Mammals and rainfall: paleoecology of the middle Miocene at La Venta (Colombia, South America)

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

162

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Third, the La Venta lowland equatorial fauna contains many primates, including the earliest undisputed representatives of tamarins, squirrel monkeys, pitheciines, and aloutattines. As such, it opens a unique window into the early evolution and diversification of these primate groups. 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 total amount of annual rainfall. After establishing the paleolatitude and paleoelevation of the La Venta area, we estimate annual rainfall based upon the relationship between mammalian macroniche structure and rainfall guided by a comparison of 16 modern tropical lowland mammalian 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 exceeds 2000 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, the dominant vegetation is drought-resistant and deciduous. Areas of intermediate rainfall between 1000–2000 mm/year with 4–6 months of dry season tend to exhibit semideciduous forests, often as riparian galleries of variable width with intervening savannas. Given the generally 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 water deficit is difficult to define and not generally available from meteorological data. Not surprisingly, comparisons reveal that species richness (total number of species) and niche structure of modern mammalian faunas in lowland tropical environments vary in predictable ways 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, in particular total nonvolant species number, the number of primate species, and the numbers of frugivorous 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 been shown that the number of species recorded at any fossil locality is sensitive to the number of specimens recovered (Stuckey, 1990). Because trends relating the absolute number of species in a fossil assemblage to rainfall may be sensitive to paleontological sampling biases, only in the Monkey Beds (see below) do we feel that paleontological sampling begins to approximate total discoverable 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, including estimates of their body size, and dietary and locomotor adaptations. By means of a comparison of the macroniche structure of the Monkey Beds assemblage with general trends in the structure of modern mammalian faunas along a rainfall gradient, we derive an estimate of the annual rainfall at La Venta. Our estimate of total annual rainfall is examined in light of the available evidence about the autecology of environmentally sensitive vertebrate and mammal groups. This estimate of the annual rainfall is then discussed in terms of the general relationship between vegetation and rainfall in the equatorial lowlands of South America. Last we discuss and speculate about the nature of the vegetational mosaic at La Venta based on the available evidence for the presence of forest, riparian mosaic, the degree of canopy closure, and rainfall seasonality.

   

163

Paleogeography The fossil vertebrate assemblage from La Venta comes from rocks of the Honda Group exposed within a fault-bounded block in the central Magdalena river valley, at 3) North latitude, at a present elevation less than 500 m above mean sea level and a mean annual rainfall of about 1000 mm. The fluvial conglomerates, sandstones, silts and clays of the Honda Group attain a total thickness of approximately 1150 m (Guerrero, 1996). The geologic age of the fossiliferous Honda Group is constrained by radiometric and paleomagnetic evidence to a 1·7 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 Honda Group, 52 nonvolant mammal species occur in the richly fossiliferous Monkey Beds. The Monkey Beds measure about 14·8 m in thickness (Guerrero, 1996) and fall within the normal polarity interval N2 of the Honda Group magnetostratigraphic section, corresponding to Chron C5AA of the GMPTS (Flynn et al., 1996). The normal polarity interval of Chron C5AA spans 150,000 years (between 13·00–12·85 Ma), and in the Honda Group, the normal polarity interval of Chron C5AA is represented by 160 m of sediment, of which the Monkey Beds represent less than 10%. Therefore, the Monkey Beds fauna could sample a time interval of 15,000 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 and western Colombia, and western Venezuela formed a peninsula bordered on the west by the Pacific Ocean and on the north and east by the developing Caribbean Sea and the extensive epicontinental 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 infer that the La Venta area was at low elevation. Among the freshwater fish are many very large species and species that today inhabit slow-moving, lowland meandering rivers (Lundberg et al., 1986). Further, among the large turtles, Podocnemis occurs today only at elevations below 100 m (Pritchard & Trebbau, 1984; Lynch, 1979). The teid lizard Paradracaena from La Venta is morphologically intermediate between two extant taxa, Dracaena and Crocodilurus, that occur today 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 at La 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 because of a mountain induced rain-shadow effect. In the middle Miocene, the geography was more directly comparable with that of the eastern piedmont of Colombia because there was no significant elevation to the Eastern Cordillera (Hoorn et al., 1995; Guerrero, 1996) and Miocene sediments were deposited continuously across a lowland area east of the Central Cordillera (Campbell & Bürgl, 1965; Lundberg et al., 1986). The best estimate of the date of

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164

1

2 3 4 5 16

Equator 6

7

15

8 14 9 10

Tropic of Capricorn

13

12

11

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.

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 the Pliocene, did the Colombian Eastern Cordillera attain its present elevation (Hooghiemstra & Ran, 1994; Hammen & Cleff, 1986; Wiel, 1991). Post-middle Miocene episodes of mountain building 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 Venta is 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 follow Wilson & Reeder (1993). The sampling areas of these faunas represent a wide range of mean annual rainfall. At one extreme, in the eastern lowlands of Ecuador, rainfall is approximately 3500 mm/year with no appreciable dry season (Can˜adas, 1983). At the other extreme, in the Caatinga region of northeastern Brazil, annual rainfall is as low as 500 mm and the dry season exceeds 7 months (Streilein, 1982a). Our sample does not include faunas living in areas receiving in excess of 4000 mm, nor less than 500 mm annual rainfall.

22–24)S 22–24)S

4)47*S 1)N–5)S

Amazonas, Venezuela

Amazonas, Venezuela

Amazonas, Brazil

Pará, Brazil

Exu, Pernambuco, Brazil

Brasilia, Brazil

Mato Grosso, Brazil

Salta, Argentina

Madre de Dios, Peru

Amazonas, Peru

Oriente, Ecuador

(5) Esmeralda

(6) Manaus

(7) Belém

(8) Caatingas

(9) Federal District

(10) Acurizal

(11) Chaco

(12) Transitional Forest Salta, Argentina

Salta, Argentina

(4) Puerto Ayacucho

(13) Low Montane

(14) Cocha Cashu

(15) Rio Cenepa (Alto Maran˜on) (16) Ecuador Tropical

Numbers correspond to the locality map (Figure 1).

22)24*S

Apure, Venezuela

(3) Puerto Páez

12)S

17)45*S

15)57*S

7)31*S

1)27*S

2)30*S

3)05*N

5)15*N

6)23*N

8)34*N

Guarico, Venezuela

(2) Masaguaral

10)N

Latitude

Miranda, Venezuela

State (province), country

200–500

100–900

1100

200

10

10

130–1830

99–195

76

75

250–1430

700

1120

1586

<500

2600

2200

2000

2250

1500

1250

1500

Annual rainfall (mm)

Seasonal xerophyllous savanna grasslands and gallery forests (5 months) Pantanal; pastures, secondary forest, cerrado and deciduous forests (7 months) Subtropical, drought-resistant, thorn forest (9 months) Transitional deciduous forest with trees 20 to 30 m tall Lower montane moist forest (2 months)

Semideciduous, submontane to montane forest (6 months) Subtropical vegetational mosaic high savanna (6 months) Seasonally flooded high grass savanna with scattered patches of low forest and palms (6 months) Savannas of the Rio Orinoco and evergreen forest/savanna mosaic Nearly continuous evergreen forest in valley up to low dense montane forest Primary upland terra firme forest; (3 months) Vicinity of Belém, now urban and suburban (2 months) Semiarid caatinga (>7 months)

Vegetation; (estimated length of dry season in months)

Schaller, 1983

Mares et al., 1981; Streilein, 1982; Mares et al., 1985 Mares et al., 1989

Pine, 1973

Malcolm, 1990

Handley, 1976

Handley, 1976

Handley, 1976

Eisenberg et al., 1979

Eisenberg et al., 1979

References

Ojeda & Mares, 1989; Mares et al., 1989 64)W 350–500 700–900 Ojeda & Mares, 1989; Mares et al., 1989 64)W 500–1500 800 Ojeda & Mares, 1989; Mares et al., 1989 70)W 400 2000 Lowland floodplain rainforest (3 months) Janson & Emmons, 1990 78)17*W 210 2880 Abandoned fields, secondary regrowth Patton et al., 1982 riparian forest, undisturbed humid forest 75–78)W 0–800/1000 1795–4795 Amazonian lowland evergreen Albuja, 1991 rainforests

63)W

57)37*W

47)54*W

40)00*W

48)29*W

60)W

65)35*W

67)40*W

67)29*W

67)35*W

66)W

Longitude

Altitude (m)

Characteristics of the 16 modern lowland mammalian faunas of tropical South America

(1) Guatopo

Locality (fauna)

Table 1

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166

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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 locomotor mode we generally follow Fleming (1973) and Andrews et al. (1979) and recognize six categories; (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 locomotor categories; for example, ‘‘terrestrial’’ (combining large and small terrestrial) and ‘‘total arboreal’’ (combining arboreal and scansorial). We are not confident that it is possible to subdivide 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 diet categories; (1) vertebrate prey, (2) ants and termites, (3) insects with some fruit, (4) fruit with some 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 combinations of 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 with fruit-eaters is mainly forced by the quality of the data with which we are working: the diets of small rodents are for the most part so poorly known that the two categories cannot be readily discriminated 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 particular niche specialization or within a body size range) relative to total number of species. (1) The Frugivore Index expresses the proportion of frugivorous species to the total number of plant-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 with leaves, L=leaves (browse), and G=grass stems and leaves (graze). (2) A Browsing Index expresses the proportion of browsing or leaf-eating species to the total number of herbivorous plant-eating species in a fauna: 100#(L)/(L+G). (3) An Arboreality Index is used to express the proportion of arboreal species to the total number 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 II and 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 the number of species in each diet, locomotor, and body size class and the values of the four indices for the 16 modern faunas.

3000 2880 2600 2250 2200 2000 2000 1586 1500 1500 1250 1120 800 800 700 500 —

Rainfall (mm) 81 62 62 45 51 70 66 66 40 22 29 41 26 44 36 22 52

# Species 13 6 5 5 6 13 11 3 3 2 2 5 2 1 0 2 6

# Primates 41 31 28 26 29 42 42 27 10 18 12 20 8 12 6 6 19

# Frugivores 5 4 5 3 4 5 3 4 2 3 2 2 4 5 3 0 16

# Browsers 3 2 2 2 0 2 1 5 3 1 3 3 2 2 7 2 6

# Grazers 49 37 35 31 33 49 46 36 15 22 17 25 14 19 16 8 41

#1) Consumers 34 25 28 14 17 21 19 26 8 18 12 17 12 26 20 12 11

#2) Consumers

83·7 83·8 80·0 83·9 87·9 85·7 91·3 75·0 66·7 81·8 70·6 80·0 57·1 63·2 37·5 75·0 46·3

Frugivore index

The number of species in each macroniche category and index values for the 16 lowland tropical faunas used in the analyses

Ecuador Tropical Rio Cenepa Belém Puerto Ayacucho Manaus Cocha Cashu Esmeralda Federal District Guatopo Puerto Páez Masaguaral Acurizal Low Montane Forest Transitional Forest Chaco Caatinga Monkey Beds, La Venta

Locality

Table 2(a)

62·5 66·7 71·4 60·0 100 71·4 75·0 44·4 40·0 75·0 40·0 40·0 66·7 71·4 30·0 0·0 72·7

Browser index

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Ecuador Tropical Rio Cenepa Belém Puerto Ayacucho Manaus Cocha Cashu Esmeralda Federal District Guatopo Puerto Páez Masaguaral Acurizal Low Montane Forest Transitional Forest Chaco Caatinga Monkey Beds, La Venta

Locality

Table 2(b)

29 18 16 16 20 27 29 9 11 5 6 5 4 5 1 2 14

# Arboreal sp. 18 17 16 9 10 17 14 16 10 5 7 12 8 12 8 8 8

# Scansorial sp. 28 23 24 18 20 22 19 34 18 9 15 23 9 23 22 12 27

# Terrestrial sp. 58 56 52 56 59 63 65 38 52 45 45 41 46 39 25 45 42

Arboreality Index 15 11 10 7 10 10 17 25 12 6 6 7 8 11 6 4 6

# Size class I 27 15 17 13 12 24 17 14 6 3 3 6 4 5 7 4 5

# Size class II 28 25 25 16 20 23 24 17 15 9 14 15 10 23 14 12 18

# Size class III 10 8 9 8 7 11 6 10 5 5 6 10 3 5 7 1 14

# Size class IV

2 3 2 1 2 2 2 1 2 0 0 3 1 1 2 1 3

# Size class V

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

# Size class VI

33 24 27 29 24 34 26 21 15 13 10 15 15 11 19 18 11

Size index

168 . .   . . 

    Table 3

169

Spearman’s rank correlations (Spearman’s rho) between total annual rainfall and the numbers and percentages of extant species within various macroniche categories Rainfall versus:

Spearman’s rho

# Species # Primate species

P-value

0·758 0·815

0·0033 0·0016

0·837 0·507 "0·240 0·723 0·483 0·723 0·477

0·0012 0·0494 0·3530 0·0051 0·0612 0·0051 0·0645

Locomotion: # Arboreal species # Scansorial species # Terrestrial species Arboreality index

0·880 0·662 0·446 0·702

0·0007 0·0104 0·0842 0·0065

Body size: # Species, # Species, # Species, # Species, # Species, Size index

0·532 0·757 0·762 0·601 0·381 0·722

0·0292 0·0034 0·0032 0·0199 0·1396 0·0052

0·651 0·790 0·795 0·532 0·413

0·0117 0·0022 0·0021 0·0395 0·1098

Diet: # Frugivores # Browsers # Grazers # 1) Consumers # 2) Consumers Frugivore index Browser index

size class I size class II size class III size class IV size class V for all species

# Arboreal species vs. # Species, size class # Species, size class # Species, size class # Species, size class # Species, size class

I II III IV V

To avoid problems posed by the nonlinearity of the data, comparisons were made among the modern faunas using the nonparametric Spearman’s rank correlation (Spearman’s rho). Rank correlations were computed between rainfall and the numbers of species within each particular dietary, locomotor or body mass category. In these analyses, our criterion for acceptance of a null hypothesis was set at probability values less than or equal to 0.05. The results are presented in Table 3 and depicted as a series of bar charts with faunas arranged along 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 linear dimensions of the teeth and bones using least-squares regression models derived from homologous measures in their living relatives. Body masses for marsupials, rodents and primates were estimated from published equations for lower first molar crown area vs. body weight (Legendre, 1989; Conroy, 1987). Body mass estimates for armadillos and glyptodonts use regressions of carapace or cranial length vs. body weight from published measurements for living armadillos (Wetzel, 1985). Body mass estimates for sloths and anteaters are based on a

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170 Table 4

Hypothesized macroniche specializations for nonvolant mammal species present in the Monkey Beds (Honda Group) La Venta area

Species

Diet

Substrate

Body weight

Marsupials Pachybiotherium minor Micoureus laventicus Thylamys colombianus Thylamys minutus Hondadelphys fieldsi Arctodictis sp. Lycopsis longirostrus

IF IF IF IF IF Ve Ve

AT A A A T T T

I I I I III IV IV

Primates Neosaimiri fieldsi Cebupithecia sarmientoi Nuciraptor rubrens Mohanamico hershkovitzi Callitrichidae sp. a Stirtonia tatacoensis

FI FL FL FL FI L

A A A A A A

II III III II II III

Rodents Echimyidae Gen et. sp. indet a ? Echimyidae incertae sedis Acarechimys cf. minutissimus ‘‘Olenopsis’’ sp. large ‘‘Scleromys’’ colombianus ‘‘Scleromys’’ schurmanni Microscleromys paradoxalis Dinomyidae inc. sedis (cf. Simplimus) sp. ‘‘Neoreomys’’ huilensis Microsteiromys jacobsi Steiromys sp. large Steiromys sp. small Prodolichotis pridiana Dolichotinae Gen. et. sp. a (large) Dolichotinae Gen. et. sp. a (small)

S S S FL FL FL S FL S FL FL FL G G G

AT AT AT T T T T A(T) T A A A T T T

II I I IV III III II IV III II III III III III III

Continued on next page

regression of distal femur bicondylar width vs. body weight for living sloths and anteaters. Body masses 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 to body 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 fossil mammals with close living relatives (some marsupials, rodents, armadillos and primates), we make dietary and locomotor assignments with more confidence than for fossil mammals with no, or only distantly related, living relatives (sloths, glyptodonts). For fossil herbivorous mammals with no living relatives (litopterns, notoungulates, astrapotheres), the hypsodonty index of Janis (1988) was used to assign species with rooted cheek teeth to frugivore–herbivore

    Table 4

171

Continued from previous page

Species

Diet

Substrate

Body weight

Litopterna Prolicaphrium sanalfonsensis Prothoatherium colombianus Megadolodus molariformis Theosodon sp.

L FL FL L

T T T T

IV III V V

Notoungulata Miocochilius anomopodus Huilatherium pluriplicatum Pericotoxodon platignathus

G L G

T SAq T

III VI VI

Astrapotheria Xenastrapotherium kraglievichi Granastrapotherium snorki

L L

SAq SAq

VI VI

Myr L L L L L L IF L Myr L L L G Myr

AT AT A AT A T T T T T T T T T T

IV IV IV IV III IV — III V III IV IV IV IV III

Xenarthra Neotamandua borealis cf. Hapalops Neonematherium flabellatum Nothrotheriinae (small) a Glossotheriopsis pascuali Megalonychidae gen et sp. indet., small Megatheriinae gen et sp. indet. Anadasypus hondanus Pseudoprepotherium confusum Pedrolypeutes praecursor Scirrotherium hondaensis Asterostemma gigantea Asterostemma ?acostae Neoglyptatelus originalis Nanoastegotherium prostatum

Symbols: dietary categories: FI=fruit with some invertebrates, S=small seeds of grasses and other plants, FL=fruit with some leaves, L=leaves (browse), and G=grass stems and leaves (graze), IF=primary insects with some fruit, Ve=primarily vertebrate prey, Myr=ants and termites. Locomotor or substrate preference: A=arboreal, AT=arboreal and terrestrial (scansorial), T=terrestrial and fossorial, and SAq=semiaquatic. Body size classes: I=less than 100 g; II=100–1000 g; III=1000 g to 10 kg; IV=10–100 kg; V=100– 500 kg; VI= >500 kg.

or folivore (browsing) classes. Fossil herbivores with ever-growing cheek teeth were assigned to the 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 Miocene Monkey Beds. These estimates are made using simple least-squares regression and secondorder polynomial regression. The results presented in Table 5 and Figure 9 are discussed below. To examine the relative contributions of different aspects of macroniche structure to the prediction of annual rainfall, principal components analysis was undertaken using species counts 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).

. .   . . 

172

90 80

Total speccies

70 60

Spearman's rho = 0.759 P–value < 0.003

50 40 30 20 10 0

High

Medium Low Locality grouped by rainfall

Very low

Figure 2. Histogram of the total number of nonvolant mammalian species in 16 localities from the tropical lowlands of South America ranked by total annual rainfall. The arrangement of the localities from left to right is in the order of decreasing rainfall, as follows: Ecuador Tropical, Rio Cenepa, Belém, Puerto Ayacucho, 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 for the purposes of statistical analysis, localities are grouped by total annual rainfall: High, greater than 2500 mm/year; medium, 2000–2500 mm/year; low, 1000–2000 mm/year; very low, less than 1000 mm.

Results Modern South American mammalian faunas Thirteen statistically significant rank correlations are found between mean annual rainfall and the 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 the number of mammalian species (species richness) and rainfall (Figure 2). At the extremes of the rainfall range of our sample of modern faunas, there are 82 nonvolant mammalian species in the Ecuadorian Oriente, whereas there are just 22 species in the Caatinga of northeastern Brazil. The high correlation of species richness with rainfall appears to be the result of several contributing factors. First, there are far greater numbers of arboreal and scansorial species in wet environments than in dry environments (Figure 3, top). This is confirmed by the significant positive correlation of our arboreality index with rainfall (rho=0·702, P>0·0065).

   

30

173

Spearman's rho = 0.880 P = 0.0007

Arboreal species

25 20 15 10 5 0

Scansorial species

20

Spearman's rho = 0.662 P = 0.01

15 10 5 0 35

Spearman's rho = 0.446 P = N.S.

Terrestrial species

30 25 20 15 10 5

Other

0 Spearman's rho = 0.315 P = N.S. 5 0

High Medium Low Very low Localities grouped by rainfall

Figure 3. The number of arboreal, scansorial, terrestrial and other (semiaquatic, fossorial) mammalian species in 16 localities from the tropical lowlands of South America ranked by total annual rainfall. For further information, see Figure 2.

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174 14

Spearman's rho = 0.815 P = 0.002

Number of primates

12 10 8 6 4

0

2 0

High

Medium Low Very low Localities ranked by rainfall

Figure 4. The number of primate species in 16 localities from the tropical lowlands of South America ranked by total annual rainfall. For further information, see Figure 2.

Substrate preference. By contrast, there is no significant correlation in the number of terrestrial species (nor in the number of either fossorial or semiaquatic species) with rainfall. Wet environments supporting evergreen forests (for example, at Rio Cenepa and Esmeralda, see Table 1) always have more arboreal species than dryer environments with either semideciduous gallery forest (Federal District) or thorn forest (Caatinga). The number of arboreal species ranges from between 20–32 in tropical evergreen forests whereas in tropical savanna mosaics and thorn forests there are one to six arboreal species (see Table 2). Primate species richness. There is an especially high and significant positive correlation between the number of arboreal primate species and rainfall (rho=0·815, P<0·0016), as noted by others (Fleagle et al., 1996; Reed & Fleagle, 1995). In high- and medium-rainfall areas (>1800 mm annual rainfall), five to 13 primate species are present whereas in low and very 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 high rainfall 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 primary consumers in general (rho=0·723, P<0·0051) [Figure 6(a)]. Among primary consumers there is 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 correlation with rainfall is the number of grazing species. The weak tendency (an insignificant rho= "0·24) for there to be more species of grazing mammals in drier environments in the inter-tropical lowlands of South America probably relates to the fact that savanna grasses are more plentiful in these environments. Intriguingly, no significant trend between species richness and rainfall characterizes secondary consumers. There appear to be as many carnivorous and insectivorous species in dry environments as there are in wet environments (rho=0·483, P<0·0612) [Figure 6(b)].

   

175

45 40 35

Total fruit eaters

30 25 20 15 10 5 0

High

Medium Low Very low Localities ranked by rainfall

Figure 5. The number of fruit-eating species in 16 localities from the tropical lowlands of South America ranked by total annual rainfall. For further information, see Figure 2.

Body size. Several significant correlations are found in the pattern of body size distribution among mammalian species in relation to rainfall (Table 3). First, there is a significant positive correlation between rainfall and the number of very small- to medium-sized species (body size classes I–IV, between 10 g to 100 kg) but no significant correlation with the number of large species (body size class V, >100 kg). A closer look reveals that there is a significant correlation between rainfall and the number of arboreal species within the very small to medium-sized class range. Arboreal species comprise the largest component of these size classes, especially for classes II and III (between 100 g and 10 kg) (see Figure 7). Indices. Three (Frugivore, Arboreality, Size) of the four indices we investigated are significantly positively correlated with rainfall. Frugivorous species account for a larger proportion of the total number of nonvolant species in wetter environments. The Frugivore Index, expressing the proportion of frugivorous species to the total number of plant-eating species or primary 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 of arboreal 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.

. .   . . 

176 (a)

Spearman's rho = 0.820; P < 0.002

Total primary consumers

50 45 40 35 30 25 20 15 10 5 0

High

Total secondary consumers

(b)

Medium Low Very low Localities ranked by rainfall

Spearman's rho = 0.483; P = N.S.

35 30 25 20 15 10 5 0

High

Medium Low Very low Localities ranked by rainfall

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 annual rainfall. For further information, see Figure 2.

Finally, only a weak and statistically insignificant relationship occurs between rainfall and the 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)].

   

177

10

Size class I

8 6 4 2 0 14

10 Size class II

Number of arboreal species

12

8 6 4 2 0 14

Size class III

12 10 8 6 4 2 0

High Medium Low Very low Localities ranked by rainfall category

Figure 7. The number of arboreal species of different size classes in 16 localities from the tropical lowlands of South America ranked by total annual rainfall. For further information, see Figure 2.

To examine the collective effects of the species counts and four indices, a principal components analysis was undertaken. Two factors account for nearly 86% of the total variance, with the first explaining 66% of the variance (Table 5). Factor loadings on the first principal components are all positive with the greatest influence attributed to the Arboreality Index and the Frugivore Index. The value of the factor scores on the first principal component show 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 above 1800 mm and areas with less than 1800 mm of rainfall. No separation was obtained between environments with medium (1800–2500 mm) and high rainfall (2500–3500 mm).

. .   . .  100 90 80 70 60 50 40 30 20 10 0

(a)

70 Arboreality index

Frugivore index

178

40 30 20

35

(d)

30 Size index

Browser index

50

0

100 80 60 40

0

60

10

(c)

20

(b)

0

25 20 15 10 5

0 Localities ranked by rainfall

Figure 8. Distribution of index values in 16 localities from tropical South America ranked by total annual rainfall. (a) Frugivore Index; (b) Arboreality Index; (c) Browsing Index; (d) Size Index. For further information, see Figure 2.

The Monkey Beds mammalian community Simple least-squares regression and second-order polynomial regressions of rainfall on species richness, diet, locomotor and body size classes are used to derive rainfall estimates for the time of deposition of the Monkey Beds (Table 6). For simple least-squares regression, these estimates range from as low as 553 mm to as high as 5440 mm. For polynomial regression the estimates range from as low as 650 mm to as high as 2333 mm. Frequency histograms of the rainfall estimates derived from both simple least squares and polynomial regressions reveal similar modal estimates of annual rainfall. The modal estimates are between 1500 and 2000 mm, with mean 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 may reflect the extraordinary high number of browsing species in the Monkey Beds assemblage (see below). The low estimates given by the Size Index reflect the lower number of very small mammal species than one would expect based on modern faunas, conceivably a problem of sampling bias or the pre-Interchange age of the La Venta fauna (i.e., before the arrival of muroid 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 highly positively correlated with rainfall today. Comparisons with modern faunas suggest that small scansorial species may be under-represented in the Monkey Beds assemblage. This is confirmed 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 than 1500 mm annual rainfall. The Monkey Beds fauna has 40% or more species than Masaguaral

    Table 5(a)

179

Eigenvalues and factor loadings from principal components analysis of 16 modern South American faunas Eigenvalues Value Value Value Value Value Value Value

1 2 3 4 5 6 7

Magnitude

Variance Prop.

9·58 1·79 1·08 0·54 0·46 0·23 0·14

0·68 0·13 0·08 0·04 0·03 0·02 0·01

Table 5(b)

Number of Primates Arboreality index Total fruit eaters Browser Total primary consumers Total secondary consumers Size class 2 Size class 3 Size class 4 Frugivore Index Browser/Grazer Index Size Index Total species Arboreal

Factor 1

Factor 2

Factor 3

0·905 0·730 0·971 0·666 0·980 0·658 0·956 0·855 0·713 0·670 0·588 0·857 0·935 0·942

"0·267 "0·626 "0·133 0·548 0·010 0·639 0·074 0·216 0·355 "0·554 0·009 "0·071 0·212 "0·262

"0·149 0·179 "0·016 0·447 "0·042 "0·030 "0·219 "0·002 "0·227 0·083 0·788 "0·265 "0·160 0·013

(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 mean annual rainfall predicts 1810 mm of rainfall for the Monkey Beds assemblage. Based on the number 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 by a relatively high number of mammalian primary consumers. By this measure, the Monkey Beds environment had an annual rainfall of about 2291 or 2333 mm. Based upon the percentage of arboreal species in the Monkey Beds assemblage, leastsquares regression predicts an annual rainfall of 1756 mm, a value that is similar to the predicted 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-one percent of the nonfrugivorous herbivores in the Monkey Beds assemblage are browsers (Table 2), 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 rainfall levels for the Monkey Beds of 1961 and 1968 mm.

0·593 0·0005 0·487 0·0026 0·675 <0·0001 0·286 0·0330 0·101 0·2315 0·664 0·0001 0·292 0·0307 0·678 <0·0001 0·440 0·0051 0·180 0·1013 0·636 0·0002 0·529 0·0014 0·377 0·0114 0·162 0·1224 0·610 0·0019 0·454 0·0042 0·317 0·0231 0·479 0·0030 minus one standard error)

P-value 1810 1811 1446 5440 1133 2291 1166 1756 1205 2026 1164 1656 2901 2178 1291 553 1961 889 1818&251 mm

0·594 0·648 0·740 0·291 0·106 0·705 0·567 0·823 0·516 0·219 0·669 0·558 0·640 0·163 0·662 0·509 0·340 0·479

Multiple Rsquared 0·0029 0·001 0·0002 0·1067 0·4814 0·0004 0·0807 <0·0001 0·0089 0·1998 0·0008 0·0049 0·0324 0·3149 0·0093 0·0098 0·0674 0·0144

P-value for 2nd order polynomial

1780 2212 1694 1253 1095 2333 1272 2138 1195 2007 1125 1503 2056 2222 1263 650 1968 899 1593&122 mm

Predicted rainfall at La Venta (mm) from 2nd-order polynomial regression

Note: With the exception of the number of grazing species, predicted rainfall is not reported when correlation between the variable and rainfall is less than 0·05. Indices are defined in the text.

# Species # Primate species # Frugivores # Browsers # Grazers # 1) Consumers # 2) Consumers # Arboreal species # Scansorial species # Terrestrial species # Species, size class II # Species, size class III # Species, size class IV # Species, size class V Arboreality Index Frugivore Index Browser Index Size Index Mean estimated rainfall for La Venta (plus or

r2

Predicted rainfall at La Venta (mm) from simple regression

Estimated annual rainfall at the time of deposition of the Monkey Beds based on a simple least-squares regression and second-order polynomial regressions on the absolute numbers of nonvolant mammals in various macroniches and indices as defined in the text

Rainfall (dependent variable) versus:

Table 6

180 . .   . . 

   

181

Mean annual rainfall (mm)

3500 3000

95% confidence interval for rainfall estimate

2500 2000 1500 1000

Monkey Beds PCI = 288

500 0 150

200 300 400 250 350 450 First principal component (68.4% of variance)

500

Figure 9. Bivariate plot of the first principal component vs. rainfall for 16 localities from tropical South America. See text for further explanation. No separation is obvious between environments with medium and high rainfall (2000–2500 mm/year vs. 2500–3500 mm/year). Most of the discrimination occurs between these two categories on one hand, and faunas from areas with less than 2000 mm/year.

Discussion Rainfall gradients and modern mammalian faunas A number of general trends have emerged in comparisons of mammalian species diversity in tropical South America in relation to rainfall. There is an overall enrichment of the number of species in wetter environments. This is probably related to the generally increased productivity, structural complexity and lack of seasonality of mature vegetation in wet tropical environments 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 of primary 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 the size classes within which arboreal locomotion is favored. Our analysis reveals a preponderance of arboreal species in size classes II and III (and not in size classes I and IV), and as recently demonstrated by Malcolm (1995), this is correlated with the physical constraints of arboreal habitat, 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 locomotion between widely-dispersed food sources separated by gaps in the canopy and understory may be too great. For large species an upper size-limit may be imposed by the physical strength of the supporting stems and branches (Christoffer, 1987). Thus, selection may favor a fairly narrow range of body sizes for arboreal species (Emmons, 1995). This finding accords with the observations of Legendre (1989) who emphasizes the presence of such a relationship for many communities 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 Cenozoic environments (Gingerich, 1989; Legendre, 1986, 1989; Gunnell, 1994). Summarizing

182

. .   . . 

worldwide data for modern mammalian communities that differ in habitat or vegetation structure and annual rainfall, Legendre (1986, 1989) shows that mammalian faunas from drier environments 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 show a similar phenomenon, with there being more species of size classes II and III (roughly equivalent to the size range mentioned above) in wetter than in drier environments. None of the above authors suggest any explanation for why there should be so many more species within this size range, but a plausible explanation may relate to the constraints on size imposed by 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 browsing species with rainfall in modern faunas may be explained by the increase in arboreal plant biomass with rainfall (Fittkau & Klinge, 1973), floristic diversity (Gentry, 1988) and year-round availability of canopy food resources (Terborgh, 1986) (at least within the rainfall range assessed here). Total mammalian species richness and the number of arboreal and scansorial species is known to be significantly positively correlated with habitat complexity, foliar-height diversity and vertical complexity in the tropics (Da Fonseca & Redford, 1983; Redford & Da Fonseca, 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 of the dry season. Despite these relationships, there are problems with predicting the predominant mature vegetation in that portion of the dry tropical life zone receiving between 1500 and 2000 mm of annual rainfall. It is in this rainfall range where the transition between open savanna, deciduous forest and evergreen forest occurs. In our data set, five localities receive between 1500 and 2000 mm annual rainfall: Cocha Cashu, Esmeralda, Federal District, Guatopo, and Puerto Páez. While all five localities experience some degree of rainfall seasonality, the length of the dry season and its influence on vegetation structure and food availability is highly variable. Puerto Páez (Venezuela) and Federal District (Brazil) both receive about 1500 mm of rainfall, and both are characterized by climates with seasonal rainfall and semi-deciduous gallery forests restricted to the margins of permanent streams, with extensive savanna grasslands in the interfluvial areas. Between 1500 and 2000 mm, the proportion of forest and savanna reverses. Localities with rainfall at or above 2000 mm are characterized by evergreen forest. While the evergreen forest canopies at localities with greater than 2000 mm of rainfall are usually continuous or nearly continuous, savanna of variable 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 Venta fauna than in the extant faunas: 15 species of browsers at La Venta vs. 0–5 species in modern Neotropical faunas. Our subjective impression is that the La Venta fauna is similar to tropical faunas of Africa and Asia in terms of the richness of browsers. In Africa and Asia, unlike in South America, there is a far greater number of sympatric species of browsers in most or all habitats, 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 at La Venta, that deserves further investigation.

   

183

A correlated phenomenon has to do with the absence in the modern Neotropical faunas of very 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 modern Neotropics. It is tempting to suggest that these apparent peculiarities of the Neotropical faunas are causally linked and have to do with recent faunal extinctions, for late Pleistocene faunas included many larger possible browsers such as elephants, litopterns, horses, glyptodonts, and giant 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 (as summarized by Kay & Madden, 1996) provide strong evidence for forest cover at the time of deposition. These include (1) the freshwater fish Colossoma macropomum, a frugivore that exploits flooded flood plain forest, (2) forest leaf-litter inhabiting snakes, (3) the forest-dwelling land tortoise Geochelone, (4) forest-dwelling jacamar (Galbula) and hoatzin (Opisthocomus) among the birds, (5) diverse arboreal marsupials, (6) numerous small sloth species, some with arboreal and/or climbing adaptations, (7) close taxonomic affinities between some armored edentates and most rodent species with living species that are forest-dwelling, (8) four litoptern species with low-crowned teeth associated with frugivory or browsing (leaf-eating) habits, (9) only two ungulate species with high-crowned cheek teeth, (10) bats known to roost and forage in multistratal 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 evidence is consistent and indicates that terrestrial forest biotopes occurred in the La Venta area during the 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 mosaic rather than a continuous-canopy, evergreen rainforest. The factors that contributed to create this 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 maintenance of vertebrate diversity in humid and wet tropical life zones is significant (Remsen & Parker, 1983). Evidence for diverse riparian aquatic environments is abundantly indicated at La Venta by the diverse freshwater fish (13 families and 23 species). The aquatic environments these fish represent include large, open river and in-shore habitats, marginal shallow waters, and relatively still, even anoxic, temporary waters. Reflecting this habitat heterogeneity, the fish fauna presents correspondingly wide dietary diversity, including algivores, detritivores, carnivores, etc. and frugivore/granivores (Lundberg et al., 1986). The heterogeneous aquatic environments 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 only in the biotically rich, complex, heterogeneous riparian environments of the wet tropical lowlands 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 La Venta fauna inhabited riparian environments (Rasmussen, 1996). Anhinga anhinga (Anhingidae), a riparian piscivore, today inhabits freshwater marshes in both the Amazon and Orinoco river systems. Aramus guarauna prefers heavily vegetated freshwater marshes, wooded swamps, and other similar fluvial wetlands. The living hoatzin (Opisthocomus hoazin), similar to the extinct Hoazinoides from La Venta, is an obligate folivore and not a proficient flier. This species occurs today only along the forested banks of rivers and streams in the Orinoco and Amazon systems. 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 Cocha Cashu (Terborgh, 1983; Salo et al., 1986; Foster, 1986, 1990; Janson & Emmons, 1990) and at La Macarena in Colombia (Hirabuki, 1990). Canopy continuity. Having established the presence of arboreal vegetation within the meander belt at the time of deposition of the Monkey Beds, and annual rainfall levels between 1500 and 2000 mm, we can only speculate on the extent or continuity of the forest canopy in the interfluvial 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 include Diclidurus (Emballonuridae), an extant aerial-pursuit insectivore that usually roosts and forages in multistory evergreen forests, and the extant phyllostomine Tonatia, an aerial foliage-gleaning insectivore that forages and roosts in mature evergreen forests and deciduous forests. Two species of Thyroptera (Thyropteridae) are found in the La Venta fauna. These are aerial pursuit insectivores that use slow, maneuverable flight and forage and roost in lowland forest edges, in tree 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, the Callitrichidae (sensu Rosenberger et al., 1990) is represented by three species. Lagonimico conclucatus, weighed about 1 kg and displays dental characters suggesting a diet of gum- and fruit-eating (Kay, 1994). Patasola magdalenae, of intermediate in body size between Saimiri and living 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 as preferring edge habitat (Soini, 1993; Rylands & de Faria, 1993; Garber, 1993). The presence of two pitheciines in the Monkey Beds suggests the presence of flooded high forest within the meander belt. The absence at La Venta of large, soft-fruit eaters usually associated with high terra 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-like microbiothere Pachybiotherium, whose closest living relative Dromiciops is a forest or forest-edge dwelling animal. Carlini et al. (1996) suggest that the high diversity of armored xenarthrans at La Venta suggests a remarkable degree of environmental heterogeneity at La Venta, unlike that found today in the continuous evergreen rainforests of the humid and wet tropics. The remarkable diversity of Cingulata at La Venta is also a strong argument for habitat heterogeneity and canopy discontinuity in the interfluvial area. Armadillos are not commonly found 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

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grassland, if present, was of reduced extent and that the forest was probably characterized by both abundant low foliage and also fruit-bearing trees. Finally, the vegetation mosaic at La Venta may have been modified by the destructive habits of the four species of large (body size class VI) and tusked herbivores, some displaying microwear features associated with branchstripping behaviors (Johnson & Madden, 1996). Thus, there is limited paleontological evidence for the presence of continuous canopy evergreen forest. Most, if not all, of the available evidence is consistent and strongly suggests an extensive vegetational mosaic and significant forest understory. The suggestive evidence for abundant low vegetation during the middle Miocene at La Venta may confirm the important historical component to the understory flora of Neotropical forests (Gentry & Emmons, 1987). Seasonality. Although the empirical evidence for fruit and foliar phenology is not extensive across the tropics, seasonality in the supply of food resources for primary consumers is considered to be a common feature of all lowland tropical environments, even in the wettest, meteorologically aseasonal, equatorial rainforests (Howe, 1984; Terborgh, 1986). It is our contention that while seasonal factors may conceivably have influenced plant phenology and food supply at La Venta in the Miocene, seasonal rainfall was probably only of secondary importance in determining the structural configuration and complexity of forest habitats. Although somewhat equivocal, the available sedimentologic evidence does not indicate pronounced rainfall seasonality (see Guerrero, 1996). Evidence for periodic flooding during deposition of the Honda Group is abundantly indicated by the predominance of overbank sediments. Periodic flooding is also suggested by the presence of freshwater fish that can survive 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 not necessarily imply a seasonal water deficit of sufficient duration to have affected vegetation structure. The fluvial sediments of the Honda Group do not display features generally associated with prolonged seasonal water deficits and savanna landscapes, such as hardened and cracked surfaces, evidence of wind erosion, alteration by fire, evaporation, hardpan, impeded drainage, slow chemical weathering, and low root biomass. The lack of sedimentologic evidence in the Honda Group for pronounced seasonality suggests that climatic seasonality was relatively insignificant in terms of vegetation structure during the middle Miocene at La Venta. Uplift of the eastern Cordillera and its effects on climate. As noted, the geographic setting of the La Venta area has been profoundly modified since Miocene times by the uplift of the Eastern Cordillera and its attendant effects on climate. Where formerly, the La Venta region was situated 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 piedmont region of Colombia. Today, northeastern Colombia experiences a seasonal pattern of atmospheric circulation involving an intensification of the northeast trade winds and a southern shift of the intertropical convergence under the influence of the northern hemisphere winter (Rudloff, 1981). In response to the increasing seasonality of precipitation, the predominant plant cover in eastern Colombia changes from forest to savanna northward. Accompanying the increasing seasonality from south to north is the gradual replacement of the architecturally complex, closed-canopy, continuous evergreen rainforest of Colombian Amazonia, by open tropical savannas with narrow deciduous riparian gallery forests of the Colombian llanos in the Orinoco drainage. Tropical savannas occur in areas where total

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annual rainfall is between 1000 and 2000 mm and rainfall is seasonal, with dry periods lasting 6 months or longer. Given our estimates of total annual rainfall and the lack of strong evidence for rainfall seasonality, it would appear that areas of extensive savanna were probably restricted 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 Miocene when the Eastern Cordillera was low and discontinuous, and the major climate-modifying barrier would have been the Central Cordillera. The westward shift of this gradient would explain why our rainfall estimates for the middle Miocene are substantially higher than those at La Venta today. Even allowing for a westward shift in this rainfall gradient, our estimates of rainfall levels between 1500 and 2000 mm seem too low by comparison with rainfall levels today east of the Andes. Based on equatorial areas of Colombia today with comparable proximity to the Cordillera, annual rainfall levels at La Venta should have been greater than 3000 mm. The latter level of rainfall supports continuous-canopy evergreen rainforest 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 to speculate whether the preponderant reason for the difference between observed and expected rainfall is related to Andean uplift or to some other global influence, the departure is noteworthy.

Summary A comparison of the species richness and composition of diet, locomotor and body size classes among 16 modern nonvolant mammalian faunas in tropical South America reveals numerous significant positive correlations with rainfall. 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 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 mm annual rainfall for the middle Miocene 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 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 probably post-date the initiation of Andean uplift.

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Nutall, C. P. (1990). A review of the Tertiary non-marine molluscan faunas of the Pebasian and other inland basins of north-western South America. Bull. Brit. Mus. Nat. Hist., Geol. 45, 165–371. Ojeda, F. A. & Mares, M. A. (1989). A biogeographic analysis of the mammals of Salta Province, Argentina. Special Publications, Museum of Texas Tech University 27, 1–66. Patton, J. L., Berlin, B. & Berlin, E. A. (1982). Aboriginal perspectives of a mammal community in Amazonian Peru: knowledge and utilization patterns among the Aguaruna Jívaro. In (M. A. Mares & H. H. Genoways, Eds) Mammalian Biology in South America, pp. 111–128. Pymatuning Laboratory of Ecology, Special Publications Series, Vol. 6. Linesville: University of Pittsburgh. Pine, R. H. (1973). Mammals (exclusive of bats) of Belém, Pará, Brazil. Acta Amazonica 3, 47–79. Pritchard, P. C. H. & Trebbau, P. (1984). The Turtles of Venezuela. Contributions to Herpetology, Society for the Study of Amphibians and Reptiles. Räsänen, M. E., Linna, A. M., Santos, J. C. R. & Negri, F. R. (1995). Late Miocene tidal deposits in the Amazonian foreland basin. Science 269, 386–390. Rasmussen, D. T. (1996). Birds. In (R. E. Kay, R. H. Madden, R. L. Cifelli & J. J. Flynn, Eds) Vertebrate Paleontology in the Neotropics: The Miocene Fauna of La Venta, Columbia. Washington D.C.: Smithsonian Institution Press. Redford, K. H. (1985). Food habits of armadillos (Xenarthra: Dasypodidae). In (G. G. Montgomery, Ed.) The Evolution and Ecology of Armadillos, Sloths, and Vermilinguas, pp. 429–437. Washington D.C.: Smithsonian Institution Press. Redford, K. H. & Da Fonseca, G. A. B. (1986). The role of gallery forests in the zoogeography of the Cerrado’s non-volant mammalian fauna. Biotropica 18(2), 126–135. Redford, K. H. & Eisenberg, J. F. (1992). Mammals of the Neotropics: Volume 2, The Southern Cone, Chile, Argentina, Uruguay, Paraguay. Chicago: The University of Chicago Press. Reed, K. E. & Fleagle, J. G. (1995). Geographic and climatic control of primate diversity. Proc. Natl. Acad. Sci. USA 92, 7874–7876. Remsen, J. V., Jr. & Parker, T. A., III. (1983). Contribution of river-created habitats to bird species richness in Amazonia. Biotropica 15(3), 223–231. Rivero-Blanco, C. & Dixon, J. R. (1979). Origin and distribution of the herpetofauna of the dry lowlands regions of northern South America. In (W. E. Duellman, Ed.) The South American Herpetofauna; Its Origin, Evolution, and Dispersal, pp. 218–240. Lawrence, Kansas: University of Kansas Museum of Natural History. Robinson, J. G. & Redford, K. H. (1986). Body size, diet and population density in Neotropical forest mammals. Am. Nat. 128, 665–680. Robinson, J. G. & Redford, K. H. (1989). Body size, diet and population variation in Neotropical forest mammal species; predictors of local extinction? In (K. H. Redford & J. F. Eisenberg, Eds) Advances in Neotropical Mammalogy, pp. 567–594. Gainesville, Florida: Sandhill Crane Press. Rodríguez, G. (1996). Trichodactylid crabs. In (R. F. Kay, R. H. Madden, R. L. Cifelli & J. J. Flynn, Eds) Vertebrate Paleontology in the Neotropics: The Miocene Fauna of La Venta, Colombia. Washington D.C.: Smithsonian Institution Press. Rosenberger, A. L., Setoguchi, T. & Shigehara, N. (1990). The fossil record of callitrichine primates. J. hum. Evol. 19, 209–236. Rudloff, W. (1981). World Climates. Stuttgart: Wissenschaftliche Verlagsgesellschaft mbH. Rylands, A. B. & de Faria, D. S. (1993). Habitats, feeding ecology, and home range size in the genus Callithrix. In (A. B. Rylands, Ed.) Marmosets and Tamarins; Systematics, Behaviour, and Ecology, pp. 262–272. Oxford: Oxford University Press. Salo, J., Kalliola, R., Häkkinen, I., Mäkinen, Y. & Niemelä, P. (1986). River dynamics and the diversity of Amazon lowland forest. Nature 322, 254–258. Schaller, G. B. (1983). Mammals and their biomass on a Brazilian ranch. Arquivos Zool., Sao Paulo 31(1), 1–36. Schwerdtfeger, W., Ed. (1976). Climates of Central and South America. In (H. E. Landsberg, Ed. in Chief) World Survey of Climatology, Vol. 12. Amsterdam: Elsevier Scientific Publishing Company. Snow, J. W. (1976). The climate of northern South America. In (Schwerdtfeger, W., Ed.) Climates of Central and South America. In (Landsberg, H. E., Ed-in Chief) World Survey of Climatology, Volume 12, pp. 295–403. Amsterdam: Elsevier Scientific Publishing Company. Soini, P. (1993). The ecology of the pygmy marmoset, Cebuella pygmaea: Some comparisons with two sympatric tamarins. In (A. B. Rylands, Ed.) Marmosets and Tamarins; Systematics, Behaviour, and Ecology, pp. 257–261. Oxford: Oxford University Press. Stehli, F. G. and Webb, S. D. (1985). The Great American Boitic Interchange. New York: Plenum Publishing Company. Stevenson, M. F. & Rylands, A. B. (1988). The marmosets, genus Callithrix. In (R. A. Mittermeier, A. B. Rylands, G. A. B. da Fonseca and A. F. Coimbra-Filho, Eds) Ecology and Behavior of Neotropical Primates, II, pp. 131–222. Washington D.C.: World Wildlife Fund. Stevenson, P. R., Quin˜ones, M. J. & Ahumada, J. A. (1994). Ecological strategies of woolly monkeys (Lagothrix lagotricha) at Tinigua National Park, Colombia. Am. J. Primatol. 32, 123–140. Streilein, K. (1982a). Ecology of small mammals in the semiarid Brazilian Caatinga. I. Climate and faunal composition. Ann. Carnegie Mus. 51(5), 79–107.

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Mustelidae

Felidae

0 0 0 0 0 0 0 1 1 0 0 0 1 1 0 1 1 0 0 0 0 0

0 1 0 0 0 0 0 1 1 0 0 0 0 1 0 1 1 0 1 0 0 0

0 1 0 0 0 0 0 1 1 0 0 0 0 0 0 0 0 0 0 0 0 1

0 1 0 0 0 0 0 1 1 0 0 0 0 0 0 0 1 0 0 0 0 0

4

0 0 1 0 0 0 0 0

0 1 0 0 1 0 1 1

1 1 1 0 1 0 1 1

1 0 1 0 1 1 1 0

0 1 1 0 0 0 1 0

0 0 0 0 0 0 0 0 1 0 1 0 1 0 0 0 1 0 0 1 0 0

0 0 0 0 0 0 1 0 0 0 0 0 1 1 0 0 1 0 0 1 0 0

6 0 1 0 0 0 0 1 1 1 1 1 0 1 1 0 0 1 0 1 1 1 1

7 0 1 0 0 0 0 0 1 0 0 0 0 1 0 0 1 0 0 1 0 0 0

8 0 1 1 0 0 0 1 1 1 0 0 0 0 1 0 0 1 0 0 0 0 0

9 0 1 1 0 0 0 0 1 1 0 0 0 1 1 0 0 1 0 0 1 0 0

10 0 1 0 1 1 0 0 1 0 0 0 1 1 1 1 0 0 1 0 0 0 0

11 0 1 0 1 1 0 0 1 0 1 1 1 0 1 1 0 1 1 0 1 0 0

12 0 1 0 0 0 0 0 1 0 0 0 0 0 1 0 0 1 0 0 1 0 0

13

0 1 0 0 0 0 0 0

13

Atelocynus microtis Cerdocyon thous Chrysocyon brachyurus Pseudalopex griseus Pseudalopex gymnocercus Pseudalopex vetulus Speothos venaticus Herpailurus yaguaroundi Leopardus pardalis Leopardus tigrinus Leopardus wiedii Oncifelis geoffroyi Panthera onca Puma concolor Conepatus chinga Conepatus semistriatus Eira barbara Galictis cuja Galictis vittata Lontra longicaudus Mustela africana Pteronura brasiliensis

3

0 1 1 0 0 0 1 1

12

Canidae

2

0 1 1 0 0 0 1 1

11

5

1

0 1 0 0 0 0 1 1

10

Species

0 1 0 1 0 0 1 1

9

Family

0 0 0 1 0 0 0 0

8

Localities (numbers follow Figure 1 and Table 1)

0 0 0 1 0 0 1 0

7

Carnivora

Tayassuidae

0 1 0 0 0 0 1 0

6

Blastocerus dichotomus Mazama americana Mazama gouazoupira Odocoileus virgianus Ozotoceros bezoarticus Catagonus wagneri Pecari tajacu Tayassu pecari

4

Cervidae

3

5

2

Species

Family

1

Localities (numbers follow Figure 1 and Table 1)

Artiodactyla

0 0 0 0 0 0 0 1 1 0 0 0 1 1 0 0 1 0 1 1 0 1

14

0 1 1 0 0 0 1 1

14

1 0 0 0 0 0 1 1 1 0 1 0 1 0 0 0 1 0 1 1 0 0

15

0 1 0 0 0 0 1 1

15

Appendix Species of mammals in sixteen localities in the Neotropics

1 0 0 0 0 0 1 1 1 1 1 0 1 1 0 0 1 0 1 1 1 1

16

0 1 1 0 0 0 1 1

16

1 1 4 1 1 1 1 1 1 1 1 1 1 1 3 3 4 1 1 1 1 1

D

8 6 6 7 8 6 6 6

D

4 1 1 1 1 1 4 1 1 5 2 5

1 1 1 1 1 1 1 1 1

L

Niche1

1 1 1 1 1 1 1 1

L

Niche1

3 3 4 3 3 3 3 3 4 3 3 3 5 4 3 3 3 3 3 3 2 4

B

5 4 4 4 4 4 4 4

B

2 3,4 3 3 3 As for genus 2 2 2 2 2 3 3 2, 3 3 2 2 3 2 2, 3 2 2

References2

1 2, 3 2,3 3 3,4 1 2 2,3

References2

192 . .   . . 

0 0 1 1 1 0

0 0 0 0 1 0

0 0 1 0 1 0

0 0 1 0 1 0

0 0 0 0 0 0

11 0 0 1 0 1 0

12

Didelphidae

Caluromys lanatus Caluromys philander Caluromysiops irrupta Chironectes minimus Didelphis albiventris Didelphis marsupialis Didelphis sp. A Glironia venusta Gracilinanus agilis Lutreolina crassicaudata Marmosa (?) sp. A Marmosa cinerea Marmosa lepida Marmosa murina

0 1 0 1 0 1 0 0 0 0 0 0 0 1

1 0 0 0 0 0 1 0 0 0 0 0 0 0 0

2 0 0 0 0 0 1 0 0 0 0 0 0 0 0

3

0 1

1 1 0 0 0 1 1 0 0 0 0 0 0 1

4

0 0

0 0

0 0

6 1 0

7 1 0

8 1 0

9 1 0

10 1 0

11 1 0

12

1 1 0 0 0 1 1 0 0 0 0 0 0 1

1 1 0 0 0 1 0 0 0 0 0 0 0 1

6 0 1 0 1 0 1 0 0 0 0 0 1 0 1

7 0 0 0 0 1 0 0 0 0 0 0 0 0 0

8 0 0 0 1 1 0 0 0 1 0 1 0 0 1

9 0 0 0 0 1 0 0 0 0 0 0 0 0 0

10 0 0 0 0 1 0 0 0 0 0 0 0 0 0

11 0 0 0 0 1 0 0 0 0 0 0 0 0 0

12

0 0 0 0 1 0 0 0 0 1 0 0 0 0

13

1 0

13

0 0 0 0 1 0

13

5

Species

0 1

4

0 0 1 1 0 0

10

Family

1 0

3

0 1 1 1 0 0

9

Localities (numbers follow Figure 1 and Table 1)

Sylvilagus brasiliensis Sylvilagus floridanus

2

0 1 0 1 0 0

8

Marsupialia

Leporidae

1

0 0 0 0 0 0

7

5

Species

0 0 0 0 1 0

6

Family

0 0 0 1 1 0

4

Localities (numbers follow Figure 1 and Table 1)

Bassaricyon alleni Bassaricyon gabbii Nasua nasua Potos flavus Procyon cancrivorus Tremarctos ornatus

3

Lagomorpha

Ursidae

Procyonidae

2

5

1

Family

Species

Localities (numbers follow Figure 1 and Table 1)

Carnivora cont

Appendix continued

1 0 1 0 0 1 0 1 0 0 0 0 0 0

14

1 0

14

0 1 1 1 1 0

14

1 0 0 1 0 1 0 0 0 0 0 0 0 1

15

1 0

15

1 0 1 1 1 1

15

1 0 0 1 0 1 0 1 0 0 0 0 1 1

16

1 0

16

1 0 1 1 1 0

16

4 4 4 1 3 3 3 3 4 1 3 3 3 3

D

8 8

D

4 4 4 4 3 4

D

3 3 3 5 4 4 4 3 3 5 4 4 4 3

L

Niche1

2 2

L

Niche1

3 3 4 3 4 4

L

Niche1

2 2 2 2 3 3 3 2 1 2 1 2 1 1

B

2 2

B

3 3 3 3 3 5

B

2 2 2 3 2, 4 2 As for genus 2, 7 2, 27 3 8 3 2 2

References2

2 5, 6

References2

As for genus 2 2 2 2, 3, 4 5

References2

    193

Tapiridae

Tapirus terrestris

1

1 0

2 0

3

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

1

4

0 0 0 0 0 0 0 1 0 0 0 1 0 0 0 0 1 0 0

0 0 0 0 1 1 0 1 0 0 0 1 0 0 0 0 1 0 0

0 0 0 0 1 1 0 1 0 0 0 1 0 0 0 0 1 0 0

0 0 0 0 1 1 0 0 0 0 1 0 0 0 0 0 1 0 0

7 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 1

8 0 0 0 0 0 0 0 0 0 0 1 0 0 1 1 0 1 0 0

9 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 1

10 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 1

11 0 0 0 0 0 0 1 0 0 0 0 0 1 0 0 0 0 1 0

12 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0

13

1

1

6 1

7

0

8

1

9

1

10

0

11

1

12

1

13

5

Species

1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

6

Family

0 0 1 0 0 0 0 1 0 0 0 1 0 0 0 0 0 0 0

4

Localities (numbers follow Figure 1 and Table 1)

Marmosa robinisoni Marmosa rubra Marmosops fuscatus Marmosops noctivagus Marmosops parvidens Metachirus nudicaudatus Micoureus constantiae Micoureus demerarae Micoureus regina Monodelphis adusta Monodelphis americana Monodelphis brevicaudata Monodelphis dimidiata Monodelphis domestica Monodelphis kunsi Philander andersoni Philander opossum Thylamys elegans Thylamys pusilla

3

Perissodactyla

Didelphidae cont

2

5

1

Family

Species

Localities (numbers follow Figure 1 and Table 1)

Marsupialia cont

Appendix continued

1

14

0 0 0 1 0 1 0 1 0 0 0 0 0 0 0 0 1 0 0

14

1

15

0 1 0 0 0 1 0 0 1 1 0 0 0 0 0 0 1 0 0

15

1

16

0 1 0 1 0 1 0 0 1 1 0 0 0 0 0 1 0 0 0

16

7

D

3 3 3 3 3 4 3 3 3 3 3 3 3 3 3 3 3 3 3

D

1

L

Niche1

4 4 4 4 4 2 3 3 3 2 2 2 4 2 2 4 4 3 4

L

Niche1

5

B

1 1 1 1 1 2 1 1 1 1 1 1 1 1 1 2 2 1 1

B

2

References2

2 2 2 2 2 2, 3 3 As for genus As for genus 2 2 2, 7 3, 4 2, 3, 7 As for genus 2 2, 7 4 4

References2

194 . .   . . 

Cebidae

Callitrichidae

Family

Primates

Callimico goeldii Callithrix jacchus Cebuella pygmaea Sanguinus fuscicollis Saguinus imperator Saguinus midas Saguinus nigricollis Alouatta belzebul Alouatta caraya Alouatta seniculus Aotus infulatus Aotus nigriceps Aotus trivirgatus Aotus vociferans Ateles belzebuth Ateles paniscus Callicebus brunneus Callicebus cupreus Callicebus troquatus Cebus albifrons Cebus apella Cebus olivaceous (=nigrivittatus) Chiropotes satanas Lagothrix lagothricha Pithicia aequatorialis Pithecia irriota Pithecia monachus Pithecia pithecia Saimiri boliviensis Saimiri sciureus Cacajao melanocephalus Callicebus moloch Callithrix argentata

Species 0 0 0 0 0 0 0 0 0 1 0 0 0 0 1 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0

1 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0

2 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0

3 0 0 0 0 0 0 0 0 0 0 0 0 1 0 1 0 0 0 0 0 0 1 1 0 0 0 0 0 0 1 0 0 0

4 0 0 0 0 0 0 0 0 0 1 0 0 1 0 1 0 0 0 1 1 1 1 1 0 0 0 0 1 0 1 1 0 0

5 0 0 0 0 0 1 0 0 0 1 0 0 0 0 0 1 0 0 0 0 1 0 1 0 0 0 0 1 0 0 0 0 0

6 0 0 0 0 0 0 0 1 0 0 1 0 0 0 0 0 0 0 0 0 1 0 1 0 0 0 0 0 0 1 0 0 0

7 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0

8 0 1 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0

9 0 0 0 0 0 0 0 0 1 0 0 0 1 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 1 1

10 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

11 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

12 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0

13

Localities (numbers follow Figure 1 and Table 1)

Appendix continued

1 0 1 1 1 0 0 0 0 1 0 1 0 0 0 1 1 0 0 1 1 0 0 1 0 1 0 0 1 0 0 0 0

14 0 0 0 0 0 0 0 0 0 1 0 0 0 1 0 0 0 1 0 1 0 0 0 0 0 0 1 0 0 1 0 0 0

15 0 0 1 1 0 0 1 0 0 1 0 0 0 1 1 0 0 0 1 1 1 0 0 0 1 0 1 0 0 1 0 1 0

16 3 4 4 4 4 4 4 7 7 7 6 6 6 6 6 6 6 6 6 4 4 4 6 6 4 4 4 4 3 3 n/a n/a n/a

D 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 n/a n/a n/a

L

Niche1

2 2 2 2 2 2 2 3 3 3 2 2 2 2 3 3 2 3 3 3 3 3 3 3 3 3 3 3 2 2 n/a n/a n/a

B

As

As

As As

As

9 9 9 9, 10 9 9 9 for genus 9 9 for genus for genus 9 for genus 9 9, 11 9, 12 9 9 9 4, 9 9 9 9 for genus 13 13 13 9 9

References2

    195

Dinomyidae Echimyidae

Dasyproctidae

Chinchillidae Ctenomyidae

Agoutidae Caviidae

Agouti paca Cavia aperea Dolichotis salinicola Galea flavidens Galea musteloides Galea spixii Kerodon rupestris Microcavia australis Lagostomus maximus Ctenomys frater Ctenomys mendocinus Dasyprocta fuliginosa Dasyprocta leporina Dasyprocta prymnolopha Dasyprocta punctata Dasyprocta sp. A Myoprocta acouchy Dinomys branickii Carterodon sulcidens Clyomys laticeps Dactylomys dactylinus Echimys braziliensis Echimys chrysurus Echimys saturnus Echimys semivillosus Echimys sp. A Echimys sp. B Isothrix bistriata Isothrix pagurus Makalata armata Mesomys hispidus Proechimys amphichoricus Proechimys brevicauda Proechimys cayennensis

1 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0

1 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0

2 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0

3 1 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 1 0 0 1

4 1 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 1 0 0 0 0 1 0 0 0 0 0 1 0 0 1 1 0 0

1 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 1 0 0 0 0 0 0 0 0 0 1 0 1 0 1 0 0 1

6 1 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 1 0 0 0 1

7 0 0 0 0 0 1 1 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

8 0 1 0 0 0 1 0 0 0 0 0 0 0 0 0 1 0 0 1 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0

9 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

10 0 0 1 0 1 0 0 1 1 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

11 0 0 0 0 1 0 0 0 0 1 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

12 0 0 0 0 0 0 0 0 0 1 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

13

5

1

Family

Species

Localities (numbers follow Figure 1 and Table 1)

Rodentia

Appendix continued

1 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 1 1 0 0 1 0 0 0 0 1 0 0 0 0 1 0 1 0

14 1 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 1 1 0 0 0 1 0 0 0 0 0 0 0 1 0 0 0 0

15

0 0 0 0 0 1 1 0 0 0

1 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 1 0 0 0 1 1 0

16 6 8 8 8 8 8 7 8 8 7 7 6 6 6 6 6 5 6 7 7 7 5 5 5 5 5 5 n/a n/a 6 4 5 5 5

D 1 2 1 2 2 2 1 4 6 6 6 1 1 1 1 1 1 1 2 6 3 3 3 3 3 4 3 3 3 4 3 2 2 2

L

Niche1

3 2 3 2 2 2 3 2 3 2 2 3 3 3 3 3 3 4 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2

B

2 3 3, 4 As for genus 1, 3, 4 14 14, 27 4 3 4 As for genus 2 As for genus As for genus 2 As for genus 2 1 1 1, 3, 8, 27 2, 15 As for genus As for genus As for genus 2 16 As for genus As for genus 2, 27 1 2 As for genus 16 5, 17

References2

196 . .   . . 

Heteromyidae Hydrochaeridae Muridae

Erethizontidae

Echimyidae cont

Family

Rodentia cont

Proechimys cuvieri Proechimys gularis Proechimys longicaudatus Proechimys quadruplicatus Proechimys semispinosus Proechimys simonsi Proechimys sp. A Proechimys sp. B Proechimys sp. C Proechimys sp. D Proechimys steerei Thrichomys apereoides Coendou bicolor Coendou melanurus Coendou prehensilis Coendou quichua Heteromys anomalus Hydrochaeris hydrochaeris Akodon boliviensis Akodon cursor Akodon lindberghi Akodon reinhardti Akodon urichi Akodon varius Bolomys lasiurus Calomys callosus Calomys hummelincki Calomys laucha Calomys tener Graomys domorum Graomys griseoflavus Holochilus brasiliensis Ichthyomys stolzmanni Juscelinomys candango

Species 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0

1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 1 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

2 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 1 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0

3 0 0 0 0 0 0 0 0 1 1 0 0 0 0 1 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

4 0 0 0 0 1 0 0 0 0 1 0 0 0 0 1 0 0 1 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0

5 1 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

6 0 0 0 0 0 0 0 0 0 0 0 0 0 1 1 0 0 1 0 0 0 0 0 0 1 0 0 0 0 0 0 1 0 0

7 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0

8 0 0 1 0 0 0 0 1 0 0 0 1 0 0 1 0 0 1 0 1 1 1 0 0 1 1 0 0 1 0 0 1 0 1

9 0 0 0 0 0 0 1 0 0 0 0 1 0 0 1 0 0 0 0 0 0 0 0 1 1 1 0 0 0 0 0 0 0 0

10 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 1 0 0 1 1 0 0

11 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 1 0 0 0 0 1 0 1 0 0 0 1 0 1 0 0

12 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 1 0 0 0 0 1 0 1 0 0 0 0 0 1 0 0

13

Localities (numbers follow Figure 1 and Table 1)

Appendix continued

0 0 0 0 0 1 0 0 0 0 1 0 0 0 1 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

14 0 0 1 0 0 1 0 0 0 0 0 0 1 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

15 0 1 0 1 1 1 0 0 0 0 0 0 0 0 0 1 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0

16 5 5 5 5 5 5 5 5 5 5 5 5 6 6 6 6 5 8 3 3 3 3 3 3 5 4 4 4 4 6 4 7 3 7

D 2 2 2 2 2 2 2 2 2 2 2 4 3 3 3 3 2 5 2 2 2 2 2 2 2 4 n/a 4 n/a 4 4 5 5 2

L

Niche1

2 2 2 2 2 2 2 2 2 2 2 2 3 2 3 2 1 4 1 1 1 1 1 1 1 1 1 1 1 1 1 2 2 1

B

As

As

As

As As

As

As As As As As

for genus for genus for genus for genus for genus 16 for genus 8 for genus for genus 16 1, 8 2 2 2 for genus 2, 6 2 3, 4 18 for genus 8 6 3, 4 3 4 for genus 3, 4 8 3, 4 3, 4 3, 4 19 1, 27

References2

    197

0 0 0 1 0 1 1 0 0 0 0 0 0 0 1 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0

0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 1 0 1

0 0 0 0 1 1 1 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 1

0 0 0 0 1 1 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 1

0 0 0 0 1 1 1 0 0 0 0 0 0 0 0 1 0 0 1 0 0 0 0 0 0 1 1 1 1 1 0 0 1 0 0 0 1

0 1 0 0 0 1 0 1 0 0 0 0 0 0 0 1 0 0 1 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0

6 0 0 0 0 1 1 1 0 0 0 1 0 0 0 0 1 0 0 1 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0

7 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0

8 1 0 0 0 1 1 1 0 0 1 0 0 1 1 0 1 1 0 0 0 1 0 1 0 1 0 0 0 0 1 0 1 0 0 0 0 0

9 0 0 0 0 0 0 1 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

10 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

11 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 1 0 0 0 1 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0

12 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 1 0 0 0 1 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0

13

Kunsia fronto Neacomys guianae Neacomys spinosus Neacomys tenuipes Nectomys squamipes Oecomys bicolor Oecomys concolor Oecomys paricola Oecomys superans Oligoryzomys eliurus Oligoryzomys fulvescens Oligoryzomys longicaudatus Oligoryzomys microtis Oligoryzomys nigripes Oryzomys albigularis Oryzomys capito Oryzomys lamia Oryzomys legatus Oryzomys macconnelli Oryzomys nitidus Oryzomys subflavus Oxymycterus paramensis Oxymycterus roberti Oxymycterus sp. a Pseudoryzomys simplex Rhipidomys couesi Rhipidomys fulviventer Rhipidomys leucodactylus Rhipidomys macconnelli Rhipidomys mastacalis Rhipidomys sp. A Rhipidomys sp. B Rhipidomys sp. C Rhipidomys venezuelae Sigmodon alstoni Wiedomys pyrrhorhinos Zygodontomys brevicaudata

4

Muridae cont

3

5

2

Species

Family

1

Localities (numbers follow Figure 1 and Table 1)

Rodentia cont

Appendix continued

0 0 0 0 1 1 0 0 1 0 0 0 1 0 0 1 0 0 1 1 0 0 0 1 0 1 0 0 0 0 0 0 0 0 0 0 0

14 0 0 1 0 1 1 1 0 1 0 0 0 0 0 0 1 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

15 0 0 1 0 1 1 1 0 0 0 0 0 0 0 0 1 0 0 1 1 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0

16 7 3 3 3 4 5 5 5 5 5 5 5 5 5 5 5 5 4 5 5 5 3 3 3 n/a 6 6 4 6 6 6 6 6 6 8 5 5

D 6 2 2 2 5 3 4 4 4 4 4 4 4 4 4 4 4 4 4 4 2 2 2 2 5 3 3 3 3 3 3 3 3 3 2 4 2

L

Niche1

2 1 1 1 2 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

B

As As

As

As As

As

As

As As

1, 27 2 2, 20 2 3 2, 8 8 21 16 for genus for genus 3 16 2, 3 28 3 for genus 4 16 3 8 3 8 for genus 1, 3 for genus for genus 4 for genus 5, 8 6 for genus for genus 6 22 1, 27 5, 23

References2

198 . .   . . 

Bradypus tridactylus Bradypus variegatus Cabassous unicinctus Chaetophractus vellerosus Chlamyphorus retusus Dasypus kappleri Dasypus novemcinctus Dasypus sabanicola Dasypus septemcinctus Euphractus sexcinctus Priodontes maximus Tolypeutes matacus Tolypeutes tricinctus Choloepus didactylus Choloepus hoffmanni Cyclopes didactylus Myrmecophaga tridactyla Tamandua tetradactyla

0 1 1 0 0 0 1 0 0 0 1 0 0 0 0 0 0 1

0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 1 1

2 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 1 1

3 0 1 0 0 0 0 1 0 0 0 1 0 0 0 0 0 1 1

4

0 0 0 1 0 0 1 0 0

0 0 1 1 0 0 1 0 0

0 0 0 1 0 0 0 0 0

0 0 1 0 0 0 0 0 0

0 0 0 0 0 0 0 0 0

8 0 0 0 0 0 0 0 0 0

9 0 0 0 0 0 0 0 0 1

10 1 0 0 0 0 0 0 0 0

11 1 0 0 0 0 0 0 0 0

12 0 0 0 0 0 0 0 0 0

13

0 0 0 0 0 1 1 0 0 0 0 0 0 1 0 1 1 1

1 0 0 0 0 1 1 0 0 0 1 0 0 1 0 1 1 1

6 0 1 1 0 0 1 1 0 1 0 0 0 0 1 0 1 1 1

7 0 0 0 0 0 0 1 0 0 1 0 0 0 0 0 0 0 1

8 0 0 1 0 0 0 1 0 1 1 1 0 1 0 0 0 1 1

9 0 0 0 0 0 0 1 0 0 1 1 1 0 0 0 0 1 1

10 0 0 0 1 1 0 0 0 0 1 1 1 0 0 0 0 1 1

11 0 0 0 1 0 0 1 0 1 1 1 1 0 0 0 0 0 1

12 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1

13 0 1 0 0 0 0 1 0 0 0 1 0 0 0 1 1 1 1

14

0 0 0 0 0 1 0 1 1

14

0 1 1 0 0 0 1 0 0 0 1 0 0 0 1 1 1 1

15

0 1 0 0 0 0 1 0 1

15

0 1 1 0 0 1 1 0 0 0 1 0 0 1 0 1 1 1

16

0 1 0 0 0 0 1 0 1

16

7 7 2 3 3 2 3 2 2 3 2 2 2 7 7 2 2 2

D

7 3 6 6 6 4 6 6 6

D

3 3 1 2 6 1 1 1 1 1 1 1 1 3 3 3 1 4

L

Niche1

5 3 4 4 4 4 4 4 4

L

Niche1

3 3 3 2 2 3 3 3 3 3 4 3 3 3 3 2 4 3

B

3 1 2 2 2 2 2 2 2

B

2, 3 2 2 3 3 2, 24 2, 3 24, 25 3 2, 24 2, 25 3, 24 As for genus 2 26 2 2 2

References2

3 2 As for genus As for genus 2 2 2 As for genus 2

References2

Note (1) Localities numbered following Figure 1. Note (2) Macroniche categories, D=diet; L=locomotion; B=body weight. For explanation of numbers see data and Methods section. Note (2) References for diet, locomotor and body weight category assignments: (1) Nowak, 1991; (2) Emmons & Feer, 1990; (3) Redford & Eisenberg, 1992; (4) Mares & Ojeda, 1989; (5) Eisenberg, 1989; (6) Ensenberg et al., 1979; (7) Streilein, 1982b; (8) Mares et al., 1989; (9) Ford & Davis, 1992; (10) Peres, 1993; (11) Van Roosmalen, 1985; (12) Terborgh, 1983; (13) Hershkovitz, 1987; (14) Mares et al., 1981; (15) Emmons, 1981; (16) Janson & Emmons, 1990; (17) Guillotin, 1982; (18) Nitikman & Mares, 1987; (19) Voss, 1988; (20) Alho, 1982; (21) Malcolm, 1990; (22) Voss, 1992; (23) Fleming, 1970; (24) Wetzel, 1985; (25) Redford, 1985; (26) Meritt, 1985; (27) Mares, pers. comm.; (28) Albuja, pers, comm.

Myrmecophagidae

Megalonychidae

Dasypodidae

Bradypodidae

1

0 0 0 0 0 0 0 0 0

7

5

Species

0 0 0 0 1 0 0 0 0

6

Family

0 0 0 0 1 0 0 0 0

4

Localities (numbers follow Figure 1 and Table 1)

Myocastor coypus Microsciurus flaviventer Sciurus aestuans Sciurus gilvigularis Sciurus granatensis Sciurus ignitus Sciurus igniventris Sciurus sanborni Sciurus spadiceus

3

Xenarthra

Myocastoridae Sciuiridae

2

5

1

Family

Species

Localities (numbers follow Figure 1 and Table 1)

Rodentia cont

Appendix continued

    199