Download Elephants versus butterflies: the ecological role of large herbivores

Journal of Biogeography, 30, 1357–1380
Elephants versus butterflies: the ecological role of
large herbivores in the evolutionary history of
two tropical worlds
Cris Cristoffer1* and Carlos A. Peres2 1CES/CEVN, Luke Air Force Base, AZ, USA, 2Centre
for Ecology, Evolution & Conservation, University of East Anglia, Norwich, UK
Abstract
Aim Large herbivores have important effects upon Paleotropical ecosystems, but attain
much lower biomass densities in the Neotropics. We assess how this difference in herbivore activity has generated different ecological and evolutionary trajectories in the
New and Old World tropics. We also propose an explanation for how the greater
biomass density in the Old World came about.
Location Data were compiled primarily from moist tropical forests, although more of
the relevant information to address most of our hypotheses was available from the
mainland areas of Africa, Asia, and South America than elsewhere.
Methods We gleaned data from published information and personal communication.
We compared body masses and a variety of other types of information for the New- and
Old-World tropics. We proposed that interhemispheric differences exist in a variety of
processes, including herbivory, frugivory, and flower visitation. We erected hypotheses
and evaluated them qualitatively, and, when information was available, tested them
using simple ratios of species in various taxonomic and trophic categories. To make the
comparisons more meaningful, we specified appropriate data selection criteria.
Results A general pattern of differences emerges from this review. Compared with
Neotropical forests, the much greater biomass densities of large herbivores in Paleotropical forests are associated with a lesser diversity of small herbivores, different
hunting methods used by indigenous humans, larger arboreal vertebrates, larger fruits,
different patterns of fruit and flower dispersion in space and time, a lesser abundance of
most types of reproductive plant parts, and other features. The existence of a species-rich
fauna of large herbivores in the pre-Holocene Neotropical rain forest was not supported.
Main conclusions The potential for large herbivores to cause functional differences
between the New and Old World tropical forests has been virtually unexplored, despite
the well-known importance of large herbivores in the Old World tropics. The evaluations of our hypotheses suggest that the abundance of large herbivores in the Old World
tropics has launched it onto a different evolutionary trajectory than that of the
NewWorld tropics. The relevant evidence, although scanty, suggests that the interhemispheric ecological differences are not an artefact of recent megafaunal extinctions in
the New World. Recent human activities have, however, reduced population sizes of
large wild herbivores in the Old World, and increased population sizes of livestock. This
has likely created a rather homogeneous, anthropogenic selection pressure that tends to
erase the evolutionary differences between the two tropical worlds.
Keywords
Macroevolution, Neotropics, Paleotropics, herbivores, rain forest, savanna, frugivory,
flower visitors.
*Correspondence: Cris Cristoffer, 56 CES/CEVN, 13970 W. Lightning Street, Luke Air Force Base, AZ 85309-1149, USA. E-mail: [email protected]
2003 Blackwell Publishing Ltd
1358 C. Cristoffer and C. A. Peres
INTRODUCTION
Biogeographers have long been aware of taxonomic differences between the biotas of the Neotropics and the Paleotropics. Taxa exclusive or nearly exclusive to one
hemisphere include bromeliads, cacti, leafcutter ants, morpho butterflies, hummingbirds, toucans, hornbills, sunbirds,
marmosets, elephants, rhinos, prosimians, prehensile-tailed
monkeys, true apes, gliding rodents (Anomaluridae or Sciuridae), among many others. Indeed, pairwise comparisons
of some New and OldWorld taxa have often been used to
exemplify convergent evolution (Bourliére, 1973; Eisenberg,
1981; Terborgh & van Schaik, 1987).
Convergence may not be as close as it appears, but these
discrepancies can be explained. We suggest that the Paleotropics are rich in large mammals whose closest counterparts
in the Neotropics are small mammals, reptiles and invertebrates. Furthermore, there are fundamental interhemispheric
differences in frugivory and flower visitation. We posit that
many of the differences between the Neotropics and the
Paleotropics have a common underlying cause: the abundance of large, tropical rain forest herbivores (hereafter,
LRFH). Since the largest tropical herbivores are all but
immune to attack from predators (Owen-Smith, 1988), their
biomass densities under non-hunted conditions may often be
greater than for smaller, predated herbivores. It seems
plausible that the lesser abundance of LRFH and total
absence of very large herbivores in the Neotropics, compared with the Paleotropics (Fa & Purvis, 1997), has
resulted in functionally different rain forest ecosystems.
Our primary focus is on lowland tropical rain forest; for
our purposes, the maps in Whitmore (1998) depict the areas
where these occur. Rain forest landscapes include a variety
of vegetation formations of smaller extent, including heath
forests, isolated savannas, etc.; however, our analysis will
not address such relatively small areas. There are also
undoubtedly quantitative abiotic differences between sites
that might confound hypotheses of the factors that determine species composition. Nevertheless, since large herbivores have been widespread and occurred at high biomass
densities in the Paleotropics (see below) until recently, the
consequences of their activities should be observable.
Indeed, at least one author has invoked the activities of large
herbivores as agents of climate change (Retallack, 2001).
There also seems to be a widely-held misconception that
large herbivores are present predominantly in savanna and
grassland habitats, but not in rain forest. There is a grain of
truth to this idea; for example, approximately twenty-nine
species of ungulates from ten genera occur in African forests,
compared with forty-three species from twenty-eight genera
in African savannas (Owen-Smith, 1982). Nevertheless, on a
local scale, forest ungulate communities can be very diverse,
including up to sixteen co-occurring species in some African
forests, compared with about nineteen species (excluding
elephants) in the most diverse savanna areas (McNaughton
& Georgiadis, 1986). Although biomass data for Asian
forests are scarcer, we will present other information
indicating that Asian herbivores affect the forests they inhabit.
By contrast, large herbivores are not typical of tropical
rain forests outside of Asia and Africa. Indeed, part of perception that large herbivores may be unimportant in rain
forests probably stems from the fact that much tropical rain
forest research has taken place in the Neotropics, where
large herbivores are nearly absent. Another source of bias
may be because of a simple lack of information and severe
difficulties in studying LRFH (e.g. Strickland, 1967; Tangley, 1997; Walsh & White, 1999).
Furthermore, several LRFH are in danger of extinction
and have been missing for decades from much of their former geographical ranges, hence researchers have been unable
to assess their ecological importance. For example, India has
been the site of a flurry of research activity pertaining to
large mammals, yet several species of large herbivores that
did occur in Indian tropical forests in the 1800s, including
Sumatran rhinos (Dicerorhinus sumatrensis) and Javan rhinos (Rhinoceros sondaicus), are now missing (Groves, 1967;
Nowak, 1999; Toon & Toon, 2002). Later we will present
information about these species as pertains to the hypotheses
raised; for the moment, let us note that there are only a few
hundred individuals of both species in the wild. These species are primarily browsers or mixed feeders, not grazers,
and rain forests, not grasslands, are their primary habitat. In
Indochina a third large odd-toed herbivore, the Malayan
tapir (Tapirus indicus), also occurs (Nowak, 1999). Therefore, this review pertains to how LRFH affected their environment over evolutionary time, rather than during the most
recent centuries of reduced range and diversity.
Note also that the great majority of recent studies on large
paleotropical herbivores have taken place in habitats where
the animals are more readily observed, such as African
savannas and the monsoon forests and alluvial grasslands of
India. Thus, our perceptions of rain forest herbivores have
been coloured by non-forest species. But make no mistake:
absence of evidence is not evidence of absence. Rain forest
herbivores existed whether or not we happened to study
them. Fortunately, recent studies have begun to lift the veil
of mystery surrounding these animals; for example, it is now
commonly accepted that African elephants probably belong
to two or more species, one of which, Loxodonta cyclotis, is
a tropical forest specialist (Tangley, 1997). Fenton et al.
(1998) reported that the woodland at half of the sites they
studied had been disturbed by high elephant densities to the
extent that the tree canopy was greatly reduced. There were
significant differences between intact and impacted sites with
regards to diversity, numbers, activity, and diets of bats.
Other studies have revealed that elephants have played a
significant role in shaping West African rain forest vegetation (Hawthorne & Parren, 2000). Furthermore, forest
elephants make up 52% of the biomass of mammalian
herbivores in the rain forest of Gabon and play a key role in
African rain forest ecosystems (Prins & Reitsma, 1989).
Later in this paper, we will summarize other natural history
literature documenting the importance of large herbivores in
rain forests.
There are undoubtedly quantitative abiotic differences
between sites that might confound hypotheses of the factors
2003 Blackwell Publishing Ltd, Journal of Biogeography, 30, 1357–1380
Macroevolutionary role of large herbivores 1359
that determine species composition. Nevertheless, since large
herbivores have been widespread in the Paleotropics until
recently, the consequences of their activities should be
observable.
Herein we define Ôlarge herbivoresÕ to include terrestrial
mammals greater than 5 kg in weight, and that obtain
most of their diet from vegetative plant parts. Phytophagous insects, on the other hand, are referred to as Ôsmall
herbivoresÕ. Rodents of the family Echimyidae that weight
less than 1 kg in weight and feed upon vegetative plant
parts will also be considered small herbivores, as will the
hoatzin (Opisthocomus hoatzin), which is volant. We also
exclude arboreal folivores larger than c. 2 kg and
belonging to several classes, because they face fundamental
ecological problems different from those of large, terrestrial ungulates (Eisenberg, 1978). Throughout this paper,
we will emphasize a comparison of the mainland Neotropics with the mainland Paleotropics. Some of our
hypotheses are less applicable to tropical islands, including
Madagascar and New Guinea, according to the rationale
we describe below. We will, however, revive discussion of
such places when appropriate data are available to make
comparisons.
Densities of LRFH and their most apparent effects
The largest terrestrial herbivores in the Neotropics, genus
Tapirus, are less than 10% of the mass of the largest
Paleotropical herbivores, but are also selective, if generalized, herbivores. Tapirs do not occur in Africa, but the okapi
(Okapia johnstoni) seems similar in some respects.
In the Paleotropics large herbivores have a greater range in
body size, attain greater biomass densities, and are more
diverse. Using data from Lekagul & McNeely (1977);
Kingdon (1997) and Fonseca et al. (1996), we compiled data
on the present-day non-volant mammal fauna in tropical
forest regions of Africa, southeast Asia, and South America.
This comparison indicates that the mean body mass of
mammals in African forests (37.45 17.19 kg; n ¼ 284)
and Thailand (98.45 43.26 kg; n ¼ 112) is significantly
greater than those in Amazonian forests (4.80 1.44 kg;
n ¼ 192). This is largely because the number of large-bodied
species is considerably greater in Afrotropical and southeast
Asian forests than in the Neotropics. In African forests, 60%
of species are larger than 1 kg, and 22% are larger than
10 kg. The corresponding figures for Thai forests are very
similar at 62% and 20%, respectively. In contrast, only 38%
and 7% of the non-volant mammal fauna found in the
Amazon exceed a body mass of 1 and 10 kg, respectively.
The weights of the sixty-six species of mammalian primary
consumers of a forest in north-eastern Gabon are uniformly
distributed across five orders of magnitude (Emmons et al.,
1983), whereas those of a typical terra firme forest of central
Amazonia are markedly skewed towards small- and midsized species (Peres, 1999). We excluded bats because their
upper size limit is probably far more constrained by flight
requirements (Brown & Maurer, 1987; Cristoffer, 1991);
nevertheless, since the size spectrum of Paleotropical bats is
2003 Blackwell Publishing Ltd, Journal of Biogeography, 30, 1357–1380
greater than that of Neotropical bats, their inclusion would
have further augmented this discrepancy.
The greater abundance of large animals in the Paleotropics
has also influenced indigenous hunting tactics. Snares and
other prey capture devices effective on large prey species are
common in the Old World, but rare in the Neotropics (Fa &
Peres, 2001). Indeed, the relatively high abundance of
ungulates such as small bovids in west African forests,
sustains thriving bushmeat markets, a phenomenon that is
virtually absent from Neotropical forests (Peres, 2000; Fa &
Peres, 2001).
The extent to which LRFH affect their environment could
vary with their species richness. Thus, we hypothesized that
the density of trees would correlate inversely with the species
richness of large herbivores, which can injure or kill them.
We used tree data from forest plots of 0.5–2.0 ha to partially
control for any effects of sampling area, and we averaged
values for eight sites in South America, five sites in Africa,
two sites in mainland tropical Asia, and four sites in island
tropical Asia, and New Guinea/Australia (Richards, 1996).
Within Asia and Australia, the species richness of large
herbivores declines in the direction from mainland Asia,
through large islands in Malaysia and Indonesia, to New
Guinea–Australia (Flannery, 1995; Francis, 2001). Although
the data points were too few for rigorous statistical testing,
there was a monotonic trend of decreasing tree abundance
with increasing number of large herbivore species. Africa
had the fewest trees per hectare, and within Asia, tree densities increased from the mainland, through Indonesian
islands, to New Guinea–Australia.
In theory, we could investigate the effects of large herbivores by means of an experiment in which biotas at several
sites were randomly split into control and treatment groups
that were identical except for large herbivores, which would
be abundant on control sites, and absent or uncommon on
treatment sites. Because this is unfeasible, we considered
natural experiments (sensu Diamond, 1996) by comparing
various tropical locations. Natural experiments differ from
field and laboratory experiments in that the experimenter
does not establish the perturbation but instead selects sites
where the perturbation is operating or has already run. We
sought sites as similar as possible, both ecologically and
taxonomically, in all variables except the abundance of large
herbivores. Thus the mainlands of both the Neotropics and
Paleotropics have assemblages of anthropoids (monkeys or
apes), megabeaked birds (toucans or hornbills), woodpeckers, trogons, parrots, specialized flower-feeding birds (hummingbirds or sunbirds), bees, butterflies, etc. Many islands
would violate this similarity condition, because islands have
disharmonic biotas with reference to the mainland (Carlquist, 1965, 1974; Eisenberg, 1981). For example, prior to
human colonization, the Hawaiian Islands had no ants,
monkeys, toucans or hornbills, parrots, or trogons, and there
were few butterflies and bees – taxa that figure in our theory
and are common in the mainland. We also exclude the
Australian tropics, which have a similar disharmonic biota
to that of New Guinea (Carlquist, 1965, 1974; Eisenberg,
1981).
1360 C. Cristoffer and C. A. Peres
The importance of large herbivores in the mainland
Paleotropics has been long recognized. Large herbivores,
especially elephants, have been implicated in blatant ecosystem alterations (Mueller-Dombois, 1972; Owen-Smith,
1988; Dinerstein, 1992; Power & Tilman, 1996; Cumming
& Brock, 1997; Keesing, 2000). Prior to the invasion by
Europeans and their weapons, large herbivores were likely to
have been a dominant influence on ecosystem structure and
dynamics (Owen-Smith, 1988). Owen-Smith (1988) summarized the feeding behaviour of very large Paleotropical
herbivores. Most of the information available is for elephants, particularly those in African savannas. Although
elephants in general are mixed feeders on grass, browse and
fruit, grass is insignificant in the diets of forest elephants in
Ghana and Ivory Coast, where woody browse and fruits are
the main components. Browsing elephants strip leaves and
break small branches, and the woody material ingested from
some trees outweighs the foliage, and small woody plants are
often eaten whole. Nearly all browsing occurs below 2 m
above ground, but trees taller than 6 m may be pushed over
to bring high branches within reach. Trees greater than
about 25 cm in diameter commonly withstand attempts to
push them over. Asian elephants appear to feed on grass to a
greater extent than the African forest species, and to push
over trees less often. Nevertheless, the damage that elephants
cause to structural features of vegetation during episodes of
low rainfall may leave a lasting impact on vegetation
structure, thereby altering habitat for many other species.
Only recently has extensive information about African
forest elephants become more readily available. Forest elephants alter the structure of their habitats by creating a
network of paths and ÔboulevardsÕ that are regularly used for
long distance migration or foraging (Turkalo & Fay, 1995;
Vanleeuwe & Gautier-Hion, 1998). We will not describe in
detail the role of elephants and other large herbivores as seed
dispersal agents (but see Barlow, 2000).
The following natural history information pertaining to
two species of Asiatic rhinos could be taken as typical for
very large herbivores living in tropical forest; we present this
information to substantiate some hypotheses to be presented
later regarding long distance movements, effects on vegetation physiognomy, seed dispersal, need for mineral licks,
etc. Sumatran rhinos (Dicerorhinus sumatrensis) inhabit
tropical rain forest (Nowak, 1999), and in Gunung Leuser
Park in Sumatra feed mainly on small trees or saplings. They
consume twigs, small branches and leaves, and fruits. To
reach higher shoots of woody saplings, animals bend or
break the stems by walking over the plant and pressing down
on the trunk with the body. Sumatran rhinos snapped plants
with stem diameters of up to 5 cm (Borner, 1979). Hubback
(1939) reported that feeding Sumatran rhinos will Ôget a
sapling behind his front horn and twist it round and round
until it is thoroughly decorticated and covered with mud
from his headÕ. A favorite fruit seems to be Mangifera, a type
of wild sour mango, and young seedlings have been seen
growing from old dung deposits. Strickland (1967) noted
that young trees had been bitten off, regenerated and been
bitten off again repeatedly. The home range size for two
adult animals was about 10 km2, but this was probably
underestimated. The animals wandered widely, and spent
very little time in the extensive swamps, which merely
functioned as paths from one patch of high ground to
another. Although the animals used trails repeatedly, the
smallest animal often wandered off the main trails. The
rhinos were attracted to wallows baited with salt, and the
tracks of several animals were found to converge at a salt
lick. Although the rhinos were capable of covering many
miles in a day, in certain areas (mud wallows, salt licks, and
feeding and resting areas), they sometimes moved less than
half a mile in a 24-hour period. Asian elephants (Elephas
maximus) co-existed with the rhinos and were even found in
the same wallow. Rhinos created wallows used by other
species. Young saplings provided the majority of the diet,
but these were invariably damaged. Some plants were so
completely damaged that they could not be identified in the
field. Trees up to 7 cm were sometimes snapped off completely up to 2 m above the ground. Uprooted trees were
stepped on and broken into smaller pieces. The damage done
by D. sumatrensis could be easily distinguished from that of
other mammals. A minimum of 40 species of plants were
eaten, but many plants were too devastated to permit identification. Although D. sumatrensis fed extensively on plants
of secondary forest and forest edge, untouched primary
forest would provide adequate habitat for this species. Indeed, under modern conditions of human disturbance (such
as hunting) in Sumatra, rhinos and elephants avoid forest
edges (Kinnaird et al., 2003).
Javan rhinos (Rhinoceros sondaicus) are also primarily
browsers. The diet consists of shoots, twigs, leaves, young
foliage, and fallen fruit; almost 150 species have been identified as food plants (Schenkel & Schenkel-Hulliger, 1969;
Hoogerwerf, 1970). In the course of feeding, branches up to
2 cm thick are torn off and trees up to 15 cm in diameter are
uprooted (Talbot, 1960). Damaged trees and shrubs often
survive and after some time put out new shoots and continue
to grow in a horizontal direction if they are uprooted
(Hoogerwerf, 1970), so certain localities have a Ôrhino
characterÕ. This appears to hamper regeneration of the forests so that they continue to form suitable forage ranges for
the rhino for long periods. According to Talbot (1960), the
animals make and use game trails, ruts in the mud up to
3 feet deep with roots and logs worn smooth by elephant
and rhino. Strickland (1967) also reported that many young
trees that had been eaten had parts of the bark scraped off
about a meter from the ground; in a few cases, he found trees
that had been scraped, but not eaten. Lekagul & McNeely
(1977) reported that R. sondaicus inhabits dense rain forests,
and in the recent past they built up large populations
(Groves, 1967).
Native pigs play an important role in plant dynamics at
the understorey level in Malaysian rain forest (Ickes et al.,
2001), affectcing stem density, species richness, growth and
possibly mortality. They also noted that although they were
unaware of any studies documenting the effects on the
understorey of large mammals such as deer, elephants,
rhinos, wild cattle and tapirs on tropical vegetation in
2003 Blackwell Publishing Ltd, Journal of Biogeography, 30, 1357–1380
Macroevolutionary role of large herbivores 1361
Southeast Asia, their impacts may be considerable. Similarly,
Hirsch & Marler (2002) observed the fate of that plants
toppled by a typhoon. All the plants ultimately died, and
herbivory by introduced Sambar deer (Cervus unicolor) and
pigs (Sus scrofa var. vittatus or Sus celebensis) was the primary cause of mortality.
Rhinos are not the only large animals whose feeding
behaviour can enhance their own habitat. Although we lack
information specific to rain forest, elephants in semi-arid
savanna preferentially browse Colophospermum mopane
that has already been browsed, even when other foods are
readily available (Smallie & O’Conner, 2000).
Large herbivores can have a number of indirect ecosystem effects. For example feeding by feral horses in salt
marsh apparently increased the diversity of foraging birds
and crabs, but decreased the density and species richness of
fishes (Levin et al., 2002). Furthermore, Cumming & Brock
(1997) document a loss of diversity in fruit bats, birds,
ants, and mantises as a consequence of high elephant
densities. Natural levels of herbivory have been shown to
diminish reproductive output, such as pollen performance
(Delph et al., 1997). Conversely, lack of herbivory could
result in greater reproductive productivity than would
occur under high herbivory pressure. Not surprisingly,
loblolly pines (Pinus taeda) grown in a herbivore-free,
CO2-rich environment are twice as likely to be reproductively mature and produce three times as many cones and
seeds as trees in ambient CO2 concentrations (LaDeau &
Clark, 2001).
Herbivores thus have many indirect effects on plants by
rendering them more susceptible to drought, other herbivores, fungi, and competitors (see also Hendrix, 1988).
Although we have emphasized elephants and other very
large herbivores, ungulates such as deer can also have profound effects and may extirpate plant species locally
(e.g. Warren, 1991; McShea et al., 1997), and deer-sized
herbivores, although present in the Neotropics, are far more
common in the Paleotropics.
Long-distance movements by LRFH
Unlike insects, large herbivores might not have the option of
specializing on particular plant species if these occur in low
biomass densities. They might be forced to feed on many
species simply to meet metabolic needs and dilute the effects
of the various toxins they ingest (Janis & du Toit, 2001).
Also, cost of locomotion per unit of body mass is lower for
large animals (Peters, 1983), thus they probably incur a
lower cost/benefit ratio in moving about to feed on a variety
of plant species.
We, therefore, hypothesized that LRFH move long distances to meet their various needs. For example, a female
forest elephant traveled with a maximum straight-line displacement of 60 km, and undertook return journeys of
more than 35 km over a home range of at least 880 km2
(Blake et al., 2001). Forest elephants move long distances in
response to fruit availability, thereby maximizing the availability of favoured food trees (White, 1994).
2003 Blackwell Publishing Ltd, Journal of Biogeography, 30, 1357–1380
Rhinoceros sondaicus may travel 15–20 km within 24 h
Groves (1967) and Dicerorhinus sumatrensis have been seen
swimming in the sea, but have also been found in remote
areas of steep montane forest (Hoogerwerf, 1970).
Talbot (1960) opined that it was difficult to believe that an
animal the size of a D. sumatrensis could get through such
rough and steep country. Undisturbed rhinos had wandered
through swift rivers five feet deep. They also used game
trails, ruts in the mud up to three feet deep with roots and
logs worn smooth by elephant and rhino. They also just
wandered cross-country. Muddy, vine-covered slopes too
steep for men to climb straight up, were ascended with ease
by wandering rhinos. The D. sumatrensis studied by
Strickland (1967) had home ranges of at least 10 km2.
Generalized herbivores and extirpation of plants
Another consequence of the generalized herbivory of large
vertebrates is that it permits a less variable population size
than that of small herbivores, hence they might preferentially
feed on certain plant species, then switch to others when the
preferred species are depleted. This is similar to the phenomenon referred to as Ôapparent competitionÕ by Holt
(1977), and reviewed by Morin (1999). Lindroth (1989)
posits essentially the same phenomenon with regards to
plants and notes that plant species can become locally
extinct because of selective feeding by generalist mammalian
herbivores because herbivore populations may not decline
appreciably when preferred plants become scarce.
By contrast, specialist herbivore populations are likely to
periodically fluctuate. Stochastic fluctuations resulting from
the combination of large and small herbivores might be more
likely to drive plants to extinction than those exposed only
to small herbivores because plants exposed to both small and
large herbivores are never free of herbivore pressure. Despite
the lack of direct evidence in support of this contention, we
hypothesize that larger herbivores can bring about local
extirpation of plant species. The literature provides support
for this hypothesis (e.g. Buechner & Dawkins, 1961;
Harper, 1969; Laws, 1970), and there is ample evidence that
animals can extinguish plant populations and species
(Niklas, 1997). The greater species richness of plants in
Neotropical than Afrotropical forests (Turner, 2001) could
thus be attributed in part to the abundance of large herbivores.
Large species writ small: the proliferation of small
Neotropical herbivores
In a review of the role that niche opportunities play in the
process of ecological adaptive radiation, Schluter (2000)
concluded that some studies of the diversity of herbivores
and the resin defenses of their prey (plants) are the first clear
indication that freedom from enemies (in that instance,
herbivores) either promotes speciation or slows extinction
rates. We hypothesized that the paucity of large Neotropical
herbivores relative to their Paleotropical counterparts
has fostered a proliferation of smaller herbivores, both
1362 C. Cristoffer and C. A. Peres
vertebrate and invertebrate. Consistent with our hypothesis,
various small Neotropical species are unmatched by OldWorld analogues.
The hoatzin, arguably the most folivorous bird on earth
(Grajal et al., 1989), is strictly Neotropical; although other
herbivorous birds exist, the hoatzin is the only bird in the
world with foregut fermentation to cope with potent allelochemics.
Leafcutter ants (Atta cephalotes and relatives) are also
found only in the New World and could be thought of as
indirectly folivorous ants. Much like large mammalian herbivores, their fungal mutualists enable them to make use of
at least eighty plant species (Steven, 1983). Furthermore, at
one Neotropical site the biomass of plants eaten by leafcutter
ants was equivalent to that of folivorous vertebrates and
only slightly less than that of all the other herbivorous
insects combined (Leigh & Windsor, 1982). It seems plausible that the metabolic needs of large leafcutter colonies can
only be supplied by a substantial quantity of vegetation from
a large variety of plants, which precludes specialization on
one or a few plant species.
Although the role of leafcutter ants in the New World
could be taken by termites (Isoptera) in the Old World, we
hypothesize to the contrary. Bignell & Eggleton (2000)
provide a world-wide summary of termite feeding groups
including soil-feeders, soil/wood interface-feeders, woodfeeders, litter-foragers, grass-feeders, and minor feeding
groups. Of these, none seem to be folivores on trees and
shrubs, although the litter-foragers and grass-feeders probably come closest. Although litter-foragers forage on leaves
and small woody items, these seem to be taken on or near the
ground, and primarily dead. Grass-feeders forage for
(usually dry) standing grass and other low vegetation stems,
usually cutting and removing it to the nest–again, not the
same as arboreal folivory.
A slightly different classification by feeding substrate was
presented by Bignell & Tayasu (2001). It included wood,
detritus, grass, wet wood, dry wood, inquiline, fungus, soil,
soil–wood interface, litter, microepiphytes, or some combination of these. Green tree and shrub leaves were not
included. Hence, tropical rain forest termites feed primarily
as detritivores, not herbivores.
Caviomorph rodents are diverse and abundant in the
Neotropics (Nowak, 1999). Neotropical forest caviomorphs
range in size from small rats of several genera to porcupines
(Erethizontidae) and pacas (Agouti paca). Although caviomorphs are trophically diverse, they are typically more herbivorous and less faunivorous than the dominant
Paleotropical rodents of the family Muridae. The Neotropical family Echimyidae includes several species of
arboreal folivores, such as bamboo rats (Kannabateomys
amblyonyx) in the Atlantic forest and Dactylomys dactylinus
in the Amazon, which can become locally abundant (Olmos
et al., 1993; Patton et al., 2000). By contrast, the continental
murid species in Paleotropical forests cannot cope with
plants that are chemically well protected; not surprisingly,
folivorous murids in Paleotropical forests only occur in
islands such as the Philippines that have few large herbivores
(Eisenberg, 1978). Herbivorous snails may also be more
abundant in the Neotropics, such as the Pantanal wetlands
of Brazil (C. Peres, pers. obs.), but we are unaware of
intercontinental comparisons of population densities.
Iguanids in the subfamily Iguaninae comprise the most
species-rich lineage of herbivorous lizards (Pough et al.,
2001), and occur in the Neotropics and Madagascar but not
on mainland Africa and Asia. By contrast, the Paleotropical
lizards in the same size range as iguanids – especially monitors of the family Varanidae – are primarily carnivorous.
Finally, we also note that butterflies are most speciose in the
Neotropics (Robbins & Opler, 1997), and most caterpillars
are herbivorous.
One could argue that the differences we propose for butterflies, ants, and bees, are simply because of random vicariant events. If this were true, then there should be many
higher insect taxa with peculiar distributions that have no
relationship to the presence or absence of large herbivores.
We hypothesized to the contrary. In fact, tropical forest
insect faunas on the various continents share a variety of
features, including low dominance and frequency of species.
Additionally, for beetles (and by inference, other orders of
insects), the most species-rich and abundant families are
remarkably constant in all comparable studies (Wagner,
2000). Thus our hypothesis was supported.
Diversity of predators of herbivorous snails
We hypothesized that the paucity or large herbivores in the
Neotropics has increased the abundance of snails. We have
no direct evidence of a greater abundance of snails in the
Neotropics, but exclusion experiments from Fennoscandia
indicate that cervids can decrease the abundance of terrestrial gastropods (Suominen, 1999). Furthermore, the following evidence is consistent with our hypothesis. A
taxonomically diverse array of unrelated Neotropical vertebrate species have become snail-eaters, and it seems
plausible that a pre-requisite for the evolution of so many
specialized predators is a corresponding abundance of herbivorous snails. Among others, specialized (and often
sympatric) snail-eaters include the limpkin (Aramus guarauma), snail kite (Rostrhamus sociabilis), slender-billed kite
(Rostrhamus hamatus), hook-billed kite (Chondrohierax
unicinctus), the caiman lizard (Dracaena guianensis), and
Dipsadinae snakes (although the Asiatic Pareatinae appear
to have similar adaptations) (Greene, 1997). Although many
vertebrates eat snails, the aforementioned taxa are found
only in the New World and are arguably the most specialized
members of their respective taxa for a diet of snails.
Herbivore motility and plant phenology
We hypothesized that plants could offset the mobility of
large herbivores by synchronizing phenology such that all
plants would be in the same stage of palatability at the same
time, thus precluding sequential selection of individuals in
the most palatable stages. Although this strategy is not
apparent among the non-reproductive portions of tropical
2003 Blackwell Publishing Ltd, Journal of Biogeography, 30, 1357–1380
Macroevolutionary role of large herbivores 1363
forest plants, an analogous situation occurs with Asian
dipterocarps, which are believed to limit the population size
of vertebrate seed-predators by mast-fruiting at supraannual intervals (Curran & Leighton, 2000).
We hypothesized that inducible defenses (sensu Karban &
Baldwin, 1997) might be more effective over short time
scales on small herbivores than on large herbivores. Some
evidence is consistent with this hypothesis. For example, a
captive tapir rejected at least 300 species of native broadleafed plants and accepted another 150, eating small quantities of each species during a feeding bout (Janzen, 1983). It
seems plausible that many food species used by tapirs are too
uncommon to serve as dietary staples. Some of their preferred foods are rare where tapirs occur in apparently typical
numbers and are common where tapirs have been selectively
overhunted. Janzen (1983) suggested that food scarcity may
be in part generated by tapir browsing. This is consistent
with dietary and radio-tracking studies that show that tapirs
feed primarily on fruits wherever conditions are favourable
(Bodmer, 1990) or otherwise typically trapline between
different regenerating canopy gaps where they selectively
browse on herbaceous plants and tree saplings (Salas &
Fuller, 1996; Salas, 1996; C. Peres & E. Dias, unpubl. data).
Similarly, okapis selectively feed on leaves, buds and small
branches (Kingdon, 1997) that are relatively scarce (Hart &
Hart, 1988, 1989). The rhinoceros feeding information
presented above also supports this. Thus LRFH probably
select forage plants when they are most palatable.
Fragile vegetation and the evolution of small arboreal
vertebrates
Emmons & Gentry (1983) speculated that larger herbivores
have selected for sturdier vegetation in the Paleotropics,
which in turn favoured the evolution of certain forms of
locomotion over others. There is evidence consistent with
the hypothesis that the activities of large herbivores in the
Paleotropics have selected for trees that are faster growing
and more responsive to light gaps. Whitmore (1998) noted
that forests in Brazil tend to be dominated by tree species
that are shade tolerant and slow growing. These hardwood
species tend to respond too slowly to canopy opening to
become attractive for silviculture. When canopy gaps are
formed, few seedlings are able to grow vigorously. Whitmore suggests that this degree of canopy disturbance leads to
the forest Ôtumbling downÕ to a mass of woody climbers and
commercially useless pioneer species. Whitmore & Silva
(1990) also noted that Amazonian trees tend to be denser
than those from other regions. Wood density is, however,
negatively correlated with growth rate (Turner, 2001), hence
Paleotropical species could have been selected for a faster
growth so that they can take advantage of disturbance (such
as light gap formation) caused by large herbivores.
There is also some evidence to support our hypothesis that
large Paleotropical herbivores could increase the geographical range size of the trees whose fruits they disperse.
Many African forest plant species have very wide distributions, whereas many Neotropical species are much more
2003 Blackwell Publishing Ltd, Journal of Biogeography, 30, 1357–1380
restricted (Richards, 1996). Dry climates have been proposed
as the mechanism that capped African gamma diversity
(Axelrod, 1952, 1972; Raven & Axelrod, 1974), but the
movements of large herbivores among forest blocks, and the
enormous distances that they disperse fruits (Blake et al.,
2001), might also have played a role in homogenizing biotas.
The removal of fragile vegetation in the Paleotropics may
have enabled climbing vertebrates to obtain sturdier supports than their Neotropical counterparts, thus providing
fewer constraints to body size increments over time. This
hypothesis is supported by the wider body size spectrum of
Paleotropical arboreal vertebrates (Cristoffer, 1987).
Trophical shifts were conjectured to be a consequence of a
smaller body size, if not phyletic dwarfism, in Neotropical
arboreal endotherms, which often eat more animal matter
(e.g. arthropods) and less vegetation. This would seem to be
a partial contradiction of the previous paragraphs, but this is
more apparent than real. There are anatomical and physiological constraints on the evolution of folivory in endothermic vertebrates (Eisenberg, 1978), and the folivorous
lifestyle is all but precluded for very small arboreal endotherms. Thus, as Neotropical arboreal endotherms are constrained to remain small to enable them to move about on
fragile vegetation, they have little choice but to feed on foods
that are easily and quickly digested.
By contrast, ectotherms and terrestrial herbivores can afford to become smaller and retain or evolve a plant diet.
Most of the small herbivores we conjectured to have filled in
for large herbivores are ectotherms or terrestrial species, and
the few folivorous arboreal endotherms listed, such as the
hoatzin, are profoundly modified behaviourally and physiologically.
There is some slight support for the hypothesis that the
feeding activities of large herbivores would extinguish some
species of epiphytes and lianas in the Paleotropics. The
richest herb and epiphyte floras in tropical forests are
probably in the wetter parts of the Neotropics (Richards,
1996). These plants would likely qualify as Ôfragile vegetationÕ (sensu Emmons & Gentry, 1983) and would be
especially susceptible to the effects of large herbivores.
The data on woody lianas is slightly more complicated.
Although lianas have similar species richness in the Neotropics and Africa, their biomass tends to be greater in the
latter (Hegarty & Caballé, 1991). This is consistent with the
idea that large herbivores remove more fragile vegetation in
the Paleotropics (Emmons & Gentry, 1983), leading to
sturdier or more massive lianas.
We hypothesized that the activities of large herbivores has
reduced the abundance of palms in the Paleotropics. Herbivorous vertebrates have been shown to cause mortality in
palms (Pacheco, 2001), presumably by feeding directly on
them. We also hypothesized that the less-effective feeding
upon lianas by Neotropical LRFH than their Paleotropical
counterparts enhances palm survival in the Neotropics by
encumbering the palmsÕ competitors. Woody lianas may
reduce the survival, growth, and fecundity of arborescent
palms (Svenning, 2001); nevertheless, palms are well
equipped to avoid liana infestation, mainly because of the
1364 C. Cristoffer and C. A. Peres
continual shedding of their long leaves (Putz, 1984; Rich
et al., 1987). Note also that the abundance canopy palms in
upland rain forests is a phenomenon largely confined to the
Neotropics, Madagascar, New Caledonia, and a few other
islands (Gentry, 1988). These also happen to be places with
few large herbivores. Thus, the available information is
consistent with our hypothesis.
Smaller fruits and frugivore motility
We hypothesized that the removal of fragile vegetation by
large herbivores could thwart reproduction of small-fruited
plants, especially in the understorey. Since both terrestrial
and arboreal herbivores are larger in the Paleotropics, we
might expect them to feed on larger fruit, and they do:
Paleotropical fruits average larger than those in the Neotropics (Mack, 1993).
Since larger animals within trophical guilds tend to have
larger home ranges, we hypothesized that Paleotropical
frugivores would forage, on average, over larger areas than
their Neotropical counterparts (cf. Fleming et al., 1987).
The available information, although limited, supports this
hypothesis.
For example, there seem to be ecologically relevant differences between the Paleotropical hornbills (Bucerotidae)
and their purported Neotropical counterparts, the toucans
(Ramphastidae, in part). Hornbills are strong-flying, wideranging birds that could only have reached islands of
Malesia or the Malay Archipelago by flying over large
stretches of open ocean (Kemp, 1995). Hornbills such as the
wreathed hornbill (Aceros undulatus) move long distances in
search of patches of figs, thereby causing local populations
to fluctuate (Kinnaird et al., 1996). Similarly, red-knobbed
hornbills cover daily distances of up to 13 km (Poonsward
& Tsuji, 1994), and large flocks of wreathed hornbills might
travel more than 10 km between feeding sites and their roost
(Leighton, 1986; Tsuji et al., 1987). Hornbills in general
favour larger fruits taken from relatively few large trees, and
some of their foods are quite scarce (Kemp, 1995). Fruits
favoured by hornbills are both produced at infrequent
intervals (Lambert & Marshall, 1981) and ephemeral
(Leighton, 1982).
By contrast, toucans are not known to travel long distances, and massive die-offs of large monospecific flocks of
Ramphastos toucans attempting to cross large rivers have
been occasionally observed in central Amazonia (A. Whittaker, pers. comm.), presumably following a generalized
failure in fruit crops. Toucans are rather clumsy and weak
flyers that may fall into the water if they fail to achieve
sufficient trajectory when crossing wide rivers (Sick, 1993).
The course of their flight is undulatory and connects treetops that are rarely far apart. Indeed, the species ranges of
Amazonian toucans are effectively separated by river barriers (Haffer, 1974). Although quantitative data on toucan
home range sizes are few, one study reported that keel-billed
toucans (Ramphastos sulfuratus) have home ranges that vary
from 18 to 111 ha in size (Graham, 2001); this is far smaller
than those of three hornbill species that vary from 370 to
1000 ha in the breeding season to as much as 2800 ha in the
non-breeding season (Poonsward & Tsuji, 1994).
Hornbills may be better adapted than toucans to exploit
widely dispersed but large clumps of food. This in turn
suggests that the type and dispersion of fruits in Neotropical
forests – at least those consumed by toucans – is significantly
different from those in Paleotropical forests. Note that
although Paleotropical fleshy fruits are somewhat larger than
those in the Neotropics, fruit productivity in Neotropical
forests is equivalent to or greater than that in the Paleotropics (Hladik, 1978; Chapman et al., 1999; Ganesh &
Davidar, 1999).
Although data are scant, Paleotropical fruit bats (family
Pteropidae) also appear to fly farther when foraging than
do Neotropical fruit bats (family Phyllostomidae) (Nowak,
1999). The roosts of the African Eidolon helvum suggest a
foraging range of at least 30 km. Eidolon makes extensive
seasonal migrations; one colony left its roost in a forest in
the Ivory Coast in February, moved northward into the
savanna zone, and migrated at least as far as the Niger
River Basin by the middle of the wet season (Thomas,
1983). Some colonies in East Africa may make a round
trip of over 2500 km. Hypsignathus forage up to 10 km
from the roost at night (Bradbury, 1977) and Epomophorus wahlberg switches day roosts every few days and
flies up to 4 km from these to nocturnal feeding areas
(Fenton et al., 1985). Rousettus leschenaulti shifts in
response to the supply of fruit and can make foraging trips
of 40–50 km in a night (Lekagul & McNeely, 1977).
Cynopterus may travel 97–113 km in one night. Many
Pteropus mariannus have been found to move between
islands in the southern Marianas on an irregular basis
(Wiles & Glass, 1990). Most Pteropus species roost in
emergent trees that rise above the forest canopy and forage far from their roosts (Pierson & Rainey, 1992), and
populations on large land masses may travel 40–60 km to
feed. Nowak characterized Pteropus as strong fliers, and
Sterndale (1884) noted that a P. giganteus landed on a
boat 320 km from land.
By contrast, most New World fruit bats do not appear to
fly so far as some Paleotropical species. Carollia perspicillata
disperse nightly, with each individual going to two to six
feeding areas and flying an average of 4.7 km per night
(Heithaus & Fleming, 1978). Vampyrodes caraccioli bats
were found to emerge from their roosts and fly 850 m to a
fruiting tree, and visit several other feeding areas within a
restricted radius (Morrison, 1980). Female Artibeus jamaicensis fly an average of 8 km to forage (Morrison, 1978),
and the same species in Barro Colorado Island, Panama, flies
1–4 km between day roosts and feeding sites (Handley et al.,
1991).
With regards to use of the understorey or canopy, Bernard
(2001) reported that short-tailed fruit-eating bats, Carollia
perspicillata and C. brevicauda, feed principally on understorey plants such as Piper, Solanum, and Vismia (Fleming,
1988). In fact, C. brevicauda was exclusively captured in
ground nets, and just 8% of the captures of C. perspicillata
were in canopy nets.
2003 Blackwell Publishing Ltd, Journal of Biogeography, 30, 1357–1380
Macroevolutionary role of large herbivores 1365
Although pteropids are on average larger than phyllostomids (Cristoffer, 1987), considerable overlap exists in body
size. In fact, one feature of the overlap suggests that the
difference between the families is explained better by environment than by phylogeny. We refer to the genus Vampyrum and, to a lesser extent, several other related genera.
Vampyrum is a large bat with a wingspan of 1 m that
demonstrates that phyllostomids can reach a fairly large size.
Vampyrum, however, is a carnivore, not a frugivore. We are
aware of no physiological or morphological constraints on
phyllostomids that would render them incapable of being
both large and frugivorous, hence look to extrinsic, ecological causes. We suggest that the frugivorous/omnivorous
Phyllostomidae and Pteropidae differ in several ways relevant to this discussion.
Phyllostomids are omnivorous in general, but some genera
are more specialized as frugivores. Some of the frugivores
may even obtain protein via seed predation (Nogueira &
Peracchi, 2003), which is so far unrecorded for pteropids.
Omnivory enables them to feed on both animal and plant
food, thus they are able to subsist on small patches of forest
understorey or scrub that lack large-fruited trees. Small
understorey trees typically have small, easily-digested fruits
that are relatively evenly dispersed compared with largefruited trees, and produce small fruit crops for an extended
periods. Even if these fruit crops fail, the omnivorous species
are not necessarily forced to undergo the uncertainties of
migration or nomadism to find new fruit sources, because
they can subsist on locally available animal food. Echolocation enables them to navigate even in the darkest forest
understorey at night. The average densities of these species
tend to be high and probably less variable locally than those
of pteropids.
Since Old World frugivorous pteropids are on average
larger than their Neotropical counterparts, they probably
feed on, and therefore disperse the seeds of, larger fruit.
However, even good night vision requires a minimum
ambient light intensity, which may not occur in the forest
understorey at night. Therefore, their roost trees tend to be
relatively exposed and well illuminated. They are unable to
subsist on local fruits alone, or on animal matter (but see
Courts, 1998), so must forage more widely. Presumably
flying long distances in the canopy would be taxing of
energy. Fortunately, their specialized retinas permit them to
navigate well under an open sky, above the canopy.
Although they require scarce, high-quality fruiting trees,
their large body size and rather narrow wings are efficient
for flying long distances. They can occur at high biomass
densities locally but are patchy both in space and time.
These syndromes are not absolute and there are species in
each family that possess at least some of the characters
typical of the other. Nevertheless, we hypothesize that there is
a general New World/Old World dichotomy among tropical
forest frugivores. When New and Old World ecological
surrogates exist, we predict that OldWorld frugivores will
reach the largest size, will be the most mobile, and will feed
on the largest fruits. Furthermore, these fruits will be more
patchy in both space and time, and their seeds will be
2003 Blackwell Publishing Ltd, Journal of Biogeography, 30, 1357–1380
dispersed a greater distance. The bat fauna of New Guinea
provides tests of this.
New Guinea is inhabited by pteropid bats, not phyllostomids (Bonaccorso, 1998). On that ground, we would
expect it to have large, mobile, species that feed and roost in
the canopy. In fact, it does, especially in coastal areas and on
islands adjacent to New Guinea. However, New Guinea
lacks large herbivores, which should have resulted in selection pressures more similar to those in the mainland tropics
of the New World than in the Old. Therefore, we hypothesized that some of the New Guinea pteropids would
resemble their Neotropical counterparts. This is confirmed:
several of the pteropid bats described in Bonaccorso (1998)
have characteristics similar to those of phyllostomids. For
example Dobsonia anderseni feeds on subcanopy as well as
canopy fruits, and sometimes roosts in tree hollows and
caves, as does D. inermis; D. minor is highly maneuverable
in the understorey, feeds on introduced Piper fruits (which
are often consumed by phyllostomids), and is often caught in
traps less than 5 m above ground. D. moluccensis is able to
access understorey fruits not available to Pteropus, which
are sympatric; it even alights on the ground to obtain them.
Finally, the subfamily Nyctimeninae, which is endemic to the
vicinity of New Guinea (one species reaches mainland Australia), is considered convergent morpho-ecologically with
phyllostomids of the subfamily Stenoderminae.
We also hypothesized that anthropoid primates would
exhibit a size and foraging dichotomy. In the Neotropics, the
tiny, diurnal monkeys (families Callitrichidae and some
Cebidae) tend to feed on fruits that produce small crops over
long periods of time (Terborgh, 1983). Superficially, it
would appear that the Paleotropics have counterparts to
small monkeys among the prosimians. For reasons too
detailed to go into here, small Neotropical primates probably do not have obvious counterparts among small Paleotropical mammals; we refer to Charles-Dominique (1983)
and Sussman & Kinzey (1984), respectively, for discussion
of how small Neotropical primates differ ecologically from
prosimians and squirrels. The peculiarly small size of many
Neotropical anthropoids has been discussed elsewhere
(Leutenegger, 1979; Sussman & Kinzey, 1984; Cristoffer,
1987). We noted that the overlap in size between phyllostomid and pteropid bats suggested that there are no phylogenetic constraints on large size in phyllostomids. The
primates exhibit a similar overlap, suggesting that the size
discrepancy is imposed by natural selection rather than by
phylogeny. In general, the predominance of small frugivores
that feed on evenly-dispersed resources in several unrelated
families of Neotropical vertebrates supports the hypothesis
that a common constraint has shaped the evolution of their
foraging behaviour.
Are consumers of reproductive plant products more
important in the Neotropics?
Herbivores cause plants to divert resources from reproductive plant products (RPP) into defenses against herbivores, or
into repairing damage caused by herbivores (Marquis, 1984;
1366 C. Cristoffer and C. A. Peres
Bazzaz et al., 1987; Simms & Rausher, 1987; Hendrix &
Trapp, 1989; Doak, 1992; Mauricio et al., 1993; Sagers &
Coley, 1995; Strauss et al., 1996; Juenger & Bergelson,
1997; Strauss, 1997; Van Der Wal et al., 2000; but see
Gronemeyer et al., 1997). We suggest that there is a tradeoff between allocation to reproduction and defense against
large herbivores, resulting in a decrease in production of
reproductive tissue. This could then stymie the diversification of animals that consume reproductive plant products,
including nectar, pollen and fragrant oils.
ASSESSING REPRODUCTIVE ALLOCATION
AT A CONTINENTAL SCALE
It is difficult to compare reproductive effort in the Neotropics with that of the Paleotropics because there is no
single currency to measure reproductive effort. Furthermore,
when we speak of reproductive enhancement of Neotropical
plants, we are making a generalization. A more realistic
theory would accommodate the likelihood that large herbivores suppress many types of reproduction but enhance a
few others. For example, although large herbivore activities
probably diminish plant reproduction in many circumstances, they might actually enhance it for those plant species
whose fruits are especially adapted for dispersal by large
vertebrates. We would then need to somehow control for the
effect of the so-called Ômegafaunal seed dispersal syndromeÕ
(Barlow, 2000), as well as for grains, as elephants at least
tend to promote grassland over forest (Owen-Smith, 1988).
Measuring the relative importance of various plant defenses against both small and large herbivores is also difficult.
We hypothesized, however, that effects on vegetation
structure would be noticeable. At least one trait more likely
to be affected by large herbivores, namely physical fragility,
has been addressed (Emmons & Gentry, 1983).
We could also speculate on what characteristics contribute
to the fragility of Neotropical plants. Whitmore (1998)
suggests that mechanical toughness rather than chemical
composition is the major deterrent to insect herbivory, and
notes that softer, young leaves are preferred to older leaves
despite their greater chemical protection. Perhaps large
herbivores are more likely to damage tough leaves than are
insects, because they can generate bite forces over a larger
area. We have no direct evidence to assess this, but note that
among folivorous insects, larger individuals are able to bite
thicker leaves (c. Bernays, 1998).
We suggest that many fragile understorey plants in the
Paleotropics simply cannot invest as much in reproduction
and, therefore, produce less RPP. This lower allocation
could cut across many taxonomic lines, and therefore the net
result would be a reduced overall availability of RPP for
consumers. We will emphasize flower nectar and pollen,
nuts, fruit pulp, and seeds within fruits (other than grains)
more than others because they have been easier to study.
One of our first hypotheses to address this question is that
the aggregate biomass density of RPP consumers (except
those that specialize on grains and megafaunal fruits) should
be greater in the Neotropics than in the Paleotropics.
However, site-to-site variation due to factors such as soil
fertility and rainfall regime could obscure differences due to
large herbivore activities (or lack thereof) and thus the differences in consumer biomass density. Ratios of trophical
categories are frequently used in insect ecology (e.g. Warren
& Gaston, 1992; Basset, 1995). Therefore, a more relevant
measure of the effects of large herbivores might, in some
cases, be ratios of the aggregate biomass of consumers of
RPP to the aggregate biomass of consumers of some other
foodstuff. Thus, we might predict that a Neotropical site will
have a higher RPP: non-RPP ratio than a Paleotropical site,
regardless of their overall productivity.
Another hypothesis based on ratios is based upon the
generalization that primary productivity is a strong nonlinear predictor of primate species richness (Kay et al., 1997;
Mittelbach et al., 2001). Furthermore, fruit abundance is a
far better predictor of primate biomass than is vegetation
biomass, and the abundance of certain RPP resources, such
as large-seeded trees in the Lecythidaceae, may explain the
geographical distribution of pitheciines such as uakaries
(Cacajao spp.) and bearded saki monkeys (Chiropotes spp.)
(Peres & Janson, 1999; Stevenson, 2001). This suggests that
a greater availability of certain types of RPP make possible a
proliferation of RPP consumers. The examples we have
already given of small frugivores are consistent with the idea
that the small fruit component of RPP resources is especially
important in the Neotropics.
It does not necessarily follow, however, that a paucity of
megafauna should result in a decrease in species richness of
all taxa. For instance, large Paleotropical herbivores may
have obligate parasites that would not occur in the Neotropics because their hosts are absent. Another example of
megaherbivore facilitation pertaining to birds, concerns
vultures. The Pleistocene of North America had a morphologically more species-rich vulture fauna than does the
extant Nearctic, presumably because the Pleistocene ecosystem, which was much richer in megafauna, provided
more large-herbivore carcasses for scavengers (Hertel,
1994).
Nevertheless, the importance of the activities of large
herbivores in determining differences between the Neotropics and Paleotropics has received little attention, despite the
fact that herbivory has been shown to have a greater effect
on plant growth habits at sites with high biomass, such as
tropical moist forests, than at sites with low biomass (Bonser
& Reader, 1995).
RPP/non-RPP ratios
One rough measure of the potential suppression of the
proliferation of RPP consumers is the ratio of RPP species to
non-RPP species. For the latter, we primarily use predators,
which are unquestionably not directly dependent upon RPP.
Table 1 shows the species richness ratios of RPP consumers
to non-RPP consumers for Neotropical and Paleotropical
regions. We were unable to find exactly comparable sites for
each table entry, hence have indicated the extent covered.
Although species–area relationships, as originally pointed
2003 Blackwell Publishing Ltd, Journal of Biogeography, 30, 1357–1380
Macroevolutionary role of large herbivores 1367
Table 1 Species richness of various animal taxa, expressed as ratios between the number of species occurring in different regions of the Newand Old World tropics
Taxa*
N/O ratio N/A ratioà Geographic regions covered
Taxa dependent upon
reproductive plant parts
Toucans and Hornbills§
2.41
Parrots
6.27
Humming-birds and sunbirds
3.65
Trogons
3.0
Bees
>1.0
Butterflies
1.50
Fruit and flower-feeding bats
3.48
Taxa not dependent upon
reproductive plant parts
Herons
Raptors–
Ibises and storks**
Jacamars and bee-eaters
Owls (Strigidae)
Nightjars and nighthawks
Ducks and geese
Swifts
Kingfishers Swallows
1.0
0.9
0.88
2.33
0.69
2.56
0.57
1.13
0.71
1.0
1.64
6.27
2.21
4.5
>1.0
2.50
4.21
0.95
0.92
0.88
1.0
1.11
1.15
0.96
1.07
0.86
0.65
All of Neotropics & Paleotropics
Brazil, Senegal, the Gambia, Kenya, northern Tanzania, Indian subcontinent
Brazil, Senegal, the Gambia, Kenya, northern Tanzania, Indian subcontinent
Brazil, Senegal, the Gambia, Kenya, northern Tanzania, Indian subcontinent
All of Neotropics & Paleotropics
Costa Rica, Malaysia, Liberia
Mainland Neotropics, mainland Paleotropics and large islands (except Madagascar)
Brazil, Senegal, the Gambia, Kenya, northern Tanzania, Indian subcontinent
South America, Asia & Africa (including Madagascar)
Neotropics & Paleotropics
Brazil, Senegal, the Gambia, Kenya, northern Tanzania, Indian subcontinent
Brazil, Senegal, the Gambia, Kenya, northern Tanzania, Indian subcontinent
Brazil, Senegal, the Gambia, Kenya, northern Tanzania, Indian subcontinent
Brazil, Senegal, the Gambia, Kenya, northern Tanzania, Indian subcontinent
Brazil, Senegal, the Gambia, Kenya, northern Tanzania, Indian subcontinent
All of Neotropics, tropical Africa, mainland tropics of Asia plus large islands
Brazil, Senegal, the Gambia, Kenya, northern Tanzania, Indian subcontinent
*Data are from Gardner (1977); Handley et al. (1991); Sick (1993); Barlow & Wacher (1997); Robbins & Opler (1997); Fry & Fry (1999);
Grimmett et al. (1999); Nowak (1999); Zimmerman et al. (1999); Clements (2000); Michener (2000); Weidensaul (2000).
Number of species in the Neotropics: number of species in the oriental tropics.
àNumber of species in the Neotropics: number of species in the Afrotropics.
§Bucerotidae and Ramphastidae excluding New World barbets.
–Cathartidae, Accipitridae and Falconidae.
**Threskiornithidae and Ciconiidae.
Includes piscivorous species only.
out by MacArthur & Wilson (1963), would predict that
larger geographical regions should have a larger species
pool, the trophic ratios should be unaffected by area size
except in the extreme cases (e.g. the loss of large predators
from small habitat fragments). The taxa used were those for
which data were available, so it is possible that they were
somehow not representative.
Many taxa which varied in food habits were excluded for
clarity. For example, the Tyrannidae as arrayed in Sibley &
Monroe (1990) encompasses several trophically diverse groups
of birds, including cotingas, manakins, tyrant flycatchers, and
others. Furthermore, splitting tyrannids into smaller clades
does not clarify the situation, because there is substantial
dietary variation even within some subfamilies. Similarly,
phyllostomid bats display virtually the same dietary breadth as
the entire order Chiroptera, although in this case we felt
comfortable enough with the data to exclude those species that
differ dramatically in diet from the Paleotropical Pteropidae.
Kingfishers sensu latu are another example. Kingfishers
include the specialized piscivores in the Neotropics (Remsen,
1990), as well as many Paleotropical taxa that are partly or
entirely insectivorous, therefore, we compared only the fishcatchers. In most cases, we took pains to assure that our
admittedly subjective demarcations were made in such a way
that the selection would favour the null hypothesis, discussed
2003 Blackwell Publishing Ltd, Journal of Biogeography, 30, 1357–1380
below, rather than our own hypothesis. Likewise, guans
(Cracidae) overlap in use of fruits with toucans (Guix et al.,
2001); again, their inclusion would have strengthened our
hypothesis at the expense of the null hypothesis. Bees were
excluded from statistical tests because we lacked numerical
data, although the differences between continents are consistent with the alternative theory. As will be seen, these
concessions made little difference.
Our null model is that the ratio of the Neotropics to
Paleotropics for consumers of RPP should not be significantly
different than the ratio for consumers of other major dietary
guilds. The alternative model is that the ratio of the Neotropics
to Paleotropics for consumers of RPP should be greater than
the ratio for consumers of other foods. A Wilcoxon signed
ranks test (Agresti & Agresti, 1979) resulted in a P value of
0.0066 for a one-sided test. Thus, we can reject the null hypothesis that RPP-dependent taxa make up the same proportion of the fauna in the Paleotropics and the Neotropics.
The greater species richness of certain trophic guilds in the
Neotropics could be because of factors other than large
herbivore activities. The Pleistocene Refugia Hypothesis
(Haffer, 1969, 1974) has been used to explain the greater
species richness of various taxa in the Neotropics compared
with the Paleotropics. An alternative hypothesis to explain
Amazonian diversity patterns is the Riverine Barrier
1368 C. Cristoffer and C. A. Peres
Hypothesis (Wallace, 1852; Hershkovitz, 1972; Gascon
et al., 2000). Unfortunately, the Pleistocene Refugia and
Riverine Barrier Hypotheses predict a greater overall species
richness because of allopatric speciation, but they do not
specify which trophic categories will be most affected. By
contrast, we predict that consumers of RPP will be relatively
more important in the Neotropics than in the Paleotropics.
In other words, alternative hypotheses may explain why
there are so many Neotropical birds, but they do not explain
why so many of them feed on RPP.
Note also that allopatric mechanisms of speciation do not
incorporate constraints on species richness. More geographical isolation events simply correlate with more species, and
from this one can infer that if the Paleotropics had more isolating events, it would have more species. This seems simplistic
to us. The results of natural experiments, such as described by
Moulton & Pimm (1986), confirm that one cannot simply
pack similar species indefinitely. If unconstrained by energetic
or other limits, then combining habitat fragments producing
allopatric speciation by forest refugia and fluvial barriers,
would result in the sum total of all the species present in each
fragment. Most of the species produced by allopatric speciation within tropical forest isolates would have ecologically
similar sister species in other isolates, and it seems unrealistic
to us that so many similar species would co-exist indefinitely
when brought back into sympatry. In reality, energy, nitrogen,
nest cavities, or some other currency would be in short supply,
and not all species would survive. Our theory incorporates this
likelihood, at least at a coarse level.
Our intention here is not necessarily to replace one or
more hypotheses with another; the truth may be better
served by a combination. Thus, the forest refuges and river
barriers hypotheses provide a mechanism for speciation,
whereas we suggest what kinds of proliferations will be most
successful in independent evolutionary experiments moulded
by large herbivores.
We hypothesized that New Guinea, which lacks large
herbivores, would be inhabited by a disproportionate number of frugivorous and flower-feeding birds. This hypothesis
was supported. Beehler et al. (1986) noted that New Guinea
is unusual in supporting large numbers of fruit- and nectarfeeders. The roster includes obligate frugivores, which are
relatively uncommon elsewhere. For example, New Guinea
has twice as many fruit-eaters and nearly twice as many
nectar-eaters, as measured by proportion of the fauna, as
comparable lowland forest in Peru. Thus in some respects,
New Guinea, which lacks herbivores even as large as tapirs,
may contrast even more vividly with Paleotropical forests
than do the Neotropics.
Neotropical vs. Paleotropical flowers and their visitors
We hypothesized that since there are fewer LRFH in the
Neotropics to damage flowers and to force plants to allocate
resources to defense against large herbivores, that the Neotropics would have a greater diversity of pollination types
and would produce more RPP than those in the Paleotropics.
In fact, several pollination ÔsubsyndromesÕ attributed to non-
flying mammals are exclusive to the New World. One of
these is referred to as the Ôupright-flowered lowland tropical
syndromeÕ and the other is the Ômossy forest syndromeÕ
(Proctor et al., 1996). The absence of these syndromes in the
Old World is explicable with reference to large herbivores.
Let us assume for the moment that large herbivores would
consume many flowers given the opportunity. If, say, an
elephant attempted to eat a downward-facing flower, it
might still inadvertently be dusted by pollen as it thrust its
trunk among them, simply because gravity would cause
pollen to fall onto the trunk as the flower shook. By contrast,
an upright flower would not normally scatter pollen onto the
trunk. Natural selection might tend to eliminate upright
flowers from the population since they would not reproduce
as successfully. Upright flowers might also be more likely to
be detected and eaten by large herbivores.
Similarly, the mossy forest pollination subsyndrome might
not be viable in forests of low stature that are frequently
browsed by large herbivores. Since mossy forests exist in
both the Old World and the New World, the absence of the
syndrome in the former might be because of feeding by large
herbivores.
Proctor et al. (1996) list several other features of Neotropical flowers that are rare or absent in the Paleotropics.
Oil-producing flowers occur primarily in the Neotropics.
Note that oil is more expensive for a plant to produce than
sugar – another indication that Neotropical plants can
allocate more to reproduction. Bees are more diverse in the
Neotropics (Michener, 2000), which is reinforced by the
more regular flowering of Neotropical canopy trees, in
contrast to the irregular condition in southeast Asia.
Sucrose-rich nectars occur in flowers pollinated by hummingbirds, but not by passerines such as sunbirds (Baker &
Baker, 1983), and hummingbirds prefer sucroses over
hexoses (Hainsworth & Wolf, 1976). In fact, hummingbirds
will not even utilize flowers that lack sucrose altogether,
whereas sunbirds in the Old World take nectar high in
monosaccharides and will not utilize flowers that lack them.
Production of disaccharides should require more energy for
the plant than monosaccarides, thus hummingbird flowers
might produce more expensive nectar than do sunbird
flowers. This again suggests a greater allocation to
reproduction in the Neotropics. Curiously, most of the
sunbirds, flower peckers and megachiropteran bats that
pollinate Asian tropical trees are not even attracted to
understorey flowers, although they may often visit or even
confine themselves to forest gaps (Bawa et al., 1990). By
contrast, in the New World some species of both hummingbird and phyllostomid bat pollinators are understorey
specialists relying heavily on a few plant taxa exhibiting
prolonged or staggered flowering periods.
The plants most strongly associated with hummingbirds
are the bromeliads (Bromeliaceae), the most numerous of all
Neotropical epiphytes; the African-violet family (Gesneriaceae), a family of herbs and epiphytes; the large herb
Heliconia spp., related to the bananas; and the climbing
passion-flowers (Passifloraceae) (Proctor et al., 1996). The
growth habits of these plants might render them especially
2003 Blackwell Publishing Ltd, Journal of Biogeography, 30, 1357–1380
Macroevolutionary role of large herbivores 1369
prone to destruction by large herbivores. In Paleotropical
rain forests pollination by birds appears to be less common
than in the Neotropics and almost confined to the canopy, in
total contrast to the hummingbird-pollinated plants (Pettet,
1977; Appanah, 1981), although Cheke & Mann (2001)
note that some sunbirds occasionally visit understorey
flowers.
Hummingbirds are more specialized for exploiting flowers
than any Old-World birds (Stiles, 1981) and are the only
family in which most foraging is accomplished while hovering. This difference in foraging styles is reflected in floral
morphology (Westerkamp, 1990). By contrast, sunbirds are
more omnivorous, and will consume flowerheads, seeds and
fruit (Cheke & Mann, 2001). Paleotropical flower visitors
normally perch while feeding, and often forage in flocks
(Stiles, 1981). These traits appear to make them less suitable
for pollinating understorey plants than for large forest trees.
Furthermore, ornithophilous plants appear to be less
numerous in West Africa than in other parts of Africa
(Pettet, 1977), which suggests that adaptation to tropical
forest is not as great as in the Neotropics. Perhaps plants
similar to hummingbird–pollinated plants would be eaten in
the Paleotropics.
We hypothesized that RPP might be more evenly dispersed
in time in the Neotropics. Mass flowering is uncommon in
the Neotropics, but has been observed in southeast Asian
rain forests (Yap & Chan, 1990). We have little information
about this for the Afrotropics.
We hypothesized that understorey plants in the Neotropics
will be able to produce flowers over a longer period of time to
attract potential pollinators. According to Bawa et al.
(1990), understorey flowers produce just a few flowers at a
time, often spread throughout the year. This perfectly suits
the non-migratory habits of hermit hummingbirds (Phaethornis spp.), but not most Paleotropical flower visitors.
Similarly, DeVries (1987) discussed the peculiar life history and longevity of Heliconius and related Neotropical
butterflies. Unlike most butterflies, Heliconius is able to
utilize the nutrients in pollen in addition to nectar (Gilbert,
1975). The pollen-feeding behaviour centres around a group
of Psiguria and Gurania (Cucurbitaceae) vines, which flower
continuously over many years and produce mostly male
flowers. Perhaps these long-lived butterflies evolved only in
the Neotropics because only there is RPP consistently
available.
We hypothesized that Neotropical flowers will be able to
allocate more energy to enhance reproduction by thermogenic
respiration. Dynastine beetles (Scarabeidae: Dynastinae) also
exemplify the reproductive extravagance of the Neotropics
(Schatz, 1990). Approximately 900 species of Neotropical
plants may rely on dynastines for pollination. These plants
expend considerable energy attracting their dynastine mutualists by elevating flower and inflorescence temperatures.
Extinct Neotropical megafauna
One might wonder why the Pleistocene megafauna in South
America did not transform Neotropical forests as do large
2003 Blackwell Publishing Ltd, Journal of Biogeography, 30, 1357–1380
herbivores in the Paleotropics. If megafauna disappeared
only a few thousand years ago in the Neotropics, how could
the presence or absence of large herbivores explain the
interhemispheric discrepancies we have described?
We suggest that there is little evidence that large herbivores were common in the rain forests of the Neotropics since
the Miocene. South America has a rich fossil record of large
vertebrates, but there is no perfect method to determine
whether they lived in tropical rain forest.
We removed from consideration fossil faunas older than
the Miocene, on the grounds that the effects produced by
extremely ancient herbivores would become progressively
less important, and less detectable, with the passage of time.
We are also reluctant to include species that are believed to
have occurred outside the tropics. As many South American
fossil localities occur outside the lowland tropics, this greatly
reduced the number of fossils for consideration.
Indeed, perhaps instead of asking why the rain forests of
the Neotropics have so few fossils of large herbivores, may
be we should turn the question on its head and ask why the
Paleotropics have so many. What percentage of large herbivore fossils in other parts of the world actually come from
rain forests, as opposed to some other biome, such as
savanna? We believe that most large herbivores, outside of
Africa and Eurasia, have lived outside of rain forests. Again,
for the sake of argument, let’s assume this is true.
The question then becomes, why are Africa and Eurasia
(hereafter, Afrasia) different?
The answer may have to do with the sheer size of nonforested biomes that have occurred in Afrasia during the
Cenozoic. A world map of savannas, such as in Bourliére
(1983a), reveals a huge savanna area in Africa, a somewhat
smaller one in Asia, a medium-sized area in the Cerrado (and
a smaller area in the Llanos) of South America, a large but
very isolated one in Australia, and the rest all small pieces.
Furthermore, if you go back in time you will find extensive
tropical savannas in Asia and subtropical savannas in Europe (Potts & Behrensmeyer, 1980; Agustı́ & Antón, 2002).
So Afrasia as a whole has been a huge staging area for
savanna vertebrates. Populations could thrive in some temporarily isolated pocket, speciate, then later intermingle. A
review of later Cenozoic vertebrate evolution (Potts &
Behrensmeyer, 1992) suggests that alternating contraction
and expansion of different environmental conditions had
major effects on speciation, extinction, and overall diversity
of organisms linked to specific climatic conditions and
vegetation.
Furthermore, savanna formations have occurred in some
part or another of Afrasia since at least the late Miocene. For
example, although tropical savanna occupies only a small
portion of Asia now, the diversity of the savanna fauna of
the late Miocene Siwaliks of the Indian subcontinent is
unmatched today (Potts & Behrensmeyer, 1980). The large
extent of savanna biome would mean that large populations
of large animals could occur, and large populations spread
over a wide geographical area are theoretically less likely to
go extinct than small and localized populations. There is
good evidence that some Old-World savanna taxa have had
1370 C. Cristoffer and C. A. Peres
enormous geographical ranges in the past: there were
baboons (Papio and Procynocephalus), ostriches (Struthio),
gazelles (Gazella), cheetahs (Acinonyx), lions (Panthera),
giraffes (Giraffidae), aardvarks (Orycteropodidae), and hippos (Hippopotamidae) in Asia as well as Africa (Potts &
Behrensmeyer, 1980). If we think of biomes as islands, then
the tropical savanna island in the Old World is old, huge,
and rich in higher taxa. Paleotropical savanna could serve as
a source of emigrants to other biomes, such as rain forest.
Indeed, savanna mammals may have repeatedly colonized
the forests of Africa (Kingdon, 1974). More recently, Smith
& Wayne (1997) implicate the savanna/rain forest ecotone,
often greater than 1000 km wide, in generating rain forest
biodiversity. With regard to the great biotic interchange
between North and South America in the Pliocene and
Pleistocene, Webb (1985) and Marshall (1988) suggested
that the greater success of the North American fauna could
be explained in part by the much greater Ôstaging areaÕ and
faunal diversity in the North.
By contrast, South America was much more isolated than
Africa, and there was no land connection between South
America and any other continent from the late Cretaceous
until the end of the Pliocene (Carroll, 1988). We suggest that
a large biome island (such as Afrasian savannas) is more
likely to produce emigrants than is a small biome island,
such as the South American savanna. This occurs for several
reasons. First, there is the sheer disparity in population sizes
of species that could serve as potential colonists. Secondly,
large areas typically have more species than small areas
(MacArthur & Wilson, 1963), hence potential colonists
from a small biome fragment attempting to establish a
beachhead in a new biome would be up against a species-rich
community of competitors, predators, diseases, parasites,
and plants protected with potent allelochemics.
To assess this possibility we perused literature pertaining
to the birds of the Neotropics and Paleotropics. We hypothesized that the ratio of species richness inhabiting savanna
and forest would differ depending on the relative size of each
biome on each continent. This was confirmed, assuming that
we rely on subjective information about niche equivalencies
from the literature. One comparison would be of Neotropical jacamars (Galbulidae) with their Paleotropical
counterparts, the bee-eaters (Meropidae). The former are
overwhelmingly forest birds, but there are approximately
three times as many species of bee-eaters restricted to open
habitats as those found mainly in forests (Fry & Fry, 1999).
A similar comparison could be made of African and South
American hornbills and toucans, using information from
Kemp (1995) and Short & Horne (2001). There is only one
species of South American toucan that prefers open habitats
(Ramphastos toco). Since there are c. 25 species of toucanlike Ramphastids in lowland South America, c. 4% of them
could be said to prefer savanna. By contrast, of those African
hornbills that exhibit a pronounced preference for either
tropical forests or savannas (defined broadly), 69% prefer
forests and 31% prefer savanna. Even red-legged seriemas
(Cariama cristata), a quintessential savanna species from
Brazil, has a relative, the black-legged seriema (Chunga
burmeisteri), that is more often found in chaco, forest, and
forest edge (Schmitt & Cole, 1981). Thus in the Cerrado
scrublands, there are few bird taxa at the level of family or
above, in which most of the species are savanna specialists.
We also hypothesized that the Brazilian Cerrado, which
occupies a much smaller fraction of the South American
continent than does forest, would show evidence of substantial colonization by forest fauna. This is confirmed.
Marinho-Filho et al. (2002) note that fewer than 17% of the
Cerrado mammal species are restricted to open areas, 29%
are exclusive to forests, and 54% occur in both. Only one
species of Cerrado cervid, the pampas deer Ozotoceros
bezoarticus, rarely occurs in forest, and even this species
lacks some features found in extreme savanna dwellers (e.g.
zebras and wild asses, family Equidae) in Afrasia. For
example, pampas deer are not highly specialized grazers
(Rodrigues & Moneiro-Filho, 1999), and they apparently
lack endurance and produce neonates that hide rather than
immediately follow the mother (Geist, 1998).
Movement into more open habitats, such as woodland
savanna, savanna, and scrub, favoured a suite of adaptations
among ungulates (Vaughan, 1978; Geist, 1998). These
include, but are not limited to: large body size, springing
ligaments in the foot, reduction of toe number, elongation of
distal foot elements, elongation of the digestive tract,
rumination, development of a rete mirabile to cool the brain
during running, and high-crowned or ever-growing teeth.
Not all ungulates of open habitats possess all of these
adaptations, but it is conceivable that successful colonists of
open habitats possessed most of them. Note that with the
possible exception of pacas, all LRFH in the Neotropics
belong to families that immigrated from North America,
which had an extensive fauna of savanna or savanna
woodland herbivores in the Miocene (MacFadden, 2000).
Furthermore, some of these may have had their ultimate
origins in Afrasia. For example, deer, family Cervidae,
occurred first in Afrasia, then North America, then South
America. We suggest that some of the adaptations acquired
by savanna species have proved useful in colonizing rain
forest.
Nevertheless, although the large mammals of rain forests
might have originated elsewhere, it also seems plausible that
few extra-forest large herbivores might have the characteristics necessary to colonize rain forests. We suggest that only
very large extents of savanna or similar biome would produce a diverse enough array of species of which at least a few
have the characteristics needed to successfully colonize rain
forest. The history of the planet is full of examples of species
with special adaptations colonizing new areas. Some of the
characteristics acquired by herbivores during the extra-forest
phase – such as high mobility – might enable large herbivores
to colonize rain forest.
One could argue that the paleofaunas existing prior to
human contact demonstrate that large herbivores inhabited
tropical rain forests. The evidence for this is, however,
equivocal. First, many South American paleofaunas are
dominated by grazers (Anaya & MacFadden, 1995) or have
other characteristics indicative of open habitats. To consider
2003 Blackwell Publishing Ltd, Journal of Biogeography, 30, 1357–1380
Macroevolutionary role of large herbivores 1371
just one example, the pollen flora of the Pleistocene Tarija
site in Bolivia is composed almost entirely of grass species,
and therefore the locality is reconstructed as a predominantly dry open-country grassland with scattered trees and
shrubs that were mostly concentrated along the margins of
rivers and lakes (Yoshida & Yamazaki, 1982). Based upon
this and morphological and isotopical data from large herbivore fossils, MacFadden & Shockley (1997) considered
many of the large herbivores from the Tarija site to be grazers. Although savannas are known to be inhabited by rich
faunas of browsers and grazers, a diverse fauna of large
grazers is inconsistent with pristine tropical rain forest habitat. Since most post-Oligocene, South American faunal
assemblages contain several species of grazers (MacFadden,
2000), we find it difficult to envision rain forest as a suitable
context for them. Furthermore, many fossil sites in South
America are at too high a latitude or too high an altitude to
sustain tropical rain forest. Thus, many of the large herbivores that lived during the later Cenozoic in South America
may not have inhabited tropical rain forest.
The caveats of Kay & Madden (1997), which pertain to
one of the best-studied Neotropical ÔforestÕ paleofaunas
containing large herbivores, are particularly instructive.
They note that we are ignorant of nearly all taphonomic
processes in tropical lowland forest environments. Hence,
taphonomic and sampling bias may impair our knowledge of
what species were present, such that taxa at the same locality
could have been derived from several different habitats.
They further note that the percentage of arboreal species is
not as high as that commonly found in modern rain forests.
They concluded that the site was more likely a forest mosaic
(e.g. disturbed riparian succession), rather than a continuous, uninterrupted, multistratal, evergreen forest. We are
unable to locate any paleofaunas from South America for
which we are reasonably certain that large herbivores were
common in uninterrupted, multistratal, evergreen forest.
Large herbivores may have been common in the vicinity of
rain forests in secondary forests (e.g., rhino references
above). Kay & Madden (1997) specifically mentioned
riparian mosaic, aquatic, river-margin, and tree-fall gap
habitats as having the potential to sustain an abundant fauna
of large herbivores. They also noted that today, open
clearings are maintained within forests by the activities of
megaherbivores (Laws, 1970; Owen-Smith, 1988). The
natural history information, we presented earlier pertaining
to African forest elephants and Asian rhinos suggests much
the same thing. We, therefore, envision ancient Neotropical
forests virtually empty of large herbivores in their interiors,
but sustaining them at the edges. Pleistocene extinctions of
Neotropical megaherbivores would not have adversely
affected the rich fauna of small herbivores, frugivores, and
flower-feeders, and might even have been of benefit to them.
The co-existence of primary forest and savanna faunas in
close proximity still occurs in South America. For example,
the Cerrado landscape of Brazil and Bolivia, which is a
mosaic of grasslands, shrublands, gallery forests, and more
continuous woodlands, is home to a mix of mammal species
from both open habitats and closed forest. In close juxta 2003 Blackwell Publishing Ltd, Journal of Biogeography, 30, 1357–1380
position can be found tree sloths (Bradypus variegatus) and
four genera of primates (Callithrix, Aotus, Cebus, and
Alouatta), as well as pampas deer and hoary foxes (Pseudoalopex vetulus) (Marinho-Filho et al., 2002). A similar
interdigitation of forest-dwelling and open-habitat species is
also apparent in the avifauna (Macedo, 2000). Note, however, that this does not mean that all the species are evenly
distributed within the habitat mosaic: a tree sloth and a
hoary fox do not occur in the same habitat. We suggest that
virtually all the trophic impacts of large extinct Neotropical
herbivores could have been confined to areas outside closedcanopy tropical evergreen forest, although the animals might
penetrate the forest temporarily to escape direct exposure to
hot sunlight, or seek cover from predators.
We hypothesized that Africa has more families of
savanna-adapted birds than the Neotropics. This was confirmed by Fry (1983). Similarly, until recent deforestation by
humans, the lowlands of Madagascar were largely forested,
and the savanna avifauna of Madagascar is depauperate
compared to that of mainland Africa. Madagascar lacks over
twenty African families, including many with important
savanna representatives (Dorst, 1972).
By contrast, although savanna dominates a large portion
of the Old-World tropics, there are places elsewhere that
tropical forest, by virtue of its large extent, dominates open
biomes. Howell (1971) notes that small savannas in Nicaragua have only twenty-six resident bird species, only a tiny
fraction of the number found in the Llanos or Cerrado.
The distribution and abundance of extant large herbivores
suggests that large body size may be a handicap to rain forest
species. We, therefore, hypothesized that selection against
large body size would be discernible in forest races or sibling
species of those species that occupy both savanna and rain
forest. This is confirmed for several species: in Africa forest
elephants, and buffalo are smaller than their savanna (bush)
counterparts (Kingdon, 1974). The same principle also often
seems to be the case when we compare species within the
same family: the forest-dwelling hyraxes (Procaviidae), hippos (Hippopotamidae), giraffes and okapis (Giraffidae) and
pantherine cats (genus Panthera) are smaller than their opencountry counterparts. In a review of Cenozoic vertebrates
and their habitats, Potts & Behrensmeyer (1992) noted that
with increasing aridity and decreasing tree cover in the midMiocene, larger-bodied rhinos replaced the medium-sized
forms. In South America, the largest cavy (family Caviidae),
Dolichotis patagonum, occurs outside of rain forest. The
same is true for deer (Blastoceros dichotomus), toucans
(Ramphastos toco), and canids (Chrysocyon brachyurus).
Furthermore, the jaguars (Panthera onca) are considerably
larger in the primarily open Pantanal wetlands than in the
rain forests of Amazonia and Belize (Sunquist & Sunquist,
2002).
Note also that all the Paleotropical rain forest herbivores
with a greater biomass than that of the largest Neotropical
herbivore belong to just three orders and three to six families
in any given forest: Proboscidea (Elephantidae), Perissodactyla (Rhinocerotidae), and Artiodactyla (Bovidae and perhaps one species each from Suidae, Hippopotamidae and
1372 C. Cristoffer and C. A. Peres
Cervidae). Several smaller species are similar in size to
Neotropical tapirs, including the Malayan tapir (Tapirus
indicus), gorilla (Gorilla gorilla), and okapi (Okapia johnstoni). Note, however, that the same families are not equally
represented in both Africa and Asia: Africa lacks rain forest
rhinos, deer, and tapirs, whereas Asia lacks rain forest
giraffids and hippos. Furthermore, several species seem to
lack the full suite of key adaptations that could occur in rain
forest herbivores. Kingdon (1974) suggested that the smaller
geographical range of gorillas than of chimpanzees (Pan
troglodytes) reflects an incomplete adaptation to a terrestrial
herbivore niche. In particular, if gorillas are compared with
similar-size bovids, it can be seen that they have relatively
unspecialized digestive tracts and are less cursorial.
The anthropoid primates also support a New-World/
Old-World dichotomy. The earliest Old-World anthropoids were adaptively more similar to the New-World
platyrrhines than to later anthropoids in their relatively
small size, paucity of folivorous taxa, and absence of
terrestrial forms (Kay & Simons, 1980; Fleagle & Kay,
1985). This suggests that Paleotropical forests were later
subjected to a drying of the climate and reduction of tree
density (McCrossin et al., 1998), that selected for terrestrial adaptations in primates. Ancestral Cercopithecus, the
most speciose African primate genus, passed through a
stage in which their habits were more terrestrial and their
habitat less densely forested (Kingdon, 1974). Their subsequent success upon recolonizing forest could have been
made possible by adaptations acquired in savanna or
woodland savanna. Note that the Old-World cercopithecids have either cheek pouches or sacculated stomachs,
adaptations that could have arisen as a result of foraging
constraints imposed by environmental change. Kingdon
(1997) also pointed out that the subfamily Cercopithecinae
is much more speciose in Africa than is the subfamily
Colobinae, and that the former recolonized forest more
recently. It thus seems plausible that the adaptations that
the Cercopithecinae acquired in non-forest environments
were particularly beneficial later. Note also that true
ruminants, which may have evolved their food processing
specialization as habitats opened up (Geist, 1998), did not
evolve in South America, but colonized it.
Furthermore, climatic changes that increased savanna at
the expense of forest might have eliminated some forestdependent species, thereby providing unexploited forest
resources for immigrant species. The general picture that
emerges is that in Africa – and perhaps in Miocene Asia – the
savanna biome has been so extensive, and the large mammal
fauna so rich, that understudies have always been available
in the savanna to enter the rain forest evolutionary theatre
and fill in for missing forest fauna.
The propensity of large herbivores to disappear from
biome fragments could be explored by examining the fauna
of islands that once were part of continuous habitat but are
now just fragments. We, therefore, hypothesized that the
species richness of large mammals from the islands of
Sundaland would be less than on the Asiatic mainland. This
was confirmed: although various islands in the area have
several species of large mammals, none has as many as
mainland Thailand (Francis, 2001).
In the Neotropics, and in most tropical areas of the world
outside of Afrasia, forest predominates over savanna. We,
therefore, hypothesized that the number of species in these
smaller savannas would be less than in Afrasia. This was
confirmed for ungulates, using data from Bourliére (1983b).
Thus, the Llanos of South America has only two ungulate
species, and both are derived from forest. The Cerrado is
considerably larger, so there was more opportunity for
evolution and persistence of savanna fauna, and there are six
or seven species of ungulates present. Overall, however,
many of the Cerrado vertebrate species are either generalized
forms that can live in both grassland or forest, or they are
closely related to, and presumably derived from, forest
forms.
Therefore, we assume that small biome islands (such as
Neotropical savannas enmeshed in a matrix of tropical forest, Caatinga, and Chaco) are more likely to import immigrants than to export emigrants. We suggest that the main
reason that there have been so many large herbivores in the
Afrasian rain forest during the latter half of the Cenozoic, is
that they have colonized from outside the forest. We,
therefore, theorized that rain forest is not a suitable biome
for most large herbivores, as we can see by looking at
tropical forests in the rest of the world.
We have conjectured that there may be an adaptation or
adaptations that animals acquire when outside the rain
forest, that they or their descendants possess when they
recolonize. The conquest of land by tetrapods might be an
instructive analogy. Evolutionary biologists argue that fish
evolved legs and toes not to walk on land but in order to
move underwater (Zimmer, 1998). The morphology of the
first tetrapods could then be considered a pre-adaptation or
exaptation to enhanced vagility on land. Perhaps large herbivores in rain forests inherited enhanced vagility from their
extra-forest ancestors. Enhanced mobility would enable the
colonists to acquire the widely distributed resources they
need, including a variety of browse and fruits, mineral licks,
drinking water, and mud wallows. This is consistent with the
fossil record, which indicates that ungulates became highly
cursorial prior to their alleged predators and a need for large
herbivores to move long distances to track resources (Janis
& Wilhelm, 1993).
We hypothesized that most large herbivores living in rain
forest in the Holocene are more mobile, and move more
widely over the landscape to meet their needs than did most
extinct, large Neotropical herbivores. We have no direct
means to compare the mobility of fossil Neotropical herbivores with herbivores from the Holocene. We do, however,
know that Holocene rain forest herbivores often move large
distances, as we noted above.
By contrast, some large Neotropical herbivores would
have been hard pressed to move long distances; the multi-ton
sloths of several families come to mind. For example, two of
the three genera of fossil sloths at one sight were highly
modified for digging (White, 1997; Bargo et al., 2000),
compromising the speed of above-ground, terrestrial
2003 Blackwell Publishing Ltd, Journal of Biogeography, 30, 1357–1380
Macroevolutionary role of large herbivores 1373
locomotion. Perhaps unsurprisingly, McDonald (1997) suggested that the earliest ground sloths inhabited open woodland, and a preference for open or semi-open habitats
persisted throughout the latter part of the Cenozoic. Similarly, only very slow locomotion was likely to have been
possible for the tank-like glyptodonts, family Glyptodontidae (Carroll, 1988). If one considers the six genera of cingulates (armored mammals such as armadillos and
glyptodonts) at one of the better-studied sites, LaVenta in
Colombia, no single habitat type emerges (Carlini et al.,
1997). Only one of the genera present, the 2-kg armadillo
Nanoastegothermium, was considered to be restricted to
humid forest, and only one other genus, Anadasypus, even
inhabited humid forest. All of the genera larger than 15 kg
were considered to be primarily inhabitants of savannas.
Food habits can also be suggestive of habitat. Although
browsers occur in both forest and savanna, a diverse array of
grazers is inconsistent with unbroken primary rain forest.
Furthermore, grazers tend to be large, so as to accommodate
long digestive tracts that can process low-nutritive-value
forage (MacFadden, 2000). There is usually a strong predominance of grazers in the mammalian paleofaunas of
South America, which suggests a period during the middle
Tertiary of extensive grasslands that were inhabited by
endemic Neotropical herbivores, such as notoungulates
(MacFadden, 1995). We, therefore, hypothesized that many
Neotropical fossil herbivores would possess dental characteristics, such as hypsodonty, associated with open-country
habitat. This was confirmed. A review of fossil mammals
from South America indicates that many species of large
herbivores were grazers; in fact, some achieved hypsodonty
millions of years before their supposed counterparts in North
America (MacFadden, 2000). Unfortunately, few fossil
assemblages can be unequivocally assigned to a particular
biome; furthermore, the fossil record for rain forests is poor.
Large herbivores in small biomes may be prone to
extinction, as follows. One could also make predictions
about how many endemics should occur in a taxon, based
upon population size. That is, species that persist in large
population sizes should be less prone to extinction, hence
there should be more surviving endemics in taxa with large
population sizes. It follows that species with large geographical ranges should be less prone to extinction, since
(other things being equal), they will have larger population
sizes (MacArthur & Wilson, 1963; Brown & Maurer, 1987).
As plants are more abundant than vertebrates, there should
be more endemic plants than vertebrates. Likewise, as
ectotherms are more abundant than endotherms, we would
predict that there should be more endemic herptiles than
endemic birds and mammals. Thus, we hypothesized that the
percentage of endemics of a typically-sized biome decrease
from plants, to ectothermic vertebrates, to endotherms.
Furthermore, since large endotherms exist at lower densities
than small endotherms, we expect that the larger endemic
endotherms will have a higher extinction rate, hence there
will be more endemics among smaller species. These
hypotheses were confirmed. The flora of the Cerrado of
Brazil and Bolivia is perhaps the richest of any savanna,
2003 Blackwell Publishing Ltd, Journal of Biogeography, 30, 1357–1380
c. 10,000 species, and about half are endemic (Heringer
et al., 1977; Oliveira-Filho & Ratter, 2002). The endemism
of the Cerrado herpetofauna is c. 21% (Colli et al., 2002),
and the avifauna, which at more than 800 species (some
specialists say over 900 species) is very rich, but has only c.
4% endemics (Silva, 1995). Finally, within the Cerrado
theriofauna it is the small species that are endemic (MarinhoFilho et al., 2002); presumably the larger population sizes of
small endemic mammals tend to buffer them from extinction.
New Guinea exhibits a similar pattern. Using figures from
Bonaccorso (1998), the endemism for vascular plants ranges
from 70% to 76%; for amphibians, 67%; for mammals,
24%; and for birds, 11%. Hence, our hypothesis was supported; over long spans of geological time, the guild of
species of large herbivores accumulating in a typical tropical
forest region, such as in the Neotropics, will not be particularly large. Only in Afrasia are conditions optimal for a
high species richness of LRFH to develop.
We earlier noted that the activities of large herbivores
might tend to retain habitat in a state compatible with their
persistence. It is also plausible that the activities of some
large herbivores could increase the likelihood that others
would colonize. We have noted that large herbivores in
tropical forests disperse large fruits and create wallows,
paths and gaps into which forage plants can grow. Perhaps
LRFH are less likely to colonize rain forest if other LRFH
have not already become successfully established.
We have no reason to assume that the effects of large
herbivores follow an all-or-nothing pattern. We noted above
that tree density increased gradually with a decrease in
species richness of large herbivores on Asian islands. Thus, it
is quite plausible that large herbivores were present in the
Pleistocene forests of the Neotropical rain forests at low
species richness and low biomass densities, thereby affecting
the forests in only a minor way.
A diverse array of large herbivores on New Guinea prior
to human occupancy of the area might have been expected to
alter tree diversity and abundance, so that the aforementioned trend would be incongruous. We, therefore, hypothesized that New Guinea would not have a diverse record of
extinct LRFH. This was confirmed: the paucity of large
herbivores in New Guinea is not new. Flannery (1995)
reported that none of the species of extinct theriofauna was
very large and only ten species (<5% of the total) are known
or suspected to have become extinct during the late Quaternary. Furthermore, the largest New Guinea mammal
known, which weighed 200–400 kg, may not have survived
past the Pliocene.
Milewski & Diamond (2000) argue that three micronutrients (iodine, cobalt and selenium) are necessary for the
metabolism of large herbivores, and that the scarcity of
sources of these micronutrients limits large herbivore abundance and distribution. They considered South America to
be a nutrient-poor continent that did not have the potential
to attain the biomass densities of large mammals that prevail
in some of the more pristine parts of Africa and Asia. Even if
a few species of LRFH were present in Neotropical forests,
their relatively small biomass densities may have hardly
1374 C. Cristoffer and C. A. Peres
affected the evolution of primary Neotropical rain forests.
Indeed, a survey of Pleistocene mammals from western
Amazonia did not reveal a single extinct taxa confined to
forest habitat; at best, some could be considered to be forest
edge species (Rancy, 1999).
As a final comment on paleofaunas, we would be remiss if
we did not explain why Central America has not been discussed. The reason is simply that there are confounding
variables that frustrate easy analysis. These include the
presence of savanna vertebrates in North America, the rugged topography (which might allow herbivores to climb
from one biome to another), the relative recency of emergence of the Panamanian Isthmus, and the fact that many of
the potential rain forest colonists originate in temperate
climates. Thus, we emphasized Neotropical rain forests in
South, not Central America.
CONCLUSION
Large herbivores affect rain forests in many ways, only some
of which have been addressed herein. Indeed, earlier drafts
of this paper contained many untested hypotheses. Given the
known importance of large herbivores in Paleotropical forests, it is rather surprising that few have speculated on the
consequences of a lack of large herbivores in Neotropical
forests. This question is of more than academic interest,
because the threats faced by large herbivores in the Paleotropics, and the introduction of exotic livestock, have
modified selection pressures on these forests. We suggest that
anthropogenic disturbances introduced by humans
throughout the low-latitude humid tropics can bring about
the same selective pressures that can functionally homogenize biotas on a pantropical scale, thus replacing the very
different, natural selection pressures that had previously
operated in the Paleo- and Neotropics.
ACKNOWLEDGMENTS
Many of the ideas presented in this paper evolved from our
days in graduate school at the University of Florida (1984–
88). We thank our fellow graduate students and professors
at that time, including John Eisenberg, John Robinson, Brian
McNab, Kent Redford, Jay Malcolm and Peter Feinsinger,
for the initial impetus, stimulating discussions and encouragement. For additional discussions over the years of tropical communities and species diversity we thank John
Terborgh, Carel van Schaik, Al Gentry, Louise Emmons,
Colin Chapman, Andrew Jones, Richard Bodmer and John
Fa. Carlos PeresÕ fieldwork in Neotropical forests (1984–
2002) has been funded by the Wildlife Conservation Society
and Conservation International. We thank Anina Carkeek
for constructive comments on the manuscript.
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BIOSKETCHES
Cris Cristoffer is a Natural Resources Planner at Luke Air
Force Base in Arizona. His primary research interest is in
developing gestalts of natural communities and how they
function, so that their pasts can be revealed and their
futures preserved. He has a special interest in comparing
the evolution and ecology of certain taxa of organisms,
and in giving advice to park managers.
Carlos Peres, Reader in Tropical Ecology at the Centre
for Ecology, Evolution and Conservation, University of
East Anglia, UK, has had a lifetime interest in the ecology
and conservation of wildlife populations in Neotropical
forests. His studies on forest vertebrate species and
assemblages focus on responses to different forms of
anthropogenic disturbance including hunting, forest
fragmentation and wildfires.
2003 Blackwell Publishing Ltd, Journal of Biogeography, 30, 1357–1380