991).
Matrices were analysed cladistically with PAUP Ver. 3.1, (Swofford, 1993). The
branch-and-bound search was used to find the most parsimonious area cladograms
for separate localities of anurans. In the analysis of grouped localities (Haffer’s
regions) of anurans, the exhaustive search option was employed. T o determine
branch support, decay indices were computed with the program AUTODECAY
Ver. 3.0. The decay index for each node represents the tree length differences (in
number of steps) between the most parsimonious tree and longer trees in which that
S. R. RON
386
node collapses. Data matrices for separated and combined localities are available
upon request to the author or they can be downloaded from the following address:
http: / /www.puce.edu.ec/Zoologia/PAE/pae.html.
In order to test whether the topology of the PAE area cladogam was mainly a
result of geographic distance alone, an area phenogam was constructed from a
painvise comparison of geographic distances between localities. Clusters were connected with the average linkage method and Euclidean distances from Minitab
1O.Xtra (Minitab, 1995). The compatibility of the topology of this phenogram with
the data matrix of the PAE was tested using Templeton’s (1983)Test of Congruence.
Duellman’s (1990) Coefficient of Biogeographic Resemblance was used to make
comparison among the anuran communities at localities analysed in the PAE.
T o determine if the data matrix of localities contained cladistically structured
data, gl statistics (Sokal & Rohlf, 1995) were calculated to evaluate the skewness of
the distribution of 10 000 randomly generated trees. Hillis & Huelsenbeck’s (1992)
critical values were used to test significant differences from unstructured data.
Lizards
The PAE of Amazonian lizards performed by Avila-Pires (1995) was extended
by adding the Central American localities of Barro Colorado (Panama; data from
Rand & Myers, 1990) and La Selva (Costa Rica; data from Guyer, 1990 & Donnelly,
1994). Species and subspecies of lizards (Squamata, excluding Serpentes and Amphisbaenia) occurring at 13 localities throughout Central America and the Amazon
Basin were analysed.
An additional PAE was performed with the same localities grouped according
with Haffer’s endemicity regions (Fig. 2).
Belkm (Eastern Para)
Central America (Barro Colorado +La Selva)
- Guiana (Amapa
Manaus Surinam)
- Inambari (Southern Peru
Meso Peru)
- Nap0 (Santa Cecilia)
- Para (Carajas)
- Rondbnia
-
-
+
+
+
The localities of Iquitos and Benjamin Constant were deleted from this analysis
because they are on the border between the Nap0 and Inambari regions.
For the PAE, same coding and analyses procedures as for anurans were conducted.
For the analysis of localities considered separately, the branch-and-bound search
was used to find the most parsimonious area cladogram(s). For the analysis of
grouped localities, the exhaustive search option was employed. Data matrices are
available upon request to the author or they can be downloaded from the address:
http:/ /www.puce.edu.ec/Zoologia/PAE/pae.html.
Primates
The PAE of Amazonian primates performed by da Silva and Oren (1996) was
extended by adding the Central American and Chocoan regions (data on species
Fi<gurc2. Loivlaiid Neotropical forrst areas of cndcmism (aftcr HafTcr 1974. 1985).
distribution for Central America and Choco primates from Emmons & Feer, 1997).
Prior to the analysis, da Silva & Oren’s (1 996) Amazonian interfluvial regions were
grouped according to Haffer’s regions of endemicity (Fig. 2).
For the PAE, same coding and analyses procedures as for anurans were conducted.
The data matrix is available upon request to the author or it can be downloaded
from the website, address 011 facing page.
RESUI.TS
Anurans
One most parsimonious area cladogram (CI = 0.7 1, tree length = 475) was obtained
from cladistic analysis on the distribution of 335 anuran species at 14 localities. Two
regions form a basal dichotomy: (1) Central America+Choco and (2) Amazon
Basin Brazilian Atlantic Forest. According to this area cladogram, the first vicariance event that separated lowland Neotropical rainforests isolated the Cis-Andean
+
Basin + Brazilim Atlantic
+ C h o c o) locdlities (Fig. ‘3).
Forest) from Trciiis-Aiidean (Ceiitr‘~1
IYithin Cis-Andcdn localities. the cnrlicst
\ c p u ,ition o c c ui rcd lietween the Xinazoii Basin arid the Brazilian Atlantic Forest.
\ \ itliiii the \ m u o n Bdsiii, tlircc distincti\e clusters \$ere defined: (1) ~e1i.m.(21
( I i i i r i i i C i i i Rcgioii (INPLL\.2?1’F Rescrl es
Trok Sauts. French Gu\ ann), and ( 3 )
L‘ppci ,Arrinzon Basin. \Yitliin Trails-Andean localitim, the t\i o Ccntral A\mcrican
l o c ditics \\el? riiorc clowlj related to each other thdn either was to the Kio Paleiicjuc
lo( h l (Choc6 Keqion). Decaj iiidcxes (in parentheses) shou rd high support fi)r
t l i c Ckntr‘~l.\me1 ic dii ( 17), Arna,mii Ba4n (1 2). Upper ,4ma7uri Ba4n (6). Coc Ii‘i
(l,isliu C’ci~corlinaz6nico (7) clade4.
Ttic dnin matrix of localities considered scparately is structured cladisticall) ( q l =
0 X. l’<O.O 1). Di$trihutions of randomh gciierated area cladograms arc s k e \ ~ c d
.h,i/on
\iwrit nil
+
+
~
to the left. indicating that the prcscnce/absencc of taxa is not random (Fiy. 4). The
number of species at each l o c d h ) , number of shared specics, dnd the Coefficient
of Biogeographic Resemblance are shown in Table 1.
The area cladogram of combined localities (Haffer’s regions of endemicit)) is full)
consistent \I ith the area clddoLg-amof the localities considered scparately. One most
parsimonious area cladogram was obtained from data on the distribution of 342
species of anurans in nine regions (Fig. 5, CI = 0.87, tree length = 394). ‘Two basal
clades were defined: (1) Cis-Andean and (2) Trans-Andean. Decay indexes showed
high support valucs for the Central American (1 7), Amazon Basin (8), and Upper
Amazon Basin (1 7) clades.
The topoloLgyof the phenogrdm of localities based on geographic distances (Fig.
6) i.; significantly incompatible with the data matrix ofthe PAE of localities considered
- 7.23, P<0.000 1).
scparatelj (hlann-\t’hitney’s
<=
One most parsimonious area cladogram (CI = 0.69, trcc length = 156)u d 5 obtained
from the cladistic analysis of the distributions of 108 species of lizards at 13 localities
(Fig. 7). As observed in anurans, there are two well-defined basal clusters: (1) CisAndean and (2) Trans-Andean. Within the Amazon Basin, there are two distinctive
clusters: (1) Upper Amazon (Napo Inambari) and (2) Guiana R o n d h i a
Para BelCm.
The highest decay indexes were for the Central American (9), Amazon Basin (6),
Guianan (5),and Santa Cecilia+Iquitos (5) cladcs. The data matrix is structured
cladistically @I = - 0.84, R 0 . 0 1). Distributions of random-generated area cladograms arc skewed to the left, indicating that the presence/absence of taxa are not
random (Fig. 4).
The area cladogram of regions is fully consistent with the area cladogram of
localitics considered separate11 (Fig. 8). One most parsimonious area cladogram M. as
obtained from data on the distribution of 107 species of lizards in eight rcgions
(CI = 0.79, tree length = 135). The highest decay indexes were for the Central
American (9), Amazon Basin (€9, Upper Amazon Basin (7), and Guianan (6) clades.
+
+
+
+
Primate5
Two most parsimonious area cladograms (CI = 0.86, tree length = 65) were
obtained from the cladistic analysis of the distribution of 56 species of primates in
eight regions (conscnsus in Fig. 9). As in the PAEs of anurans and liLards, there arc
two well-defined basal clusters: (1) Central America Choco and (2) Amazon Basin.
h‘ithin the Amazon Basin, there are three distinctive clusters: (1) Upper Amazonia
(Napo Inambari), (2) Guiana, and (3) Belkm Para. The highest decay indexes
were for the Upper Amazon Basin (5),Trans-Andean (4), and Amazon Basin (3)
clades.
The data matrix is structured cladistically @I = - 1.13, W O . 0 1). Distributions of
random-generated area cladograms are skewed to the left, indicating that presence/
absence of taxa are not random (Fig. 4).
+
+
+
'
:
1400
'
Anurans
1200 -
1000 -
c
800 -
600 -
most parsimonious
400- area
cladogra
1
200-
0
450 500
"
'
~
"
550
"
'
600
'
'
650
I
'
700
750
800
800 I
700
I
1
Lizards
-
600 500
400
300 -
200
100
0
140 160 180 200 220 240 260 280
300
800
Primates
700
600
500
400
300
200
most parsimonious
area cladogram
100
0
60
\
85 110 135 160 185 210 235 260 285
La Selva (Costa Rica)
Barro Colorado (Panama)
INPA Reserves (Brazil)
Cocha Cashu (Peru)
Santa Cecilia (Ecuador)
Yasuni (Ecuador)
Loreto (Peru)
Cuzco Amazonico (Peru)
Explorama (Peru)
Panguana (Peru)
Beltm (Brazil)
Trois Sauts (French Guiana)
Rio Palenque (Ecuador)
Borackia
0.10
0.08
0.06
0.08
0.07
0.09
0.09
0.09
0.12
0.09
0.18
0
0.41
0.47
0.43
0.39
0.41
0.43
0.43
0.34
0.54
0.02
0.03
0.57
0.54
0.48
0.8
0.59
0.66
0.33
0.38
0.02
0.03
2
5
25
72
2
5
51
24
49
45
0.28
0.10
0.03
0.03
0.03
0.04
0.04
0.04
0.04
0.05
0.04
0.16
0
CC
INPA
BC
LS
2
5
29
42
66
84
0.73
0.53
0.59
0.58
0.3
0.43
0.02
0.01
0.78
0.68
0.58
0.62
0.64
0.31
0.41
0.02
0.03
YA
2
4
32
45
a5
SC
2
4
23
33
51
55
66
0.48
0.58
0.61
0.25
0.39
0.02
0.02
LO
0.6
0.7
0.3
0.4
0
0
2
5
24
55
44
40
32
66
CA
0.6
0.4
0.4
0
0
2
5
25
41
47
44
38
37
66
EX
0.3
0.4
0
0
2
5
24
44
47
42
39
41
37
61
PA
0.5
0
0.1
2
5
15
18
19
18
13
17
18
14
36
BEL
0
0
2
5
30
25
30
31
25
25
24
22
23
61
TS
3
F
65
0
*
G
tl
g
$
'
4
2
"
2
g
1
2
2
1
2
; :
O
1
e8
O
0
BO
8
8
m
6
7
1
1
1
1
1
1
1
1
1
1
30
RP
rainforests. See Figure 1 for location of sites. The total number of species at each site is shown in boldface in the common cell. Abbreviations in headings
correspond to sites in the first column
TABLE
1. Number of shared species (upper right) and coefficients of biogeographic resemblance (italics, lower left) between 14 localities of Neotropical lowland
392
S. R. RON
Figure 5 . Most parsimonious area cladogram (tree length = 394, CI = 0.87, RI =0.74) for Parsimony
Analysis of Endemicity applied to presence/absence of 342 species of anurans in eight Neotropical
regions (defined after Haffer, 1974, 1985). An ‘empty’ region (no species) was used to root the area
cladogram. Decay indexes are shown in circles. Position of nodes and internodes on the map is not
informative; branching pattern indicates sequence of geographic divergence among regions.
DISCUSSION
Kcariance events and endemism of lowland anuran faunas
The results found in this study show that the earliest biogeographical divergence
in time occurred between Cis- and Trans-Andean anuran biotas. The isolation of
South America during nearly all of the Cenozoic and the elevation of the Andes as
a geographic barrier between lowland forests have been decisive for the patterns of
endemism of Neotropical forests.
Within the Amazon Basin, the cluster that has the best support is the Upper
Amazon. The existence of a strong Eastern and Western Amazonian separation has
been postulated previously for other groups of organisms (Haffer, 1987; Prum, 1988;
Prance, 1990; Avila-Pires, 1995; da Silva & Oren, 1996). Another well-supported
BIOGEOGRAPHY O F NEOl'ROPIC:.L\L IL4INFOKESTS
3 93
-r
-T-
Fi<pre 6. Area phenogram from paimise comparison of geographic distances between the localities
considered in the Parsimony Analysis of Endemicity of aiiurans (Fig. 1). Clusters tvere connected with
the average linkage method and Euclidean distances. 'lhc topolocqof this phenogram was significantly
incompatible with the data matrix of the Pi1E (hlann-\\hitney's
7.23, P<O.OOOl).Underlined
localities indicate Amazon Basin, bold-underlined Upper Amazon Basin.
<=
~~
event is the early separation of eastern Amazonia south from the Amazon River
(Beltm) from thc other regions in the Amazon Basin.
The topology of the area cladogram of anurans is not a result of geographic
distance alone. The most significant incongruousness between the area cladogram
and the phenogram of geoq-aphic distances are the placement of (1) Rio Palenque
(Choco Region), (2) La Selva Barro Colorado (Central America), (3)BoracCia, and
(4) BelCm. It should be noted that between those regions and their sister localities
(as defined by the phenogram of geographic distances), there are always geographic
or biotic barriers (e.g. the Andes between the Chocoan Region and the northwestern
Amazonian localities, the xeric habitats between the Atlantic Forest and the rainforests
of the lower Amazon Basin).
The results support somc previous hypotheses for the historical biogeopaphy of
the anurans of lowland Neotropical forests. Some localities form clades that are
coincident with areas of endemism defined by Lynch (1979) (i.e. Upper Amazon
Basin, Guianas). The distinctiveness of Cis- and Trans-Andean amphibian communities outlined by Duellman (1990) also is apparent in the area cladograms.
+
:'II
'eru yz3
Rondonia
2-
$0,
LOC
Hiotic and ahiotic conditions are important forces dctcrmiiiing thc distril)utioii of'
aiiuraii spccics in the Keotropics. Some correlations hetLvecii species richiivss and
rc.I)roducti\.c modes with gcographj- and ccological conditions have h c n rvportcd
I,y1e11. 1979; hell111at1, 1988. 1990; llucllrnan 8r Thonias, 1 Wi). The iiitc,rprctations of those relationships ha\.e postulated that contempoi.ary factors arc
[ l i t . inaiii regulatory fbrce of tlie distrihution of anuran tam.
( hi t l i r x other liarid, during the last dccadc it has becoine incrcasingl!- clear to
c.oiiimuiiit~-ccwlogists that taxonomic co~iipo~icnts
of communitics can onl! l i t .
Figure 8. XIost parsimonious area cladograni jtrcc length = 135, CI = 0.79, RI = 0 . 7 1 ) for Parsirnoiiy
.\naly-sis of Endemicity applied to presencc/abscncr of 107 species and subspccics of lizards at seven
Neotropical regions (defined after Haffer. 197.1, 1985). An ‘cmpty’ locality (no species) was used to
root the area cladogram. Decay indexes are shown in circles. Position of nodes and internodrs on the
map is not informative; branching pattrrn indicates sequence of geographic di\crgcnce among regions.
adequately interpreted in a historical and biogeographic context (Brooks & 3lcLennan, 1991; Ricklefs & Schluter, 1993).Numbers of species within ecological categories
cannot be considered independent measurements if there is a common evolutionary
history. Ecological traits can be shared among members of a monophylctic group
as a result of shared history rather than as a result of independent adaptations to
shared contemporary conditions (Brooks & McLennan, 1991).
E\,olutionary history has only recently been considered to explain patterns of
community structure of Neotropical anurans. Despite previous works that favoured
non-historical interpretations for patterns of anuran species richness (e.g. Duellman,
1988), recent studies have demonstrated that history has been a driving force
determining diversity in the Amazon Region (Zimmerman & Simbcrloff, 1996).
The combined evidence suggests that both history and ecology ha\.e been decisivc
forces determining the distributions of Neotropical anurans. An indication of a
strong historical component in the area cladograms of anurans found in the present
i
ic
stud\ i 4 the fact that they arc similar to those of other taxonomic groups 11.c.l i ~ , i t d ~
, t i i d prtmnte5) characterizcd by ha\,ing different natural histories. Therefore, siniilar it\
15 tinlikel\ to bc <I consequence of d strong ecological (non-historical) siynal.
C:c )injiarisorts among groups of vertebrates are constrained by the unequal dcfingeographic rcgions by different authors and the disparate a\-ailabilit!. of
tlata.
cladograms of anurans, primates, and lizards have missing regions relati\~c
to one another, and thc samples within the regions are not uniform. Tkspitc
thcsc. pro1)lerns, P:lE analysis reveals remarkable congruericies among groups of
\.cmc.ljrates.
rllic PXEs of localities considered separately resultrd in topologies \\-ith cladcs
it ions o f
that matched Haffer’s regions of endemicity (1969, 1974, 1985). \‘$Thenlocalities are
combined according with Haffer’s regions and the PAE performed, the resultant
area cladograms are consistent with the area cladograms of localities considered
separately. By coding separate localities, PAE defines biogeographic units (clades).
These units support biogeographic regions defined in previous studies (Haffer, 1974;
Lynch, 1979).
Strong congruencies exist among the most inclusive clades of the area cladograms
of anurans, lizards, passerine birds (Bates, Hackett & Cracraft, 1998), and primates
(Fig. 10). All of them ha\re, or at least were not conflicting with, the following
features: (1) a basal separation between Cis- and Trans-Andean regions, (2) a Central
t\merican cladc, (3) the Choco Region being the sister area to the Central American
clade, (4) an Upper Amazon Basin cladc (Napo Inambari), (5) a Guianan clade,
(6) an Amazon Basin clade, and (7) the Brazilian Atlantic Forest being the sister
area to the Amazon Basin cladc.
For birds, Prum (1988) presents area cladograms with the Brazilian Atlantic Forest
nested within the lower Amazon Basin regions (Fig. 10). This difference may be a
’
ts
consequence of the dispersal abilities of the taxa analyscd. The xeric en\;ironmen
that separate the Amazon Basin from the Brazilian Atlantic Forest may be less
important geographic barriers for those taxa of birds than they are for forest anurans.
The differences in dispersal abilities, physiological tolerances, and behavioral patterns
among taxonomic groups can generate area cladograms with incongruent topologies
for the same region. All those topologies are the true ‘version’ of biogeographic
history for each group.
All data matrices have significant cladistic structure, and the resultant area
cladopams have high consistency values. The general congruence between PAE
and area cladograms obtained through cladistic biogeography (Fig. 10)is an indication
that distributional patterns are historically structured (Cracraft, 1994).
+
1icnriance ecents uitliin the Amnlon region
It is unclear what barriers were responsible for the vicariance patterns implied
by the area cladograms for the Amazon Basin. Pleistocene events have been
postulated as vicariant factors for thc region (Haffer, 1969, 1974). The Pleistocene
Refuges Hypothesis (PRH)states that during the Pleistoccne, decreases in temperature
and humidity in the Amazon Basin left relatively small ‘islands’ of tropical rainforests
surrounded by xeric habitats (Haffer, 1969, 1974). This process has been regarded
as responsible for the distribution patterns of many groups of animals and plants in
the Neotropics (e.g. Lynch, 1979; Duellman, 1982; Brown, 1987; Prance, 198’7).
A criticism of the PRH is that its evidence comes only from present biotic patterns.
Recent analyses of the distributions of Pleistocene biotas (Webb & Rancy, 1996;
Colinvaux, 1996) contradict the biotic scenario proposed by the PRH. Palynological
data “show unequivocally that the Amazon lowlands were forested in glacial timcs
as they are now” (Colinvaux, 1996).
Brooks & McLennan (1991) suggested that under the PRH, speciation should
have occurred in parapatric or peripheral, isolated allopatric modes. The relationships
generated by these speciation modes should show polytomic topoloLgy(i.e. various
branches emerging consecutively from a single ancestor; Wiley, 1981). This is not
the case for the phylogenies of the groups of birds that Prum (1988) analysed to
tlcriw his biogeographical lq~iothcses. If thc phylogenies are pol>.tomic, arc3
~.l;itlograriisare expected to be polytomic as well. Howc\.er, the area cladogranis
1)ropo~cdfix birds (Prum, 1988; Rates, Hackett & Cracraft, 1998), primates (da
Sill-a & O r m . 1996; this study), anuraiis (this study), and lizards (X\,ila-Pires, 199~5:
this study) sho\v dichotomous topologies (i.e. hierarchical cpisodes in lvhich an
anwstral cntity is partitioned in tkvo). If Brook & hlclennan's (1 99 I ) prcdictions
are correct, the area cladograms resulting from this study do not lend support to
the PRH. An additional expectation under the refuges hypothesis scenario is that
species are predominantly Pleistocene or post-Pleistocene in age. However, the
few data available on species age of Neotropical frogs (using albumin sequence
differentiation on the genera Bufo and LRptodac~lus)suggest that species date from
the Tertiary, with few species appearing in the Pleistocene (Heyer & Maxson, 1982;
Heyer, 1988; H a s , Dunsky & Maxson, 1995).
An alternative hypothesis to account for diversity patterns in the Amazon Basin
is the Riverine Barrier Hypothesis (Wallace, 1852; Hershkovitz, 1972; Ayres, 1986).
According to it, large rivers act as geographic barriers that promote genetic
differentiation and therefore speciation. Support has come from analyses of distribution and genetic differentiation of mammals (Ayres & Clutton-Brock, 1992;
Peres, Patton & da Silva, 1996) and birds (Capparella, 1988, 1992).
In the anuran area cladogram, all localities within each of Haffer's endemicity
regions are monophyletic. Haffer's endemicity regions are delimited by large rivers
and therefore the monophyly of localities within them is consistent with the Riverine
Barrier Hypothesis. However, more localities within each region should be analysed
in order to offer stronger support.
Some biogeographic generalities across taxa have been observed in this studj .
However, because of the scant data available on the distribution of ancient biotas
and past environmental conditions, any hypotheses that try to account for the
specific events responsible for those biogeographic generalities are speculative. Extant
fossil data are still insufficient to give an accurate picture of past conditions in the
Amazon Basin. The purpose of the present study is to give proximal hypotheses of
the biogeography of Neotropical lowland forests. Ultimate questions should be
addressed with the accumulation of data on past environmental conditions and
distributions of fossil biotas.
The Ecuadorian Foundation for Science and Technology (FUNDACYT), under
the sponsorship of the Department of Biological Sciences of Universidad Catolica
del Ecuador, awarded the fellowship that funded the author's research at the
University of Kansas. W.E. Duellman, L. Trueb, E.O. Wiley, C. Raxworthy and
A. Maglia provided numerous valuable comments. Special thanks to H. da Silva
and R. Prum with whom I had interesting discussions about the methodologics used
in this investigation. L. A. Coloma provided important suggestions and assistance
with some taxonomic issues.
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