Insular Mammals Research Articles

A global assessment of nested patterns in insular mammal assemblages

A global assessment of nested patterns in insular mammal assemblages

The paradox of anthropogenic enrichment: homogenization and downsizing of insular mammals

The paradox of anthropogenic enrichment: homogenization and downsizing of insular mammals

Insular giant leporid matured later than predicted by scaling

The island syndrome describes morphological, behavioral, and life history traits that evolve in parallel in endemic insular organisms. A basic axiom of the island syndrome is that insular endemics slow down their pace of life. Although this is already confirmed for insular dwarfs, a slow life history in giants may not be adaptive, but merely a consequence of increasing body size. We tested this question in the fossil insular giant leporid Nuralagus rex. Using bone histology, we constructed both a continental extant taxon model derived from experimentally fluorochrome-labeled Lepus europaeus to calibrate life history events, and a growth model for the insular taxon. N.rex grew extremely slowly and delayed maturity well beyond predictions from continental phylogenetically corrected scaling models. Our results support the life history axiom of the island syndrome as generality for insular mammals, regardless of whether they have evolved into dwarfs or giants.

Evolution: The rise and fall of island dwarfs and giants

Islands are arenas for a range of striking evolutionary phenomena, including the island rule- the tendency for larger animals to shrink and smaller animals to enlarge. A new study of insular mammals finds such body size shifts predispose these evolutionary marvels to greater extinction risk.

Dwarfism and gigantism drive human-mediated extinctions on islands

Islands have long been recognized as distinctive evolutionary arenas leading to morphologically divergent species, such as dwarfs and giants. We assessed how body size evolution in island mammals may have exacerbated their vulnerability, as well as how human arrival has contributed to their past and ongoing extinctions, by integrating data on 1231 extant and 350 extinct species from islands and paleo islands worldwide spanning the past 23 million years. We found that the likelihood of extinction and of endangerment are highest in the most extreme island dwarfs and giants. Extinction risk of insular mammals was compounded by the arrival of modern humans, which accelerated extinction rates more than 10-fold, resulting in an almost complete demise of these iconic marvels of island evolution.

Inferring longevity from advanced rib remodelling in insular dwarf deer

AbstractDwarfed insular mammals are of significant interest to evolutionary biology because of their morphological and physiological adaptations triggered by variables inherent to geographical isolation. One life history trait that is expected to be modified in relation to body size reduction is extended longevity facilitated by ecological parameters such as predator and competitor release and fluctuating resource availability. However, systematic examination of longevity in extreme cases of dwarfism is difficult as such cases are largely represented by fossils of extinct species. We studied seven rib fragments of the extraordinary endemic Pleistocene dwarf deer Candiacervus (size 2) to test whether its bone matrix shows evidence for extensive bone remodelling typically seen in large and long-living mammals. We found that all ribs had well-remodelled Haversian bone, implying several generations of resorption and re-deposition processes. Osteon density was high relative to small bone cross-section size, with examples of porosity similar to that seen in elderly animals. We report the first combined micro-morphological and micro-morphometric record of Candiacervus rib histology, agreeing with previous literature discussing the evolutionary biology of dwarf ruminants. Further experimental validation of osteon density in extant deer will confirm whether dwarfed Candiacervus indeed lived longer than expected for its body mass.

Palaeohistology reveals a slow pace of life for the dwarfed Sicilian elephant

The 1-m-tall dwarf elephant Palaeoloxodon falconeri from the Pleistocene of Sicily (Italy) is an extreme example of insular dwarfism and epitomizes the Island Rule. Based on scaling of life-history (LH) traits with body mass, P. falconeri is widely considered to be ‘r-selected’ by truncation of the growth period, associated with an early onset of reproduction and an abbreviated lifespan. These conjectures are, however, at odds with predictions from LH models for adaptive shifts in body size on islands. To settle the LH strategy of P. falconeri, we used bone, molar, and tusk histology to infer growth rates, age at first reproduction, and longevity. Our results from all approaches are congruent and provide evidence that the insular dwarf elephant grew at very slow rates over an extended period; attained maturity at the age of 15 years; and had a minimum lifespan of 68 years. This surpasses not only the values predicted from body mass but even those of both its giant sister taxon (P. antiquus) and its large mainland cousin (L. africana). The suite of LH traits of P. falconeri is consistent with the LH data hitherto inferred for other dwarfed insular mammals. P. falconeri, thus, not only epitomizes the Island Rule but it can also be viewed as a paradigm of evolutionary change towards a slow LH that accompanies the process of dwarfing in insular mammals.

Source pool diversity and proximity shape the compositional uniqueness of insular mammal assemblages worldwide

AbstractAimIslands have been the test bed of several theories in community ecology, biogeography, and evolutionary biology. Progress within these disciplines has given a more comprehensive and mechanistic understanding of the processes governing variation in species richness among islands. However, it remains unclear whether these same processes also explain variation in species and phylogenetic composition among islands. Integrating theory from ecology and biogeography, we infer the roles of dispersal, selection, and stochasticity on the composition of insular assemblages within archipelagos. We further assess the influence of source pool diversity and connectivity on the compositional uniqueness of insular assemblages.LocationIsland systems worldwide.TaxonMammals.MethodsWe compiled data on species composition of nonvolant mammals on ~200 islands in nine archipelagos distributed worldwide from the literature. We used variation partitioning to quantify the relative influence of the environment (selection) and geographic distance (dispersal) relative to a null model (stochasticity, randomness) on taxonomic and phylogenetic compositional turnover within archipelagos. We then used a linear mixed model to gain further insight into the underlying mechanisms shaping variation in assemblage composition among islands at a global scale. Specifically, we assessed the influence of source pool diversity, isolation from the source pool, and island characteristics on compositional uniqueness.ResultsOur results suggest that within‐archipelago variation in the composition of insular mammal assemblages is associated with stochastic or unmeasured processes rather than abiotic selection or dispersal limitation. The diversity and proximity of the source pool, as well as some island characteristics, explained variation in phylogenetic, but not taxonomic, compositional uniqueness globally. Globally, isolated islands associated with phylogenetically diverse source pools exhibit high phylogenetic uniqueness whereas well‐connected islands associated with phylogenetically clustered source pools show the opposite trend. Phylogenetically unique assemblages also tend occur on islands with a small elevational span and low annual temperature variation.Main conclusionsTaken together, our results suggest that source pool diversity, along with the potential for colonization from those pools, has a strong influence on the composition of insular mammal assemblages worldwide.

The intriguing giant deer from the Bate cave (Crete): could paleohistological evidence question its taxonomy and nomenclature?

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.

Rapid size change associated with intra-island evolutionary radiation in extinct Caribbean \u201cisland-shrews\u201d

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.

Brain Changes during Phyletic Dwarfing in Elephants and Hippos

Of all known insular mammals, hippos and elephants present the extremes of body size decrease, reducing to 4 and a mere 2% of their ancestral mainland size, respectively. Despite the numerous studies on these taxa, what happens to their relative brain size during phyletic dwarfing is not well known, and results are sometimes conflicting. For example, relative brain size increase has been noted in the Sicilian dwarf elephant, Palaeoloxodon falconeri, whereas relative brain size decrease has been postulated for Malagasy dwarf hippos. Here, I perform an analysis of brain, skull, and body size of 3 insular elephants (Palaeoloxodon “mnaidriensis,” P. tiliensis, and P. falconeri) and 3 insular hippos (Hippopotamus madagascariensis, H. lemerlei, and H. minor) to address this issue and to test whether relative brain size in phyletic dwarf species can be predicted. The results presented here show that the encephalization of all insular elephants and hippos is higher than that of their continental relatives. P. falconeri in particular has an enormous encephalization increase, which has so far not been reported in any other insular mammal. Insular brain size cannot be reliably predicted using either static allometric or ontogenetic scaling models. The results of this study indicate that insular dwarf species follow brain-body allometric relationships different from the expected patterns seen for their mainland relatives.

The 100 Most Cited Papers Concerning the Insular Cortex of the Brain: A Bibliometric Analysis.

Background: The insula is one of the most researched brain regions with many highly cited papers. However, unlike the literature of other fields, there is currently no study that has identified the 100 most cited papers within the literature of the insula. The aim of the current study was to fill in the knowledge gap by determining which publications concerning the insula have been cited most often, who contributed to them, and what topics they were dealing with.Methods: The Web of Science online database was searched to identify the 100 most cited publications mentioning the insular cortex in their titles, abstracts or keywords. To systematically exclude irrelevant publications, the search strategy was finalized as: TS = (insula OR insular OR “island of Reil”) NOT TS = (“insular biogeography” OR “insular mammal*” OR “*insular lymphatic*”) NOT WC = (“Geochemistry and Geophysics” OR “Ecology”). The identified publications were sorted in descending order of citation count. The 100 most cited publications concerning the insula of the brain were identified and their bibliometric data was extracted and assessed. The VOSviewer software was used with default parameters to generate a bubble map that analyzes and visualizes the words/phrases used in the titles and abstracts of the publications.Results: There were 67 articles on experiments/lab studies and 33 meta-analyses/reviews but no opinion or methods paper. They had an average of 943.4 citations (or 62.9 citations per year), 93.5 references and 13.4 pages. There were 35 papers published in open access. USA was the major contributing country. The most top-ranked publications were concerning emotion, salience and pain.Conclusion: Two-thirds of the publications concerned the normal brain function/mechanism (n = 67), whereas 20 publications concerned disease/therapeutic intervention and another 13 concerned normal anatomy. For the 67 original articles, 57 used human subjects whereas 10 used animal models. MRI was the commonest modality (n = 37), followed by PET (n = 16). Nine articles investigated by histology, two by multiple modalities and three by other modality.

A new method for testing evolutionary rate variation and shifts in phenotypic evolution

Abstract Quantifying phenotypic evolutionary rates and their variation across phylogenetic trees is a major issue in evolutionary biology. A number of phylogenetic comparative methods (PCMs) currently perform such task. However, available PCMs can locate rate shifts pertaining to entire portions of the phylogeny, but not those expected to occur at the level of individual species and lineages, such as with the idea that body size changes more rapidly in insular vertebrates. Still, most PCMs cannot deal with fossil phylogenies, albeit fossils provide highly desirable information when it comes to understand trait variation and evolution. We developed a PCM based on phylogenetic ridge regression, which we named RRphylo, which assigns an evolutionary rate to each branch of the phylogeny, and is designed to locate rate shifts relating to entire clades, as well as to unrelated tree tips. We tested RRphylo on simulated trees and data to assess its performance under different conditions. Then, we repeated its application with two real case scenarios, the evolution of flight in ornithodirans and mammals and body size evolution in insular mammals, which are usually subsumed to evolve under different range regimes than terrestrial and continental species respectively. RRphylo performs well across all different conditions. The simulation experiments demonstrated it has low Type I and Type II error rate. We found significant evidence that flight accelerates the rate of body size evolution in vertebrates, and that the acquisition of very large body size slows down the rate. Still, insular mammals body size evolution is not faster than in continental species. RRphylo is a new PCM ideal to estimate variation and shift in the rate of phenotypic evolution with fossil data. In addition to testing evolutionary rate variation, it is open to a variety of further questions, such as the evolution of rates in time, the estimation of ancestral states and the estimation of phenotypic trends over time.

Geographical distribution and conservation status of an endemic insular mammal: the Vulnerable fish-eating batMyotis vivesi

AbstractEndemic insular species are particularly vulnerable to anthropogenic threats. The fish-eating batMyotis vivesiis restricted mainly to the islands of the Gulf of California in Mexico and although several aspects of its biology have been studied there are no recent accounts of its current distribution. We conducted several expeditions during 2001–2016 to verify the current geographical distribution of this bat, and to record the presence of introduced predators. We identified the localities in which maternity colonies occur, estimated the size of the bat population on Partida Norte Island in 2003, and monitored bat presence on this island during 2004–2016. We found fish-eating bats on 36 islands and maternity colonies on 19 islands. Introduced ratsRattus rattusor catsFelis catuswere captured on seven islands where the bats were present, and on five islands where they were absent. We estimated a population of c. 30,000 fish-eating bats in May 2003 and we confirmed the species’ presence on Partida Norte Island during 2004–2016. Based on the information compiled from our surveys and previous studies, we discuss the adequacy of the species’ current categorization as Vulnerable on the IUCN Red List, and its conservation status conferred by Mexican conservation authorities.

The effect of area and isolation on insular dwarf proboscideans

AbstractAimWe investigated the hypothesis that insular body size of fossil elephants is directly related to isolation and surface area of the focal islands.LocationPalaeo‐islands worldwide.MethodsWe assembled data on the geographical characteristics (area and isolation) of islands and body size evolution of palaeo‐insular species for 22 insular species of fossil elephants across 17 islands.ResultsOur results support the generality of the island rule in the sense that all but one of the elephants experienced dwarfism on islands. The smallest islands generally harbour the smallest elephants. We found no support for the hypothesis that body size of elephants declines with island isolation. Body size is weakly and positively correlated with island area for proboscideans as a whole, but more strongly correlated for Stegodontidae when considered separately. Average body size decrease is much higher when competitors are present.Main conclusionsBody size in insular elephants is not significantly correlated with the isolation of an island. Surface area, however, is a significant predictor of body size. The correlation is positive but relatively weak; c. 23% of the variation is explained by surface area. Body size variation seems most strongly influenced by ecological interactions with competitors, possibly followed by time in isolation. Elephants exhibited far more extreme cases of dwarfism than extant insular mammals, which is consistent with the substantially more extended period of deep geological time that the selective pressures could act on these insular populations.

How large are the extinct giant insular rodents? New body mass estimations from teeth and bones

The island rule entails a modification of the body size of insular mammals, a character related with numerous biological and ecological variables. From the Miocene to human colonization (Holocene), Mediterranean and Canary Islands were unaltered natural ecosystems, with paleofaunas formed with endemic giant rodents among other mammals. Our aim is to create methods to estimate the body masses of fossil island rodents and address the nature of ecological pressures driving the island rule. We created regression equations based on extant rodent data and used these to estimate the body masses of the extinct species. Our results show strong correlations between teeth, cranial and postcranial measurements and body mass, except for the length of the long bones, the transversal diameter of the distal tibia and the anteroposterior diameter of the proximal tibia, where the equations were less reliable. The use of equations obtained from a more homogeneous group (suborder and family) is preferable when analyzing the area of the first molar. The new regressions were applied to estimate the body masses of some Mediterranean and Canarian fossil rodents (Canariomys, C. bravoi 1.5 kg and C. tamarani 1 kg; Hypnomys, H. morpheus 230 g and H. onicensis 200 g; and Muscardinus cyclopeus 100 g). Our results indicate that under absence of predation, resource availability (island area) is the key factor that determines the size of the Canariomys sp. However, under presence of specialized predators (birds of prey), body size evolution is less pronounced (Hypnomys sp.).

Distribution and spread of an introduced insular population of red-bellied squirrels (Sciurus aureogaster) in Florida

Introduced populations of species pose one of the greatest threats to the persistence of native species. Documentation of distribution, range expansion and habitat use of introduced populations are key components of developing effective management strategies for the control and eradication of invasive species. In 2006 and 2007, we surveyed four islands in Biscayne National Park for nests to evaluate the presence of red-bellied squirrels (Sciurus aureogaster) and the distribution and index of dispersion of their nests in the Florida Keys archipelago within the Atlantic Ocean. Red-bellied squirrels were initially introduced to Elliott Key, Florida, USA in in 1938. We documented evidence of squirrels on two additional islands, Sands Key and Old Rhodes Key, which adds to concerns of spread of this introduced squirrel to areas with endangered endemic insular mammals. Squirrel nests were documented only in mixed-hardwood forest, and nests had a clumped distribution within this forest type. Range expansion was a chief concern to the National Park Service, as continued spread could result in squirrels exiting the park, and prompted management action. Understanding nest site selection and distribution was critical for developing an eradication strategy for the introduced population of red-bellied squirrels from south Florida.

The enigmatic bovid Duboisia santeng (Dubois, 1891) from the Early–Middle Pleistocene of Java: A multiproxy approach to its paleoecology

During the Pleistocene, the Sunda Islands to which Java belongs were frequently connected with the East Asian mainland, permitting faunal elements of Indo-Chinese origin entering Java. Therefore, most Javanese mammalian taxa are close if not identical to their mainland relatives. In particular, three fossil bovids, commonly found in the Early–Middle Pleistocene “Stegodon-Homo erectus fauna” (Bubalus palaeokerabau, Bibos palaesondaicus, and Epileptobos groeneveldtii), do not show any feature consistent with the evolutionary pattern of typical insular mammals. However, a fourth Javanese bovid, Duboisia santeng has been regarded as a typical insular endemic species due to its small size. However, since Duboisia has been claimed to be present in the late Middle Pleistocene of what is now peninsular Malaysia, the actual endemic insular status of this taxon needs further confirmation.In this study we aim to contribute to the debate by analyzing the autecology of Javanese Duboisia santeng, delving into its paleobiogeographic history and evolution. The multiproxy approach adopted here (body mass estimate, paleohabitat predictions, morphological comparison, mesowear analysis and Dental Areal Surface Texture Analysis DASTA) gave mutually consistent results and proved to be useful in supporting hypothesis regarding the complex evolution of insular faunas.

Of mice and mammoths: generality and antiquity of the island rule

AbstractAimWe assessed the generality of the island rule in a database comprising 1593 populations of insular mammals (439 species, including 63 species of fossil mammals), and tested whether observed patterns differed among taxonomic and functional groups.LocationIslands world‐wide.MethodsWe measured museum specimens (fossil mammals) and reviewed the literature to compile a database of insular animal body size (Si = mean mass of individuals from an insular population divided by that of individuals from an ancestral or mainland population, M). We used linear regressions to investigate the relationship between Si and M, and ANCOVA to compare trends among taxonomic and functional groups.ResultsSi was significantly and negatively related to the mass of the ancestral or mainland population across all mammals and within all orders of extant mammals analysed, and across palaeo‐insular (considered separately) mammals as well. Insular body size was significantly smaller for bats and insectivores than for the other orders studied here, but significantly larger for mammals that utilized aquatic prey than for those restricted to terrestrial prey.Main conclusionsThe island rule appears to be a pervasive pattern, exhibited by mammals from a broad range of orders, functional groups and time periods. There remains, however, much scatter about the general trend; this residual variation may be highly informative as it appears consistent with differences among species, islands and environmental characteristics hypothesized to influence body size evolution in general. The more pronounced gigantism and dwarfism of palaeo‐insular mammals, in particular, is consistent with a hypothesis that emphasizes the importance of ecological interactions (time in isolation from mammalian predators and competitors was 0.1 to > 1.0 Myr for palaeo‐insular mammals, but < 0.01 Myr for extant populations of insular mammals). While ecological displacement may be a major force driving diversification in body size in high‐diversity biotas, ecological release in species‐poor biotas often results in the convergence of insular mammals on the size of intermediate but absent species.

Higher extinction rates of dasyurids on Australo‐Papuan continental shelf islands and the zoogeography of New Guinea mammals

AbstractAimContemporary patterns of mammalian species richness on islands are influenced by well‐understood biogeographical variables. Whether or not mammalian orders differ in their rates of persistence, however, remains uncertain. Our aims were to assess the persistence of four mammalian orders on Australo‐Papuan continental shelf islands in relation to the faunas within adjacent zoogeographic provinces. We also aimed to define New Guinea's mammalian zoogeographic provinces quantitatively.LocationNew Guinea and 274 Australo‐Papuan continental shelf islands.MethodsWe compiled 4194 distributional records for 264 of New Guinea's native mammals. Records were allocated to existing mapped bioregions. We used cluster analysis to allocate bioregions to zoogeographic provinces. Using generalized linear models, we determined the persistence of insular mammals as proportions of the species present within adjacent zoogeographic provinces. Persistence rates were calculated for four major orders (Dasyuromorphia, Diprotodontia, Peramelemorphia and Rodentia).ResultsThe classification dendrogram grouped New Guinea's bioregions into three areas corresponding to the Oceanic, Tumbanan and Austral provinces. In all but two zoogeographic provinces, the proportions of Dasyuromorphia persisting on islands were lower than other orders. Overall, species of Dasyuromorphia were much less likely to persist on Australo‐Papuan continental shelf islands.Main conclusionsUnlike the other orders considered, dasyuromorphs are carnivorous and insectivorous and require large home ranges relative to body size. We suggest that the resulting low population densities might expose species in this order to higher rates of extinction on islands. Translocations of threatened mammals to predator‐free islands are common, but our results suggest that insurance populations of threatened dasyurids on small islands may be less secure than translocations of other taxa. Our results support calls for insurance populations of the rapidly declining dasyurid, the Tasmanian devil (Sarcophilus harrisii), to be established on mainland Australia rather than on islands alone.