Michèle E. Morgan

Faunal and environmental change in the late Miocene Siwaliks of northern Pakistan

Abstract The Siwalik formations of northern Pakistan consist of deposits of ancient rivers that existed throughout the early Miocene through the late Pliocene. The formations are highly fossiliferous with a diverse array of terrestrial and freshwater vertebrates, which in combination with exceptional lateral exposure and good chronostratigraphic control allows a more detailed and temporally resolved study of the sediments and faunas than is typical in terrestrial deposits. Consequently the Siwaliks provide an opportunity to document temporal differences in species richness, turnover, and ecological structure in a terrestrial setting, and to investigate how such differences are related to changes in the fluvial system, vegetation, and climate. Here we focus on the interval between 10.7 and 5.7 Ma, a time of significant local tectonic and global climatic change. It is also the interval with the best temporal calibration of Siwalik faunas and most comprehensive data on species occurrences. A methodological focus of this paper is on controlling sampling biases that confound biological and ecological signals. Such biases include uneven sampling through time, differential preservation of larger animals and more durable skeletal elements, errors in age-dating imposed by uncertainties in correlation and paleomagnetic timescale calibrations, and uneven taxonomic treatment across groups. We attempt to control for them primarily by using a relative-abundance model to estimate limits for the first and last appearances from the occurrence data. This model also incorporates uncertainties in age estimates. Because of sampling limitations inherent in the terrestrial fossil record, our 100-Kyr temporal resolution may approach the finest possible level of resolution for studies of vertebrate faunal changes over periods of millions of years. Approximately 40,000 specimens from surface and screenwash collections made at 555 localities form the basis of our study. Sixty percent of the localities have maximum and minimum age estimates differing by 100 Kyr or less, 82% by 200 Kyr or less. The fossils represent 115 mammalian species or lineages of ten orders: Insectivora, Scandentia, Primates, Tubulidentata, Proboscidea, Pholidota, Lagomorpha, Perissodactyla, Artiodactyla, and Rodentia. Important taxa omitted from this study include Carnivora, Elephantoidea, and Rhinocerotidae. Because different collecting methods were used for large and small species, they are treated separately in analyses. Small species include insectivores, tree shrews, rodents, lagomorphs, and small primates. They generally weigh less than 5 kg. The sediments of the study interval were deposited by coexisting fluvial systems, with the larger emergent Nagri system being displaced between 10.1 and 9.0 Ma by an interfan Dhok Pathan system. In comparison to Nagri floodplains, Dhok Pathan floodplains were less well drained, with smaller rivers having more seasonally variable flow and more frequent avulsions. Paleosol sequences indicate reorganization of topography and drainage accompanying a transition to a more seasonal climate. A few paleosols may have formed under waterlogged, grassy woodlands, but most formed under drier conditions and more closed vegetation. The oxygen isotopic record also indicates significant change in the patterns of precipitation beginning at 9.2 Ma, in what may have been a shift to a drier and more seasonal climate. The carbon isotope record demonstrates that after 8.1 Ma significant amounts of C4 grasses began to appear and that by 6.8 Ma floodplain habitats included extensive C4 grasslands. Plant communities with predominantly C3 plants were greatly diminished after 7.0 Ma, and those with predominantly C4 plants, which would have been open woodlands or grassy woodlands, appeared as early as 7.4 Ma. Inferred first and last appearances show a constant, low level of faunal turnover throughout the interval 10.7–5.7-Ma, with three short periods of elevated turnover at 10.3, 7.8, and 7.3–7.0 Ma. The three pulses account for nearly 44% of all turnover. Throughout the late Miocene, species richness declined steadily, and diversity and richness indices together with data on body size imply that community ecological structure changed abruptly just after 10 Ma, and then again at 7.8 Ma. Between 10 and 7.8 Ma the large-mammal assemblages were strongly dominated by equids, with more balanced faunas before and after. The pattern of appearance and disappearance is selective with respect to inferred habits of the animals. Species appearing after 9.0 Ma are grazers or typical of more open habitats, whereas many species that disappear can be linked to more closed vegetation. We presume exceptions to this pattern were animals of the mixed C3/C4 communities or the wetter parts of the floodplain that did not persist into the latest Miocene. The pace of extinction accelerates once there is C4 vegetation on the floodplain. The 10.3 Ma event primarily comprises disappearance of taxa that were both common and of long duration. The event does not correlate to any obvious local environmental or climatic event, and the pattern of species disappearance and appearance suggests that biotic interactions may have been more important than environmental change. The 7.8 Ma event is characterized solely by appearances, and that at 7.3 Ma by a combination of appearances and disappearances. These two latest Miocene events include more taxa that were shorter ranging and less common, a difference of mode that developed between approximately 9.0 and 8.5 Ma when many short-ranging and rare species began to make appearances. Both events also show a close temporal correlation to changes in floodplain deposition and vegetation. The 7.8 Ma event follows the widespread appearance of C4 vegetation and is coincident with the shift from equid-dominated to more evenly balanced large-mammal assemblages. The 7.3 to 7.0 Ma event starts with the first occurrence of C4-dominated floras and ends with the last occurrence of C3-dominated vegetation. Absence of a consistent relationship between depositional facies and the composition of faunal assemblages leads us to reject fluvial system dynamics as a major cause of faunal change. The close correlation of latest Miocene species turnover and ecological change to expansion of C4 plants on the floodplain, in association with oxygen isotopic and sedimentological evidence for increasingly drier and more seasonal climates, causes us to favor explanations based on climatic change for both latest Miocene pulses. The Siwalik record supports neither “coordinated stasis” nor “turnover pulse” evolutionary models. The brief, irregularly spaced pulses of high turnover are characteristic of both the stasis and pulse models, but the high level of background turnover that eliminates 65–70% of the initial species shows there is no stasis in the Siwalik record. In addition, the steadily declining species richness and abrupt, uncoordinated changes in diversity do not fit either model.

A 16-Ma record of paleodiet using carbon and oxygen isotopes in fossil teeth from Pakistan

Abstract The Siwalik Sequence of northern Pakistan contains a 16-Ma record of paleosol carbonate and fossil teeth from which a record of paleovegetation can potentially be reconstructed and compared. The carbon isotopic composition of paleosol carbonate and organic matter from Siwalik strata reflects a major paleoecological change on the floodplains of major rivers beginning7.3 Ma ago. By 6 Ma C 3 -dominated plant communities, probably composed of mostly trees and shrubs, were displaced by nearly continuous C 4 grassland. We find that the carbon isotopic ratios in herbivore tooth enamel reflect this dramatic ecologic shift. Carbonate in enamel older than 7 Ma averages −11‰ in δ 13 C PDB , consistent with a largely C 3 diet. Enamel from the Plio-PIeistocene averages +1.9‰ in δ 13 C, similar to the value displayed by modern C 4 grazers. Analysis of post-burial carbonate cements, and the concordance with isotopic evidence from paleosols argues strongly against major isotopic alteration of the enamel, while coexisting bone may have been altered early in burial. This study confirms that enamel apatite is useful for paleodietary reconstruction much further back in the geologic record than was previously thought.

Ecological changes in Miocene mammalian record show impact of prolonged climatic forcing

Geohistorical records reveal the long-term impacts of climate change on ecosystem structure. A 5-myr record of mammalian faunas from floodplain ecosystems of South Asia shows substantial change in species richness and ecological structure in relation to vegetation change as documented by stable isotopes of C and O from paleosols. Between 8.5 and 6.0 Ma, C4 savannah replaced C3 forest and woodland. Isotopic historical trends for 27 mammalian herbivore species, in combination with ecomorphological data from teeth, show three patterns of response. Most forest frugivores and browsers maintained their dietary habits and disappeared. Other herbivores altered their dietary habits to include increasing amounts of C4 plants and persisted for >1 myr during the vegetation transition. The few lineages that persisted through the vegetation transition show isotopic enrichment of δ13C values over time. These results are evidence for long-term climatic forcing of vegetation structure and mammalian ecological diversity at the subcontinental scale.

Neogene Siwalik mammalian lineages: Species longevities, rates of change, and modes of speciation

Abstract A long depositional sequence from northern Pakistan provides a good fossil record of terrestrial vertebrates for the interval of 18-7 Ma. Making allowances for possible range extensions, we use this record as a direct measure of species longevities. There is a correlation between body size and longevity, smaller mammals frequently being short-lived and larger taxa showing durations up to ca. 10 m.y. The distribution of small mammal longevities indicates an exponential decrease in frequency from a high modal value in the smallest increment measured (0–200,000 yrs). The most frequent value for large mammals is also the smallest increment measured (1 m.y.), but that distribution may not be unimodal. Small mammal taxa of short duration are concentrated late in the sequence, after 9 Ma especially. The middle Miocene fauna is more stable, with species showing longer durations. The contrast in longevities corresponds with hypothesized greater environmental stability in the middle Miocene. For comparison, the Paleogene sequence of Wyoming indicates short median species durations, with few surveyed taxa lasting over 2 m.y. Siwalik mammals show diverse modes of evolution, but stasis in at least some features is usual, with species boundaries corresponding to morphological breaks. Up to half of the Siwalik rodent and artiodactyl species surveyed likely immigrated from outside the biogeographic province, and for a few, historical data are sufficient to stipulate when and by what route they came to the Indian subcontinent.

Patterns of faunal turnover and diversity in the Neogene Siwaliks of Northern Pakistan

Abstract The fluvial Neogene Siwalik formations of northern Pakistan contain a long and richly fossiliferous sequence of terrestrial vertebrate faunas in which patterns of faunal turnover and changes in diversity can be documented and analyzed for intervals having durations of 0.5 m.y. The complete sequence extends from circa 18.5 to 1 Ma, but the part between 18.5 and 5.5 Ma is best sampled, and most intervals within it are well represented. Thirteen orders of Siwalik mammals have been identified, with well-sampled intervals having 50 or more species. Most Siwalik mammals, however, are either rodents or artiodactyls. Bovids are the most common and most speciose of the larger mammals, while murid and “cricetid” rodents dominate the small mammal assemblages. Between 18.5 and 5.5 Ma species diversity varied considerably. Among artiodactyls and rodents the number of species first increased between 15 and 13 Ma and then fell. Data on stratigraphic ranges of rodents and artiodactyls show that faunal change in the Siwaliks was episodic, occurring during short intervals with high turnover followed by longer periods with considerably less change. Maxima of first appearances occurred at approximately 13.5 and 8.5 Ma, while maxima of last occurrences were at 12.5 and 8.0 Ma. Some of the observed faunal events can be correlated to climatic and environmental changes. The Middle Miocene diversification occurred during a period of global cooling, while the latest Miocene decline in diversity and increased turnover accompanied oxygen and carbon isotopic changes that correlate to globally increasing seasonality and aridity. Other correlations are ambiguous. The marked decrease in diversity and the major turnover events between 13 and 8 Ma do not correspond to known local or global events. The Neogene Siwaliks and Paleogene Bighorn-Crazy Mountains sequence in Wyoming and Montana share many similarities. They have equivalent levels of temporal resolution and similar levels of completeness of their fossil records. Siwalik ordinal abundance and diversity patterns differ markedly from those of the Paleogene, but generic, and probably species, diversity was approximately the same, although the Siwalik faunas may have been slightly less diverse. Over time, changes in diversity were of comparable magnitude, with monotonic trends persisting for more than 5 million years. The magnitude of faunal turnover was also similar, ranging from less than half to 3.5 times that expected. In both sequences faunal change appears to have been episodic, with strong pulses between intervals of low turnover. The Siwaliks, in contrast to the Paleogene sequence, may have had more distinct pulses and longer intervals between pulses. Neither sequence has peaks of first occurrences coinciding with peaks of last occurrences.

Isotopic ecology and dietary profiles of Liberian chimpanzees

An extensive suite of isotopic data (delta(13)C, delta(15)N, and delta(18)O) from enamel apatite and bone collagen of adult male and female wild chimpanzees establishes baseline values for Pan troglodytes verus in a primary rainforest setting. The Ganta chimpanzee sample derives from a restricted region in northern Liberia. Diet is examined using stable light isotopes at three life stages-infant, young juvenile, and adult-and developmental differences are investigated within and between individual males and females. The isotopic data are very homogeneous with few exceptions. Juvenile females show consistent enrichment in (13)C relative to infants, while juvenile males do not. These data suggest that age at weaning may be more variable for male offspring who survive to adulthood than for female offspring. Alternatively, or additionally, the weaning diet of males and females may differ, with greater consumption of technologically extracted insects and/or nuts by young females. Metabolic differences, including growth and hormone-mediated responses, may also contribute to the observed variation. The Ganta chimpanzee data offer an independent and objective line of evidence to primatologists interested in the dietary strategies of the great apes and to paleoanthropologists seeking comparative models for reconstructing early hominin subsistence patterns. Despite the high diversity of dietary items consumed by chimpanzees, isotopic signatures of chimpanzees from a primary rainforest setting exhibit narrow ranges of variation similar to chimpanzees in more open habitats.

Faunal interchange and Miocene terrestrial vertebrates of southern Asia

Problems of stratigraphic completeness and poor temporal resolution make analysis of faunal change in terrestrial sequences difficult. The fluvial Neogene Siwalik formations of India and Pakistan are an exception. They contain a long vertebrate record and have good chronostrati- graphic control, making it possible to assess the influence of biotic interchange on Siwalik fossil communities. In Pakistan, the interval between 18 and 7 Ma has been most intensively studied and changes in diversity and relative abundance of ruminant artiodactyls and muroid rodents are documented with temporal resolution of 200,000 years. Within this interval, diversity varies con- siderably, including an abrupt rise in species number between 15 and 13 Ma, followed by a decline in ruminant diversity after 12 Ma and a decline in muroid diversity in two steps at 13 and 10 Ma. Significant changes in relative abundance of taxa include an increase in bovids between 16.5 and 15 Ma, a decrease in tragulids after 9 Ma, and a very abrupt increase in murids at 12 Ma. Megacri- cetodontine rodents also decrease significantly at 12 Ma, and smaller declines -re recorded among myocricetodontine and copemyine rodents after 16 Ma. An increase of dendromurine rodents at 15.5 Ma is also observed. There is also a trend of progressive size increase among giraffoids and bovids throughout the sequence. We have also investigated relationships between biotic interchange and diversity, body size, and relative abundance, concluding that (1) the rapid increase in ruminant and muroid diversity was largely due to immigration, whereas in situ speciation had only a secondary role; (2) during intervals of increasing diversity, resident lineages did not have higher than average rates of in situ speciation; (3) during intervals with rising diversity, greater extinction did not accompany increased immi- gration; (4) during intervals with falling diversity, there may have been greater extinction in recently invading lineages; and (5) change in diversity was independent of changes in relative abundance and body size.

Comparative paleoecology of Paleogene and Neogene mammalian faunas: Trophic structure and composition

Abstract Trophic structure and composition are examined in two important biotic records, one the Paleogene of Wyoming and Montana, and the other from the Neogene of Pakistan. The Paleogene sequence spans approximately 10 million years and encompasses four North American Land Mammal Ages (Torrejonian, Tiffanian, Clarkforkian, and Wasatchian). The Neogene sequence spans approximately 17 m.y. and includes most of the Miocene and Pliocene with the best documented interval spanning from 16 to 7 Ma. Five basic trophic categories (primary consumers: herbivores, frugivores, omnivores: secondary consumers: insectivores, carnivores) are recognized for Paleogene and Neogene mammals based on tooth morphology, body size, and analogy with modern mammalian groups. The Paleogene mammalian biota is characterized as one in which both trophic structure and taxonomic composition change through the history of the record. The Neogene mammalian biota maintains a relatively consistent trophic structure through most of the record, although taxonomic composition changes substantially through time. Based on comparisons of trophic structure from the Paleogene and Neogene records with that of selected modern mammalian faunas, Paleogene habitats fluctuated between closed, humid forests and more open, drier woodlands. Neogene trophic structure indicates that savanna woodlands were the typical habitat present through most of the sequence. Only after 7 Ma did these woodlands give way to more open grasslands in Pakistan.

Comparative paleoecology of Paleogene and Neogene mammalian faunas: body-size structure

Abstract Species size is correlated with many aspects of life history, ecology, and behavior, which means that size changes within species, lineages, and faunas represent an important component of evolutionary paleoecology. Comparison of Paleogene mammalian faunas from the Bighorn, Clarks Fork, and Crazy Mountains basins of Wyoming and Montana with Neogene mammalian faunas from the Siwalik Group of northern Pakistan reveals similarities and differences in patterns of size change through intervals of 10 m.y. Two approaches to size change are presented. The first is to evaluate changes in the size distribution of faunas over three time intervals in each sequence. Rank-ordered size distributions, or cenograms, are used to depict faunal size structure for non-carnivorous species. The slopes and gaps in different regions of the size spectrum reflect conditions of vegetation and climate, by analogy with modern mammalian faunas (Legendre, 1986, 1989). For the Paleogene and Neogene faunas, subtle changes over time in size structure reflect changes in local vegetation and climate. The Paleogene cenograms suggest a habitat shift from mesic to humid forest, and the Neogene cenograms suggest a shift from open woodland to savannah scrub. These interpretations are supported by concurrent changes in trophic structure, faunal turnover, and in floral and geologic indicators. The second approach focuses on size change within species and lineages in several families of predominantly herbivorous species. For 60 Paleogene species and 39 Neogene species, change in average species size over successive biostratigraphic intervals is assessed by a criterion of doubling or halving of body mass relative to the preceding interval. New occurrences are compared to established species of the same genus and of the same family. In both records, size increases occur slightly more often than size decreases. The size distribution of groups changes more often through appearances of species of more than double or less than half the size of established species of the same group or by disappearances, rather than through rapid change of size within species. The pattern of change in median size and size range of contemporaneous species varies among families in both records. Three causes of evolutionary size change—climatic change, competition, and predation—are evaluated. In both records, climatic change and interspecific competition are considered the principle mechanisms for the observed changes.

Taphonomy of vertebrate assemblages from the Paleogene of northwestern Wyoming and the Neogene of northern Pakistan

Abstract We compare the taphonomy of vertebrate assemblages from two long continental records—the early Paleogene of the Bighorn Basin, Wyoming, and the Neogene Siwalik sequence of northern Pakistan. Both sequences contain a similar array of fluvial facies, and the abundance of these facies differs among formations. We document environments of preservation of vertebrate localities over time to determine comparability of fossil assemblages within and between sequences. Changes in sample size and species richness are noted to reveal potential sampling effects on patterns of faunal turnover. Preservational history determined the environment, sample size, quality of specimens, taxonomic composition, and spatial and temporal resolution of fossil assemblages and thereby the quality of the fossil record and its suitability for further analyses. In both sequences, changes in prevailing taphonomic processes reflect changes in lithofacies and habitat distribution. Correlated changes are found in fossil productivity, species richness, and faunal composition. Both sequences contain some episodes of apparent faunal change in which appearances and disappearances of rare taxa can be attributed principally to changes in sample size. The Paleogene record has high taxonomic resolution (i.e., to genus or species) for most mammalian fossil remains. Temporal and spatial averaging of Paleogene fossil assemblages changes with lithofacies. The Neogene record has higher taxonomic resolution for remains of small mammals ( Different preservational circumstances impose different constraints on paleocological and evolutionary analyses. The best opportunities for paleocommunity reconstruction are provided by high taxonomic resolution, large samples, nd varied environments of preservation. These circumstances are found in limited portions of each record. The best opportunities for documenting evolution within lineages and species-replacement patterns are provided by high taxonomic resolution, high temporal resolution, and consistent preservational context. These taphonomic attributes pertain to the more common Paleogene mammals, particularly from the rich paleosol localities of the Willwood Formation, and to the more common Neogene small mammals from abandoned-channel fills of the Siwalik record.