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Community evolution in forest habitats
Community
Peter Andrews Department of Palaeontology, Natural History Museum, Cromwell Road, London, U.K. Received 1 April 1991 Revision received 5 October 1991 and accepted 5 October 1991 Kgwords: Eocene, Miocene, community, evolution, ecology, primates.
evolution
in forest habitats
Hominoid primates have had a mainly tropical forest distribution throughout their history. At present, the forest habitats occupied by apes include a variety of vegetation types, for example lowland evergreen tropical forest, montane evergreen forests, medium altitudesemi-deciduous forests, and even deciduous forest-scrub. A similar spectrum of vegetation types appears to have been occupied by Eocene and Oligocene primates, as well as at least some of the Miocene apes in Africa. The nature of these habitats is investigated both by reviewing the adaptations of the mammals in relation to the floral composition and by investigating the community structure of the mammalian faunas. Community structure is measured by body size spectra, dietary guilds, trophic patterns and diversity indices, both analysed separately and in combination using multivariate techniques. Comparisons are made between the Eocene and Present in order to document the changes in community structure which occurred during this time, with special attention being given to primates. Taxonomic shifts that have occurred in the East African mammalian faunas between Miocene and Present have produced little change in the community structure, indicating that Miocene forest habitats were structurally similar to those of today, whereas the differences observed in the Eocene faunas represent both a taxonomic and an ecologic change. Between the late Eocene and early Miocene there was a reorganization ofmammalian community structure for which an explanation must be sought, either in changes in the relationships between mammals and plants between the Eocene and Present or in ecological changes in forest habitats during this time. Journal of Human Euolution (1992) 22,423-43&I
Introduction In 1970, John Napier attempted a synthesis ofwhat was then known about palaeoecology in the Cenozoic. He drew on a very wide variety ofsources, including pollen, coral distribution, sedimentary analyses, and interpretations of insect, snail and mammal faunas (Napier, 1970). Some of our interpretations have changed since that time with increasing knowledge but the rationale behind palaeoecology remains the same: “paleoecology provides the opportunity for asking questions about primate evolution”, for example through the relation between adaptive significance of primate morphologies and the environment in which primates lived (Napier, 1970: 56). This is as true today as when Napier wrote these words. Also, and remarkably ahead of his time, Napier claimed that palaeoecology could “confirm inferences obtained from comparative studies of living animals regarding the probable characters of common inheritance with the palaeocological situation in which they are believed to have evolved” (Napier, 1970: 56). By these means, the adaptive significance of characters relating to such behaviours as knuckle-walking of apes, slow climbing of lorises, loss of thumb in African colobines, and many others, can be assessed. In his 1970 paper, Napier raised many questions, most of which we are no more able to answer today than he was then. I am going to consider a topic that he touched on briefly; the distributions offossil primates in relation to changing forest types from the Eocene to Present. Tropical rain forest has been important in the adaptive radiation ofmany groups ofprimates, ive in various types offorest, and then as now for the great majority ofliving primates (88%) 1’ “we can make the assumption that the key to the zoogeographic history of the primates and the adaptations that led to the emergence of the major radiations, lies in the distribution, the 0047-2484/92/4-50423
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P. ANDREWS
floristic composition and the seasonality of Cenozoic forests” (Napier, 1970:76). But were these forests of the past structurally and ecologically similar to those of today? The living apes occupy a range of forest types at the present time, extending even to dry deciduous forestbush (Collins & McGrew, 1988). Similarly, in the past, fossil apes have been reported from tropical rain forest (Andrews & Van Couvering, 1975; Kappelman, 199 I), more open types ofwoodland (Andrews & Evans, 1979), open country (Shipman, 1986), and monsoon forest (Andrews, 1990). Some of these interpretations have been disputed, but it is clear that different groups of fossil apes had a wide range of habitat preference. What is not clear from these studies, however, is how past forest habitats compare with recent ones and whether there has been any substantial change in the nature of the habitats themselves, which may have affected the adaptive radiation of the hominoid primates. In this paper, therefore, I am going to investigate the ecological characteristics ofpast habitats and make comparisons with present day tropical forests, to try and determine the extent to which it is possible to interpret the past and to what extent forest habitats, and their mammalian communities, may have changed through time. I will focus on two sets of data, faunas and floras from the Eocene of southern England and the Miocene of East Africa, and these will be compared with analyses ofrecent tropical floras and faunas. The fossil biota are ones with which I have some first hand knowledge, and they are chosen on this basis, with no implication that they are representative of, for instance, the Eocene of North America or the Miocene of Eurasia. Perhaps this work will stimulate others more familiar with these times and regions to accord them similar treatment, either to substantiate or refute my conclusions.
Recent forest
zones
A detailed account offorest zones will be published elsewhere (Andrews, in prep.), and for the purposes of the present paper a short summary must suffice: Tropical rain forest (TRF; Richards, 1952) is characterized by abundance of trees, lianes and epiphytes, with complex one- to four-storied canopy structure; most tree species are broad-leaved evergreen species; confined today to lowland tropical areas with high year-round rainfall. Paratropical rain forest (Wolfe, 1979) is structurally similar to TRF but with never more than two tree stories; it is characterized by low proportions offacultatively deciduous tree species and conifers, and also some temperate species; found today in the high-latitude tropics. Tropical deciduous forest and semi-evergreen forest are structural variants of TRF; species richness and canopy complexity are both less than in TRF; they are confined to tropical regions but in areas of seasonal drought, either caused climatically, e.g., in rainshadow areas, or edaphically, e.g., where the soil is poor. Tropical montane forest is characterized by extreme variation in canopy structure arising from topographic variation, varying from evergreen to deciduous; often growing in poor light conditions due to prevailing cloud; limited to areas above 1500 metres near the equator, but lower towards the tropics. Summerwet forest is characterized by more open, forest/grassland mosaic pattern of vegetation; deciduous tree species predominate in the strongly seasonal climates; found today at the limits and beyond of the tropics, sometimes called subtropical or monsoon forests. Temperate/subtropical evergreen forest (Wolfe, 1979) is composed ofbroad-leaved evergreen tree species with simple canopy structure; it is structurally simple, may have sclerophyllous adaptations in seasonal winterwet climates and it is taxonomically distinct; it merges with mesophytic forests at higher latitudes. Deciduous temperate forest has lower species richness than any of the preceding types; it is composed either ofdeciduous broad-leaved species or conifers, or a mixture ofboth; structurally it is similar to the temperate/subtropical evergreen forest.
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Diet Substrate (81 (A) Figure 1. Ecological diversity spectra for six tropical rain forest faunas. (A) Locomotor adaptations according to use of substrate: T, terrestrial; B, semi-terrestrial, with some use of bushes and fallen trees ( =SGM ofAndrews et&., 1979); A, arboreal; S, scansorial; W, aquatic; R, aerial; F, fossorial. (B) Dietary guilds: I, insectivorous; F, frugivorous; B, herbivorous browsing; G, herbivorous grazing; C, carnivorous; 0, omnivorous. All six faunas are from lowland, wet evergreen forest from the following regions: 28, Hkamti, Burma; 29, South Tenawerim, Burma; 38, Ulu Langat. Malaysia; 39, Gunong Benom, Malaysia; 48, Irangi, Zaire; 49, Semliki, Uganda. The vertical scale gives the percentage numbers ofspecies present in each ecological category.
The mammalian communities supported by these different forest types may be distinguished by their ecological characteristics, which in turn relate to structural aspects of the vegetation. This has been observed in preliminary form (Harrison, 1962; Fleming, 1973; Andrews et al., 1979; Eisenberg & Redford, 1982), and I am currently attempting to define this relationship more precisely (Andrews, in prep.). Figure 1, for example, shows ecological diversity spectra for six present-day mammalian faunas, from three regions of Asia and Africa. All are from lowland evergreen tropical rain forest, and despite the fact that the species composition differs between the three regions, the range of ecological variation for substrate use (Figure 1A) and dietary guild (Figure 1B) are extremely similar for all the faunas. In other words, the ecological spectra for these faunas are to a large extent independent of species composition. This has important implications for the study of fossil faunas, where the ecological preferences of the constituent species are unknown and the fauna1 composition is different from present-day faunas. Another example is taken from the data in Andrews et al. (1979, Figures 5 & 6). In this earlier work, I included under the heading “lowland forest” several different forest types
I’. ANDREWS
426
A
mill
mL lranpi
Semliki
Seredou
IILL Rwenrori
Budongo
C
hIilL iu
IlLL
llbl
Semliki
Lemera
D
Mt. Kenya
4llb
Ey
Sokoke
Tana
Jebel Mara
E 4ibl
UiliHb Banagi
Kapiti
Figure 2. Ecological diversity spectra for 15 tropical African faunas taken from Andrews et al. (1979), showing distribution of dietary adaptations for five vegetation types: A, lowland wet evergreen tropical rain forest (TRF); B, semi-evergreen TRF; C, montane TRF; D, deciduous and riverine tropical forest; E, Savannah woodland/open deciduous forest. Details of sites are in Table 2 of Andrews et al. (1979). The dietary categories are the same as for Figure 1.
which are distinguished in the zonal classification given above. Figure 2 shows dietary guild spectra for some of the mammalian faunas analysed in my earlier work ( 1979)) ranging from wet evergreen TRF at Seredou, Semliki and Irangi at the top, to Savannah woodland at Rukwa, Banagi and Kapiti at the bottom. All these sites are from the tropical region of Africa. They demonstrate a transition from faunas dominated by insectivores, frugivores and browsing herbivores at the top of Figure 2, to faunas dominated by grazing and browsing herbivores and carnivores at the bottom. The ecological spectra vary, therefore, according to the degree of forest cover, and comparison of Figures 1 and 2 shows that mammalian community structure within the tropical region of Africa varies more greatly according to forest type than does the community structure in similar forest types from one continent to another (Figures 1 & 2). Primate
origins
Primate origins must lie in the Cretaceous/Paleocene, them (Gingerich, 1986). Cretaceous temperatures
although it is proving hard to recognize were higher than those of today, with
COMMUNITY
EVOLUTION
IN FOREST HABITATS
427
tropical influences extending to high latitudes, about 50”, and during this period the angiosperms replaced the gymnosperms as the dominant tree form. Many modern forms were present by the end of the period, and arboreal ecosystems began to emerge with the coevolution ofplants, insects, birds and mammals in complex food webs. During the Paleocene, world temperatures were initially high, before becoming cooler in the late Paleocene (Krause & Maas, 1990). Mammalian faunas consisted largely of archaic groups. The primate-like animals such as Plesiudapis were robustly built, similar in many respects to the larger scansorial mammals such as squirrels of today. The development ofprimates, and the spread of herbivorous artiodactyls and perissodactyls in the early Eocene, coincided with a further period of global warming (Shackleton, 1984)) although the evidence for mammalian change and stable isotopes does not always coincide (Krause & Maas, 1990). Primates were probably one of the earliest arboreal groups of mammals, but little is known of the life forms of these pre-Eocene forms. By the beginning of the Eocene, primates were a diverse group of mainly arboreal, forest-living mammals with a great variety of body sizes, foraging patterns and life styles. It is at this stage that the story can begin about primates and their forest habitats.
Eocene Eocene sediments are known mainly from areas that today are non-tropical, although the Fayum deposits are now recognized to be late Eocene in age and probably had tropical climates at that time. Apart from this, Eocene fossils are unknown from tropical Africa, but in one sense this is not so important because, as Napier stressed in 1970, there has been little change in tropical climates during the Cenozic. This view has been challenged by Shackleton (1984), who suggested that for much of the Eocene and Oligo-Miocene, sea temperatures at low latitudes were actually lower than today’s, but the oxygen isotope temperature interpretations are at variance with those of corals and foraminifera, both of which indicate tropical temperatures comparable with those of today (Adams et al., 1990). It seems more likely, therefore, that terrestrial habitats at low latitudes in the African Eocene would also have been similar to tropical habitats today, with the cooling of world temperatures having affected mainly the higher latitudes, resulting in contraction of the equatorial region. Globally, it is clear that Eocene climates were warmer than those of today, particularly during the early Eocene, when temperatures approached those of the Cretaceous, so that the Eocene floras and faunas had a tropical aspect. This is indicated by the oxygen isotope record for the early part of the Eocene, and there is additional evidence from the distribution of symbiotic corals and larger foraminifera that the latitudinal limits of the tropical zone were at least 10” wider in the early and middle Eocene than at present (Adams el al., 1990). Modern corals, with symbiotic dinoflagellate algae, are today limited to tropical waters where the mean annual surface temperatures exceed 16°C (Rosen, 1984), and there are records of their presence during the middle Eocene in southern England. The larger foraminifera, which are also symbiotic with algae and diatoms, are even more restricted by temperature, but again extend to southern England in the middle Eocene. Many of the major mammalian groups were present by the beginning of the Eocene, so that the faunas had a more modern look than did those from the Paleocene, but there were still many differences at the family level. Rodents were abundant and were mainly represented by extinct families, but the presence ofglirids imparts a slightly more modern look to the fauna (Hooker, 1989). In the Insectivora, talpids were present, but no soricids. Primates
P. ANDREWS
428
were represented by adapids and omomyids, two extinct families similar in grade to lemuriform primates today. Carnivores were present as stem groups, as were the much more diverse artiodactyls, most ofwhich were only distantly related to the living forms. Perissodactyls, on the other hand, were represented by primitive equoids, rhinocerotoids and ancylopods (Hooker, 1989). Rather than attempting a general review of the Eocene mammalian evidence, in this paper I am going to concentrate my attention on the English record from the Eocene. Some of the evidence is at variance with the American Eocene (Krause & Maas, 1990), but by concentrating on a single geographic region, and comparing it with a similarly selected geographic region for the Miocene (East Africa in this case), it will be possible to make specific comparisons that would not be possible in a general survey. Eocene terrestrialfIorafrom
the London Clay
During the early part of the Eocene, the botanical evidence from the London Clay flora shows the presence of both tropical and temperate taxa, with 18% of living relatives having exclusively tropical distributions today (Collinson, 1983). This figure may be slightly low, for some taxa that originated with exclusively tropical distributions may subsequently have spread to temperate regions, increasing the apparent temperate contribution to Eocene floras. The London Clay flora has apparent affinities as follows, scored for all places where the extant genera currently live (or where the families of extinct genera live todaycosmopolitan genera are scored once for each of four climatic zones) : 13 1 tropical genera 86 subtropical genera 60 temperate genera 17 north temperate genera. Palms are important constituents of the tropical element of the London Clay flora, and the semi-mangrove Nipa palms were locally abundant, with two species oftrue mangroves rarely present also (Collinson, 1983). Mangroves today extend to 32”N and slightly further to the south, to the limits ofkilling frosts where mean temperatures of the coldest month is in excess ofZO”C, or, in other words, where annual temperature variation in small (Walsh, 1974). The mean annual temperature based on the flora is 25-26°C for this part of the early Eocene in southern Britain, and the oxygen isotope figures for the same period is 20-27°C (Buchardt, 1978). The temperature variation during the annual cycle must have been an important variable at the latitude of 4 1” which was the position of the London basin at that time, but there is no evidence to indicate its limits. Similarly, there must have been considerable seasonal fluctuations in insolation and rainfall, and these are indicated in part by the presence of growth rings in wood, but the nature of the vegetation indicates year-round abundance of rainfall. This could be accounted for by the fact that the London Clay (which is a marine deposit, intertidal to continental shelf) was sampling the vegetation rafted out from the nearby shore lines, where narrow strips of coastal forest could have been maintained by coastal rains and high humidity from monsoon-like winds off the sea, together with riverine or groundwater forests in low lying areas. Seasonality is directly indicated by the presence of growth rings on 31% of a twig sample (Collinson, 1983). This is similar to growth ring incidence in present day tropical deciduous forests, which are typically two-storied forests in which the upper discontinuous storey is composed mainly of obligate deciduous tree species and the lower storey includes both deciduous and many evergreen species.
COMMUNITY
EVOLUTION
IN FOREST
HABITATS
429
Eocene mammalian faunas of southern England The taxonomic composition ofEocene faunas will not be considered here, except in terms of species richness. Instead, I will be looking at patterns ofecological diversity of the faunas and relating these to patterns observed in present day habitats. This method was first developed for interpreting the palaeoecology of Pleistocene and Miocene faunas (Andrews et al., 1979), but it has since been applied with considerable success to Eocene faunas by Hooker (in press; Collinson & Hooker, 1987). All of the size estimates and interpretations of diet and locomotion used here have been taken from Hooker (in press), Difficulties in interpreting past diet, size and locomotor patterns in fossil mammals increase with added age, but this is true of any method ofpalaeoecological reconstruction, particularly methods that rely on taxonomic affinity with living animals to assess possible ecologies of their extinct relatives. Dietary guilds in the Eocene may differ from those ofthe present because ofthe low abundance and diversity ofgrasses, and interpretations of Eocene diets need to take this into account. There may also be differences arising from the ante-predator adaptations of flowering plants where, for instance, plants have co-evolved a fruiting strategy with particular mammal species to promote fruit dispersal by species that do not damage their seed and to protect the fruit from more destructive predators. At this early stage of mammalian evolution, some differences in the relationship between mammals and plants might be expected, which in turn could affect our interpretations of the habitat structure in the Eocene. The early Eocene floras from the London Clay are associated with faunas that show high ratios ofsemi-terrestrial scrambling mammals relative to large terrestrial ones, high numbers of insectivorous species as in the Paleocene, but higher proportions of arboreal forms than were present in the Paleocene. One to three primate species were present in sites such as Wittering and Abbey Wood (Collinson & Hooker, 1987), mostly insectivorous arboreal forms. By the middle Eocene, the faunas are less skewed towards semi-terrestrial scrambling mammals, with larger terrestrial mammal species more abundant, and frugivores becoming as well represented as insectivores. In all ofthese aspects, the late middle Eocene mammalian faunas of southern England are more similar to tropical forest faunas of the present time, and by the end ofthe middle Eocene this similarity is enhanced by the increase in proportions of browsing herbivores, for example at Creechbarrow (Collinson & Hooker, 1987). This similarity, however, is not so much with tropical evergreen forest faunas as with faunas from more highly seasonal forested habitats, such as paratropical forests (Wolfe, 1979). These are characterized by tree canopies with reduced physical differentiation, reduced species richness, greater seasonality offruiting and flowering, and usually reduced diversity oflianes and eiphytes (Wolfe, 1979). There is also a significant and increasing temperate contribution to the flora. Species richness in the series of middle to late Eocene faunas from the south of England declines considerably, although part ofthis may be due to taphonomic causes. The number of species known at present from middle Eocene deposits at Creechbarrow is 42, seven ofwhich are primates (Hooker, in press). The primates are mostly small, with five species less than 1 kg and the rest less than 10 kg (Figure 3A). Insectivorous species outnumber frugivores and herbivores (Figure 3B). The major change in the late Eocene is towards lower species richness, both for mammals in general and for primates in particular. The green clay at How Ledge, Isle of Wight, contains 32 species ofwhich five are primates, but the fauna appears to be size-biased, with large mammals under-represented, and it is likely that both species numbers and community structure ofthis fauna would have been similar to that ofthe middle Eocene fauna from Creechbarrow. Towards the end of the late Eocene, however, greater
430
P. ANDREWS
EF(Af) S-D(Af)
n
Weight (kg)
SO
^_
KO
FT
MB
M-F(AF) DF(Af)
n Diet
Figure 3. Numbers of species of primates in fossil and recent forest faunas. (A) Distribution of primate species according to body size, as indicated on the Figure. (B) Distribution according to dietary guilds: 1, insectivorous; F, frugivorous; B, leaf-eating or other vegetarian. The sites are as follows: EOCENE-CB, Creechbarrow; HO, Mammal Bed, Hordle; HL, How Ledge limestone green clay, Isle of Wight; HA, Lignite Bed, Hatherwood Limestone Member, Headon Hill; LF, Lacy’s Farm Limestone Member, Headon Hill outlier (Hooker, 1991); MIOCENE-SO, Songhor, Kenya; KO, Koru, Kenya; FT, Fort Ternan, Kenya; MB, Maboko Island, Kenya; RECENT-EF (Af), mean of three African faunas from lowland evergreen tropical rain forest (TRF); S-D (Af), mean ofthree African faunas from semi-evergreen TRF; DF (Afi, one African fauna from deciduous forest; MF (Af), mean of three African faunas from montane TRF; EF (As), mean of three Malayan faunas from lowland evergreen TRF; S-DF (As), mean of two Chinese faunas from semi-evergreen TRF; EF (Am), mean of two faunas from tropical America (Panama), evergreen TRF.
changes fauna
occur.
The lignite
and one fewer primate
bed of the Hatherwood (31 and 4, respectively)
Limestone compared
has one fewer
species
with How Ledge,
in the
but it has
considerably higher proportions of browsers, and by the time of the Lower Bernbridge Limestone the community structure ofthe fauna is unlike that ofany living forest fauna. Only one primate species is present in a fauna of 22 species, with many large terrestrial mammal
COMMUNITY
species,
few aboreal
could
and scansorial
be indicative
taphonomic is some
of open,
artefact.
evidence
Limestone
equitability
few arboreal
species.
been
(Hooker,
accumulation
by means
expectation
which
against
because
and
they
expected,
however,
mammals
and the other
tropical
faunas)
conditions
that would
have
were the same.
different
taphonomic
to rely on comparisons emerge
The faunas
different
within
1 kg body weight,
or to differences
sites. This trend
could be due to the climatic
oxygen
records.
with
isotope closed
conditions
conditions
at the
correlate
although of this trend
mammals
that
is the change
from faunas
[small
ground
& Redford,
(LGM)
of Andrews
et al., 19791.
A second
trend,
Eocene,
with a further
Oligocene. where
faunas.
scrambling
much
Moreover, mammals
occupancy
or foraging
up a large
proportion
insectivorous frugivory
of the Eocene most that
structure.
also have Arboreal
within
way
to more
[large ground
dominated
by insectivorous
in the North The latter
to explain
mammals
in the middle American
were
Eocene, related
(Figure
in forest
habitats, the general
3). Frugivorous
to
of large numbers
in terms ofmodern
mammals
to late
and into the
is probably
but the presence
although
A
scram-
ground
comparadwellers
a large terrestrial component in their and scansorial species, which today
species
are
(see belowj.
at the end of the Eocene
conditions,
open
only forest faunas
domination
observed
is hard
by the
mentioned,
et al., 1979, or semi-arboreal
mammals
the Eocene.
diets in the Eocene, the primates
already
giving
from faunas
of the frugivorous
of the frugivorous
and frugivorous
is apparent
to more open
majority
by small, semi-terrestrial,
of Andrews
browsing
during
it is
in the later
documented
change
even when
to frugivore
of the trend
with
mammalian
the great
more abundant
period
dominated
is the change
increases
from forest
throughout
tive forest
the reverse
with
of the forest has changed
(SGM)
to herbivorous
ofinsectivory
change
offrugivores
related,
change
of the
19821 to large terrestrial
and early Eocene,
This is almost
frequency
the habitat
small
also partly
in the Paleocene
either
and in its absence
that is independently
the nature
mammals
ofEisenberg
if taphonomic
to early Oligocene
relatively
is apparent
it is possible
animals
mammals
cooling
beginning
by small
of these patterns,
throughout,
become
however,
in
and open country
even
in habitat,
be
It is to be
one is dominated in forested
also be due to the vegetation
later on. The same trend,
considered, bling
forest
It could
differences.
of size
of the late Paleocene
mammals
may
of similarities
fossil faunas.
by small mammals
but larger
a
by investigat-
Distributions
or because
where
measures
and between
from this analysis are dominated
faunas
has yet been made
conditions
arising
size, but they do not give any
observed
weighted
biases
(1990) have proposed
bias, for example
habitats,
is the
of the sites have
on possible
of equivalent
(as today
No investigation
unwise
less then
from
many
& Maas
of tooth
because
by large mammals
to differing
Two trends
be different
faunas
small,
are generally
because
size distributions.
in the source
at this level has
faunas
taphonomic
averages
in the Bembridge
fauna
but there are
is no information
observed
similarities
may
respect
faunas.
of weighted
be a
but there
and small mammals,
fossils. Krause
to indicate
to measure
of ecological
accumulation,
mammalian
This pattern or it could
aspect,
for example
bias is unlikely,
ofthe
non-forest
The mammal
oflarge
1986), but there
ing size distributions similar
where
be supposed
levels,
in press).
Collection
and preservation
series of tests that might
at similar
proportions
sites,
bias.
of browsers.
at this time and place,
unit has a similar,
unit (Hooker,
for all of these
of taphonomic
well collected
during
Marls
and similar
431
HABITATS
and high proportions
conditions
and elastic
IN FOREST
conditions
The Bembridge
high dietary A problem
species
non-forested
for forested
organic
possibility
EVOLUTION
were
divided
trend
bats, which
or
niche make
between
towards
greater
today
make up
P. ANDREWS
432
another group of high level forest frugivores, forests (Sige & Aguilar, 1987).
were apparently
not present
in the Eocene
Miocene The Miocene period saw continued temperature decline together with world-wide mountain-building activity which started in the Oligocene. Particularly important in the Old World was the Alpine-Himalayan system stretching right across Europe and Asia from the Atlas mountains to Southeast Asia. This had profound implications for the region ofwhat is now southern Europe and the Middle East, for throughout the Mesozoic and Paleogene this area was covered by sea, the ancient Tethys, which linked the Mediterranean, Black and Caspian Seas with the Indian Ocean. The Tethyan seaway ceased to exist in its original form when the African Plate contacted Asia close to the beginning of the Miocene (Adams et al., 1983). This is indicated by minor differences in foraminiferal faunas between the Mediterranean and Indo-Pacific regions which first appear during the Aquitanian, and by mid-Burdigalian times there is evidence for a major barrier separating these marine faunas (Whybrow et al., 1982). In other words, there had occurred by this time a broad land bridge connecting Africa with Europe and Asia, and this had great influences on the development of mammalian faunas in all three regions. Miocene terrestrialfEora
During the early Miocene, there is a large and diverse flora known from tropical East Africa. This was originally described by Chesters (1957), but more recently it has been extensively studied by Margaret Collinson, who has generously made available some ofher unpublished observations. Twenty-one fossil plant sites have been recognized on Rusinga Island and 24 on the nearby Mfwangano Island. These sites have yielded 59 species that have been determined to nearest living relatives, mostly at the generic level, and there is almost an equal number of undetermined morphological groups. The following groups have been categorized by Collinson: some very common like Celtis; the large forest trees Sterculia and are moderately common but restricted to Mfwangano Island. These are indicative of closed evergreen forest. 2. Trees/shrubs, including many deciduous taxa and again with some very common species, such as Grewia, and many moderately common; this assemblage indicates deciduous forest. 3. Woody lianes, at least six species, which are characteristic of open areas along rivers in closed forest or in more open forests. 4. Woody/herbaceous lianes, many species, very common. 1. Forest
trees,
Entandrophragma
These can be provisionally taken to indicate the presence in these areas during the early Miocene of at least three types of forest: tropical evergreen, tropical semi-evergreen, and deciduous. At R 117 on Rusinga Island, where we excavated in 1980 (Collinson & Andrews, in prep.), we collected seeds and fruit of over 50 species, together with abundant twigs, buds and thorns (the latter making up 3.5% of twig remains), and the flora is dominated by deciduous trees/shrubs, such as Lannea, Terminalia, zizyphus, Grewia, Cordia and abundant twining and climbing plants, both herbaceous and woody. This flora represents category 2 above, and it is in fact very similar to that growing in the drier parts of the region today (Andrews, 1973). The present day vegetation in this part of western Kenya is closest to
COMMUNITY
deciduous
forest,
Miocene
highly
seasonal,
EVOLUTION
single
canopy
deciduous
woodland
it is likely that all three types were well represented
data it is not possible
to elaborate
433
IN FOREST HABITATS
or forest.
in the region,
During
the
but with available
further.
Miocene mammalian faunas Unfortunately in East they
there
Africa.
are no primate
Fragmentary
do not provide
sufficient
mammals
are extremely
(Pickford,
198 1)) and mammal
floras may be taken
fossils preserved
plant
remains
information
abundant
with
at some
to reconstruct
in the same a rough
geological
guide
mammal
the flora.
the other
localities,
vegetation
but hand,
on Rusinga
to the plant
to the probable
localities
localities,
On
formations
sites are in close proximity
as providing
any of the rich plant
are present
Island
so the fossil
types present
at
that time. Some
of the early
palaeofloras
Miocene
been
Songhor,
tropical
rain forest faunas, from animals
fossil faunas, faunas (Figure
faunas
have
been
(compare
the fossil and recent computer-generated same fauna
reducing
the distinction
non-forest
faunas.
faunas
has been
The
between
loss of both
ofwhich
ofEuclidean
pattern
4D)
as it is by loss of many
of its large-size to different
simply
of the primate sites in being
both
by size (Figure
3A) and
diet
them to the right
(Figure
and
the
two
and some loss of with
that there more
of the Songhor small.
large fauna,
However,
to try and identify (Figure
forest
between
fauna
and some
similar
the origin,
This indicates
affinities
4C
of the large
towards
the right,
fauna.
faunas more
of the 24 Figure
4A) between
the Songhor
mammals,
richness
moving
by
4B shows the
Removal
is intermediate
types ofTRF
between
Similarly,
down
(Figure
of the forest
the Eocene
lowland
after the removal
towards
from
from
(both
4. Figure
removed).
in the Songhor
mammals
the conclusion
has not yet been extended
the type of forest. Examining just the species
apparent
and small
ofEuclidean
have been manipulated
the points
Songhor categories
of body sizes,
bias in the Songhor
in Figure
distances, telescopes
(Figure
forest species
function
from the same fauna.
fauna
biased
analysed
species
for the
from a suite of 23 present
calculated
in the unbiased
This supports
those
faunas
fauna
more
of the larger
to find some correspondence
distances
100 kg.
to present-day
and least for forest
observed
large
fauna
two are shown
(32:/b of the original
than
variables
of taphonomic
a series of recent
of the small species
removed.
numbers,
faunas,
the 24 largest
species
with
faunas
is not close because
4B & C), with some movement
(Figures
discrimination
contrast
for non-forest
has little effect on the pattern 4C), and removal
a proportion
of the Songhor
4A but with Euclidean
(Figure
similar
the ecological
4A with 4D). In order
from the fauna
shows the effect of removing
analysis
distances
modifications,
as Figure
species
Figure
greater
biases to those indicated
fauna is strikingly
4 combines
of the
with living
can be compared
guilds using the simple multivariate
but the match mammalian
patterns
the
1975;
with only 2 1.4% of specimens
that the fossil faunas to similar
with
Couvering,
as to the nature
diversity
biased,
by eliminating
in Figure
4D) are greatest
accumulation
biased
biased
1989). Euclidean
faunas,
species
the Songhor
shown
(Figure
is also clearly
associated
& Van
10 kg, and only 8.374 from animals
artificially
and montane)
(Andrews
in its ecological
that have been subjected
and dietary
day faunas
that are loosely
affinities
( 1984) has shown
zonal strata (Gauch,
smallest
than
4). The analysis
locomotor distance
but the fauna
greater
so that, for instance,
that
forest
has clear affinities
work by Dreyer
closely with recent
from East Africa
to have
et al., 198 I), but there is little information
for instance,
coming
Preliminary
faunas
shown
et al., 1979; Evans
Andrews forest.
have
this
more closely
3)) the Miocene
to those
of today.
3B) show
similar
faunas Species diversity
434
P. ANDREWS
(A)
(6)
s-w
b S-G
Figure 4. Multivariate distance analysis (Euclidean Distance) based on the combination of 20 classes from three ecological variables: body size, locomotor substrate adaptation and dietary guild. The distances are shown with respect to 23 recent mammalian faunas grouped here in four habitat types: TRF, lowland tropical rain forest; MF, montane tropical rain forest; S-W, savanna woodland; S-G, savanna grassland. Three versionsofone moderntropicalrain forestfaunaare shown with distances from this set of23 faunas, with the reference fauna in every case at the point oforigin ofthe axes: (A) complete fauna from the tropical rain forest habitat at Irangi, Zaire, comprising 76 species excluding bats; (B) shows the same fauna reduced by 32% (n= 52)) with the 24 smallest species removed from the analysis; (C) shows the same fauna again (n = 52), this time with the 24 largest species removed; (D) the Songhor fauna (n = 57), with Euclidean distances from the same set of23 modern faunas. On the vertical axis, Euclidean distance (De) measures the distance of the selected fauna in the 20 classes from the 23 comparative faunas: as species are removed from the TRF fauna in A, the values of De either diminish if the species removed are highly diagnostic of the habitat (as in B), or remain the same if the species are undiagnostic (as in C). On the horizontal axis, Euclidean distance (Dp) is the proportional distance for the same variables, and as species are removed from the marker fauna it may increase, depending on the nature of species removed; removal of species in size in B and C alters the proportions ofspecies present in all the feeding and locomotor categories in such a way as to make the reference sample more dissimilar to all of the comparative faunas.
patterns for primate faunas from present day evergreen and semi-evergreen
forest habitats,
suggesting comparability of the fossil primate faunas with recent primate distributions from these habitats. On a more qualitative basis, there are also strong indications of ecological comparability of the early Miocene mammalian faunas with those of today based on the
COMMUNITY
EVOLUTION
IN FOREST HABITATS
435
relative abundances of major groups of mammals. For example, the 48 species known from Songhor (excluding bats and carnivores) include the same range of animals as are seen today in tropical forests, with similar proportions of small rodents, both herbivorous and omnivorous species, and similar proportions of large and small primates, flying squirrels, insectivores, artiodactyls and so on (Andrews et al., 1979). When these are grouped on the basis of taxonomic/trophic categories, their distribution compares very closely with those of recent tropical forest faunas. Faunas from other early Miocene sites in East Africa show similar levels of ecological correspondence to that just illustrated for Songhor, and it seems possible to conclude from this that at this stage of the Miocene the faunas from tropical rain forest habitats were essentially modern in their ecological structure.
Discussion Two contrasting conclusions have been drawn from the analyses of the Eocene and Miocene biota. Eocene floras from southern England have been shown to be taxonomically comparable to those of present day paratropical forests, but the community structure of the mammalian faunas associated with the floras indicates structural differences from comparable habitats today. There appears to have been a different combination and range of niches available, as reflected in the distribution of ground and arboreal mammals in the Eocene forests. The Miocene floras and faunas from East Africa, however, were similar to present day tropical forest habitats, both in taxonomic diversity and in the apparent community structure distribution of ecological niches. This contrast in mammalian between Eocene and Miocene faunas is mirrored in corresponding ecological differences in the primate faunas. For much of the Eocene Period, the presence oflarge numbers offrugivorous ground-living or low-level mammals is probably indicative of conditions unlike any present today. In modern Old World tropical forests, for example, the only low level frugivores are the ground squirrels, forest papionins, granivorous rodents, and opportunistically frugivorous herbivores such as suids and tragulids (Figure 1B). In the Eocene there were high species numbers of didelphids, pseudosciurid paramyid and theridomyid rodents, none of which were probably more than semi-scansorial in degree of arboreality, and all were probably foraging near ground level. In the tree canopies, the primates were the only upper canopy foragers, but during the early part of the Eocene they were mainly insectivorous, only later becoming more herbivorous (Figure 3B). During this same period, early to late Eocene, the primates also became larger, which correlates with their changed diets, but which did not proceed so far as was reached subsequently in the Miocene, by which time the primate faunas appear modern in terms of their dietary and size distributions (Figure 3; and see Fleagle, 1978). Taxonomically, of course, the primate faunas in the Miocene were dominated by apes in contrast to those of today, which are dominated by monkeys, and the replacement of one by the other is the subject ofdebate (Napier, 1970; Andrews, 1981). The abundance of low-canopy-level frugivores in the Eocene would seem to indicate the abundance of fruit supplies in this part of the Eocene forest habitats. The opportunities available today for low-level frugivores are limited by the abundance of arboreal frugivores, particularly birds and insects, which eat much of the fruit while still in the upper canopy of forest habitats. It may be inferred, therefore, that both the mammalian and non-mammalian upper canopy feeders were less effective feeders or less abundant than they are today. Such a
436
P.ANDREWS
conclusion is not reflected in the taxonomic composition of the Eocene floras, which is similar to that of today’s tropical and paratropical forest (Collinson, 1983; Wolfe, 1979). It is possible, however, that the life histories of the trees making up the forest flora were different from those of related trees today, in particular the fruiting strategies (but see below). Fruit production predicates the presence ofanimals to eat and distribute the fruit, and in ecological terms a delicate balance between seed dispersal and seed predation has developed by coevolution between animals and plants over long periods of time. Plants living in stable conditions with low levels ofseed predation are under pressure to extend their fruiting seasons to minimize competition with limited numbers of dispersal agents (i.e., mammals or birds). In this case, small numbers of fruit are produced over long periods of time, and most of them are eaten in place on the trees. Where seed predation is high, however, pressure will be for plants to synchronize their fruiting, in which case large quantities of fruit are produced (by any one plant species) over a short period of time, and much of this falls uneaten to the ground, where it becomes available to terrestrial frugivores. Based on these premises, it may be hypothesized that during the Eocene, the latter fruiting strategy was widespread, but as arboreal and aerial frugivores evolved, the fruiting strategies of forest trees may have co-evolved to one of non-overlapping fruit production. It is suggested, therefore, that between the Eocene of southern England and the early Miocene of East Africa, there was an evolutionary shift in community ecology, but with several provisos which must be mentioned briefly. Firstly, differences in mammalian faunas are not matched by known differences in the floras, although this is not to say they did not occur. I would not wish to imply that the faunas provide better information on vegetation structure than the actual floras, but it does appear that the changes in mammalian community structure could be pointing to a feature for which an explanation must be sought in the floras. Secondly, the Eocene faunas described were all from high latitudes, and although tropical climates are inferred for these latitudes during the Eocene, apparently comparable to those of tropical East Africa in the Miocene, there would clearly have been ecological differences arising from the differences in latitude, e.g., incidence of solar radiation and distribution of rainfall. Seasonality would inevitably have been greater as a result of these features, perhaps mainly in distribution of rainfall. Thirdly, little is known of the range of community types in either the Eocene or the early Miocene tropical forest faunas. Additional work is urgently needed to produce a geographically wide range of community types. Fourthly, the community structure of more open country faunas in the early Miocene was very different from those of any living open country community, but comparisons have not yet been made with open country faunas from the Eocene. Much remains to be done, therefore, but as a first generalization it may be tentatively concluded that an episode of community evolution occurred in tropical forest mammalian faunas between the Eocene and Miocene Epochs.
Acknowledgements I am very grateful to Leslie Aiello and Michael Day for organizing the meeting and volume in memory of John Napier. Drs Jerry Hooker and Margaret Collinson helped greatly in the preparation of this manuscript with ideas, critical advice and some unpublished information. I am also grateful to Libby Andrews, Hugh Owen, Chris Stringer, Tania King and Philip Gingerich, as well as two anonymous referees, for their comments on this manuscript.
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HABITATS
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References Adams, C. G., Gentry, A. W. & Whybrow, P. J. (1983). Dating the terminal Tethyan event. In (J. E. Meulenkamp, Ed.) Reconstruction ofMarine Paleoenuironments, pp. 273-298. Utrecht: Micropaleontology Bulletin. Adams, C. G., Lee, D. E. & Rosen, B. R. (1990). Conflicting isotopic and biotic evidence for tropical sea-surface temperatures during the Tertiary. Palaeogeog. Palaeoclimat. Palaeoecol. 77,28%3 13. Andrews, P. (1973). The vegetation ofRusinga Island. Jl E. Africa nat. Hist. Sot. 142, l-8. Andrews, P. (1981). Species diversity and diet in monkeys and apes during the Miocene. In (C. B. Stringer, Ed.! Aspects of Human Evolution, pp. 2% 1.London: Taylor and Francis. Andrews, P. (1990). Palaeoecology of the Miocene fauna from Pasalar, Turkey. J. hum. Euol. 19,56%582. Andrews, P. & Evans, E. M. N. (1979). The environment of Ramapitheclcc in Africa. Paleobiology 5,22-30. Andrews, P., Lord, J, & Evans, E. M. N. (1979). Patterns of ecological diversity in fossil and modern mammalian faunas, Biol. J. Linn. Sot. 11, 177-205. Andrews, P. & Van Couvering, J. H. (1975). Palaeoenvironments in the East African Miocene. In (F. S. Szalay, Ed.) Approaches to Primate Paleobiology, pp. 62-103. Base]: Karger. Buchardt, B. (1978). Oxygen isotope palaeotemperatures from the Tertiary period in the North Sea area. _Vature, Lond. 275,121-123.
Chesters, K. I. M. (1957). The Miocene flora ofRusinga Island, Lake Victoria, Kenya. Palaeontographica 101,3&67. Collins, D. A. & McCrew, W. C. (1988). Habitats of three groups of chimpanzees (Pan troglodytes) in western Tanzania compared. J. hum. Euol. 17,553-574. Collinson, M. E. (1983). Fossil Plants of the London Clay. Palaeontological Association Field Guides to Fossils No. 1. London: The Palaeontological Association. Collinson, M. E. & Hooker, J. J. (1987). Vegetational and mammalian fauna1 changes in the early Tertiary of southern England. In (E. M. Friis, W. G. Chaloner & P. R. Crane, Eds) The Origins of Angiosperms and their Biological Consequenres, pp. 259-304. Cambridge: Cambridge University Press. Dreyer, S. K. (1984). The theory and use ofmethods for the study ofmammalian palaeoecology. Ph.D. Dissertation. University oflondon. Eisenberg, J. F. & Redford, K. H. (1982). Comparative niche structure and evolution of mammals of the Nearctic and southern South America. Pymatuning Lab. Ecol. Spec. Pub. 6, 77-84. Evans, E. M. N., Van Couvering, J, H. & Andrews, P. (1981). Palaeoecology ofMiocene sites in East Africa. J. hum. Eool. 10, 35.-48.
Fleagle,J. Fleming.
G. (1978). Size distributions ofliving and fossil faunas. Paleobiology4,67-76. (1973). Numbers of mammal species in north and central America forest communities.
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555-563.
Gauch, H. G. (1989). h!ultivariate Ana&siJ in Community Ecology. Cambridge: Cambridge University Press. Gingerich, P. D. (1986). Plesiadapis and delineation of the order Primates. In (B. Wood, L. Martin & P. Andrews, Eds) Major Topics in Primate and Human Evolution, pp. 3246. Cambridge: Cambridge University Press. Harrison. J. L. (1962). The distribution offeeding habits among animals in a tropical rain forest. J. anim. Ecol. 31, 53-64.
Hooker. J. J. ( 1986). Mammals from the Bartonian (middle/late Eocene) of the Hampshire Basin, southern England. Bull. BY. hlus. nat. hist. (Geol.) 39, 191478. Hooker, J. J. (1989). British mammals in the Tertiary Period. Biol. J. Linn. SOL.38,9-21. Hooker, J. J. (in press). British mammalian palaeocommunities across the Eocene-Oligocene transition and their environmental implications. In (D. R. Prothrro, Ed.) Eocene-Oligocene climatic and biotic euolution. Princeton: Princeton University Press. Kappelman. J. (1991). The paleoenvironment ofKenyapithecus at Fort Tcrnan. J. hum. Euol. 20,95-129. Krause, D. M’. & Maas. M. C. (1990). The biogeographic origins of late Paleocene-early Eocene mammalian immigrants to the western interior of North America. In (T. M. Bown & K. D. Rose, Eds) Damn of the Age 01 Mammals in the northern Part of the Roc& hfountain Interior, .North America. Geological Society Special Paper 243, Boulder, Colorado. Napier, J. R. j 1970). Paleoecology and catarrhine evolution. In IJ. R. Napier & P. H. Napier, Eds) Old World Monkq~, pp. 53-95. New York: Academic Press. Pickford, M. i 1981). Preliminary Miocene mammalian biostratigraphy for western Kenya. 3. hum. Eool. 10,73-97. Pickford, M. & Andrews, P. (1981). The Tinderet Miocene sequence in Kenya. 3. hum. Eool. 10, 1 I-33. Richards, P. W. ( 19521. The Tropical Rain Forest. An Ecological Study. Cambridge: Cambridge University Press. Rosen, B. R. (1984). Reefcoral biogeography and climate through thelate Cainozoic. In (P. Benchley, Ed.) Fos& and Climate, pp. 201-262. Chichester: Wiley. Shackleton, ( 1984). Oxygen isotope evidence for Cenozoic climatic change. In (P. Benchley, Ed.) Fossilsand Climate, pp. 27-34. Chichester: Wiley. Shipman, P. (1986) Paleoecology ofFort Ternan reconsidered. 3. hum. Euol.15, 1933204. Sige, B. & Aguilar, J, P. (1987). L’extension stratigraphique des megachiropteres dans le Miocene d’Europe meridionalr. C.r. hebd. Seam. Acad. Sci. Paris ‘304,469-474.
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Walsh. G. E. (1974). Mangroves: areview. In iR.J. Reimold & W. H. Queen, Eds) Ecolog~ofHalophytes, pp. 51-174. New York: Academic Press. Fl’hybrow, P. J., Collinson. M. E., Daams, R., Gentry, A. W. & McClure, H. A. (1982). Geology, fauna (Bovidae, Rodentia) and flora from the early Miocene ofeastern Saudi Arabia. 7ert.Res. 4,105-120. Wolfe, J. (1979). Temperature parameters of humid to mesic forests of eastern Asia and relation ofother regions of the northern hemisphere and Australasia. Prof. Pap. U.S. Cd. SW. 1106, l-37.
Peter Andrews Department of Palaeontology, Natural History Museum, Cromwell Road, London, U.K. Received 1 April 1991 Revision received 5 October 1991 and accepted 5 October 1991 Kgwords: Eocene, Miocene, community, evolution, ecology, primates.
evolution
in forest habitats
Hominoid primates have had a mainly tropical forest distribution throughout their history. At present, the forest habitats occupied by apes include a variety of vegetation types, for example lowland evergreen tropical forest, montane evergreen forests, medium altitudesemi-deciduous forests, and even deciduous forest-scrub. A similar spectrum of vegetation types appears to have been occupied by Eocene and Oligocene primates, as well as at least some of the Miocene apes in Africa. The nature of these habitats is investigated both by reviewing the adaptations of the mammals in relation to the floral composition and by investigating the community structure of the mammalian faunas. Community structure is measured by body size spectra, dietary guilds, trophic patterns and diversity indices, both analysed separately and in combination using multivariate techniques. Comparisons are made between the Eocene and Present in order to document the changes in community structure which occurred during this time, with special attention being given to primates. Taxonomic shifts that have occurred in the East African mammalian faunas between Miocene and Present have produced little change in the community structure, indicating that Miocene forest habitats were structurally similar to those of today, whereas the differences observed in the Eocene faunas represent both a taxonomic and an ecologic change. Between the late Eocene and early Miocene there was a reorganization ofmammalian community structure for which an explanation must be sought, either in changes in the relationships between mammals and plants between the Eocene and Present or in ecological changes in forest habitats during this time. Journal of Human Euolution (1992) 22,423-43&I
Introduction In 1970, John Napier attempted a synthesis ofwhat was then known about palaeoecology in the Cenozoic. He drew on a very wide variety ofsources, including pollen, coral distribution, sedimentary analyses, and interpretations of insect, snail and mammal faunas (Napier, 1970). Some of our interpretations have changed since that time with increasing knowledge but the rationale behind palaeoecology remains the same: “paleoecology provides the opportunity for asking questions about primate evolution”, for example through the relation between adaptive significance of primate morphologies and the environment in which primates lived (Napier, 1970: 56). This is as true today as when Napier wrote these words. Also, and remarkably ahead of his time, Napier claimed that palaeoecology could “confirm inferences obtained from comparative studies of living animals regarding the probable characters of common inheritance with the palaeocological situation in which they are believed to have evolved” (Napier, 1970: 56). By these means, the adaptive significance of characters relating to such behaviours as knuckle-walking of apes, slow climbing of lorises, loss of thumb in African colobines, and many others, can be assessed. In his 1970 paper, Napier raised many questions, most of which we are no more able to answer today than he was then. I am going to consider a topic that he touched on briefly; the distributions offossil primates in relation to changing forest types from the Eocene to Present. Tropical rain forest has been important in the adaptive radiation ofmany groups ofprimates, ive in various types offorest, and then as now for the great majority ofliving primates (88%) 1’ “we can make the assumption that the key to the zoogeographic history of the primates and the adaptations that led to the emergence of the major radiations, lies in the distribution, the 0047-2484/92/4-50423
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Press Limited
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P. ANDREWS
floristic composition and the seasonality of Cenozoic forests” (Napier, 1970:76). But were these forests of the past structurally and ecologically similar to those of today? The living apes occupy a range of forest types at the present time, extending even to dry deciduous forestbush (Collins & McGrew, 1988). Similarly, in the past, fossil apes have been reported from tropical rain forest (Andrews & Van Couvering, 1975; Kappelman, 199 I), more open types ofwoodland (Andrews & Evans, 1979), open country (Shipman, 1986), and monsoon forest (Andrews, 1990). Some of these interpretations have been disputed, but it is clear that different groups of fossil apes had a wide range of habitat preference. What is not clear from these studies, however, is how past forest habitats compare with recent ones and whether there has been any substantial change in the nature of the habitats themselves, which may have affected the adaptive radiation of the hominoid primates. In this paper, therefore, I am going to investigate the ecological characteristics ofpast habitats and make comparisons with present day tropical forests, to try and determine the extent to which it is possible to interpret the past and to what extent forest habitats, and their mammalian communities, may have changed through time. I will focus on two sets of data, faunas and floras from the Eocene of southern England and the Miocene of East Africa, and these will be compared with analyses ofrecent tropical floras and faunas. The fossil biota are ones with which I have some first hand knowledge, and they are chosen on this basis, with no implication that they are representative of, for instance, the Eocene of North America or the Miocene of Eurasia. Perhaps this work will stimulate others more familiar with these times and regions to accord them similar treatment, either to substantiate or refute my conclusions.
Recent forest
zones
A detailed account offorest zones will be published elsewhere (Andrews, in prep.), and for the purposes of the present paper a short summary must suffice: Tropical rain forest (TRF; Richards, 1952) is characterized by abundance of trees, lianes and epiphytes, with complex one- to four-storied canopy structure; most tree species are broad-leaved evergreen species; confined today to lowland tropical areas with high year-round rainfall. Paratropical rain forest (Wolfe, 1979) is structurally similar to TRF but with never more than two tree stories; it is characterized by low proportions offacultatively deciduous tree species and conifers, and also some temperate species; found today in the high-latitude tropics. Tropical deciduous forest and semi-evergreen forest are structural variants of TRF; species richness and canopy complexity are both less than in TRF; they are confined to tropical regions but in areas of seasonal drought, either caused climatically, e.g., in rainshadow areas, or edaphically, e.g., where the soil is poor. Tropical montane forest is characterized by extreme variation in canopy structure arising from topographic variation, varying from evergreen to deciduous; often growing in poor light conditions due to prevailing cloud; limited to areas above 1500 metres near the equator, but lower towards the tropics. Summerwet forest is characterized by more open, forest/grassland mosaic pattern of vegetation; deciduous tree species predominate in the strongly seasonal climates; found today at the limits and beyond of the tropics, sometimes called subtropical or monsoon forests. Temperate/subtropical evergreen forest (Wolfe, 1979) is composed ofbroad-leaved evergreen tree species with simple canopy structure; it is structurally simple, may have sclerophyllous adaptations in seasonal winterwet climates and it is taxonomically distinct; it merges with mesophytic forests at higher latitudes. Deciduous temperate forest has lower species richness than any of the preceding types; it is composed either ofdeciduous broad-leaved species or conifers, or a mixture ofboth; structurally it is similar to the temperate/subtropical evergreen forest.
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16 -
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TBASWRF
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Diet Substrate (81 (A) Figure 1. Ecological diversity spectra for six tropical rain forest faunas. (A) Locomotor adaptations according to use of substrate: T, terrestrial; B, semi-terrestrial, with some use of bushes and fallen trees ( =SGM ofAndrews et&., 1979); A, arboreal; S, scansorial; W, aquatic; R, aerial; F, fossorial. (B) Dietary guilds: I, insectivorous; F, frugivorous; B, herbivorous browsing; G, herbivorous grazing; C, carnivorous; 0, omnivorous. All six faunas are from lowland, wet evergreen forest from the following regions: 28, Hkamti, Burma; 29, South Tenawerim, Burma; 38, Ulu Langat. Malaysia; 39, Gunong Benom, Malaysia; 48, Irangi, Zaire; 49, Semliki, Uganda. The vertical scale gives the percentage numbers ofspecies present in each ecological category.
The mammalian communities supported by these different forest types may be distinguished by their ecological characteristics, which in turn relate to structural aspects of the vegetation. This has been observed in preliminary form (Harrison, 1962; Fleming, 1973; Andrews et al., 1979; Eisenberg & Redford, 1982), and I am currently attempting to define this relationship more precisely (Andrews, in prep.). Figure 1, for example, shows ecological diversity spectra for six present-day mammalian faunas, from three regions of Asia and Africa. All are from lowland evergreen tropical rain forest, and despite the fact that the species composition differs between the three regions, the range of ecological variation for substrate use (Figure 1A) and dietary guild (Figure 1B) are extremely similar for all the faunas. In other words, the ecological spectra for these faunas are to a large extent independent of species composition. This has important implications for the study of fossil faunas, where the ecological preferences of the constituent species are unknown and the fauna1 composition is different from present-day faunas. Another example is taken from the data in Andrews et al. (1979, Figures 5 & 6). In this earlier work, I included under the heading “lowland forest” several different forest types
I’. ANDREWS
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A
mill
mL lranpi
Semliki
Seredou
IILL Rwenrori
Budongo
C
hIilL iu
IlLL
llbl
Semliki
Lemera
D
Mt. Kenya
4llb
Ey
Sokoke
Tana
Jebel Mara
E 4ibl
UiliHb Banagi
Kapiti
Figure 2. Ecological diversity spectra for 15 tropical African faunas taken from Andrews et al. (1979), showing distribution of dietary adaptations for five vegetation types: A, lowland wet evergreen tropical rain forest (TRF); B, semi-evergreen TRF; C, montane TRF; D, deciduous and riverine tropical forest; E, Savannah woodland/open deciduous forest. Details of sites are in Table 2 of Andrews et al. (1979). The dietary categories are the same as for Figure 1.
which are distinguished in the zonal classification given above. Figure 2 shows dietary guild spectra for some of the mammalian faunas analysed in my earlier work ( 1979)) ranging from wet evergreen TRF at Seredou, Semliki and Irangi at the top, to Savannah woodland at Rukwa, Banagi and Kapiti at the bottom. All these sites are from the tropical region of Africa. They demonstrate a transition from faunas dominated by insectivores, frugivores and browsing herbivores at the top of Figure 2, to faunas dominated by grazing and browsing herbivores and carnivores at the bottom. The ecological spectra vary, therefore, according to the degree of forest cover, and comparison of Figures 1 and 2 shows that mammalian community structure within the tropical region of Africa varies more greatly according to forest type than does the community structure in similar forest types from one continent to another (Figures 1 & 2). Primate
origins
Primate origins must lie in the Cretaceous/Paleocene, them (Gingerich, 1986). Cretaceous temperatures
although it is proving hard to recognize were higher than those of today, with
COMMUNITY
EVOLUTION
IN FOREST HABITATS
427
tropical influences extending to high latitudes, about 50”, and during this period the angiosperms replaced the gymnosperms as the dominant tree form. Many modern forms were present by the end of the period, and arboreal ecosystems began to emerge with the coevolution ofplants, insects, birds and mammals in complex food webs. During the Paleocene, world temperatures were initially high, before becoming cooler in the late Paleocene (Krause & Maas, 1990). Mammalian faunas consisted largely of archaic groups. The primate-like animals such as Plesiudapis were robustly built, similar in many respects to the larger scansorial mammals such as squirrels of today. The development ofprimates, and the spread of herbivorous artiodactyls and perissodactyls in the early Eocene, coincided with a further period of global warming (Shackleton, 1984)) although the evidence for mammalian change and stable isotopes does not always coincide (Krause & Maas, 1990). Primates were probably one of the earliest arboreal groups of mammals, but little is known of the life forms of these pre-Eocene forms. By the beginning of the Eocene, primates were a diverse group of mainly arboreal, forest-living mammals with a great variety of body sizes, foraging patterns and life styles. It is at this stage that the story can begin about primates and their forest habitats.
Eocene Eocene sediments are known mainly from areas that today are non-tropical, although the Fayum deposits are now recognized to be late Eocene in age and probably had tropical climates at that time. Apart from this, Eocene fossils are unknown from tropical Africa, but in one sense this is not so important because, as Napier stressed in 1970, there has been little change in tropical climates during the Cenozic. This view has been challenged by Shackleton (1984), who suggested that for much of the Eocene and Oligo-Miocene, sea temperatures at low latitudes were actually lower than today’s, but the oxygen isotope temperature interpretations are at variance with those of corals and foraminifera, both of which indicate tropical temperatures comparable with those of today (Adams et al., 1990). It seems more likely, therefore, that terrestrial habitats at low latitudes in the African Eocene would also have been similar to tropical habitats today, with the cooling of world temperatures having affected mainly the higher latitudes, resulting in contraction of the equatorial region. Globally, it is clear that Eocene climates were warmer than those of today, particularly during the early Eocene, when temperatures approached those of the Cretaceous, so that the Eocene floras and faunas had a tropical aspect. This is indicated by the oxygen isotope record for the early part of the Eocene, and there is additional evidence from the distribution of symbiotic corals and larger foraminifera that the latitudinal limits of the tropical zone were at least 10” wider in the early and middle Eocene than at present (Adams el al., 1990). Modern corals, with symbiotic dinoflagellate algae, are today limited to tropical waters where the mean annual surface temperatures exceed 16°C (Rosen, 1984), and there are records of their presence during the middle Eocene in southern England. The larger foraminifera, which are also symbiotic with algae and diatoms, are even more restricted by temperature, but again extend to southern England in the middle Eocene. Many of the major mammalian groups were present by the beginning of the Eocene, so that the faunas had a more modern look than did those from the Paleocene, but there were still many differences at the family level. Rodents were abundant and were mainly represented by extinct families, but the presence ofglirids imparts a slightly more modern look to the fauna (Hooker, 1989). In the Insectivora, talpids were present, but no soricids. Primates
P. ANDREWS
428
were represented by adapids and omomyids, two extinct families similar in grade to lemuriform primates today. Carnivores were present as stem groups, as were the much more diverse artiodactyls, most ofwhich were only distantly related to the living forms. Perissodactyls, on the other hand, were represented by primitive equoids, rhinocerotoids and ancylopods (Hooker, 1989). Rather than attempting a general review of the Eocene mammalian evidence, in this paper I am going to concentrate my attention on the English record from the Eocene. Some of the evidence is at variance with the American Eocene (Krause & Maas, 1990), but by concentrating on a single geographic region, and comparing it with a similarly selected geographic region for the Miocene (East Africa in this case), it will be possible to make specific comparisons that would not be possible in a general survey. Eocene terrestrialfIorafrom
the London Clay
During the early part of the Eocene, the botanical evidence from the London Clay flora shows the presence of both tropical and temperate taxa, with 18% of living relatives having exclusively tropical distributions today (Collinson, 1983). This figure may be slightly low, for some taxa that originated with exclusively tropical distributions may subsequently have spread to temperate regions, increasing the apparent temperate contribution to Eocene floras. The London Clay flora has apparent affinities as follows, scored for all places where the extant genera currently live (or where the families of extinct genera live todaycosmopolitan genera are scored once for each of four climatic zones) : 13 1 tropical genera 86 subtropical genera 60 temperate genera 17 north temperate genera. Palms are important constituents of the tropical element of the London Clay flora, and the semi-mangrove Nipa palms were locally abundant, with two species oftrue mangroves rarely present also (Collinson, 1983). Mangroves today extend to 32”N and slightly further to the south, to the limits ofkilling frosts where mean temperatures of the coldest month is in excess ofZO”C, or, in other words, where annual temperature variation in small (Walsh, 1974). The mean annual temperature based on the flora is 25-26°C for this part of the early Eocene in southern Britain, and the oxygen isotope figures for the same period is 20-27°C (Buchardt, 1978). The temperature variation during the annual cycle must have been an important variable at the latitude of 4 1” which was the position of the London basin at that time, but there is no evidence to indicate its limits. Similarly, there must have been considerable seasonal fluctuations in insolation and rainfall, and these are indicated in part by the presence of growth rings in wood, but the nature of the vegetation indicates year-round abundance of rainfall. This could be accounted for by the fact that the London Clay (which is a marine deposit, intertidal to continental shelf) was sampling the vegetation rafted out from the nearby shore lines, where narrow strips of coastal forest could have been maintained by coastal rains and high humidity from monsoon-like winds off the sea, together with riverine or groundwater forests in low lying areas. Seasonality is directly indicated by the presence of growth rings on 31% of a twig sample (Collinson, 1983). This is similar to growth ring incidence in present day tropical deciduous forests, which are typically two-storied forests in which the upper discontinuous storey is composed mainly of obligate deciduous tree species and the lower storey includes both deciduous and many evergreen species.
COMMUNITY
EVOLUTION
IN FOREST
HABITATS
429
Eocene mammalian faunas of southern England The taxonomic composition ofEocene faunas will not be considered here, except in terms of species richness. Instead, I will be looking at patterns ofecological diversity of the faunas and relating these to patterns observed in present day habitats. This method was first developed for interpreting the palaeoecology of Pleistocene and Miocene faunas (Andrews et al., 1979), but it has since been applied with considerable success to Eocene faunas by Hooker (in press; Collinson & Hooker, 1987). All of the size estimates and interpretations of diet and locomotion used here have been taken from Hooker (in press), Difficulties in interpreting past diet, size and locomotor patterns in fossil mammals increase with added age, but this is true of any method ofpalaeoecological reconstruction, particularly methods that rely on taxonomic affinity with living animals to assess possible ecologies of their extinct relatives. Dietary guilds in the Eocene may differ from those ofthe present because ofthe low abundance and diversity ofgrasses, and interpretations of Eocene diets need to take this into account. There may also be differences arising from the ante-predator adaptations of flowering plants where, for instance, plants have co-evolved a fruiting strategy with particular mammal species to promote fruit dispersal by species that do not damage their seed and to protect the fruit from more destructive predators. At this early stage of mammalian evolution, some differences in the relationship between mammals and plants might be expected, which in turn could affect our interpretations of the habitat structure in the Eocene. The early Eocene floras from the London Clay are associated with faunas that show high ratios ofsemi-terrestrial scrambling mammals relative to large terrestrial ones, high numbers of insectivorous species as in the Paleocene, but higher proportions of arboreal forms than were present in the Paleocene. One to three primate species were present in sites such as Wittering and Abbey Wood (Collinson & Hooker, 1987), mostly insectivorous arboreal forms. By the middle Eocene, the faunas are less skewed towards semi-terrestrial scrambling mammals, with larger terrestrial mammal species more abundant, and frugivores becoming as well represented as insectivores. In all ofthese aspects, the late middle Eocene mammalian faunas of southern England are more similar to tropical forest faunas of the present time, and by the end ofthe middle Eocene this similarity is enhanced by the increase in proportions of browsing herbivores, for example at Creechbarrow (Collinson & Hooker, 1987). This similarity, however, is not so much with tropical evergreen forest faunas as with faunas from more highly seasonal forested habitats, such as paratropical forests (Wolfe, 1979). These are characterized by tree canopies with reduced physical differentiation, reduced species richness, greater seasonality offruiting and flowering, and usually reduced diversity oflianes and eiphytes (Wolfe, 1979). There is also a significant and increasing temperate contribution to the flora. Species richness in the series of middle to late Eocene faunas from the south of England declines considerably, although part ofthis may be due to taphonomic causes. The number of species known at present from middle Eocene deposits at Creechbarrow is 42, seven ofwhich are primates (Hooker, in press). The primates are mostly small, with five species less than 1 kg and the rest less than 10 kg (Figure 3A). Insectivorous species outnumber frugivores and herbivores (Figure 3B). The major change in the late Eocene is towards lower species richness, both for mammals in general and for primates in particular. The green clay at How Ledge, Isle of Wight, contains 32 species ofwhich five are primates, but the fauna appears to be size-biased, with large mammals under-represented, and it is likely that both species numbers and community structure ofthis fauna would have been similar to that ofthe middle Eocene fauna from Creechbarrow. Towards the end of the late Eocene, however, greater
430
P. ANDREWS
EF(Af) S-D(Af)
n
Weight (kg)
SO
^_
KO
FT
MB
M-F(AF) DF(Af)
n Diet
Figure 3. Numbers of species of primates in fossil and recent forest faunas. (A) Distribution of primate species according to body size, as indicated on the Figure. (B) Distribution according to dietary guilds: 1, insectivorous; F, frugivorous; B, leaf-eating or other vegetarian. The sites are as follows: EOCENE-CB, Creechbarrow; HO, Mammal Bed, Hordle; HL, How Ledge limestone green clay, Isle of Wight; HA, Lignite Bed, Hatherwood Limestone Member, Headon Hill; LF, Lacy’s Farm Limestone Member, Headon Hill outlier (Hooker, 1991); MIOCENE-SO, Songhor, Kenya; KO, Koru, Kenya; FT, Fort Ternan, Kenya; MB, Maboko Island, Kenya; RECENT-EF (Af), mean of three African faunas from lowland evergreen tropical rain forest (TRF); S-D (Af), mean ofthree African faunas from semi-evergreen TRF; DF (Afi, one African fauna from deciduous forest; MF (Af), mean of three African faunas from montane TRF; EF (As), mean of three Malayan faunas from lowland evergreen TRF; S-DF (As), mean of two Chinese faunas from semi-evergreen TRF; EF (Am), mean of two faunas from tropical America (Panama), evergreen TRF.
changes fauna
occur.
The lignite
and one fewer primate
bed of the Hatherwood (31 and 4, respectively)
Limestone compared
has one fewer
species
with How Ledge,
in the
but it has
considerably higher proportions of browsers, and by the time of the Lower Bernbridge Limestone the community structure ofthe fauna is unlike that ofany living forest fauna. Only one primate species is present in a fauna of 22 species, with many large terrestrial mammal
COMMUNITY
species,
few aboreal
could
and scansorial
be indicative
taphonomic is some
of open,
artefact.
evidence
Limestone
equitability
few arboreal
species.
been
(Hooker,
accumulation
by means
expectation
which
against
because
and
they
expected,
however,
mammals
and the other
tropical
faunas)
conditions
that would
have
were the same.
different
taphonomic
to rely on comparisons emerge
The faunas
different
within
1 kg body weight,
or to differences
sites. This trend
could be due to the climatic
oxygen
records.
with
isotope closed
conditions
conditions
at the
correlate
although of this trend
mammals
that
is the change
from faunas
[small
ground
& Redford,
(LGM)
of Andrews
et al., 19791.
A second
trend,
Eocene,
with a further
Oligocene. where
faunas.
scrambling
much
Moreover, mammals
occupancy
or foraging
up a large
proportion
insectivorous frugivory
of the Eocene most that
structure.
also have Arboreal
within
way
to more
[large ground
dominated
by insectivorous
in the North The latter
to explain
mammals
in the middle American
were
Eocene, related
(Figure
in forest
habitats, the general
3). Frugivorous
to
of large numbers
in terms ofmodern
mammals
to late
and into the
is probably
but the presence
although
A
scram-
ground
comparadwellers
a large terrestrial component in their and scansorial species, which today
species
are
(see belowj.
at the end of the Eocene
conditions,
open
only forest faunas
domination
observed
is hard
by the
mentioned,
et al., 1979, or semi-arboreal
mammals
the Eocene.
diets in the Eocene, the primates
already
giving
from faunas
of the frugivorous
of the frugivorous
and frugivorous
is apparent
to more open
majority
by small, semi-terrestrial,
of Andrews
browsing
during
it is
in the later
documented
change
even when
to frugivore
of the trend
with
mammalian
the great
more abundant
period
dominated
is the change
increases
from forest
throughout
tive forest
the reverse
with
of the forest has changed
(SGM)
to herbivorous
ofinsectivory
change
offrugivores
related,
change
of the
19821 to large terrestrial
and early Eocene,
This is almost
frequency
the habitat
small
also partly
in the Paleocene
either
and in its absence
that is independently
the nature
mammals
ofEisenberg
if taphonomic
to early Oligocene
relatively
is apparent
it is possible
animals
mammals
cooling
beginning
by small
of these patterns,
throughout,
become
however,
in
and open country
even
in habitat,
be
It is to be
one is dominated in forested
also be due to the vegetation
later on. The same trend,
considered, bling
forest
It could
differences.
of size
of the late Paleocene
mammals
may
of similarities
fossil faunas.
by small mammals
but larger
a
by investigat-
Distributions
or because
where
measures
and between
from this analysis are dominated
faunas
has yet been made
conditions
arising
size, but they do not give any
observed
weighted
biases
(1990) have proposed
bias, for example
habitats,
is the
of the sites have
on possible
of equivalent
(as today
No investigation
unwise
less then
from
many
& Maas
of tooth
because
by large mammals
to differing
Two trends
be different
faunas
small,
are generally
because
size distributions.
in the source
at this level has
faunas
taphonomic
averages
in the Bembridge
fauna
but there are
is no information
observed
similarities
may
respect
faunas.
of weighted
be a
but there
and small mammals,
fossils. Krause
to indicate
to measure
of ecological
accumulation,
mammalian
This pattern or it could
aspect,
for example
bias is unlikely,
ofthe
non-forest
The mammal
oflarge
1986), but there
ing size distributions similar
where
be supposed
levels,
in press).
Collection
and preservation
series of tests that might
at similar
proportions
sites,
bias.
of browsers.
at this time and place,
unit has a similar,
unit (Hooker,
for all of these
of taphonomic
well collected
during
Marls
and similar
431
HABITATS
and high proportions
conditions
and elastic
IN FOREST
conditions
The Bembridge
high dietary A problem
species
non-forested
for forested
organic
possibility
EVOLUTION
were
divided
trend
bats, which
or
niche make
between
towards
greater
today
make up
P. ANDREWS
432
another group of high level forest frugivores, forests (Sige & Aguilar, 1987).
were apparently
not present
in the Eocene
Miocene The Miocene period saw continued temperature decline together with world-wide mountain-building activity which started in the Oligocene. Particularly important in the Old World was the Alpine-Himalayan system stretching right across Europe and Asia from the Atlas mountains to Southeast Asia. This had profound implications for the region ofwhat is now southern Europe and the Middle East, for throughout the Mesozoic and Paleogene this area was covered by sea, the ancient Tethys, which linked the Mediterranean, Black and Caspian Seas with the Indian Ocean. The Tethyan seaway ceased to exist in its original form when the African Plate contacted Asia close to the beginning of the Miocene (Adams et al., 1983). This is indicated by minor differences in foraminiferal faunas between the Mediterranean and Indo-Pacific regions which first appear during the Aquitanian, and by mid-Burdigalian times there is evidence for a major barrier separating these marine faunas (Whybrow et al., 1982). In other words, there had occurred by this time a broad land bridge connecting Africa with Europe and Asia, and this had great influences on the development of mammalian faunas in all three regions. Miocene terrestrialfEora
During the early Miocene, there is a large and diverse flora known from tropical East Africa. This was originally described by Chesters (1957), but more recently it has been extensively studied by Margaret Collinson, who has generously made available some ofher unpublished observations. Twenty-one fossil plant sites have been recognized on Rusinga Island and 24 on the nearby Mfwangano Island. These sites have yielded 59 species that have been determined to nearest living relatives, mostly at the generic level, and there is almost an equal number of undetermined morphological groups. The following groups have been categorized by Collinson: some very common like Celtis; the large forest trees Sterculia and are moderately common but restricted to Mfwangano Island. These are indicative of closed evergreen forest. 2. Trees/shrubs, including many deciduous taxa and again with some very common species, such as Grewia, and many moderately common; this assemblage indicates deciduous forest. 3. Woody lianes, at least six species, which are characteristic of open areas along rivers in closed forest or in more open forests. 4. Woody/herbaceous lianes, many species, very common. 1. Forest
trees,
Entandrophragma
These can be provisionally taken to indicate the presence in these areas during the early Miocene of at least three types of forest: tropical evergreen, tropical semi-evergreen, and deciduous. At R 117 on Rusinga Island, where we excavated in 1980 (Collinson & Andrews, in prep.), we collected seeds and fruit of over 50 species, together with abundant twigs, buds and thorns (the latter making up 3.5% of twig remains), and the flora is dominated by deciduous trees/shrubs, such as Lannea, Terminalia, zizyphus, Grewia, Cordia and abundant twining and climbing plants, both herbaceous and woody. This flora represents category 2 above, and it is in fact very similar to that growing in the drier parts of the region today (Andrews, 1973). The present day vegetation in this part of western Kenya is closest to
COMMUNITY
deciduous
forest,
Miocene
highly
seasonal,
EVOLUTION
single
canopy
deciduous
woodland
it is likely that all three types were well represented
data it is not possible
to elaborate
433
IN FOREST HABITATS
or forest.
in the region,
During
the
but with available
further.
Miocene mammalian faunas Unfortunately in East they
there
Africa.
are no primate
Fragmentary
do not provide
sufficient
mammals
are extremely
(Pickford,
198 1)) and mammal
floras may be taken
fossils preserved
plant
remains
information
abundant
with
at some
to reconstruct
in the same a rough
geological
guide
mammal
the flora.
the other
localities,
vegetation
but hand,
on Rusinga
to the plant
to the probable
localities
localities,
On
formations
sites are in close proximity
as providing
any of the rich plant
are present
Island
so the fossil
types present
at
that time. Some
of the early
palaeofloras
Miocene
been
Songhor,
tropical
rain forest faunas, from animals
fossil faunas, faunas (Figure
faunas
have
been
(compare
the fossil and recent computer-generated same fauna
reducing
the distinction
non-forest
faunas.
faunas
has been
The
between
loss of both
ofwhich
ofEuclidean
pattern
4D)
as it is by loss of many
of its large-size to different
simply
of the primate sites in being
both
by size (Figure
3A) and
diet
them to the right
(Figure
and
the
two
and some loss of with
that there more
of the Songhor small.
large fauna,
However,
to try and identify (Figure
forest
between
fauna
and some
similar
the origin,
This indicates
affinities
4C
of the large
towards
the right,
fauna.
faunas more
of the 24 Figure
4A) between
the Songhor
mammals,
richness
moving
by
4B shows the
Removal
is intermediate
types ofTRF
between
Similarly,
down
(Figure
of the forest
the Eocene
lowland
after the removal
towards
from
from
(both
4. Figure
removed).
in the Songhor
mammals
the conclusion
has not yet been extended
the type of forest. Examining just the species
apparent
and small
ofEuclidean
have been manipulated
the points
Songhor categories
of body sizes,
bias in the Songhor
in Figure
distances, telescopes
(Figure
forest species
function
from the same fauna.
fauna
biased
analysed
species
for the
from a suite of 23 present
calculated
in the unbiased
This supports
those
faunas
fauna
more
of the larger
to find some correspondence
distances
100 kg.
to present-day
and least for forest
observed
large
fauna
two are shown
(32:/b of the original
than
variables
of taphonomic
a series of recent
of the small species
removed.
numbers,
faunas,
the 24 largest
species
with
faunas
is not close because
4B & C), with some movement
(Figures
discrimination
contrast
for non-forest
has little effect on the pattern 4C), and removal
a proportion
of the Songhor
4A but with Euclidean
(Figure
similar
the ecological
4A with 4D). In order
from the fauna
shows the effect of removing
analysis
distances
modifications,
as Figure
species
Figure
greater
biases to those indicated
fauna is strikingly
4 combines
of the
with living
can be compared
guilds using the simple multivariate
but the match mammalian
patterns
the
1975;
with only 2 1.4% of specimens
that the fossil faunas to similar
with
Couvering,
as to the nature
diversity
biased,
by eliminating
in Figure
4D) are greatest
accumulation
biased
biased
1989). Euclidean
faunas,
species
the Songhor
shown
(Figure
is also clearly
associated
& Van
10 kg, and only 8.374 from animals
artificially
and montane)
(Andrews
in its ecological
that have been subjected
and dietary
day faunas
that are loosely
affinities
( 1984) has shown
zonal strata (Gauch,
smallest
than
4). The analysis
locomotor distance
but the fauna
greater
so that, for instance,
that
forest
has clear affinities
work by Dreyer
closely with recent
from East Africa
to have
et al., 198 I), but there is little information
for instance,
coming
Preliminary
faunas
shown
et al., 1979; Evans
Andrews forest.
have
this
more closely
3)) the Miocene
to those
of today.
3B) show
similar
faunas Species diversity
434
P. ANDREWS
(A)
(6)
s-w
b S-G
Figure 4. Multivariate distance analysis (Euclidean Distance) based on the combination of 20 classes from three ecological variables: body size, locomotor substrate adaptation and dietary guild. The distances are shown with respect to 23 recent mammalian faunas grouped here in four habitat types: TRF, lowland tropical rain forest; MF, montane tropical rain forest; S-W, savanna woodland; S-G, savanna grassland. Three versionsofone moderntropicalrain forestfaunaare shown with distances from this set of23 faunas, with the reference fauna in every case at the point oforigin ofthe axes: (A) complete fauna from the tropical rain forest habitat at Irangi, Zaire, comprising 76 species excluding bats; (B) shows the same fauna reduced by 32% (n= 52)) with the 24 smallest species removed from the analysis; (C) shows the same fauna again (n = 52), this time with the 24 largest species removed; (D) the Songhor fauna (n = 57), with Euclidean distances from the same set of23 modern faunas. On the vertical axis, Euclidean distance (De) measures the distance of the selected fauna in the 20 classes from the 23 comparative faunas: as species are removed from the TRF fauna in A, the values of De either diminish if the species removed are highly diagnostic of the habitat (as in B), or remain the same if the species are undiagnostic (as in C). On the horizontal axis, Euclidean distance (Dp) is the proportional distance for the same variables, and as species are removed from the marker fauna it may increase, depending on the nature of species removed; removal of species in size in B and C alters the proportions ofspecies present in all the feeding and locomotor categories in such a way as to make the reference sample more dissimilar to all of the comparative faunas.
patterns for primate faunas from present day evergreen and semi-evergreen
forest habitats,
suggesting comparability of the fossil primate faunas with recent primate distributions from these habitats. On a more qualitative basis, there are also strong indications of ecological comparability of the early Miocene mammalian faunas with those of today based on the
COMMUNITY
EVOLUTION
IN FOREST HABITATS
435
relative abundances of major groups of mammals. For example, the 48 species known from Songhor (excluding bats and carnivores) include the same range of animals as are seen today in tropical forests, with similar proportions of small rodents, both herbivorous and omnivorous species, and similar proportions of large and small primates, flying squirrels, insectivores, artiodactyls and so on (Andrews et al., 1979). When these are grouped on the basis of taxonomic/trophic categories, their distribution compares very closely with those of recent tropical forest faunas. Faunas from other early Miocene sites in East Africa show similar levels of ecological correspondence to that just illustrated for Songhor, and it seems possible to conclude from this that at this stage of the Miocene the faunas from tropical rain forest habitats were essentially modern in their ecological structure.
Discussion Two contrasting conclusions have been drawn from the analyses of the Eocene and Miocene biota. Eocene floras from southern England have been shown to be taxonomically comparable to those of present day paratropical forests, but the community structure of the mammalian faunas associated with the floras indicates structural differences from comparable habitats today. There appears to have been a different combination and range of niches available, as reflected in the distribution of ground and arboreal mammals in the Eocene forests. The Miocene floras and faunas from East Africa, however, were similar to present day tropical forest habitats, both in taxonomic diversity and in the apparent community structure distribution of ecological niches. This contrast in mammalian between Eocene and Miocene faunas is mirrored in corresponding ecological differences in the primate faunas. For much of the Eocene Period, the presence oflarge numbers offrugivorous ground-living or low-level mammals is probably indicative of conditions unlike any present today. In modern Old World tropical forests, for example, the only low level frugivores are the ground squirrels, forest papionins, granivorous rodents, and opportunistically frugivorous herbivores such as suids and tragulids (Figure 1B). In the Eocene there were high species numbers of didelphids, pseudosciurid paramyid and theridomyid rodents, none of which were probably more than semi-scansorial in degree of arboreality, and all were probably foraging near ground level. In the tree canopies, the primates were the only upper canopy foragers, but during the early part of the Eocene they were mainly insectivorous, only later becoming more herbivorous (Figure 3B). During this same period, early to late Eocene, the primates also became larger, which correlates with their changed diets, but which did not proceed so far as was reached subsequently in the Miocene, by which time the primate faunas appear modern in terms of their dietary and size distributions (Figure 3; and see Fleagle, 1978). Taxonomically, of course, the primate faunas in the Miocene were dominated by apes in contrast to those of today, which are dominated by monkeys, and the replacement of one by the other is the subject ofdebate (Napier, 1970; Andrews, 1981). The abundance of low-canopy-level frugivores in the Eocene would seem to indicate the abundance of fruit supplies in this part of the Eocene forest habitats. The opportunities available today for low-level frugivores are limited by the abundance of arboreal frugivores, particularly birds and insects, which eat much of the fruit while still in the upper canopy of forest habitats. It may be inferred, therefore, that both the mammalian and non-mammalian upper canopy feeders were less effective feeders or less abundant than they are today. Such a
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conclusion is not reflected in the taxonomic composition of the Eocene floras, which is similar to that of today’s tropical and paratropical forest (Collinson, 1983; Wolfe, 1979). It is possible, however, that the life histories of the trees making up the forest flora were different from those of related trees today, in particular the fruiting strategies (but see below). Fruit production predicates the presence ofanimals to eat and distribute the fruit, and in ecological terms a delicate balance between seed dispersal and seed predation has developed by coevolution between animals and plants over long periods of time. Plants living in stable conditions with low levels ofseed predation are under pressure to extend their fruiting seasons to minimize competition with limited numbers of dispersal agents (i.e., mammals or birds). In this case, small numbers of fruit are produced over long periods of time, and most of them are eaten in place on the trees. Where seed predation is high, however, pressure will be for plants to synchronize their fruiting, in which case large quantities of fruit are produced (by any one plant species) over a short period of time, and much of this falls uneaten to the ground, where it becomes available to terrestrial frugivores. Based on these premises, it may be hypothesized that during the Eocene, the latter fruiting strategy was widespread, but as arboreal and aerial frugivores evolved, the fruiting strategies of forest trees may have co-evolved to one of non-overlapping fruit production. It is suggested, therefore, that between the Eocene of southern England and the early Miocene of East Africa, there was an evolutionary shift in community ecology, but with several provisos which must be mentioned briefly. Firstly, differences in mammalian faunas are not matched by known differences in the floras, although this is not to say they did not occur. I would not wish to imply that the faunas provide better information on vegetation structure than the actual floras, but it does appear that the changes in mammalian community structure could be pointing to a feature for which an explanation must be sought in the floras. Secondly, the Eocene faunas described were all from high latitudes, and although tropical climates are inferred for these latitudes during the Eocene, apparently comparable to those of tropical East Africa in the Miocene, there would clearly have been ecological differences arising from the differences in latitude, e.g., incidence of solar radiation and distribution of rainfall. Seasonality would inevitably have been greater as a result of these features, perhaps mainly in distribution of rainfall. Thirdly, little is known of the range of community types in either the Eocene or the early Miocene tropical forest faunas. Additional work is urgently needed to produce a geographically wide range of community types. Fourthly, the community structure of more open country faunas in the early Miocene was very different from those of any living open country community, but comparisons have not yet been made with open country faunas from the Eocene. Much remains to be done, therefore, but as a first generalization it may be tentatively concluded that an episode of community evolution occurred in tropical forest mammalian faunas between the Eocene and Miocene Epochs.
Acknowledgements I am very grateful to Leslie Aiello and Michael Day for organizing the meeting and volume in memory of John Napier. Drs Jerry Hooker and Margaret Collinson helped greatly in the preparation of this manuscript with ideas, critical advice and some unpublished information. I am also grateful to Libby Andrews, Hugh Owen, Chris Stringer, Tania King and Philip Gingerich, as well as two anonymous referees, for their comments on this manuscript.
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