Mammals and rainfall: paleoecology of the middle Miocene at La Venta (Colombia, South America)
39
Richard F. Kay & Richard H. Madden Department of Biological Anthropology and Anatomy, Duke University Medical Center, Durham, North Carolina 27710, U.S.A. Received 11 September 1995 Revision received 11 June 1996 and accepted 9 October 1996 Keywords: Miocene, Colombia, paleoecology, tropics, rainfall. Mammals and rainfall: paleoecology of the middle Miocene at La Venta (Colombia, South America) A comparison of the species richness and macroniche composition of diet, locomotor and body-size classes among 16 nonvolant mammalian faunas in tropical South America reveals numerous significant positive correlations with rainfall. In particular, significant and strong positive correlations with rainfall are found in 18 attributes, including the number of nonvolant mammal species, number of primate species, number of frugivores, primary consumers, arborealists, and the number of species between 100 g to 10 kg in body weight. Estimates of annual rainfall derived from least-squares and polynomial regressions and principal components analysis yield a modal estimate of between 1500 and 2000 mm annual rainfall for the Monkey Beds assemblage at La Venta. This level of rainfall is associated today with the transition between savanna and forest environments in lowland equatorial South America. Paleontological evidence strongly suggests the presence of forest biotopes at La Venta. Paleontologic and sedimentologic evidence together indicate a dynamic and heterogeneous riparian mosaic associated with the shifting course of meandering rivers. Faunal evidence also suggests that habitat heterogeneity and canopy discontinuity extended into the interfluvial area. Seasonal rainfall was probably only of secondary importance in shaping the structural and spatial configuration of the dominantly forested mosaic habitat at La Venta. The fossil record is not consistent with the presence of extensive primary or undisturbed, continuous-canopy, evergreen tropical rainforest. The reconstructed middle Miocene environment at La Venta differs significantly from modern environments of similar geography on the piedmont east of the Andes at the same latitude. This in turn suggests that the extensive evergreen rainforests of the upper Amazonian piedmont that today receive more than 4000 mm of rainfall may post-date the initiation of Andean uplift. ? 1997 Academic Press Limited Journal of Human Evolution (1997) 32, 161–199 Introduction Through the collaborative efforts of a joint U.S.–Colombian scientific team betwen 1982 and 1992, the Miocene vertebrate fauna from La Venta, Colombia, has been revised and placed within a more refined stratigraphic and geochronologic framework (Kay et al., 1996). For three reasons this paleofauna is especially important for understanding South American faunal evolution. The first is its geographic position. A major impediment to understanding the continent-wide evolution of mammalian faunas is the paucity of good fossil sites within the tropical zone. Even though 70% of the land mass of the continent is situated within the tropics, that is, north of 23) South latitude, La Venta is practically the only place where a Tertiary tropical lowland paleofauna can be studied in geochronologic context. Second, the La Venta fauna holds special significance because of its temporal position. It is well known that the paleofaunas of South America underwent a massive readjustment, called the ‘‘Great Faunal Interchange’’ (Stehli & Webb, 1985), beginning in the late Miocene, when the Isthmus of Panama was formed. The fossil record of this readjustment is best known from southern South America, and our knowledge about the consequences of this biotic interchange on tropical lowland faunas in particular is limited. La Venta is one of the few places in South America where the paleoecology of a lowland tropical forest fauna can be studied from a time prior to the interchange. 0047–2484/97/020161+39 $25.00/0/hu960104 ? 1997 Academic Press Limited
Transcript of Mammals and rainfall: paleoecology of the middle Miocene at La Venta (Colombia, South America)
Richard F. Kay &Richard H. MaddenDepartment of Biological Anthropologyand Anatomy, Duke University MedicalCenter, Durham, North Carolina27710, U.S.A.
Received 11 September 1995Revision received 11 June 1996and accepted 9 October 1996
Keywords:Miocene, Colombia,paleoecology, tropics, rainfall.
Mammals and rainfall: paleoecology ofthe middle Miocene at La Venta(Colombia, South America)
A comparison of the species richness and macroniche composition of diet,locomotor and body-size classes among 16 nonvolant mammalian faunas intropical South America reveals numerous significant positive correlations withrainfall. In particular, significant and strong positive correlations with rainfallare found in 18 attributes, including the number of nonvolant mammalspecies, number of primate species, number of frugivores, primary consumers,arborealists, and the number of species between 100 g to 10 kg in body weight.Estimates of annual rainfall derived from least-squares and polynomialregressions and principal components analysis yield a modal estimate ofbetween 1500 and 2000 mm annual rainfall for the Monkey Beds assemblageat La Venta. This level of rainfall is associated today with the transitionbetween savanna and forest environments in lowland equatorial SouthAmerica. Paleontological evidence strongly suggests the presence of forestbiotopes at La Venta. Paleontologic and sedimentologic evidence togetherindicate a dynamic and heterogeneous riparian mosaic associated with theshifting course of meandering rivers. Faunal evidence also suggests that habitatheterogeneity and canopy discontinuity extended into the interfluvial area.Seasonal rainfall was probably only of secondary importance in shaping thestructural and spatial configuration of the dominantly forested mosaic habitatat La Venta. The fossil record is not consistent with the presence of extensiveprimary or undisturbed, continuous-canopy, evergreen tropical rainforest. Thereconstructed middle Miocene environment at La Venta differs significantlyfrom modern environments of similar geography on the piedmont east of theAndes at the same latitude. This in turn suggests that the extensive evergreenrainforests of the upper Amazonian piedmont that today receive more than4000 mm of rainfall may post-date the initiation of Andean uplift.
? 1997 Academic Press Limited
Journal of Human Evolution (1997) 32, 161–199
Introduction
Through the collaborative efforts of a joint U.S.–Colombian scientific team betwen 1982 and1992, the Miocene vertebrate fauna from La Venta, Colombia, has been revised and placedwithin a more refined stratigraphic and geochronologic framework (Kay et al., 1996). For threereasons this paleofauna is especially important for understanding South American faunalevolution. The first is its geographic position. A major impediment to understanding thecontinent-wide evolution of mammalian faunas is the paucity of good fossil sites within thetropical zone. Even though 70% of the land mass of the continent is situated within the tropics,that is, north of 23) South latitude, La Venta is practically the only place where a Tertiarytropical lowland paleofauna can be studied in geochronologic context.Second, the La Venta fauna holds special significance because of its temporal position. It is
well known that the paleofaunas of South America underwent a massive readjustment, calledthe ‘‘Great Faunal Interchange’’ (Stehli & Webb, 1985), beginning in the late Miocene, whenthe Isthmus of Panama was formed. The fossil record of this readjustment is best known fromsouthern South America, and our knowledge about the consequences of this biotic interchangeon tropical lowland faunas in particular is limited. La Venta is one of the few places in SouthAmerica where the paleoecology of a lowland tropical forest fauna can be studied from a timeprior to the interchange.
0047–2484/97/020161+39 $25.00/0/hu960104 ? 1997 Academic Press Limited
162 . . . .
Third, the La Venta lowland equatorial fauna contains many primates, including theearliest undisputed representatives of tamarins, squirrel monkeys, pitheciines, and aloutattines.As such, it opens a unique window into the early evolution and diversification of these primategroups.In this paper, we attempt to reconstruct the paleoenvironment at La Venta in terms of the
single most important or determinant characteristic of lowland tropical environments, the totalamount of annual rainfall. After establishing the paleolatitude and paleoelevation of the LaVenta area, we estimate annual rainfall based upon the relationship between mammalianmacroniche structure and rainfall guided by a comparison of 16 modern tropical lowlandmammalian faunas.Both floral diversity and the complexity of vegetation in the lowland tropics is strongly
correlated with annual rainfall (Gentry, 1988). In environments where rainfall exceeds2000 mm/year and a dry season lasts fewer than 4 months, evergreen rainforest predominates.In regions with less than 1000 mm of rainfall and dry intervals longer than 6 months, thedominant vegetation is drought-resistant and deciduous. Areas of intermediate rainfallbetween 1000–2000 mm/year with 4–6 months of dry season tend to exhibit semideciduousforests, often as riparian galleries of variable width with intervening savannas. Given thegenerally close correspondence between mean annual rainfall and the length of the dry season,in the analyses that follow, mean annual rainfall is used as a surrogate for dry-season length.We prefer total annual rainfall to dry season length because environmentally significant waterdeficit is difficult to define and not generally available from meteorological data. Notsurprisingly, comparisons reveal that species richness (total number of species) and nichestructure of modern mammalian faunas in lowland tropical environments vary in predictableways with rainfall.It is the purpose of this paper to present our general findings about the relationship between
mean annual rainfall and mammalian niche structure in modern Neotropical environments, inparticular total nonvolant species number, the number of primate species, and the numbers offrugivorous and arboreal species.Species-sampling problems are universally recognized to constitute a significant impediment
to reconstructing the habitat of ancient mammalian communities. In particular, it has beenshown that the number of species recorded at any fossil locality is sensitive to the number ofspecimens recovered (Stuckey, 1990). Because trends relating the absolute number of speciesin a fossil assemblage to rainfall may be sensitive to paleontological sampling biases, only in theMonkey Beds (see below) do we feel that paleontological sampling begins to approximate totaldiscoverable species diversity (Madden et al., 1996).Our attempt to reconstruct the middle Miocene environment at La Venta is predicated on
our knowledge of the autecology of the nonvolant mammals from the Monkey Beds, includingestimates of their body size, and dietary and locomotor adaptations. By means of a comparisonof the macroniche structure of the Monkey Beds assemblage with general trends in thestructure of modern mammalian faunas along a rainfall gradient, we derive an estimate of theannual rainfall at La Venta. Our estimate of total annual rainfall is examined in light of theavailable evidence about the autecology of environmentally sensitive vertebrate and mammalgroups. This estimate of the annual rainfall is then discussed in terms of the generalrelationship between vegetation and rainfall in the equatorial lowlands of South America. Lastwe discuss and speculate about the nature of the vegetational mosaic at La Venta based on theavailable evidence for the presence of forest, riparian mosaic, the degree of canopy closure,and rainfall seasonality.
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Paleogeography
The fossil vertebrate assemblage from La Venta comes from rocks of the Honda Groupexposed within a fault-bounded block in the central Magdalena river valley, at 3) Northlatitude, at a present elevation less than 500 m above mean sea level and a mean annualrainfall of about 1000 mm. The fluvial conglomerates, sandstones, silts and clays of the HondaGroup attain a total thickness of approximately 1150 m (Guerrero, 1996). The geologic age ofthe fossiliferous Honda Group is constrained by radiometric and paleomagnetic evidence to a1·7 Ma interval beginning about 13·5 Ma and ending at about 11·8 Ma (Flynn et al., 1996;Guerrero, 1996; Madden et al., 1996).Approximately 142 species of vertebrates have been described from the Honda Group at La
Venta (Kay & Madden, 1996). Of the 72 species of mammals now known from the HondaGroup, 52 nonvolant mammal species occur in the richly fossiliferous Monkey Beds. TheMonkey Beds measure about 14·8 m in thickness (Guerrero, 1996) and fall within the normalpolarity interval N2 of the Honda Group magnetostratigraphic section, corresponding toChron C5AA of the GMPTS (Flynn et al., 1996). The normal polarity interval of Chron C5AAspans 150,000 years (between 13·00–12·85 Ma), and in the Honda Group, the normal polarityinterval of Chron C5AA is represented by 160 m of sediment, of which the Monkey Bedsrepresent less than 10%. Therefore, the Monkey Beds fauna could sample a time interval of15,000 years or less.In the middle Miocene, the La Venta region was situated within five degrees of the
geographic equator in the equatorial tropics. At that time, northern Ecuador, central andwestern Colombia, and western Venezuela formed a peninsula bordered on the west by thePacific Ocean and on the north and east by the developing Caribbean Sea and the extensiveepicontinental brackish environments of the upper Amazon basin (Whitmore & Stewart, 1965;Duque-Caro, 1979, 1980, 1990; Nutall, 1990; Hoorn, 1994; Hoorn et al., 1995; Räsänen et al.,1995).While there is no evidence from the fossil vertebrates or invertebrates to suggest direct
marine influences at La Venta (Lundberg, 1996; Domning, 1996; Rodríguez, 1996), we inferthat the La Venta area was at low elevation. Among the freshwater fish are many very largespecies and species that today inhabit slow-moving, lowland meandering rivers (Lundberget al., 1986). Further, among the large turtles, Podocnemis occurs today only at elevations below100 m (Pritchard & Trebbau, 1984; Lynch, 1979). The teid lizard Paradracaena from La Ventais morphologically intermediate between two extant taxa, Dracaena and Crocodilurus, that occurtoday only in rainforests or along forest edges at elevations below 90 m (Rivero-Blanco &Dixon, 1979; Hoogmoed, 1979). Likewise, limbless amphibians of the family Typhlonectidae(Hecht & LaDuke, 1996) occur today only at lowland elevations near sea level. Crocodilians,of which there are many large individuals, diverse morphologies, and high species richness atLa Venta, only rarely are found at elevations above 500 m in South America today (Medem,1981, 1983).The La Venta area today is situated in the valley of the Magdalena River, between the
Central and Eastern Cordilleras of the Colombian Andes. The area is very dry today becauseof a mountain induced rain-shadow effect. In the middle Miocene, the geography was moredirectly comparable with that of the eastern piedmont of Colombia because there was nosignificant elevation to the Eastern Cordillera (Hoorn et al., 1995; Guerrero, 1996) andMiocene sediments were deposited continuously across a lowland area east of the CentralCordillera (Campbell & Bürgl, 1965; Lundberg et al., 1986). The best estimate of the date of
164 . . . .
the initial uplift of the Eastern Cordillera is post-middle Miocene (Campbell & Bürgl, 1965;Guerrero, 1996; Hoorn et al., 1995) and only following important episodes of uplift during thePliocene, did the Colombian Eastern Cordillera attain its present elevation (Hooghiemstra &Ran, 1994; Hammen & Cleff, 1986; Wiel, 1991). Post-middle Miocene episodes of mountainbuilding made the climate at La Venta today very different from that of the middle Miocene.
Data and methods
The overall structure of the nonvolant mammalian fauna from the Monkey Beds at La Ventais compared with that of 16 modern mammalian faunas from the South American tropics(Figure 1, Table 1, Appendix). For these 16 modern faunas, taxonomic allocations followWilson & Reeder (1993). The sampling areas of these faunas represent a wide range of meanannual rainfall. At one extreme, in the eastern lowlands of Ecuador, rainfall is approximately3500 mm/year with no appreciable dry season (Canadas, 1983). At the other extreme, in theCaatinga region of northeastern Brazil, annual rainfall is as low as 500 mm and the dry seasonexceeds 7 months (Streilein, 1982a). Our sample does not include faunas living in areasreceiving in excess of 4000 mm, nor less than 500 mm annual rainfall.
10
Equator
Tropic ofCapricorn
14
15
1213 11
9
76
5432 1
16
8
Figure 1. Map of South America showing the distribution of the 16 modern lowland mammalian localities.Outlined areas greater than 1000 m above sea level. Numbers correspond to the localities listed in Table 1.
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Table1Characteristicsofthe16
modernlowlandmam
malianfaunas
oftropicalSouthAmerica
Locality
(fauna)
State(province),
country
Latitude
Longitude
Altitude
(m)
Annual
rainfall
(mm)
Vegetation;
(estimatedlengthof
dryseason
inmonths)
References
(1)G
uatopo
Miranda,Venezuela
10)N
66)W
250–1430
1500
Semideciduous,submontanetomontane
forest(6months)
Eisenbergetal.,1979
(2)M
asaguaral
Guarico,Venezuela
8)34
*N67
)35*W
751250
Subtropicalvegetationalm
osaichigh
savanna(6months)
Eisenbergetal.,1979
(3)PuertoPáez
Apure,Venezuela
6)23
*N67
)29*W
761500
Seasonallyfloodedhighgrasssavanna
with
scatteredpatchesoflowforestand
palms(6months)
Handley,1976
(4)PuertoAyacucho
Amazonas,Venezuela
5)15
*N67
)40*W
99–195
2250
SavannasoftheRioOrinocoand
evergreenforest/savannamosaic
Handley,1976
(5)Esmeralda
Amazonas,Venezuela
3)05
*N65
)35*W
130–1830
2000
Nearlycontinuousevergreenforestin
valleyup
tolowdensemontaneforest
Handley,1976
(6)M
anaus
Amazonas,Brazil
2)30
*S60
)W10
2200
Primaryupland
terrafirmeforest;(3
months)
Malcolm,1990
(7)Belém
Pará,Brazil
1)27
*S48
)29*W
102600
VicinityofBelém,nowurbanand
suburban(2months)
Pine,1973
(8)Caatingas
Exu,Pernambuco,Brazil
7)31
*S40
)00*W
200
<500
Semiaridcaatinga(>7months)
Maresetal.,1981;
Streilein,1982;Mares
etal.,1985
(9)FederalDistrict
Brasilia,Brazil
15)57*S
47)54*W
1100
1586
Seasonalxerophylloussavanna
grasslandsandgalleryforests(5months)
Maresetal.,1989
(10)Acurizal
MatoGrosso,Brazil
17)45*S
57)37*W
100–900
1120
Pantanal;pastures,secondaryforest,
cerradoanddeciduousforests(7months)
Schaller,1983
(11)Chaco
Salta,Argentina
22)24*S
63)W
200–500
700
Subtropical,drought-resistant,thorn
forest(9months)
Ojeda&Mares,1989;
Maresetal.,1989
(12)TransitionalForest
Salta,Argentina
22–24)S
64)W
350–500
700–900
Transitionaldeciduousforestwith
trees
20to30mtall
Ojeda&Mares,1989;
Maresetal.,1989
(13)Low
Montane
Salta,Argentina
22–24)S
64)W
500–1500
800
Lowermontanemoistforest(2months)
Ojeda&Mares,1989;
Maresetal.,1989
(14)CochaCashu
MadredeDios,Peru
12)S
70)W
400
2000
Lowland
floodplainrainforest(3months)
Janson
&Emmons,
1990
(15)RioCenepa
(Alto
Maranon)
Amazonas,Peru
4)47
*S78
)17*W
210
2880
Abandonedfields,secondaryregrowth
riparianforest,undisturbedhumidforest
Patton
etal.,1982
(16)EcuadorTropical
Oriente,Ecuador
1)N–5
)S75–78)W
0–800/1000
1795–4795Amazonianlowland
evergreen
rainforests
Albuja,1991
Numberscorrespond
tothelocalitymap( Figure1).
166 . . . .
The physical attributes and adaptations of each mammal species are assigned to body mass,locomotor, and diet categories. For body mass we recognize six categories; (I) 10–100 g, (II)100 g to 1 kg, (III) 1–10 kg, (IV) 10–100 kg, (V) 100–500 kg, and (VI) >500 kg. For locomotormode we generally follow Fleming (1973) and Andrews et al. (1979) and recognize sixcategories; (1) large terrestrial (>1 kg body mass), (2) small terrestrial (<1 kg body mass), (3)arboreal, (4) arboreal and terrestrial (or scansorial), (5) aquatic (including semi-aquatic) and (6)fossorial (including semi-fossorial). Our analyses include combinations of these locomotorcategories; for example, ‘‘terrestrial’’ (combining large and small terrestrial) and ‘‘totalarboreal’’ (combining arboreal and scansorial). We are not confident that it is possible tosubdivide dietary categories as finely for extinct species as can be done for living ones (e.g.,Eisenberg, 1981, 1989; Robinson & Redford, 1986, 1989). Accordingly, we employ eight dietcategories; (1) vertebrate prey, (2) ants and termites, (3) insects with some fruit, (4) fruit withsome animals, (5) small seeds of grasses and other plants, (6) fruit with leaves, (7) leaves(browse), and (8) stems and leaves of grasses (graze). Our analysis also uses some combinationsof these dietary categories; for example ‘‘herbivores’’ (combines categories 6, 7 and 8) and‘‘frugivores’’ (combines categories 4, 5 and 6). The latter combination of seed-eaters withfruit-eaters is mainly forced by the quality of the data with which we are working: the diets ofsmall rodents are for the most part so poorly known that the two categories cannot be readilydiscriminated from the literature.We also consider whether the proportions of species in various guilds vary with rainfall. Four
indices were devised to express the number of species within a guild (that is, with a particularniche specialization or within a body size range) relative to total number of species. (1) TheFrugivore Index expresses the proportion of frugivorous species to the total number ofplant-eating species in a fauna:
100# (FI+FL+S)/(FI+FL+S+L+G)
where FI=fruit with invertebrates, S=small seeds of grasses and other plants, FL=fruit withleaves, L=leaves (browse), and G=grass stems and leaves (graze). (2) A Browsing Indexexpresses the proportion of browsing or leaf-eating species to the total number of herbivorousplant-eating species in a fauna:
100# (L)/(L+G).
(3) An Arboreality Index is used to express the proportion of arboreal species to the totalnumber of nonvolant species:
100# (A+AT)/(A+AT+SAq+T)
where A=arboreal, AT=arboreal and terrestrial (scansorial), T=terrestrial and/or fossorial,and SAq=semiaquatic. (4) The Size Index expresses the proportion of species in size classes IIand III relative to those in class IV:
100# (Class II+Class III)/Class IV
where the size classes are II=100–1000 g; III=1–10 kg; IV=10–500 kg. Table 2 presents thenumber of species in each diet, locomotor, and body size class and the values of the fourindices for the 16 modern faunas.
167
Table2(a)
Thenumber
ofspeciesineach
macronichecategory
andindex
values
forthe16
lowlandtropicalfaunas
usedintheanalyses
Locality
Rainfall
(mm)
#Species
#Primates
#Frugivores
#Browsers
#Grazers
#1)
Consumers
#2)
Consumers
Frugivore
index
Browser
index
EcuadorTropical
3000
8113
415
349
3483·7
62·5
RioCenepa
2880
626
314
237
2583·8
66·7
Belém
2600
625
285
235
2880·0
71·4
PuertoAyacucho
2250
455
263
231
1483·9
60·0
Manaus
2200
516
294
033
1787·9
100
CochaCashu
2000
7013
425
249
2185·7
71·4
Esmeralda
2000
6611
423
146
1991·3
75·0
FederalDistrict
1586
663
274
536
2675·0
44·4
Guatopo
1500
403
102
315
866·7
40·0
PuertoPáez
1500
222
183
122
1881·8
75·0
Masaguaral
1250
292
122
317
1270·6
40·0
Acurizal
1120
415
202
325
1780·0
40·0
Low
MontaneForest
800
262
84
214
1257·1
66·7
TransitionalForest
800
441
125
219
2663·2
71·4
Chaco
700
360
63
716
2037·5
30·0
Caatinga
500
222
60
28
1275·0
0·0
MonkeyBeds,LaVenta
—52
619
166
4111
46·3
72·7
168 . . . .
Table2(b)
Locality
#Arboreal
sp.
#Scansorial
sp.
#Terrestrial
sp.
Arboreality
Index
#Size
classI
#Size
classII
#Size
classIII
#Size
classIV
#Size
classV
#Size
classVI
Size
index
EcuadorTropical
2918
2858
1527
2810
20
33RioCenepa
1817
2356
1115
258
30
24Belém
1616
2452
1017
259
20
27PuertoAyacucho
169
1856
713
168
10
29Manaus
2010
2059
1012
207
20
24CochaCashu
2717
2263
1024
2311
20
34Esmeralda
2914
1965
1717
246
20
26FederalDistrict
916
3438
2514
1710
10
21Guatopo
1110
1852
126
155
20
15PuertoPáez
55
945
63
95
00
13Masaguaral
67
1545
63
146
00
10Acurizal
512
2341
76
1510
30
15Low
MontaneForest
48
946
84
103
10
15TransitionalForest
512
2339
115
235
10
11Chaco
18
2225
67
147
20
19Caatinga
28
1245
44
121
10
18MonkeyBeds,LaVenta
148
2742
65
1814
30
11
169
To avoid problems posed by the nonlinearity of the data, comparisons were made amongthe modern faunas using the nonparametric Spearman’s rank correlation (Spearman’s rho).Rank correlations were computed between rainfall and the numbers of species within eachparticular dietary, locomotor or body mass category. In these analyses, our criterion foracceptance of a null hypothesis was set at probability values less than or equal to 0.05. Theresults are presented in Table 3 and depicted as a series of bar charts with faunas arrangedalong the ordinate in order of decreasing annual rainfall (Figures 2–7).The nonvolant mammal species from the Monkey Beds at La Venta were assigned to diet,
locomotor and body size classes based on the results of studies in Kay et al. (1996) (Table 4).The body mass of each mammal species from the Monkey Beds is estimated from lineardimensions of the teeth and bones using least-squares regression models derived fromhomologous measures in their living relatives. Body masses for marsupials, rodents andprimates were estimated from published equations for lower first molar crown area vs. bodyweight (Legendre, 1989; Conroy, 1987). Body mass estimates for armadillos and glyptodontsuse regressions of carapace or cranial length vs. body weight from published measurements forliving armadillos (Wetzel, 1985). Body mass estimates for sloths and anteaters are based on a
Spearman’s rank correlations (Spearman’s rho) between totalannual rainfall and the numbers and percentages of extant specieswithin various macroniche categories
Rainfall versus: Spearman’s rho P-value
# Species 0·758 0·0033# Primate species 0·815 0·0016
Diet:# Frugivores 0·837 0·0012# Browsers 0·507 0·0494# Grazers "0·240 0·3530# 1) Consumers 0·723 0·0051# 2) Consumers 0·483 0·0612Frugivore index 0·723 0·0051Browser index 0·477 0·0645
Locomotion:# Arboreal species 0·880 0·0007# Scansorial species 0·662 0·0104# Terrestrial species 0·446 0·0842Arboreality index 0·702 0·0065
Body size:# Species, size class I 0·532 0·0292# Species, size class II 0·757 0·0034# Species, size class III 0·762 0·0032# Species, size class IV 0·601 0·0199# Species, size class V 0·381 0·1396Size index for all species 0·722 0·0052
# Arboreal species vs.# Species, size class I 0·651 0·0117# Species, size class II 0·790 0·0022# Species, size class III 0·795 0·0021# Species, size class IV 0·532 0·0395# Species, size class V 0·413 0·1098
Table 3
170 . . . .
regression of distal femur bicondylar width vs. body weight for living sloths and anteaters. Bodymasses for litopterns, notoungulates and astrapotheres were estimated using dental dimensions(Litopterna) and mean estimates from diverse skeletal, cranial and dental dimensions(Notoungulata and Astrapotheria; Cifelli & Villarroel, 1996; Cifelli & Guerrero, 1996; Johnson& Madden, 1996; Madden, 1996). Using these estimates, individual species were assigned tobody weight classes.The assignment of extinct species to locomotor and dietary classes is made by analogy with
living species with similar morphology and known locomotor and diet habits. For fossilmammals with close living relatives (some marsupials, rodents, armadillos and primates), wemake dietary and locomotor assignments with more confidence than for fossil mammals withno, or only distantly related, living relatives (sloths, glyptodonts). For fossil herbivorousmammals with no living relatives (litopterns, notoungulates, astrapotheres), the hypsodontyindex of Janis (1988) was used to assign species with rooted cheek teeth to frugivore–herbivore
Hypothesized macroniche specializations for nonvolant mammalspecies present in the Monkey Beds (Honda Group) La Venta area
Species Diet SubstrateBodyweight
MarsupialsPachybiotherium minor IF AT IMicoureus laventicus IF A IThylamys colombianus IF A IThylamys minutus IF A IHondadelphys fieldsi IF T IIIArctodictis sp. Ve T IVLycopsis longirostrus Ve T IV
PrimatesNeosaimiri fieldsi FI A IICebupithecia sarmientoi FL A IIINuciraptor rubrens FL A IIIMohanamico hershkovitzi FL A IICallitrichidae sp. a FI A IIStirtonia tatacoensis L A III
RodentsEchimyidae Gen et. sp. indet a S AT II? Echimyidae incertae sedis S AT IAcarechimys cf. minutissimus S AT I‘‘Olenopsis’’ sp. large FL T IV‘‘Scleromys’’ colombianus FL T III‘‘Scleromys’’ schurmanni FL T IIIMicroscleromys paradoxalis S T IIDinomyidae inc. sedis (cf. Simplimus) sp. FL A(T) IV‘‘Neoreomys’’ huilensis S T IIIMicrosteiromys jacobsi FL A IISteiromys sp. large FL A IIISteiromys sp. small FL A IIIProdolichotis pridiana G T IIIDolichotinae Gen. et. sp. a (large) G T IIIDolichotinae Gen. et. sp. a (small) G T III
Continued on next page
Table 4
171
or folivore (browsing) classes. Fossil herbivores with ever-growing cheek teeth were assigned tothe grazing category.Significantly correlated aspects of mammalian macroniche structure and rainfall for the 16
modern localities are used to derive estimates of the annual rainfall for the middle MioceneMonkey Beds. These estimates are made using simple least-squares regression and second-order polynomial regression. The results presented in Table 5 and Figure 9 are discussedbelow. To examine the relative contributions of different aspects of macroniche structure tothe prediction of annual rainfall, principal components analysis was undertaken using speciescounts and untransformed indices (Frugivore, Browsing, Arboreality, and Size) (Table 6,Figure 10). For all statistical analyses we use Statview 4.1 for the MacIntosh (Abacus Concepts,1992).
Continued from previous page
Species Diet SubstrateBodyweight
LitopternaProlicaphrium sanalfonsensis L T IVProthoatherium colombianus FL T IIIMegadolodus molariformis FL T VTheosodon sp. L T V
NotoungulataMiocochilius anomopodus G T IIIHuilatherium pluriplicatum L SAq VIPericotoxodon platignathus G T VI
AstrapotheriaXenastrapotherium kraglievichi L SAq VIGranastrapotherium snorki L SAq VI
XenarthraNeotamandua borealis Myr AT IVcf. Hapalops L AT IVNeonematherium flabellatum L A IVNothrotheriinae (small) a L AT IVGlossotheriopsis pascuali L A IIIMegalonychidae gen et sp. indet., small L T IVMegatheriinae gen et sp. indet. L T —Anadasypus hondanus IF T IIIPseudoprepotherium confusum L T VPedrolypeutes praecursor Myr T IIIScirrotherium hondaensis L T IVAsterostemma gigantea L T IVAsterostemma ?acostae L T IVNeoglyptatelus originalis G T IVNanoastegotherium prostatum Myr T III
Symbols: dietary categories: FI=fruit with some invertebrates, S=smallseeds of grasses and other plants, FL=fruit with some leaves, L=leaves(browse), and G=grass stems and leaves (graze), IF=primary insects with somefruit, Ve=primarily vertebrate prey, Myr=ants and termites. Locomotor orsubstrate preference: A=arboreal, AT=arboreal and terrestrial (scansorial),T=terrestrial and fossorial, and SAq=semiaquatic. Body size classes: I=lessthan 100 g; II=100–1000 g; III=1000 g to 10 kg; IV=10–100 kg; V=100–500 kg; VI=>500 kg.
Table 4
172 . . . .
Results
Modern South American mammalian faunas
Thirteen statistically significant rank correlations are found between mean annual rainfall andthe absolute numbers and percentages of mammal species occupying various dietary,substrate, and body size classes (Table 3).
Total species richness. There is a strong positive correlation (rho=0·758, P>0·0033) between thenumber of mammalian species (species richness) and rainfall (Figure 2). At the extremes of therainfall range of our sample of modern faunas, there are 82 nonvolant mammalian species inthe Ecuadorian Oriente, whereas there are just 22 species in the Caatinga of northeasternBrazil. The high correlation of species richness with rainfall appears to be the result of severalcontributing factors. First, there are far greater numbers of arboreal and scansorial species inwet environments than in dry environments (Figure 3, top). This is confirmed by the significantpositive correlation of our arboreality index with rainfall (rho=0·702, P>0·0065).
90
0High
Locality grouped by rainfall
Tota
l spe
ccie
s
Very lowMedium Low
50
80
70
60
40
30
20
10
Spearman's rho = 0.759P–value < 0.003
Figure 2. Histogram of the total number of nonvolant mammalian species in 16 localities from the tropicallowlands of South America ranked by total annual rainfall. The arrangement of the localities from left toright is in the order of decreasing rainfall, as follows: Ecuador Tropical, Rio Cenepa, Belém, PuertoAyacucho, Manaus, Cocha Cashu, Federal District, Esmeralda, Puerto Páez, Guatopo, Masaguaral,Acurizal, Salta Low Montane, Salta Transitional, Salta Chaco, Caatingas. For visual clarity only, but not forthe purposes of statistical analysis, localities are grouped by total annual rainfall: High, greater than2500 mm/year; medium, 2000–2500 mm/year; low, 1000–2000 mm/year; very low, less than 1000 mm.
173
0High
Localities grouped by rainfall
Oth
er
Very lowMedium Low
5
Spearman's rho = 0.315P = N.S.
5
0
Spearman's rho = 0.446P = N.S.
0
10
15
20
30
35
25
Terr
estr
ial s
peci
es
5
0
Spearman's rho = 0.662P = 0.01
0
10
15
20
Sca
nso
rial
spe
cies
5
0
Spearman's rho = 0.880P = 0.0007
0
10
15
30A
rbor
eal s
peci
es
20
25
Figure 3. The number of arboreal, scansorial, terrestrial and other (semiaquatic, fossorial) mammalianspecies in 16 localities from the tropical lowlands of South America ranked by total annual rainfall. Forfurther information, see Figure 2.
174 . . . .
Substrate preference. By contrast, there is no significant correlation in the number of terrestrialspecies (nor in the number of either fossorial or semiaquatic species) with rainfall. Wetenvironments supporting evergreen forests (for example, at Rio Cenepa and Esmeralda, seeTable 1) always have more arboreal species than dryer environments with either semi-deciduous gallery forest (Federal District) or thorn forest (Caatinga). The number of arborealspecies ranges from between 20–32 in tropical evergreen forests whereas in tropical savannamosaics and thorn forests there are one to six arboreal species (see Table 2).
Primate species richness. There is an especially high and significant positive correlationbetween the number of arboreal primate species and rainfall (rho=0·815, P<0·0016), asnoted by others (Fleagle et al., 1996; Reed & Fleagle, 1995). In high- and medium-rainfallareas (>1800 mm annual rainfall), five to 13 primate species are present whereas in low andvery low rainfall areas (<1800 mm annual rainfall), there are between none and five species(Figure 4).
Preferred diet. A second factor contributing to the greater number of mammalian species in highrainfall habitats relates to the greater number of frugivorous species (rho=0·837, P<0·0012)(see Figure 5). A similar and significant positive trend with rainfall extends to primaryconsumers in general (rho=0·723, P<0·0051) [Figure 6(a)]. Among primary consumers thereis a significant positive correlation between the number of browsing species and rainfall(rho=0·507, P<0·0494). The only primary-consumer diet class that has a negative correlationwith rainfall is the number of grazing species. The weak tendency (an insignificantrho="0·24) for there to be more species of grazing mammals in drier environments in theinter-tropical lowlands of South America probably relates to the fact that savanna grasses aremore plentiful in these environments.Intriguingly, no significant trend between species richness and rainfall character-
izes secondary consumers. There appear to be as many carnivorous and insectivorousspecies in dry environments as there are in wet environments (rho=0·483, P<0·0612)[Figure 6(b)].
0High
Localities ranked by rainfall
Nu
mbe
r of
pri
mat
es
Very lowMedium Low
14Spearman's rho = 0.815
P = 0.002
2
4
6
8
10
12
0
Figure 4. The number of primate species in 16 localities from the tropical lowlands of South America rankedby total annual rainfall. For further information, see Figure 2.
175
Body size. Several significant correlations are found in the pattern of body size distributionamong mammalian species in relation to rainfall (Table 3). First, there is a significant positivecorrelation between rainfall and the number of very small- to medium-sized species (body sizeclasses I–IV, between 10 g to 100 kg) but no significant correlation with the number of largespecies (body size class V, >100 kg). A closer look reveals that there is a significant correlationbetween rainfall and the number of arboreal species within the very small to medium-sizedclass range. Arboreal species comprise the largest component of these size classes, especially forclasses II and III (between 100 g and 10 kg) (see Figure 7).
Indices. Three (Frugivore, Arboreality, Size) of the four indices we investigated are significantlypositively correlated with rainfall. Frugivorous species account for a larger proportion of thetotal number of nonvolant species in wetter environments. The Frugivore Index, expressingthe proportion of frugivorous species to the total number of plant-eating species or pri-mary consumers, is significantly positively correlated with rainfall (rho=0·723, P<0·0051)[Figure 8(a)]. As previously mentioned, the Arboreality Index expressing the proportion ofarboreal species is also significantly positively correlated with rainfall (rho=0·795, P<0·0021)[Figure 8(b)].The Size Index, expressing the proportion of species in size classes II and III relative to
those in class IV, is significantly correlated with rainfall (rho=0·722, P>0·0052) [Figure 8(d)].As noted above, the largest number of arboreal species are found in size classes II and III,whereas fewer arboreal species are found in size classes IV.
0High
Localities ranked by rainfall
Tota
l fru
it e
ater
s
Very lowMedium Low
45
5
10
15
20
25
30
35
40
Figure 5. The number of fruit-eating species in 16 localities from the tropical lowlands of South Americaranked by total annual rainfall. For further information, see Figure 2.
176 . . . .
Finally, only a weak and statistically insignificant relationship occurs between rainfall andthe proportion of browsing species (the Browsing Index) among herbivorous mammals(browsers and grazers) in the lowlands of tropical South America (rho=0·477, P>0·0645)[Figure 8(c)].
0
30
0High
Localities ranked by rainfall
Tota
l sec
onda
ry c
onsu
mer
s
Very lowMedium Low
35
5
10
15
20
25
30
Spearman's rho = 0.483;P = N.S.
0High
Localities ranked by rainfall
Tota
l pri
mar
y co
nsu
mer
s
Very lowMedium Low
50
10
20
40
Spearman's rho = 0.820;P < 0.002
5
15
25
35
45
(a)
(b)
Figure 6. The number of (a) primary consumers (species that eat plant material) and (b) secondary consumers(insectivores, carnivores) in 16 localities from the tropical lowlands of South America ranked by total annualrainfall. For further information, see Figure 2.
177
To examine the collective effects of the species counts and four indices, a principalcomponents analysis was undertaken. Two factors account for nearly 86% of the totalvariance, with the first explaining 66% of the variance (Table 5). Factor loadings on the firstprincipal components are all positive with the greatest influence attributed to the ArborealityIndex and the Frugivore Index. The value of the factor scores on the first principal componentshow a strong correlation with rainfall (r=0·81). Examination of the rainfall levels (Figure 9)shows that most of the discrimination occurs between localities with rainfall levels above1800 mm and areas with less than 1800 mm of rainfall. No separation was obtained betweenenvironments with medium (1800–2500 mm) and high rainfall (2500–3500 mm).
HighLocalities ranked by rainfall category
Very lowMedium Low0
Siz
e cl
ass
III
14
2
10
4
6
8
12
0
Siz
e cl
ass
II
14
2
10
4
6
8
12
0
Siz
e cl
ass
I
2
10
4
6
8N
um
ber
of a
rbor
eal s
peci
es
Figure 7. The number of arboreal species of different size classes in 16 localities from the tropical lowlandsof South America ranked by total annual rainfall. For further information, see Figure 2.
178 . . . .
The Monkey Beds mammalian community
Simple least-squares regression and second-order polynomial regressions of rainfall on speciesrichness, diet, locomotor and body size classes are used to derive rainfall estimates for the timeof deposition of the Monkey Beds (Table 6). For simple least-squares regression, these estimatesrange from as low as 553 mm to as high as 5440 mm. For polynomial regression the estimatesrange from as low as 650 mm to as high as 2333 mm. Frequency histograms of the rainfallestimates derived from both simple least squares and polynomial regressions reveal similarmodal estimates of annual rainfall. The modal estimates are between 1500 and 2000 mm, withmean estimates for both methods of 1789 mm and 1563 mm, respectively (Figure 9).The Frugivore and Size Indices produce the lowest rainfall estimates using both least
squares and polynomial regression. The low estimates given by the Frugivore Index mayreflect the extraordinary high number of browsing species in the Monkey Beds assemblage (seebelow). The low estimates given by the Size Index reflect the lower number of very smallmammal species than one would expect based on modern faunas, conceivably a problem ofsampling bias or the pre-Interchange age of the La Venta fauna (i.e., before the arrival ofmuroid rodents).Rainfall estimates below mean are also produced by the Arboreality Index, the number of
species in size classes II and III and the number of scansorial species, attributes that are highlypositively correlated with rainfall today. Comparisons with modern faunas suggest that smallscansorial species may be under-represented in the Monkey Beds assemblage. This isconfirmed in part by their low abundance as fossils (Madden et al., 1996).In overall species richness (52 species), the Monkey Beds assemblage compares favorably
with mammalian communities in areas of the modern Neotropics receiving more than1500 mm annual rainfall. The Monkey Beds fauna has 40% or more species than Masaguaral
Localities ranked by rainfall0
Bro
wse
r in
dex 100
60
20
40
80
0
(c)
0
Siz
e in
dex
35
20
30
(d)
5
10
25
15
0
Fru
givo
re in
dex
100
60
20
40
80
(a)
0
Arb
orea
lity
inde
x
70
20
30
(b)
10
90
10
30
50
7060
50
40
Figure 8. Distribution of index values in 16 localities from tropical South America ranked by total annualrainfall. (a) Frugivore Index; (b) Arboreality Index; (c) Browsing Index; (d) Size Index. For furtherinformation, see Figure 2.
179
(29 species, 1250 mm annual rainfall) and Chaco (36 species, 700 mm annual rainfall)(Table 2). A least-squares regression of the number of nonvolant mammalian species on meanannual rainfall predicts 1810 mm of rainfall for the Monkey Beds assemblage. Based on thenumber of species of primates in the 16 modern faunas, the rainfall estimate is 1811 mm(Table 6).The strong positive correlation between the number of primary consumers and rainfall
makes this variable a good predictor of rainfall. The Monkey Beds fauna is characterized bya relatively high number of mammalian primary consumers. By this measure, the MonkeyBeds environment had an annual rainfall of about 2291 or 2333 mm.Based upon the percentage of arboreal species in the Monkey Beds assemblage, least-
squares regression predicts an annual rainfall of 1756 mm, a value that is similar to thepredicted annual rainfall of 1811 mm based upon the presence of six primate species.A noteworthy feature of the Monkey Beds assemblage is the extraordinarily high number of
browsing species (16 species) compared with modern faunas (none to five species). Seventy-onepercent of the nonfrugivorous herbivores in the Monkey Beds assemblage are browsers (Table2), a fact that explains the high and disparate rainfall estimates obtained by extrapolation.A more directly comparable estimator is the Browsing Index that yields estimated rainfalllevels for the Monkey Beds of 1961 and 1968 mm.
Eigenvalues and factor loadings from principal components analy-sis of 16 modern South American faunas
Eigenvalues Magnitude Variance Prop.
Value 1 9·58 0·68Value 2 1·79 0·13Value 3 1·08 0·08Value 4 0·54 0·04Value 5 0·46 0·03Value 6 0·23 0·02Value 7 0·14 0·01
Table 5(a)
Factor 1 Factor 2 Factor 3
Number of Primates 0·905 "0·267 "0·149Arboreality index 0·730 "0·626 0·179Total fruit eaters 0·971 "0·133 "0·016Browser 0·666 0·548 0·447Total primary consumers 0·980 0·010 "0·042Total secondary consumers 0·658 0·639 "0·030Size class 2 0·956 0·074 "0·219Size class 3 0·855 0·216 "0·002Size class 4 0·713 0·355 "0·227Frugivore Index 0·670 "0·554 0·083Browser/Grazer Index 0·588 0·009 0·788Size Index 0·857 "0·071 "0·265Total species 0·935 0·212 "0·160Arboreal 0·942 "0·262 0·013
Table 5(b)
180 . . . .
Table6
Estimated
annualrainfallatthetimeofdepositionoftheMonkey
Bedsbased
onasimpleleast-squares
regression
andsecond-order
polynom
ialregressionson
theabsolutenumbersofnonvolantmam
malsinvariousmacroniches
andindices
asdefined
inthetext
Rainfall(dependent
variable)versus:
r2P-value
Predictedrainfall
atLaVenta(mm)
from
simple
regression
MultipleR-
squared
P-valuefor
2ndorder
polynomial
Predictedrainfall
atLaVenta(mm)
from
2nd-order
polynomial
regression
#Species
0·593
0·0005
1810
0·594
0·0029
1780
#Primatespecies
0·487
0·0026
1811
0·648
0·001
2212
#Frugivores
0·675
<0·0001
1446
0·740
0·0002
1694
#Browsers
0·286
0·0330
5440
0·291
0·1067
1253
#Grazers
0·101
0·2315
1133
0·106
0·4814
1095
#1)Consumers
0·664
0·0001
2291
0·705
0·0004
2333
#2)Consumers
0·292
0·0307
1166
0·567
0·0807
1272
#Arborealspecies
0·678
<0·0001
1756
0·823
<0·0001
2138
#Scansorialspecies
0·440
0·0051
1205
0·516
0·0089
1195
#Terrestrialspecies
0·180
0·1013
2026
0·219
0·1998
2007
#Species,sizeclassII
0·636
0·0002
1164
0·669
0·0008
1125
#Species,sizeclassIII
0·529
0·0014
1656
0·558
0·0049
1503
#Species,sizeclassIV
0·377
0·0114
2901
0·640
0·0324
2056
#Species,sizeclassV
0·162
0·1224
2178
0·163
0·3149
2222
ArborealityIndex
0·610
0·0019
1291
0·662
0·0093
1263
FrugivoreIndex
0·454
0·0042
553
0·509
0·0098
650
BrowserIndex
0·317
0·0231
1961
0·340
0·0674
1968
SizeIndex
0·479
0·0030
889
0·479
0·0144
899
Meanestim
atedrainfallforLaVenta(plusorminusonestandarderror)
1818
&251mm
1593
&122mm
Note:With
theexceptionofthenumberofgrazingspecies,predictedrainfallisnotreportedwhencorrelationbetweenthevariableandrainfallislessthan0·05.Indicesare
definedinthetext.
181
Discussion
Rainfall gradients and modern mammalian faunas
A number of general trends have emerged in comparisons of mammalian species diversity intropical South America in relation to rainfall. There is an overall enrichment of the numberof species in wetter environments. This is probably related to the generally increasedproductivity, structural complexity and lack of seasonality of mature vegetation in wet tropicalenvironments receiving at least 3500 mm annual rainfall.Our analysis confirms that the association of wetter environments with more arboreal,
nonvolant mammalian species contributes importantly to overall enrichment in the number ofprimary consumers in general, as observed by many other workers (Fleming, 1973; August,1983). The association of wetter environments with more arboreal species extends also to thesize classes within which arboreal locomotion is favored. Our analysis reveals a preponderanceof arboreal species in size classes II and III (and not in size classes I and IV), and as recentlydemonstrated by Malcolm (1995), this is correlated with the physical constraints of arborealhabitat, and in particular, with the degree of canopy connectivity.We speculate that the spatial patchiness of food resources in the arboreal milieu is closely
related to the size of the animal. For very small species, the metabolic cost of locomotionbetween widely-dispersed food sources separated by gaps in the canopy and understory may betoo great. For large species an upper size-limit may be imposed by the physical strength of thesupporting stems and branches (Christoffer, 1987). Thus, selection may favor a fairly narrowrange of body sizes for arboreal species (Emmons, 1995). This finding accords with theobservations of Legendre (1989) who emphasizes the presence of such a relationship for manycommunities of living mammals.Cenogram analysis (bivariate graphs of body size rank vs. body size for mammalian primary
consumers, first used by Emmons et al., 1983) has been employed to reconstruct Cenozoicenvironments (Gingerich, 1989; Legendre, 1986, 1989; Gunnell, 1994). Summarizing
500
3500
0150
First principal component (68.4% of variance)
Mea
n a
nn
ual
rai
nfa
ll (
mm
)2500
3000
2000
1500
1000
500
200 300 400 450350250
Monkey Beds PCI = 288
95% confidence intervalfor rainfall estimate
Figure 9. Bivariate plot of the first principal component vs. rainfall for 16 localities from tropical SouthAmerica. See text for further explanation. No separation is obvious between environments with medium andhigh rainfall (2000–2500 mm/year vs. 2500–3500 mm/year). Most of the discrimination occurs betweenthese two categories on one hand, and faunas from areas with less than 2000 mm/year.
182 . . . .
worldwide data for modern mammalian communities that differ in habitat or vegetationstructure and annual rainfall, Legendre (1986, 1989) shows that mammalian faunas from drierenvironments have fewer species in the 500 and 8000 g size range. For this reason,least-squares regression slopes for species in this size range are steeper for more open, drier,environments than in more ‘‘closed’’, wetter, environments (Gingerich, 1989). Our data showa similar phenomenon, with there being more species of size classes II and III (roughlyequivalent to the size range mentioned above) in wetter than in drier environments. None ofthe above authors suggest any explanation for why there should be so many more specieswithin this size range, but a plausible explanation may relate to the constraints on size imposedby the arboreal milieu, as discussed above.The above-noted strong positive correlations between the number of mammalian primary
consumers, the number of arboreal species, and the number of frugivorous and browsingspecies with rainfall in modern faunas may be explained by the increase in arboreal plantbiomass with rainfall (Fittkau & Klinge, 1973), floristic diversity (Gentry, 1988) and year-roundavailability of canopy food resources (Terborgh, 1986) (at least within the rainfall rangeassessed here). Total mammalian species richness and the number of arboreal and scansorialspecies is known to be significantly positively correlated with habitat complexity, foliar-heightdiversity and vertical complexity in the tropics (Da Fonseca & Redford, 1983; Redford & DaFonseca, 1986; August, 1983; Malcolm, 1995).The general relationship between increasing annual rainfall and the structure and
complexity of vegetation in lowland tropical environments is well-established (Monasterio &Sarmiento, 1984) as is the inverse relationship between mean annual rainfall and the length ofthe dry season. Despite these relationships, there are problems with predicting the predomi-nant mature vegetation in that portion of the dry tropical life zone receiving between 1500 and2000 mm of annual rainfall. It is in this rainfall range where the transition between opensavanna, deciduous forest and evergreen forest occurs. In our data set, five localities receivebetween 1500 and 2000 mm annual rainfall: Cocha Cashu, Esmeralda, Federal District,Guatopo, and Puerto Páez. While all five localities experience some degree of rainfallseasonality, the length of the dry season and its influence on vegetation structure and foodavailability is highly variable. Puerto Páez (Venezuela) and Federal District (Brazil) bothreceive about 1500 mm of rainfall, and both are characterized by climates with seasonalrainfall and semi-deciduous gallery forests restricted to the margins of permanent streams, withextensive savanna grasslands in the interfluvial areas. Between 1500 and 2000 mm, theproportion of forest and savanna reverses. Localities with rainfall at or above 2000 mm arecharacterized by evergreen forest. While the evergreen forest canopies at localities withgreater than 2000 mm of rainfall are usually continuous or nearly continuous, savanna ofvariable extent is reported to occur at Puerto Ayacucho (2250 mm) (Handley, 1976; Snow,1976).Finally, several discrepancies should be noted for which we can propose only speculative
explanations. The first has to do with there being so many more browsers in the La Ventafauna than in the extant faunas: 15 species of browsers at La Venta vs. 0–5 species in modernNeotropical faunas. Our subjective impression is that the La Venta fauna is similar to tropicalfaunas of Africa and Asia in terms of the richness of browsers. In Africa and Asia, unlike inSouth America, there is a far greater number of sympatric species of browsers in most or allhabitats, particularly among the artiodactyls, but also the elephants, hyraxes and primates.Thus, it is the apparently impoverished numbers of browsers in the modern Neotropics, not atLa Venta, that deserves further investigation.
183
A correlated phenomenon has to do with the absence in the modern Neotropical faunas ofvery large mammals (i.e., >350 kg) compared with the tropical faunas of Asia and Africa.Again, the La Venta fauna more closely resembles those of Africa and Asia than the modernNeotropics. It is tempting to suggest that these apparent peculiarities of the Neotropical faunasare causally linked and have to do with recent faunal extinctions, for late Pleistocene faunasincluded many larger possible browsers such as elephants, litopterns, horses, glyptodonts, andgiant sloths, all having gone extinct within the past 10,000 years.
Conclusions
The paleoenvironment at La Venta
Forest. The presence of certain fossil vertebrates in the Monkey Beds assemblage (assummarized by Kay & Madden, 1996) provide strong evidence for forest cover at the time ofdeposition. These include (1) the freshwater fish Colossoma macropomum, a frugivore that exploitsflooded flood plain forest, (2) forest leaf-litter inhabiting snakes, (3) the forest-dwelling landtortoise Geochelone, (4) forest-dwelling jacamar (Galbula) and hoatzin (Opisthocomus) among thebirds, (5) diverse arboreal marsupials, (6) numerous small sloth species, some with arborealand/or climbing adaptations, (7) close taxonomic affinities between some armored edentatesand most rodent species with living species that are forest-dwelling, (8) four litoptern specieswith low-crowned teeth associated with frugivory or browsing (leaf-eating) habits, (9) only twoungulate species with high-crowned cheek teeth, (10) bats known to roost and forage inmultistratal evergreen forests, (11) diverse monkeys all of which are arboreal, and (12)pitheciine monkeys that today are not known to occur in seasonally dry forest. This evidenceis consistent and indicates that terrestrial forest biotopes occurred in the La Venta area duringthe time of deposition of the Monkey Beds.
Riparian mosaic.While evidence for the presence of forest at La Venta may be indisputable (Kay& Madden, 1996), there is considerable evidence indicating a complex vegetation mosaicrather than a continuous-canopy, evergreen rainforest. The factors that contributed to createthis mosaic were probably numerous, and almost certainly included fluvial processes(Guerrero, 1996).The contribution to vegetational complexity associated with fluvial processes within
meander belts, and in turn, the contribution of this vegetational complexity to the mainten-ance of vertebrate diversity in humid and wet tropical life zones is significant (Remsen &Parker, 1983). Evidence for diverse riparian aquatic environments is abundantly indicated atLa Venta by the diverse freshwater fish (13 families and 23 species). The aquatic environmentsthese fish represent include large, open river and in-shore habitats, marginal shallow waters,and relatively still, even anoxic, temporary waters. Reflecting this habitat heterogeneity, thefish fauna presents correspondingly wide dietary diversity, including algivores, detritivores,carnivores, etc. and frugivore/granivores (Lundberg et al., 1986). The heterogeneous aquaticenvironments are typical of lowland meander belts in the equatorial tropics (Lundberg, 1996).In terms of number of taxa, body-size range, and presumed feeding ecology, the diversity of
La Venta crocodilians is unparalleled in the Cenozoic record of tropical South America(Langston & Gasparini, 1996). The highest diversities of living crocodilians are attained onlyin the biotically rich, complex, heterogeneous riparian environments of the wet tropicallowlands of western Amazonia (Medem, 1981, 1983).
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Judging from the habits of their closest living relatives, most of the fossil birds in the LaVenta fauna inhabited riparian environments (Rasmussen, 1996). Anhinga anhinga (Anhingidae),a riparian piscivore, today inhabits freshwater marshes in both the Amazon and Orinocoriver systems. Aramus guarauna prefers heavily vegetated freshwater marshes, wooded swamps,and other similar fluvial wetlands. The living hoatzin (Opisthocomus hoazin), similar to theextinct Hoazinoides from La Venta, is an obligate folivore and not a proficient flier. This speciesoccurs today only along the forested banks of rivers and streams in the Orinoco and Amazonsystems.The fossil vertebrate evidence for a dynamic riparian succession at La Venta accords with
abundant sedimentologic features associated with the shifting course of meandering rivers(Guerrero, 1996). Possibly analogous modern environments have been described at CochaCashu (Terborgh, 1983; Salo et al., 1986; Foster, 1986, 1990; Janson & Emmons, 1990) andat La Macarena in Colombia (Hirabuki, 1990).
Canopy continuity. Having established the presence of arboreal vegetation within the meanderbelt at the time of deposition of the Monkey Beds, and annual rainfall levels between 1500 and2000 mm, we can only speculate on the extent or continuity of the forest canopy in theinterfluvial area. The diverse chiropteran fauna of 11 species (nine genera, five families)described by Czaplewski (1996) includes a number of living genera and species. These includeDiclidurus (Emballonuridae), an extant aerial-pursuit insectivore that usually roosts and foragesin multistory evergreen forests, and the extant phyllostomine Tonatia, an aerial foliage-gleaninginsectivore that forages and roosts in mature evergreen forests and deciduous forests. Twospecies of Thyroptera (Thyropteridae) are found in the La Venta fauna. These are aerial pursuitinsectivores that use slow, maneuverable flight and forage and roost in lowland forest edges, intree gaps and successional areas.Honda Group rocks have yielded more fossil platyrrhines than any other fossil assemblage
on the continent. Most primate species at La Venta were small. Among these, theCallitrichidae (sensu Rosenberger et al., 1990) is represented by three species. Lagonimicoconclucatus, weighed about 1 kg and displays dental characters suggesting a diet of gum- andfruit-eating (Kay, 1994). Patasola magdalenae, of intermediate in body size between Saimiri andliving callitrichids (about 700 g), probably was a mixed fruit- and insect-eater (Kay &Meldrum, 1996). A third species has not been named. Callitrichidae are often described aspreferring edge habitat (Soini, 1993; Rylands & de Faria, 1993; Garber, 1993). The presenceof two pitheciines in the Monkey Beds suggests the presence of flooded high forest within themeander belt. The absence at La Venta of large, soft-fruit eaters usually associated with highterra firme forest, is also suggestive of high vegetational heterogeneity.Among the 11 species and ten genera of marsupials now known for the La Venta fauna
(Bown & Fleagle, 1993; Dumont & Bown, 1996; Goin, 1996), occurs the shrew-likemicrobiothere Pachybiotherium, whose closest living relative Dromiciops is a forest or forest-edgedwelling animal. Carlini et al. (1996) suggest that the high diversity of armored xenarthrans atLa Venta suggests a remarkable degree of environmental heterogeneity at La Venta, unlikethat found today in the continuous evergreen rainforests of the humid and wet tropics. Theremarkable diversity of Cingulata at La Venta is also a strong argument for habitatheterogeneity and canopy discontinuity in the interfluvial area. Armadillos are not commonlyfound to inhabit riverine areas subjected to frequent flooding (O. Linares, pers. comm.).In particular, the high number of terrestrial browsing mammals and the very low diversity
of grazing mammals in the Monkey Beds assemblage suggests strongly that open savanna
185
grassland, if present, was of reduced extent and that the forest was probably characterized byboth abundant low foliage and also fruit-bearing trees. Finally, the vegetation mosaic at LaVenta may have been modified by the destructive habits of the four species of large (body sizeclass VI) and tusked herbivores, some displaying microwear features associated with branch-stripping behaviors (Johnson & Madden, 1996). Thus, there is limited paleontological evidencefor the presence of continuous canopy evergreen forest. Most, if not all, of the availableevidence is consistent and strongly suggests an extensive vegetational mosaic and significantforest understory. The suggestive evidence for abundant low vegetation during the middleMiocene at La Venta may confirm the important historical component to the understory floraof Neotropical forests (Gentry & Emmons, 1987).
Seasonality. Although the empirical evidence for fruit and foliar phenology is not extensiveacross the tropics, seasonality in the supply of food resources for primary consumers isconsidered to be a common feature of all lowland tropical environments, even in the wettest,meteorologically aseasonal, equatorial rainforests (Howe, 1984; Terborgh, 1986). It is ourcontention that while seasonal factors may conceivably have influenced plant phenology andfood supply at La Venta in the Miocene, seasonal rainfall was probably only of secondaryimportance in determining the structural configuration and complexity of forest habitats.Although somewhat equivocal, the available sedimentologic evidence does not indicatepronounced rainfall seasonality (see Guerrero, 1996). Evidence for periodic flooding duringdeposition of the Honda Group is abundantly indicated by the predominance of overbanksediments. Periodic flooding is also suggested by the presence of freshwater fish that cansurvive in temporary waters (Lepidosiren) and species that forage in inundated forest (Colossoma).While episodic flooding was almost certainly caused by fluctuations in rainfall, they do notnecessarily imply a seasonal water deficit of sufficient duration to have affected vegetationstructure. The fluvial sediments of the Honda Group do not display features generallyassociated with prolonged seasonal water deficits and savanna landscapes, such as hardenedand cracked surfaces, evidence of wind erosion, alteration by fire, evaporation, hardpan,impeded drainage, slow chemical weathering, and low root biomass. The lack of sedimento-logic evidence in the Honda Group for pronounced seasonality suggests that climaticseasonality was relatively insignificant in terms of vegetation structure during the middleMiocene at La Venta.
Uplift of the eastern Cordillera and its effects on climate. As noted, the geographic setting of the LaVenta area has been profoundly modified since Miocene times by the uplift of the EasternCordillera and its attendant effects on climate. Where formerly, the La Venta region wassituated on a gently sloping piedmont plain, today it is situated in a mountainous valley.Climatic comparisons for the La Venta Miocene are best made then with the eastern piedmontregion of Colombia. Today, northeastern Colombia experiences a seasonal pattern ofatmospheric circulation involving an intensification of the northeast trade winds and asouthern shift of the intertropical convergence under the influence of the northern hemispherewinter (Rudloff, 1981). In response to the increasing seasonality of precipitation, thepredominant plant cover in eastern Colombia changes from forest to savanna northward.Accompanying the increasing seasonality from south to north is the gradual replacement ofthe architecturally complex, closed-canopy, continuous evergreen rainforest of ColombianAmazonia, by open tropical savannas with narrow deciduous riparian gallery forests of theColombian llanos in the Orinoco drainage. Tropical savannas occur in areas where total
186 . . . .
annual rainfall is between 1000 and 2000 mm and rainfall is seasonal, with dry periods lasting6 months or longer. Given our estimates of total annual rainfall and the lack of strong evidencefor rainfall seasonality, it would appear that areas of extensive savanna were probablyrestricted to areas farther north during the middle Miocene.Perhaps more significant is the east-west rainfall gradient wherein rainfall increases
from east to west in association with increasing proximity to the Cordillera (Snow, 1976).This rainfall gradient was presumably shifted further westward in the middle Miocenewhen the Eastern Cordillera was low and discontinuous, and the major climate-modifyingbarrier would have been the Central Cordillera. The westward shift of this gradientwould explain why our rainfall estimates for the middle Miocene are substantially higher thanthose at La Venta today. Even allowing for a westward shift in this rainfall gradient, ourestimates of rainfall levels between 1500 and 2000 mm seem too low by comparison withrainfall levels today east of the Andes. Based on equatorial areas of Colombia today withcomparable proximity to the Cordillera, annual rainfall levels at La Venta should have beengreater than 3000 mm. The latter level of rainfall supports continuous-canopy evergreenrainforest across both riparian and interfluvial areas at this latitude of eastern Colombia today(Hirabuki, 1990; Stevenson et al., 1994; Klein & Klein, 1976). While it may be premature tospeculate whether the preponderant reason for the difference between observed and expectedrainfall is related to Andean uplift or to some other global influence, the departure isnoteworthy.
Summary
A comparison of the species richness and composition of diet, locomotor and body size classesamong 16 modern nonvolant mammalian faunas in tropical South America reveals numeroussignificant positive correlations with rainfall. Significant and strong positive correlations withrainfall are found in 18 attributes, including the number of nonvolant mammal species,number of primate species, number of frugivores, primary consumers, arborealists, and thenumber of species between 100 g and 10 kg in body weight.Estimates of annual rainfall derived from simple least squares and polynomial regressions
and principal components analysis yield a modal estimate of between 1500 and 2000 mmannual rainfall for the middle Miocene Monkey Beds assemblage at La Venta. This level ofrainfall is associated today with the transition between savanna and forest environments inlowland equatorial South America.Paleontological evidence strongly suggests the presence of forest biotopes at La Venta.
Paleontologic and sedimentologic evidence together indicate a dynamic riparian mosaicassociated with the shifting course of meandering rivers. Faunal evidence also suggests thathabitat heterogeneity and canopy discontinuity extended into the interfluvial area. Seasonalrainfall was probably only of secondary importance in shaping the structural and spatialconfiguration of the dominantly forested mosaic habitat at La Venta. The fossil record is notconsistent with the presence of extensive primary or undisturbed, continuous-canopy,evergreen tropical rainforest.The reconstructed middle Miocene environment at La Venta differs significantly from
modern environments of similar geography on the piedmont east of the Andes at the samelatitude. This in turn suggests that the extensive evergreen rainforests of the upper Amazonianpiedmont probably post-date the initiation of Andean uplift.
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Acknowledgements
We thank the many people who helped us collect and study the geology and paleontology ofthe La Venta region of Colombia, a list of which appears in Kay et al., 1996. Especially helpfulin preparing this paper were Drs Mary Maas, Peter Andrews, and several anonymousreviewers. We especially thank the editors of this volume, Drs Kaye Reed and Mario Gagnon.
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Monasterio, M. & Sarmiento, G. (1984). Ecological diversity and human settlements in the tropical northern Andes.In (W. Lauer, Ed.) Natural Environment and Man in Tropical Mountain Ecosystems, pp. 295–305. Stuttgart: Franz SteinerVerlag Wiesbaden Bmbh.
Nitikman, L. Z. & Mares, M. A. (1987). Ecology of small mammals in a gallery forest of central Brazil. Ann. CarnegieMus. 56(2), 75–95.
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Nutall, C. P. (1990). A review of the Tertiary non-marine molluscan faunas of the Pebasian and other inland basinsof north-western South America. Bull. Brit. Mus. Nat. Hist., Geol. 45, 165–371.
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192 . . . .
App
en
dix
Sp
ec
ies
of
ma
mm
als
insix
tee
nlo
ca
liti
es
inth
eN
eo
tro
pic
s
Artiodactyla
Localities(numbersfollowFigure1andTable1)
Niche1
References2
Family
Species
12
34
56
78
910
1112
1314
1516
DL
B
Cervidae
Blastocerusdichotomus
00
00
00
00
01
10
00
00
81
51
Mazamaamericana
10
01
11
10
11
01
11
11
61
42,3
Mazamagouazoupira
00
00
01
11
01
11
01
01
61
42,3
Odocoileusvirgianus
01
11
00
00
00
00
00
00
71
43
Ozotocerosbezoarticus
00
00
00
00
11
10
00
00
81
43,4
Tayassuidae
Catagonuswagneri
00
00
00
00
00
10
00
00
61
41
Pecaritajacu
11
01
11
10
11
11
01
11
61
42
Tayassupecari
00
01
11
10
11
00
01
11
61
42,3
Carnivora
Localities(numbersfollowFigure1andTable1)
Niche1
References2
Family
Species
12
34
56
78
910
1112
1314
1516
DL
B
Canidae
Atelocynusmicrotis
00
00
00
00
00
00
00
11
11
32
Cerdocyonthous
01
11
00
11
11
11
10
00
11
33,4
Chrysocyonbrachyurus
00
00
00
00
11
00
00
00
41
43
Pseudalopexgriseus
00
00
00
00
00
11
00
00
11
33
Pseudalopexgymnocercus
00
00
00
00
00
11
00
00
11
33
Pseudalopexvetulus
00
00
00
00
00
00
00
00
11
3Asforgenus
Speothosvenaticus
00
00
01
10
10
00
00
11
11
32
Felidae
Herpailurusyaguaroundi
11
11
00
11
11
11
11
11
11
32
Leoparduspardalis
11
11
10
10
11
00
01
11
11
42
Leopardustigrinus
00
00
00
10
00
01
00
01
13
2Leoparduswiedii
00
00
10
10
00
01
00
11
14
32
Oncifelisgeoffroyi
00
00
00
00
00
11
00
00
11
33
Pantheraonca
10
00
11
11
01
10
01
11
11
53
Pumaconcolor
11
00
01
10
11
11
11
01
11
42,3
Mustelidae
Conepatuschinga
00
00
00
00
00
11
00
00
31
33
Conepatussemistriatus
11
00
00
01
00
00
00
00
31
32
Eirabarbara
11
01
11
10
11
01
11
11
44
32
Galictiscuja
00
00
00
00
00
11
00
00
11
33
Galictisvittata
01
00
00
11
00
00
01
11
11
32
Lontralongicaudus
00
00
11
10
01
01
11
11
15
32,3
Mustelaafricana
00
00
00
10
00
00
00
01
12
22
Pteronurabrasiliensis
00
10
00
10
00
00
01
01
15
42
193
App
en
dix
co
nti
nu
ed
Carnivora
cont
Localities(numbersfollowFigure1andTable1)
Niche1
References2
Family
Species
12
34
56
78
910
1112
1314
1516
DL
B
Procyonidae
Bassaricyonalleni
00
00
00
00
00
00
00
11
43
3Asforgenus
Bassaricyongabbii
00
01
10
00
00
00
01
00
43
32
Nasuanasua
00
00
11
10
11
01
01
11
44
32
Potosflavus
10
01
11
10
00
00
01
11
43
32
Procyoncancrivorus
11
00
00
11
11
01
11
11
34
32,3,4
Ursidae
Tremarctosornatus
00
00
00
00
00
00
00
10
44
55
Lagomorpha
Localities(numbersfollowFigure1andTable1)
Niche1
References2
Family
Species
12
34
56
78
910
1112
1314
1516
DL
B
Leporidae
Sylvilagusbrasiliensis
10
00
00
11
11
11
11
11
82
22
Sylvilagusfloridanus
01
10
00
00
00
00
00
00
82
25,6
Marsupialia
Localities(numbersfollowFigure1andTable1)
Niche1
References2
Family
Species
12
34
56
78
910
1112
1314
1516
DL
B
Didelphidae
Caluromyslanatus
00
01
11
00
00
00
01
11
43
22
Caluromysphilander
10
01
11
10
00
00
00
00
43
22
Caluromysiopsirrupta
00
00
00
00
00
00
01
00
43
22
Chironectesminimus
10
00
00
10
10
00
00
11
15
23
Didelphisalbiventris
00
00
00
01
11
11
10
00
34
32,4
Didelphismarsupialis
11
11
11
10
00
00
01
11
34
32
Didelphissp.A
00
01
10
00
00
00
00
00
34
3Asforgenus
Glironiavenusta
00
00
00
00
00
00
01
01
33
22,7
Gracilinanusagilis
00
00
00
00
10
00
00
00
43
12,27
Lutreolinacrassicaudata
00
00
00
00
00
00
10
00
15
23
Marmosa(?)sp.A
00
00
00
00
10
00
00
00
34
18
Marmosacinerea
00
00
00
10
00
00
00
00
34
23
Marmosalepida
00
00
00
00
00
00
00
01
34
12
Marmosamurina
10
01
11
10
10
00
00
11
33
12
s s s
194 . . . .
Ap
pe
nd
ixc
on
tin
ue
d
Marsupialia
cont
Localities(numbersfollowFigure1andTable1)
Niche1
References2
Family
Species
12
34
56
78
910
1112
1314
1516
DL
B
Didelphidae
Marmosarobinisoni
01
00
00
00
00
00
00
00
34
12
cont
Marmosarubra
00
00
00
00
00
00
00
11
34
12
Marmosopsfuscatus
10
00
00
00
00
00
00
00
34
12
Marmosopsnoctivagus
00
00
00
00
00
00
01
01
34
12
Marmosopsparvidens
00
00
11
10
00
00
00
00
34
12
Metachirusnudicaudatus
00
00
11
10
00
00
01
11
42
22,3
Micoureusconstantiae
00
00
00
00
00
01
00
00
33
13
Micoureusdemerarae
10
01
11
00
00
00
01
00
33
1Asforgenu
Micoureusregina
00
00
00
00
00
00
00
11
33
1Asforgenu
Monodelphisadusta
00
00
00
00
00
00
00
11
32
12
Monodelphisamericana
00
00
00
10
10
00
00
00
32
12
Monodelphisbrevicaudata
10
01
11
00
01
00
00
00
32
12,7
Monodelphisdimidiata
00
00
00
00
00
01
00
00
34
13,4
Monodelphisdomestica
00
00
00
01
10
00
00
00
32
12,3,7
Monodelphiskunsi
00
00
00
00
10
00
00
00
32
1Asforgenu
Philanderandersoni
00
00
00
00
00
00
00
01
34
22
Philanderopossum
00
01
11
10
10
00
01
10
34
22,7
Thylamyselegans
00
00
00
00
00
11
10
00
33
14
Thylamyspusilla
00
00
00
01
01
10
00
00
34
14
Perissodactyla
Localities(numbersfollowFigure1andTable1)
Niche1
References2
Family
Species
12
34
56
78
910
1112
1314
1516
DL
B
Tapiridae
Tapirusterrestris
10
01
11
10
11
01
11
11
71
52
195
App
en
dix
co
nti
nu
ed
Primates
Localities(numbersfollowFigure1andTable1)
Niche1
References2
Family
Species
12
34
56
78
910
1112
1314
1516
DL
B
Callitrichidae
Callimicogoeldii
00
00
00
00
00
00
01
00
33
29
Callithrixjacchus
00
00
00
01
10
00
00
00
43
29
Cebuellapygmaea
00
00
00
00
00
00
01
01
43
29
Sanguinusfuscicollis
00
00
00
00
00
00
01
01
43
29,10
Saguinusimperator
00
00
00
00
00
00
01
00
43
29
Saguinusmidas
00
00
01
00
00
00
00
00
43
29
Saguinusnigricollis
00
00
00
00
00
00
00
01
43
29
Cebidae
Alouattabelzebul
00
00
00
10
00
00
00
00
73
3Asforgenus
Alouattacaraya
00
00
00
00
11
01
10
00
73
39
Alouattaseniculus
11
10
11
00
00
00
01
11
73
39
Aotusinfulatus
00
00
00
10
00
00
00
00
63
2Asforgenus
Aotusnigriceps
00
00
00
00
00
00
01
00
63
2Asforgenus
Aotustrivirgatus
00
01
10
00
01
00
00
00
63
29
Aotusvociferans
00
00
00
00
00
00
00
11
63
2Asforgenus
Atelesbelzebuth
10
01
10
00
00
00
00
01
63
39
Atelespaniscus
00
00
01
00
00
00
01
00
63
39,11
Callicebusbrunneus
00
00
00
00
00
00
01
00
63
29,12
Callicebuscupreus
00
00
00
00
00
00
00
10
63
39
Callicebustroquatus
00
00
10
00
00
00
00
01
63
39
Cebusalbifrons
00
00
10
00
00
00
01
11
43
39
Cebusapella
00
00
11
11
11
00
11
01
43
34,9
Cebusolivaceous(=nigrivittatus)
11
11
10
00
00
00
00
00
43
39
Chiropotessatanas
00
01
11
10
00
00
00
00
63
39
Lagothrixlagothricha
00
00
00
00
00
00
01
00
63
39
Pithiciaaequatorialis
00
00
00
00
00
00
00
01
43
3Asforgenus
Pitheciairriota
00
00
00
00
00
00
01
00
43
313
Pitheciamonachus
00
00
00
00
00
00
00
11
43
313
Pitheciapithecia
00
00
11
00
00
00
00
00
43
313
Saimiriboliviensis
00
00
00
00
00
00
01
00
33
29
Saimirisciureus
00
01
10
10
00
00
00
11
33
29
Cacajaomelanocephalus
00
00
10
00
00
00
00
00
n/a
n/a
n/a
Callicebusmoloch
00
00
00
00
01
00
00
01
n/a
n/a
n/a
Callithrixargentata
00
00
00
00
01
00
00
00
n/a
n/a
n/a
s s s s s s s s s s s
196 . . . .
Ap
pe
nd
ixc
on
tin
ue
d
Rodentia
Localities(numbersfollowFigure1andTable1)
Niche1
References2
Family
Species
12
34
56
78
910
1112
1314
1516
DL
B
Agoutidae
Agoutipaca
11
11
11
10
00
00
01
11
61
32
Caviidae
Caviaaperea
00
00
00
00
10
00
00
00
82
23
Dolichotissalinicola
00
00
00
00
00
10
00
00
81
33,4
Galeaflavidens
00
00
00
00
00
00
00
00
82
2Asforgenu
Galeamusteloides
00
00
00
00
00
11
00
00
82
21,3,4
Galeaspixii
00
00
00
01
10
00
00
00
82
214
Kerodonrupestris
00
00
00
01
00
00
00
00
71
314,27
Microcaviaaustralis
00
00
00
00
00
10
00
00
84
24
Chinchillidae
Lagostomusmaximus
00
00
00
00
00
10
00
00
86
33
Ctenomyidae
Ctenomysfrater
00
00
00
00
00
01
10
00
76
24
Ctenomysmendocinus
00
00
00
00
00
10
00
00
76
2Asforgenu
Dasyproctidae
Dasyproctafuliginosa
00
00
10
00
00
00
00
11
61
32
Dasyproctaleporina
11
01
01
00
00
00
00
00
61
3Asforgenu
Dasyproctaprymnolopha
00
00
00
11
00
00
00
00
61
3Asforgenu
Dasyproctapunctata
00
00
00
00
01
01
11
00
61
32
Dasyproctasp.A
00
00
00
00
10
00
00
00
61
3Asforgenu
Myoproctaacouchy
00
00
11
00
00
00
01
11
51
32
Dinomyidae
Dinomysbranickii
00
00
00
00
00
00
01
10
61
41
Echimyidae
Carterodonsulcidens
00
00
00
00
10
00
00
00
72
21
Clyomyslaticeps
00
00
00
00
10
00
00
00
76
21,3,8,27
Dactylomysdactylinus
00
00
00
00
00
00
01
01
73
22,15
Echimysbraziliensis
00
01
10
00
00
00
00
11
53
2Asforgenu
Echimyschrysurus
00
00
00
10
00
00
00
00
53
2Asforgenu
Echimyssaturnus
00
00
00
00
00
00
00
05
32
Asforgenu
Echimyssemivillosus
11
10
00
00
00
00
00
00
53
22
Echimyssp.A
00
00
00
00
00
00
01
00
54
216
Echimyssp.B
00
00
01
00
00
00
00
00
53
2Asforgenu
Isothrixbistriata
00
00
10
00
00
00
00
00
n/a
32
Asforgenu
Isothrixpagurus
00
00
01
00
00
00
00
00
n/a
32
2,27
Makalataarmata
00
00
00
10
00
00
00
11
64
21
Mesomyshispidus
00
01
11
00
00
00
01
01
43
22
Proechimysamphichoricus
00
00
10
00
00
00
00
00
52
2Asforgenu
Proechimysbrevicauda
00
00
00
00
00
00
01
00
52
216
Proechimyscayennensis
00
01
01
10
00
00
00
00
52
25,17
s s s s s s s s s s s
197
App
en
dix
co
nti
nu
ed
Rodentia
cont
Localities(numbersfollowFigure1andTable1)
Niche1
References2
Family
Species
12
34
56
78
910
1112
1314
1516
DL
B
Echimyidae
Proechimyscuvieri
00
00
01
00
00
00
00
00
52
2Asforgenu
cont
Proechimysgularis
00
00
00
00
00
00
00
01
52
2Asforgenu
Proechimyslongicaudatus
00
00
00
00
10
00
00
10
52
2Asforgenu
Proechimysquadruplicatus
00
00
00
00
00
00
00
01
52
2Asforgenu
Proechimyssemispinosus
10
00
10
00
00
00
00
01
52
2Asforgenu
Proechimyssimonsi
00
00
00
00
00
00
01
11
52
216
Proechimyssp.A
00
00
00
00
01
00
00
00
52
2Asforgenu
Proechimyssp.B
00
00
00
00
10
00
00
00
52
28
Proechimyssp.C
00
01
00
00
00
00
00
00
52
2Asforgenu
Proechimyssp.D
00
01
10
00
00
00
00
00
52
2Asforgenu
Proechimyssteerei
00
00
00
00
00
00
01
00
52
216
Thrichomysapereoides
00
00
00
01
11
00
00
00
54
21,8
Erethizontidae
Coendoubicolor
00
00
00
00
00
00
00
10
63
32
Coendoumelanurus
00
00
00
10
00
00
00
00
63
22
Coendouprehensilis
01
11
11
10
11
01
01
00
63
32
Coendouquichua
00
00
00
00
00
00
00
01
63
2Asforgenu
Heteromyidae
Heteromysanomalus
11
00
00
00
00
00
00
00
52
12,6
Hydrochaeridae
Hydrochaerishydrochaeris
01
11
10
10
10
00
11
11
85
42
Muridae
Akodonboliviensis
00
00
00
00
00
01
10
00
32
13,4
Akodoncursor
00
00
00
00
10
00
00
00
32
118
Akodonlindberghi
00
00
00
00
10
00
00
00
32
1Asforgenu
Akodonreinhardti
00
00
00
00
10
00
00
00
32
18
Akodonurichi
10
00
10
00
00
00
00
00
32
16
Akodonvarius
00
00
00
00
01
11
10
00
32
13,4
Bolomyslasiurus
00
00
00
10
11
00
00
00
52
13
Calomyscallosus
00
00
00
01
11
01
10
00
44
14
Calomyshummelincki
00
10
00
00
00
00
00
00
4n/a
1Asforgenu
Calomyslaucha
00
00
00
00
00
10
00
00
44
13,4
Calomystener
00
00
00
00
10
00
00
00
4n/a
18
Graomysdomorum
00
00
00
00
00
01
00
00
64
13,4
Graomysgriseoflavus
00
00
00
00
00
10
00
00
44
13,4
Holochilusbrasiliensis
00
00
00
10
10
11
10
00
75
23,4
Ichthyomysstolzmanni
00
00
00
00
00
00
00
01
35
219
Juscelinomyscandango
00
00
00
00
10
00
00
00
72
11,27
198 . . . .
App
en
dix
co
nti
nu
ed
Rodentia
cont
Localities(numbersfollowFigure1andTable1)
Niche1
References2
Family
Species
12
34
56
78
910
1112
1314
1516
DL
B
Muridae
Kunsiafronto
00
00
00
00
10
00
00
00
76
21,27
cont
Neacomysguianae
00
00
01
00
00
00
00
00
32
12
Neacomysspinosus
00
00
00
00
00
00
00
11
32
12,20
Neacomystenuipes
10
00
00
00
00
00
00
00
32
12
Nectomyssquamipes
00
11
10
10
10
00
01
11
45
23
Oecomysbicolor
11
11
11
10
10
00
01
11
53
12,8
Oecomysconcolor
10
11
10
10
11
00
00
11
54
18
Oecomysparicola
00
00
01
00
00
00
00
00
54
121
Oecomyssuperans
00
00
00
00
00
00
01
10
54
116
Oligoryzomyseliurus
00
00
00
00
10
00
00
00
54
1Asforgenus
Oligoryzomysfulvescens
00
10
00
10
01
00
00
00
54
1Asforgenus
Oligoryzomyslongicaudatus
00
00
00
00
00
11
10
00
54
13
Oligoryzomysmicrotis
00
00
00
00
10
00
01
00
54
116
Oligoryzomysnigripes
00
00
00
00
10
00
00
00
54
12,3
Oryzomysalbigularis
10
00
00
00
00
00
00
00
54
128
Oryzomyscapito
10
00
11
10
10
00
01
11
54
13
Oryzomyslamia
00
00
00
00
10
00
00
00
54
1Asforgenus
Oryzomyslegatus
00
00
00
00
00
01
10
00
44
14
Oryzomysmacconnelli
00
00
11
10
00
00
01
11
54
116
Oryzomysnitidus
00
00
00
00
00
00
01
01
54
13
Oryzomyssubflavus
00
00
00
00
10
00
00
00
52
18
Oxymycterusparamensis
00
00
00
00
00
01
10
00
32
13
Oxymycterusroberti
00
00
00
00
10
00
00
00
32
18
Oxymycterussp.a
00
00
00
00
00
00
01
00
32
1Asforgenus
Pseudoryzomyssimplex
00
00
00
00
10
00
00
00
n/a
51
1,3
Rhipidomyscouesi
00
00
10
00
00
00
01
00
63
1Asforgenus
Rhipidomysfulviventer
00
00
10
00
00
00
00
00
63
1Asforgenus
Rhipidomysleucodactylus
00
00
10
00
00
01
10
01
43
14
Rhipidomysmacconnelli
00
00
10
00
00
00
00
00
63
1Asforgenus
Rhipidomysmastacalis
00
00
11
10
10
00
00
00
63
15,8
Rhipidomyssp.A
01
00
00
00
00
00
00
00
63
16
Rhipidomyssp.B
00
00
00
00
10
00
00
00
63
1Asforgenus
Rhipidomyssp.C
00
00
10
00
00
00
00
00
63
1Asforgenus
Rhipidomysvenezuelae
10
00
00
00
00
00
00
00
63
16
Sigmodonalstoni
01
11
00
00
00
00
00
00
82
122
Wiedomyspyrrhorhinos
00
00
00
01
00
00
00
00
54
11,27
Zygodontomysbrevicaudata
01
11
10
00
00
00
00
00
52
15,23
199
App
en
dix
co
nti
nu
ed
Rodentia
cont
Localities(numbersfollowFigure1andTable1)
Niche1
References2
Family
Species
12
34
56
78
910
1112
1314
1516
DL
B
Myocastoridae
Myocastorcoypus
00
00
00
00
00
11
00
00
75
33
Sciuiridae
Microsciurusflaviventer
00
00
00
00
00
00
00
11
33
12
Sciurusaestuans
00
00
10
10
00
00
00
00
64
2Asforgenus
Sciurusgilvigularis
00
01
11
00
00
00
00
00
64
2Asforgenus
Sciurusgranatensis
11
00
00
00
00
00
00
00
64
22
Sciurusignitus
00
00
00
00
00
00
01
00
44
22
Sciurusigniventris
00
01
10
00
00
00
00
11
64
22
Sciurussanborni
00
00
00
00
00
00
01
00
64
2Asforgenus
Sciurusspadiceus
00
00
00
00
01
00
01
11
64
22
Xenarthra
Localities(numbersfollowFigure1andTable1)
Niche1
References2
Family
Species
12
34
56
78
910
1112
1314
1516
DL
B
Bradypodidae
Bradypustridactylus
00
00
01
00
00
00
00
00
73
32,3
Bradypusvariegatus
10
01
00
10
00
00
01
11
73
32
Dasypodidae
Cabassousunicinctus
10
00
00
10
10
00
00
11
21
32
Chaetophractusvellerosus
00
00
00
00
00
11
00
00
32
23
Chlamyphorusretusus
00
00
00
00
00
10
00
00
36
23
Dasypuskappleri
00
00
11
10
00
00
00
01
21
32,24
Dasypusnovemcinctus
11
01
11
11
11
01
01
11
31
32,3
Dasypussabanicola
00
10
00
00
00
00
00
00
21
324,25
Dasypusseptemcinctus
00
00
00
10
10
01
00
00
21
33
Euphractussexcinctus
00
00
00
01
11
11
00
00
31
32,24
Priodontesmaximus
10
01
01
00
11
11
01
11
21
42,25
Tolypeutesmatacus
00
00
00
00
01
11
00
00
21
33,24
Tolypeutestricinctus
00
00
00
00
10
00
00
00
21
3Asforgenus
Megalonychidae
Choloepusdidactylus
00
00
11
10
00
00
00
01
73
32
Choloepusho
ffmanni
00
00
00
00
00
00
01
10
73
326
Myrmecophagidae
Cyclopesdidactylus
00
00
11
10
00
00
01
11
23
22
Myrmecophagatridactyla
01
11
11
10
11
10
01
11
21
42
Tamanduatetradactyla
11
11
11
11
11
11
11
11
24
32
Note(1)LocalitiesnumberedfollowingFigure1.
Note(2)M
acronichecategories,D=diet;L=locomotion;B=bodyweight.ForexplanationofnumbersseedataandMethodssection.
Note(2)Referencesfordiet,locomotorandbodyweightcategoryassignments:(1)Nowak,1991;(2)Emmons&Feer,1990;(3)Redford&Eisenberg,1992;(4)M
ares&
Ojeda,1989;(5)Eisenberg,1989;(6)Ensenbergetal.,1979;(7)Streilein,1982b;(8)Maresetal.,1989;(9)Ford&Davis,1992;(10)Peres,1993;(11)VanRoosmalen,1985;
(12)Terborgh,1983;(13)H
ershkovitz,1987;(14)Maresetal.,1981;(15)Emmons,1981;(16)Janson&Emmons,1990;(17)Guillotin,1982;(18)Nitikman&Mares,1987;
(19)Voss,1988;(20)Alho,1982;(21)M
alcolm,1990;(22)Voss,1992;(23)Fleming,1970;(24)W
etzel,1985;(25)Redford,1985;(26)Meritt,1985;(27)Mares,pers.comm.;
(28)Albuja,pers,comm.
