A Review of “Evolution of Island Mammals: Adaptation and Extinction of Placental Mammals on Islands”

BackgroundThe Caribbean offers a unique opportunity to study evolutionary dynamics in insular mammals. However, the recent extinction of most Caribbean non-volant mammals has obstructed evolutionary studies, and poor DNA preservation associated with tropical environments means that very few ancient DNA sequences are available for extinct vertebrates known from the region’s Holocene subfossil record. The endemic Caribbean eulipotyphlan family Nesophontidae (“island-shrews”) became extinct ~ 500 years ago, and the taxonomic validity of many Nesophontes species and their wider evolutionary dynamics remain unclear. Here we use both morphometric and palaeogenomic methods to clarify the status and evolutionary history of Nesophontes species from Hispaniola, the second-largest Caribbean island.ResultsPrincipal component analysis of 65 Nesophontes mandibles from late Quaternary fossil sites across Hispaniola identified three non-overlapping morphometric clusters, providing statistical support for the existence of three size-differentiated Hispaniolan Nesophontes species. We were also able to extract and sequence ancient DNA from a ~ 750-year-old specimen of Nesophontes zamicrus, the smallest non-volant Caribbean mammal, including a whole-mitochondrial genome and partial nuclear genes. Nesophontes paramicrus (39-47 g) and N. zamicrus (~ 10 g) diverged recently during the Middle Pleistocene (mean estimated divergence = 0.699 Ma), comparable to the youngest species splits in Eulipotyphla and other mammal groups. Pairwise genetic distance values for N. paramicrus and N. zamicrus based on mitochondrial and nuclear genes are low, but fall within the range of comparative pairwise data for extant eulipotyphlan species-pairs.ConclusionsOur combined morphometric and palaeogenomic analyses provide evidence for multiple co-occurring species and rapid body size evolution in Hispaniolan Nesophontes, in contrast to patterns of genetic and morphometric differentiation seen in Hispaniola’s extant non-volant land mammals. Different components of Hispaniola’s mammal fauna have therefore exhibited drastically different rates of morphological evolution. Morphological evolution in Nesophontes is also rapid compared to patterns across the Eulipotyphla, and our study provides an important new example of rapid body size change in a small-bodied insular vertebrate lineage. The Caribbean was a hotspot for evolutionary diversification as well as preserving ancient biodiversity, and studying the surviving representatives of its mammal fauna is insufficient to reveal the evolutionary patterns and processes that generated regional diversity.

In this editorial, we provide a brief introduction and summarize the 10 research articles included in this Special Issue on Applications of stable isotope analysis in mammalian ecology. The first three articles report correction and discrimination factors that can be used to more accurately estimate the diets of extinct and extant mammals using stable isotope analysis. The remaining seven applied research articles use stable isotope analysis to address a variety of wildlife conservation and management questions from the oceans to the mountains.

Mammals exhibit vast ecological diversity, including a panoply of locomotor behaviours. The foundations of this diversity were established in the Mesozoic, but it was only after the end-Cretaceous mass extinction that mammals began to increase in body size, diversify into many new species and establish the extant orders. Little is known about the palaeobiology of the mammals that diversified immediately after the extinction during the Palaeocene, which are often perceived as ‘archaic’ precursors to extant orders. Here, we investigate the locomotor ecology of Palaeocene mammals using multivariate and disparity analyses. We show that tarsal measurements can be used to infer locomotor mode in extant mammals, and then demonstrate that Palaeocene mammals occupy distinctive regions of tarsal morphospace relative to Cretaceous and extant therian mammals, that is distinguished by their morphological robustness. We find that many Palaeocene species exhibit tarsal morphologies most comparable with morphologies of extant ground-dwelling mammals. Disparity analyses indicate that Palaeocene mammals attained similar morphospace diversity to the extant sample. Our results show that mammals underwent a post-extinction adaptive radiation in tarsal morphology relating to locomotor behaviour by combining a basic eutherian bauplan with anatomical specializations to attain considerable ecomorphological diversity.

Climate change is amongst the main threats to biodiversity. Considering extant mammals endured Quaternary climate change, we analyzed the extent to which this past change predicts current mammals’ extinction risk at global and biogeographical scales. We accessed range dynamics by modeling the potential distribution of all extant terrestrial mammals in the Last Glacial Maximum (LGM, 21,000 years ago) and in current climate conditions and used extinction risk from IUCN red list. We built General Linear Mixed-Effects Models to test the magnitude with which the variation in geographic range (ΔRange) and a proxy for abundance (ΔSuitability) between the LGM and present-day predicts current mammal’s extinction risk. We found past climate change most strongly reduced the geographical range and climatic suitability of threatened rather than non-threatened mammals. Quaternary range contractions and reduced suitability explain around 40% of species extinction risk, particularly for small-bodied mammals. At global and biogeographical scales, all groups that suffered significant Quaternary range contractions now contain a greater proportion of threatened species when compared to groups whose ranges did not significantly contract. This reinforces the importance of using historical range contractions as a key predictor of extinction risk for species in the present and future climate change scenarios and supports current efforts to fight climate change for biodiversity conservation.

Island Mammal Extinctions are Determined by Interactive Effects of Life History, Island Biogeography, Mesopredator Suppression

The Carnivora occupy a wide range of feeding niches in concordance with the enormous diversity in their skull and dental form. It is well established that differences in crown morphology are linked to variations in the material properties of the foods ingested and masticated. However, how tooth root form is related to dietary specialization is less well known. In the present study, we investigate the relationship between tooth root morphology and dietary specialization in terrestrial carnivores (canids, felids, hyaenids, and ursids). We specifically address the question of how variation in tooth root surface area is related to bite force potentials as one of the crucial masticatory performance parameters in feeding ecology. We applied computed tomography imaging to reconstruct and quantify dental root surface area in 17 extant carnivore species. Moreover, we computed maximal bite force at several tooth positions based on a dry skull model and assessed the relationship of root surface area to skull size, maximal bite force, food properties, and prey size. We found that postcanine tooth root surface areas corrected for skull size serve as a proxy for bite force potentials and, by extension, dietary specialization in carnivores. Irrespective of taxonomic affinity, species that feed on hard food objects have larger tooth roots than those that eat soft or tough foods. Moreover, carnivores that prey on large animals have larger tooth root surface areas. Our results show that tooth root morphology is a useful indicator of bite force production and allows inferences to be made about dietary ecology in both extant and extinct mammals.

The research describes for the first time a possible case of pituitary gigantism in fossil mammals, precisely in deer. The pathology was detected in 2 long bones (tibia and metatarsus) belonging to an individual of an unusual large size found at the Bate cave (Rethymnon, Northern Crete). It formed the basis of Candiacervus major, the largest among the endemic deer species recorded in the Pleistocene‐Early Holocene of Crete. Radiological and histomorphological examinations highlighted a reduction in cortical bone thickness and the presence of wide lacunae inside of the bone tissue. The pathological conditions suggest a pituitary gigantism diagnosis also supported by some morphological evidence, such as the extremely elongated distal part of the metatarsal diaphysis, the proportionally small proximal epiphysis, and some bone gracility. The diagnosis of a case of pituitary gigantism as presumed responsible for the extraordinary elongation of the tibia and the metatarsal bone is intriguing as they are, respectively, the paratype and the holotype of the C. major. The species represents a case of a deviation from the “island rule” in Pleistocene large mammals. The new evidence recommends a taxonomic and nomenclatural revision of this species. The main outcomes of this research are as follows: (i) a case of pituitary gigantism is described for the first time in an extinct mammal; (ii) it is underlined that paleohistology may provide interesting clues for disentangling taxonomic and nomenclatural issues; (iii) one of the very few cases of gigantism in insular mammals is being questioned.

Very little is known about the extinct mammals and how many extant mammals are found in Eritrea. Data have been gathered with the objectives of clearly defining the extinct, extirpated and endangered mammals in Eritrea. Findings indicate that seventeen taxa of fossil and subfossil mammals in six orders were found in Eritrea, extending from the late Oligocene to the Holocene. Faunal correlation among paleontological sites in the Horn of Africa and East Africa indicate that the best close correlation are the Haïdalo site in Djibouti and the Chilga site in Ethiopia. Provisional findings on extant mammals indicate that for its small size, Eritrea is extremely diverse; it is predicted that similar species richness would be found for fossil fauna. Of the 132 species of mammals known from Eritrea, 114 are terrestrial. Of these, 71.1% of species are small mammals (less then 10 kg adult body mass), 73.7% are nocturnal, and about 21.9% are fossorial, a possible explanation why they survived hunting and the 30-year war between Ethiopia and Eritrea. It has been postulated that the center of evolution of some small mammal taxa might have been in Ethiopia; this hypothesis should be tested for Eritrea. The 11 extirpated and 8 endangered mammals in Eritrea are listed. From the 3rd century BC until the 20th century AD, elephants were sighted in areas where they are not found today. The observation of more than 28 elephants by Shoshani and colleagues in 2001 was a rare phenomenon for Eritrea; the previous last sighting of a large herd was 46 years ago. In 2003 at least 83 elephants were also observed. Elephants (Loxodonta africana) in Eritrea are endangered; being very large and a keystone species, protecting them would also preserve other animals and plants in the same ecosystem. The symbiotic relationship between elephants and doum palms is critical to the survival of these two species. Conservation programs must include public awareness and education, emphasizing the role animals play in a balanced nature. Protecting the unique natural heritage of Eritrea is an asset to be promoted through ecotourism for this and future generations. This report is the first combined account on the extinct and extant mammalian fauna of Eritrea. Prior to 1993 all publications concerning faunal assemblages from Eritrea were under the heading of Ethiopia, since Eritrea was a province of Ethiopia. Data presented here, it is hoped, will serve as a basis for future research on the paleozoogeography and neozoogeography of Eritrean mammals.

Living saurian reptiles exhibit a wide range of diets, from carnivores to strict herbivores. Previous research suggests that the tooth shape in some lizard clades correlates with diet, but this has not been tested using quantitative methods. I investigated the relationship between phenotypic tooth complexity and diet in living reptiles by examining the entire dentary tooth row in over 80 specimens comprising all major dentigerous saurian clades. I quantified dental complexity using orientation patch count rotated (OPCR), which discriminates diet in living and extinct mammals, where OPCR-values increase with the proportion of dietary plant matter. OPCR was calculated from high-resolution CT-scans, and I standardized OPCR-values by the total number of teeth to account for differences in tooth count across taxa. In contrast with extant mammals, there appears to be greater overlap in tooth complexity values across dietary groups because multicusped teeth characterize herbivores, omnivores, and insectivores, and because herbivorous skinks have relatively simple teeth. In particular, insectivorous lizards have dental complexities that are very similar to omnivores. Regardless, OPCR-values for animals that consume significant amounts of plant material are higher than those of carnivores, with herbivores having the highest average dental complexity. These results suggest reptilian tooth complexity is related to diet, similar to extinct and extant mammals, although phylogenetic history also plays a measurable role in dental complexity. This has implications for extinct amniotes that display a dramatic range of tooth morphologies, many with no modern analogs, which inhibits detailed dietary reconstructions. These data demonstrate that OPCR, when combined with additional morphological data, has the potential to be used to reconstruct the diet of extinct amniotes. J. Morphol. 278:500-522, 2017. © 2017 Wiley Periodicals, Inc.

Size plays an important role in mammalian ecology. Accurate prediction of body mass is therefore critical for inferring aspects of ecology in extinct mammals. The unique digestive physiology of extant ruminant artiodactyls, in particular, is suggested to place constraints on their body mass depending on the type of food resources available. Therefore, reliable body mass estimates could provide insight into the habitat preferences of extinct ruminants. While most regression equations proposed thus far have used craniodental predictors, which for ungulates may produce misleading estimates based on indirect relationships between tooth dimensions and size, postcranial bones support the body and may be more accurate predictors of body mass. Here, I use phylogenetically informed bivariate and multiple regression techniques to establish predictive equations for body mass in 101 species of extant ruminant artiodactyls based on 56 postcranial measurements. Within limb elements, stepwise multiple regression models were typically preferred, though bivariate models often received comparable support based on Akaike's information criterion scores. The globally preferred model for predicting mass is a model including both proximal and distal width of the humerus, though several models from the radioulna received comparable support. In general, widths of long bones were good predictors, while lengths and midshaft circumferences were not. Finally, I show that where the best elements for prediction are unavailable for fossil taxa, selection of the model with lowest percent prediction error for the lowest level clade to which the fossil can be assigned could be a productive and novel way forward for predicting mass and subsequently aspects of ecology in fossil mammals.

A wide range of anthropogenic disturbances accompanied the spread of European settlement across Australia after 1788. They included widespread land clearance, changed fire regimes, harvesting/persecution of native biota, hydrological change through damming and irrigation, and the introduction of new species (Lunney et al. 1997; Calver et al. 1998 and included references). In concert, these changes have contributed to the extinction of 17 mammalian species (Recher & Lim 1990), representing over 6% of the original mammalian fauna and about half of mammal extinctions worldwide in the last 200 years (Dickman et al. 1993). It seems unlikely that the situation has stabilized, because over 17% of extant Australian mammal species have suffered range reductions since colonization (Dickman et al. 1993). Garkaklis et al. (1998, 2000) highlighted that the extinct mammals included many burrowers and diggers, so a suite of species involved in soil turnover, nutrient cycling, and plant propagule dispersal have disappeared. The disruption of such critical processes in the face of anthropogenic stressors is a critical tenet of health theory and suggests a loss of health in the as a whole (Costanza et al. 1998; Rapport 1998a,b). Recent experimental evidence confirmed the significant role of the invasive predators the red fox (Vulpes vulpes) and feral house cat (Felis catus) in the decline of several extant mammals (e.g., Kinnear et al. 1998; Risbey et al. 1999; Risbey et al. 2000 and, by implication, in the extinction of related species. Control of invasive predators is now a major part of recovery plans for a range of Australian mammals (Maxwell et al. 1996), primarily by baiting with the toxin sodium monofluoroacetate (commonly referred to as compound 1080, pronounced 'ten-eighty') (see Twigg & King 1991 for a major review). However, wildlife advocates are often uneasy about poisoning campaigns, so delicate public relations issues are involved (Calver & King 1986; Temple 1990; Marks et al. 2000). Cancers in human health are a tempting metaphor for the destruction wrought by invasive vertebrates to health (Robert Colona, quoted in Stokstad 2000; Stone 2000. In the case of cancers, there is evidence that physiological or psychosocial distress may depress immune system function and contribute to the onset of disease. Malignant cells then proliferate and may disperse, disrupting normal functioning and causing death. Similarly, anthropogenic disturbances may predispose to invasion by alien species, which displace indigenous species or modify processes and disrupt health. Furthermore, the metaphor can be extended to embrace treatments for cancer, with the use of toxins to eradicate or control invasive species seen as for ecosystems. Several authors have explored the parallel between human health and health (e.g., Ehrenfeld 1995; Rapport 1998a. Others have noted the power of such metaphors to encourage community involvement in environmental issues (O'Laughlin 1996; Calver 2000). In this paper, we extend the concept of the human health/ecosystem health metaphor as an educational tool, using the Australian case study of controlling destructive invasive predators by poison baiting. The destructive invasive species can be regarded as cancer cells in the and the poison baiting as to eradicate or contain them. The metaphor may allay community disapproval of poisoning as a control method by relating it to a familiar form of medical treatment used to protect human health. We develop the metaphor by: (1) overviewing the nature of human cancers and the applications, side effects, and limitations of human (2) overviewing characteristics of species introductions and the applications and limitations of chemical control of invasive species, with special reference to predator control in Western Australia as an example of ecosystem chemotherapy; (3) assessing the validity of the ecosystem chemotherapy metaphor by applying it to a range of and commenting on its potential in community education. The discussion reveals that the for ecosystems metaphor is robust in some cases and has potential as an educational tool. It is especially useful in highlighting the value of prevention, as opposed to cure, in the case of invasive species and emphasizing the importance of allowing local communities to make decisions about local health.

Primates

Biogeographia vol. XXV - 2004 (Printed December, 30 q' 2004) Marine Biogeography of the Mediterranean Sea: patterns and dynamics of biodiversity Mediterranean Island mammals: are they a priority for biodiversity conservation? SPARTACO GIPPOLITI, GIOVANNI AMORI Irtituro per 10 Studio degli Ecoristemi, CNR c/0 Dzjyzzrtimerzto di Bio/ogizz Animrzle 5 a’e[[’U0m0, lfiziverszriz “LIZ Srzpz'mzzz’§ Via A. Borelli 50- 00161 Roma (Italy) e—mrzz'l: 5przrtrzco[o6u5@/7oz7mzz'/. com Keywords: Mediterranean islands, feral mammals, conservation priorities, biodiversity, taxonomy. SUMMARY The importance of taxonomy in biological conservation is now well established. However, the risk involved in assigning specific or subspecific status to feral mammals or mammals introduced in the Mediterranean Islands ancient time, has been generally overlooked. In fact, these ‘antropochorous taxa’, especially ungulates such as ‘wild’ goats and ‘wild’ sheep, have became the focus of many national and international conservation activities because of their high aesthetic, symbolic and hunting value. This, however, has often lead to a misallocation of conservation resources thereby indirectly damaging die fiiture prospects for the few true surviving insular paleoendemic mammals such as the Cretan and Sicilian shrews Cracidurrl zim17m77zrm71i and C'ratz'z2'1mz rimlzz, respectively. Conservation policies simply based on protection of anthropocorous mammals — or of birds of prey whose populations depend on such insular mammals — need to lie carefully re—assessed. Actually, there is scattered evidence that this approach represents a further threat to the whole Mediterranean island biodiversity. Great caution is especially needed in small, protected, ‘ocean—lille’ islands where mammals — especially ungulates — are not hunted and endernism rate is usually high. Here, the growth of ungulate populations can have disastrous effects on biodiversity throughout both disappearance of several endemic plants which lack defence from grazing, and a likely cascade effect on invertebrate Communities. Nowadays, knowledge of each island palaeoecology is essential to assess the best management options for antrophocorous mammals in the interest of Mediterranean biodiversity conservation. INTRODUCTION The importance of taxonomy in the conservation assessments has often been emphasised in the last years (McNeely, 2002). It is obviously not possible to protect what is not believed to exist and it is not recognised by taxonomy. This is the case of the tuatara, Sp/Jenodon spp., as revealed by a well-known study on its systematic (Daugherty et al., 1990). On the other hand, the opposite problem also exists. A formal taxonomic recognition could justify considerable conservation

A recent paper published in PLoS Biology [1] deals with the contention of whether the rates of morphological evolution are accelerated on islands relative to the mainland. Because of the scarcity of empirical data, the long-held supposition that insular mammals can evolve faster than their continental counterparts remains debatable. In this context, the work in [1] represents a valuable contribution. Indeed, the author has collected and provided a wealth of data of considerable interest. Nevertheless, the main conclusion of [1] may not be fully supported by the data when they are critically analysed. In the cited work, island and mainland rate comparisons were carried out by regression analyses obtained when log rates in darwins were plotted against log times in million years. The author claimed that the regression line of the island species was above the line of the mainland species over a large range of data, indicating that the evolutionary rates for island species were greater than those for mainland species. However, this claim deserves some reflection. Rates in darwins (d) were calculated as (ln x2– ln x1)/Δt, where x1 and x2 correspond to linear measurements of the same structure for a descendant and its ancestor, which are separated by Δt million years. Whenever using the darwin to describe the evolutionary rate of change, a caveat must be born in mind: darwins accurately describe rates of change, only provided that evolutionary changes (ln x2– ln x1) resulted from steady accumulation in a monotonic fashion over the entire period of time (Δt). If this is not the case, then the resulting rates of evolution may be mathematical artefacts of the length of the interval over which they are measured. In other words, the values obtained will not describe solely the sequence of changes and their tempo, but rather will include dependences on the arbitrary choices of starting and ending points from which the rates are calculated [2]. The difficulties related to the implicit assumption of a monotonic relationship between change and elapsed time, with no provision for reversal changes or punctuation, becomes especially relevant when comparing data differing widely in their time intervals. This seems to be the case in [1], where there are fewer island data points for the largest time intervals (six higher than 21,000 y) and fewer mainland data points for the smallest time intervals (two below 2,400 y). Not surprisingly, under these circumstances, data from islands showed higher values of d than their continental counterpart, despite the lack of a significant difference in their evolutionary changes. In contrast, when only those samples from island and mainland that were sampled over the same period of time (2,400–21,000 y) were included in the analysis, we failed to detect any significant difference in the rate of morphological evolution among insular and continental mammals. An accelerated evolution among island mammals may be a real feature that we do not refuse. However, the validity of this claim remains an open question that deserves further research. In any event, we should be aware of the necessity to provide reliable analyses, free of those mathematical artefacts associated with the interpretation of data.

Reading the black book: The number, timing, distribution and causes of listed extinctions in Australia