Kathleen M. Muldoon

Oligocene mammals from Ethiopia and faunal exchange between Afro-Arabia and Eurasia

Afro-Arabian mammalian communities underwent a marked transition near the Oligocene/Miocene boundary at approximately 24 million years (Myr) ago. Although it is well documented that the endemic paenungulate taxa were replaced by migrants from the Northern Hemisphere, the timing and evolutionary dynamics of this transition have long been a mystery because faunas from about 32 to 24 Myr ago are largely unknown. Here we report a late Oligocene fossil assemblage from Ethiopia, which constrains the migration to postdate 27 Myr ago, and yields new insight into the indigenous faunal dynamics that preceded this event. The fauna is composed of large paenungulate herbivores and reveals not only which earlier taxa persisted into the late Oligocene epoch but also demonstrates that one group, the Proboscidea, underwent a marked diversification. When Eurasian immigrants entered Afro-Arabia, a pattern of winners and losers among the endemics emerged: less diverse taxa such as arsinoitheres became extinct, moderately species-rich groups such as hyracoids continued into the Miocene with reduced diversity, whereas the proboscideans successfully carried their adaptive radiation out of Afro-Arabia and across the world.

Primate energy expenditure and life history

Significance Measurements of daily energy expenditure indicate that primates, including humans, expend only half of the calories expected for mammals of similar body size. As energy expenditure is central to organismal biology, these results hold important implications for life history, evolutionary biology, and foraging ecology for primates and other mammals. Specifically, we show that primates’ remarkably low metabolic rates account for their distinctively slow rates of growth, reproduction, and aging. Humans and other primates are distinct among placental mammals in having exceptionally slow rates of growth, reproduction, and aging. Primates’ slow life history schedules are generally thought to reflect an evolved strategy of allocating energy away from growth and reproduction and toward somatic investment, particularly to the development and maintenance of large brains. Here we examine an alternative explanation: that primates’ slow life histories reflect low total energy expenditure (TEE) (kilocalories per day) relative to other placental mammals. We compared doubly labeled water measurements of TEE among 17 primate species with similar measures for other placental mammals. We found that primates use remarkably little energy each day, expending on average only 50% of the energy expected for a placental mammal of similar mass. Such large differences in TEE are not easily explained by differences in physical activity, and instead appear to reflect systemic metabolic adaptation for low energy expenditures in primates. Indeed, comparisons of wild and captive primate populations indicate similar levels of energy expenditure. Broad interspecific comparisons of growth, reproduction, and maximum life span indicate that primates’ slow metabolic rates contribute to their characteristically slow life histories.

The climatic niche diversity of malagasy primates: a phylogenetic perspective.

Background Numerous researchers have posited that there should be a strong negative relationship between the evolutionary distance among species and their ecological similarity. Alternative evidence suggests that members of adaptive radiations should display no relationship between divergence time and ecological similarity because rapid evolution results in near-simultaneous speciation early in the clades history. In this paper, we performed the first investigation of ecological diversity in a phylogenetic context using a mammalian adaptive radiation, the Malagasy primates. Methodology/Principal Findings We collected data for 43 extant species including: 1) 1064 species by locality samples, 2) GIS climate data for each sampling locality, and 3) the phylogenetic relationships of the species. We calculated the niche space of each species by summarizing the climatic variation at localities of known occurrence. Climate data from all species occurrences at all sites were entered into a principal components analysis. We calculated the mean value of the first two PCA axes, representing rainfall and temperature diversity, for each species. We calculated the K statistic using the Physig program for Matlab to examine how well the climatic niche space of species was correlated with phylogeny. Conclusions/Significance We found that there was little relationship between the phylogenetic distance of Malagasy primates and their rainfall and temperature niche space, i.e., closely related species tend to occupy different climatic niches. Furthermore, several species from different genera converged on a similar climatic niche. These results have important implications for the evolution of ecological diversity, and the long-term survival of these endangered species.

THE SUBFOSSIL OCCURRENCE AND PALEOECOLOGICAL SIGNIFICANCE OF SMALL MAMMALS AT ANKILITELO CAVE, SOUTHWESTERN MADAGASCAR

Abstract Small mammals are rarely reported from subfossil sites in Madagascar despite their importance for paleoenvironmental reconstruction, especially as it relates to recent ecological changes on the island. We describe the uniquely rich subfossil small mammal fauna from Ankilitelo Cave, southwestern Madagascar. The Ankilitelo fauna is dated to the late Holocene (∼500 years ago), documenting the youngest appearances of the extinct giant lemur taxa Palaeopropithecus, Megaladapis, and Archaeolemur, in association with abundant remains of small vertebrates, including bats, tenrecs, carnivorans, rodents, and primates. The Ankilitelo fauna is composed of 34 mammalian species, making it one of the most diverse Holocene assemblages in Madagascar. The fauna comprises the 1st report of the short-tailed shrew tenrec (Microgale brevicaudata) and the ring-tailed mongoose (Galidia elegans) in southwestern Madagascar. Further, Ankilitelo documents the presence of southwestern species that are rare or that have greatly restricted ranges today, such as Nasolos shrew tenrec (M. nasoloi), Grandidiers mongoose (Galidictis grandidieri), the narrow-striped mongoose (Mungotictis decemlineata), and the giant jumping rat (Hypogeomys antimena). A simple cause for the unusual small mammal occurrences at Ankilitelo is not obvious. Synergistic interactions between climate change, recent fragmentation and human-initiated degradation of forested habitats, and community-level processes, such as predation, most likely explain the disjunct distributions of the small mammals documented at Ankilitelo.

Paleoenvironment of Ankilitelo Cave (late Holocene, southwestern Madagascar): implications for the extinction of giant lemurs

Following human arrival, Madagascar suffered well-documented megafaunal extinctions and widespread deforestation. Although humans are widely considered to be the primary cause of the extinctions, the relative contributions of climate change and human activities to this ecological transformation remain uncertain. Reconstructing the habitats of the giant lemurs of Madagascar can provide key information for understanding the evolutionary mechanisms involved in their extinction. In this study, I present a faunal analysis of the subfossil assemblage from Ankilitelo Cave, southwestern Madagascar. This assemblage documents the latest known occurrence of five species of extinct giant lemur, in association with abundant well-preserved small mammal remains. I compared the small mammal fauna at Ankilitelo with 27 extant Malagasy mammal communities spanning the range of Madagascars habitat types. Similarities in species composition between modern communities and Ankilitelo were assessed using cluster analysis. Ecological similarities were examined by assigning each species to dietary, locomotor, activity pattern, and body size categories. Multiple discriminant analysis was then used to classify Ankilitelo relative to modern habitat types in Madagascar, based on the ecological structure of the subfossil fauna. Results indicate that the habitat surrounding Ankilitelo during the late Holocene was similar to the succulent woodlands of modern southwestern Madagascar. This suggests that approximately 500yr BP, these semi-arid habitats supported a subfossil lemur community that included the highly-suspensory Palaeopropithecus, and deliberate slow-climber Megaladapis, as well as Archaeolemur, Pachylemur, and Daubentonia robusta. In such environments, these giant lemurs would likely have been highly vulnerable to increasing human pressure in southwestern Madagascar.

Testing Bergmann's rule and the resource seasonality hypothesis in Malagasy primates using GIS-based climate data

We tested four major hypotheses on the ecological aspects of body mass variation in extant Malagasy strepsirrhines: thermoregulation, resource seasonality/scarcity, resource quality, and primary productivity. These biogeographic hypotheses focus on the ecological aspects of body mass variation, largely ignoring the role of phylogeny for explaining body mass variation within lineages. We tested the independent effects of climate and resource-related variables on variation in body mass among Malagasy primates using recently developed comparative methods that account for phylogenetic history and spatial autocorrelation. We extracted data on lemur body mass and climate variables for a total of 43 species from 39 sites. Climatic data were obtained from the WorldClim database, which is based on climate data from weather stations compiled around the world. Using generalized linear models that incorporate parameters to account for phylogenetic and spatial autocorrelation, we found that diet and climate variables were weak predictors of lemur body mass. Moreover, there was a strong phylogenetic effect relative to the effects of space on lemur body mass in all models. Thus, we failed to find support for any of the four hypotheses on patterns of geography and body mass in extant strepsirrhines. Our results indicate that body mass has been conserved since early in the evolutionary history of each genus, while species diversified into different environmental niches. Our findings are in contrast to some previous studies that have suggested resource and climate related effects on body mass, though these studies have examined this question at different taxonomic and/or geographic scales.

Evidence for dietary niche separation based on infraorbital foramen size variation among subfossil lemurs.

The size of the infraorbital foramen (IOF) has been used in drawing both phylogenetic and ecological inferences regarding fossil taxa. Within the order Primates, frugivores have relatively larger IOFs than folivores or insectivores. This study uses relative IOF size in lemurs to test prior trophic inferences for subfossil lemurs and to explore the pattern of variation within and across lemur families. The IOFs of individuals belonging to 12 extinct lemur species were measured and compared to those of extant Malagasy strepsirhines. Observations matched expectations drawn from more traditional approaches (e.g. dental morphology and microwear, stable isotope analysis) remarkably well. We confirm that extinct lemurs belonging to the families Megaladapidae and Palaeopropithecidae were predominantly folivorous and that species belonging to the genus Pachylemur (Lemuridae) were frugivores. Very high values for relative IOF area in Archaeolemur support frugivory but are also consistent with omnivory, as certain omnivores use facial touch cues while feeding. These results provide additional evidence that the IOF can be used as an informative osteological feature in both phylogenetic and paleoecological interpretations of the fossil record.

The Dwarf and Mouse Lemurs of Madagascar: Ecological niche modeling of mouse lemurs ( Microcebus spp.) and its implications for their species diversity and biogeography

Recent studies of lemur species diversity have particularly focused on mouse lemurs (Cheirogaleidae: Microcebus) – small, nocturnal, and superficially monotypic creatures (Radespiel et al., 2012; Zimmermann and Radespiel, 2014). Microcebus is widespread across the diverse habitats of Madagascar, and are present in primary, secondary, and disturbed forest types where suitable area remains (Mittermeier et al., 2010). Until the end of the last century, it was assumed that diversity in mouse lemurs consisted only of two morphologically and geographically distinct species – a larger, grayish western morph, Microcebus murinus, and a smaller, reddish eastern species, M. rufus (Mittermeier et al., 1994). Each of these species was thought to have broad distribution, encompassing a relatively diverse array of climates and habitats. In addition, mouse

Primates as Predictors of Mammal Community Diversity in the Forest Ecosystems of Madagascar

The geographic distribution of species is the typical metric for identifying priority areas for conservation. Since most biodiversity remains poorly studied, a subset of charismatic species, such as primates, often stand as surrogates for total biodiversity. A central question is therefore, how effectively do primates predict the pooled species richness of other mammalian taxa? We used lemurs as indicator species to predict total non-primate mammal community richness in the forest ecosystems of Madagascar. We combine environmental and species occurrence data to ascertain the extent to which primate diversity can predict (1) non-primate mammal α-diversity (species richness), (2) non-primate complementarity, and (3) non-primate β-diversity (species turnover). Our results indicate that primates are effective predictors of non-primate mammal community diversity in the forest ecosystems of Madagascar after controlling for habitat. When individual orders of mammals are considered, lemurs effectively predict the species richness of carnivorans and rodents (but not afrosoricids), complementarity of rodents (but not carnivorans or afrosoricids), and all individual components of β-diversity. We conclude that lemurs effectively predict total non-primate community richness. However, surrogate species alone cannot achieve complete representation of biodiversity.

Giant subfossil lemur graveyard discovered, submerged, in Madagascar.

In October, 2014, we organized a paleontological expedition toinvestigate flooded freshwatercavesinTsimanampetsotsa NationalPark, Madagascar, located in the arid southwestern region of thecountry where the karst landscape is pocked with dry caves andlarge water-filled sinkholes (Fig. 1). Our team of nine scuba diverswas led by Phillip Lehman of the Dominican Republic SpeleologicalSociety (Supplementary Online Material [SOM] Video 1). The dis-covery of subfossils in Tsimanampetsotsa was made initially byRyan Dart of Antananarivo. The director of Tsimanampetsotsa Na-tional Park, Mr. Lovasoa Dresy, immediately recognized theirimportance to science and encouraged the work reported here.Substantial numbers of subfossil remains were found in threecaves. In Aven Cave we discovered what is likely to be the singlelargest cache of giant subfossil lemurs ever uncovered. The othertwo fossiliferous caves were Mitoho and Malaza Manga. Subfossilshad been previously reported from around the entrance to MitohoCave (Perrier de la B^athie, 1934; Goodman and Jungers, 2014 ) butno underwater investigation of remains inside any of these caveshad been conducted prior to this expedition. Thus the primaryobjective was to establish the paleontological potential of thesecaves, with the principal aim of assessing the biodiversity of thesubfossil content of Aven (Fig.1).Avenisakarsticdissolutioncaveorsinkholeproducedbywaterdraining through the porous limestone shelf. It is a classic verticalsink hole with deep horizontal cave passageways, each ending in acollapse of limestone blocks. In the complex of tunnels and pas-sages, many sections can be accessed only through narrow re-strictions, a challenge that requires advanced cave divingtechniques as a precondition to safe exploration of this dark, un-charted subterranean environment (Fig. 2C). It is readily apparentthat these spaces were dry in the past as there is substantial spe-leothem (stalactite and stalagmite) formation. The full extent ofAvens passageways has yet to be explored, but our team laid about268 m of safety line during the expedition, running at an averagedepth of 42 m.Theopeningof the sinkholeis some25 min circumference, andthe water table is located 10e12 m below the rim. A small island inthe center of the water pool is the very top of a debris cone, whatsleft of the collapsed overhead rock (Fig. 1). The mound falls gentlyintothe depths of the lit cavern toabout25 m, fromwherethe caveextends into the blackness in all directions. It is in this transitionalzone where most of the more visible subfossil remains have beenlocated.Duringthesurvey,standardcavemappingtechniqueswereemployed to locate and mark areas with materials of interest, suchas dense bone accumulations or the location of important speci-mens. It became immediately apparent that there were multiplesites of import and hundreds of cranial and postcranial remains