Sarah Federman

Implications of lemuriform extinctions for the Malagasy flora

Significance Madagascar is a conservation priority because of its unique and threatened biodiversity. Lemurs, by acting as seed dispersers, are essential to maintaining healthy and diverse forests on the island. However, in the past few thousand years, at least 17 lemur species, many of which were inferred seed dispersers, have gone extinct. We outline the substantial impact that these extinctions have likely had on Malagasy forests by comparing the gape sizes and diets of living and extinct lemurs to identify large-seeded Malagasy plants that appear to be without extant animal dispersers. Additionally, we identify living lemurs that are endangered yet occupy unique and essential dispersal niches. This information can inform conservation initiatives targeting the protection and restoration of these vulnerable ecosystems. Madagascar’s lemurs display a diverse array of feeding strategies with complex relationships to seed dispersal mechanisms in Malagasy plants. Although these relationships have been explored previously on a case-by-case basis, we present here the first comprehensive analysis of lemuriform feeding, to our knowledge, and its hypothesized effects on seed dispersal and the long-term survival of Malagasy plant lineages. We used a molecular phylogenetic framework to examine the mode and tempo of diet evolution, and to quantify the associated morphological space occupied by Madagascar’s lemurs, both extinct and extant. Using statistical models and morphometric analyses, we demonstrate that the extinction of large-bodied lemurs resulted in a significant reduction in functional morphological space associated with seed dispersal ability. These reductions carry potentially far-reaching consequences for Malagasy ecosystems, and we highlight large-seeded Malagasy plants that appear to be without extant animal dispersers. We also identify living lemurs that are endangered yet occupy unique and essential dispersal niches defined by our morphometric analyses.

The biogeographic origin of a radiation of trees in Madagascar: implications for the assembly of a tropical forest biome

BackgroundMadagascar’s rain forests are characterized by extreme and uneven patterns of species richness and endemicity, the biogeographic and evolutionary origins of which are poorly understood.MethodsHere we use a time-calibrated phylogeny of a dominant group of trees in Madagascar’s eastern rain forests, Canarium, and related Burseraceae (Canarieae), to test biogeographic hypotheses regarding the origin and radiation of the flora of this unique biome.ResultsOur findings strongly support the monophyly of Malagasy Canarium, suggesting that this clade represents a previously undocumented in situ radiation. Contrary to expectations of dispersal from Africa during the Oligocene, concurrent with the formation of Madagascar’s rain forest biome, our analyses support a late Miocene origin for Malagasy Canarium, probably by long distance dispersal from Southeast Asia.DiscussionOur study illustrates the importance of considering long distance dispersal as a viable explanation for clades with pantropical distributions diversifying subsequent to the Oligocene, and it highlights the formation of the Indo-Australian Archipelago and associated fast-moving equatorial surface currents, suggesting an under-appreciated evolutionary link among tropical centers of endemism.ConclusionsWe postulate that the relatively recent establishment and radiation of Canarium in Madagascar may have been facilitated by the highly stochastic climates associated with these forest ecosystems.

Cryptic species diversity in sub-Antarctic islands: A case study of Lepidonotothen

The marine fauna of the Southern Ocean is well known for an impressive adaptive radiation of fishes, the notothenioids. However, when compared to other marine areas, the frigid waters of the Southern Ocean also contain a seemingly large proportion of cryptic species. The documented instances of speciation in the absence of morphological change are largely observed in invertebrate taxa, in particular around peri- and sub-Antarctic islands such as South Georgia, which has been dubbed a cryptic species hotspot. This prevalence of cryptic species raises the question of how generalizable these patterns are for Antarctic vertebrates. Here we examine aspects of genotype and phenotype in an Antarctic notothenioid fish species, Lepidonotothen nudifrons, which is distributed in near shore habitats of the Antarctic Peninsula, South Orkney Islands, South Georgia, and the South Sandwich Islands. The results of our analyses show that L. nudifrons comprises two species. We highlight that cryptic species are phenomena not restricted to invertebrate lineages, raising the possibility that the species diversity of notothenioids and other Southern Ocean fishes is under-described. In addition, our findings raise several questions about the evolutionary origin and maintenance of morphological stasis in one of the most extreme habitats on earth.

Cradles and museums of Antarctic teleost biodiversity

Isolated in one of the most extreme marine environments on Earth, teleost fish diversity in Antarctica’s Southern Ocean is dominated by one lineage: the notothenioids. Throughout the past century, the long-term persistence of this unique marine fauna has become increasingly threatened by regional atmospheric and, to a lesser extent oceanic, warming. Developing an understanding of how historical temperature shifts have shaped source–sink dynamics for Antarctica’s teleost lineages provides critical insight for predicting future demographic responses to climate change. We use a combination of phylogenetic and biogeographic modelling to show that high-latitude Antarctic nearshore habitats have been an evolutionary sink for notothenioid species diversity. Contrary to expectations from island biogeographic theory, lower latitude regions of the Southern Ocean that include the northern Antarctic Peninsula and peripheral island archipelagos act as source areas to continental diversity. These peripheral areas facilitate both the generation of new species and repeated colonization of nearshore Antarctic continental regions. Our results provide historical context to contemporary trends of global climate change that threaten to invert these evolutionary dynamics.Phylogenetic and biogeographic modelling show that high-latitude Antarctic nearshore habitats have been an evolutionary sink for species diversity of notothenioids, which dominate teleost fish diversity in the Southern Ocean.

A revision of Canarium L. (Burseraceae) in Madagascar

ABSTRACT Trees in the genus Canarium L. are known to comprise an important component of the structure of Madagascars moist forests, but recent work on Canarium in Madagascar reveals that the genus also comprises an important part of their diversity as well. To date, published Floras for Madagascar have recognized only three taxa of Canarium, but here we recognize 33 species, 27 of them new to science; this increases the number of accepted species in the genus by 33% worldwide and establishes Madagascar as a primary center of diversity for the genus. Despite its name, C. madagascariense Engl. proves to be one of the rarest and geographically most restricted species. Most Malagasy Canarium species are narrow endemic, and this is consistent with recent floristic and taxonomic research in other taxonomic groups on the island. The species of Canarium in Madagascar can be distinguished using mostly vegetative characters, and this will prove useful to foresters, ecologists, and conservationists. Most moist forests in Madagascar include multiple species of Canarium, and one important avenue of future research will be to further investigate the interdependence of the species of Canarium and the frugivorous lemurs that eat the pericarp of their fruits and possibly disperse their seeds.

Isolation of 13 novel highly polymorphic microsatellite loci for the Amazonian Palm Mauritia flexuosa L.f. (Arecaceae)

Mauritia flexuosa L.f. (Arecaceae) is a New World tropical palm that generally grows in isolated swamps along meandering rivers and is in danger of fragmentation through unsustainable harvest practices. To explore gene flow among populations of M. flexuosa in Amazonia, we developed 13 novel, polymorphic microsatellite loci for M. flexuosa. Further studies will employ these loci to investigate the impacts of artisanal gold mining and wild-harvest on gene flow among populations of M. flexuosa.

The Paucity of Frugivores in Madagascar May Not Be Due to Unpredictable Temperatures or Fruit Resources

The evolution of ecological idiosyncrasies in Madagascar has often been attributed to selective pressures stemming from extreme unpredictability in climate and resource availability compared to other tropical areas. With the exception of rainfall, few studies have investigated these assumptions. To assess the hypothesis that Madagascar’s paucity of frugivores is due to unreliability in fruiting resources, we use statistical modeling to analyze phenology datasets and their environmental correlates from two tropical wet forests, the Réserve Naturelle Intégrale Betampona in Madagascar, and Kibale National Park in Uganda. At each site we found that temperature is a good environmental predictor of fruit availability. We found no evidence of a significant difference in the predictability of fruit availability between the two sites, although the shorter duration of phenological monitoring at Betampona (two years, versus 15 years at Kibale) limits our ability to infer long-term patterns. Comparisons of long-term temperature data from each site (15 years from Kibale and 14 from Betampona) indicate that temperature is more predictable at Betampona than at Kibale. However, there does appear to be a difference between the two sites in the total fruit availability at any given time, with fruit being generally less abundant at Betampona. Our results appear contrary to the prevailing hypothesis of a selective force imposed by unpredictable resource availability or temperature, and we suggest other possible explanations for Madagascar’s unique biota.

Molecular data support the existence of two species of the Antarctic fish genus Cryodraco (Channichthyidae)

Antarctic notothenioids represent one of the few strongly supported examples of adaptive radiation in marine fishes. The extent of population connectivity and structure is unknown for many species, thereby limiting our understanding of the factors that underlie speciation dynamics in this radiation. Here, we assess the population structure of the widespread species Cryodraco antarcticus and its sister species Cryodraco atkinsoni, whose taxonomic status is currently debated. Combining both population genetic and phylogenetic approaches to species delimitation, we provide evidence that C. atkinsoni is a distinct species. Our analyses show that C. atkinsoni and C. antarcticus are recently diverged sister lineages, and the two species differ with regard to patterns of population structure. A systematic and accurate account of species diversity is a critical prerequisite for investigations into the complex processes that underlie the history of speciation in the notothenioid adaptive radiation.

Disentangling the Influence of Urbanization and Invasion on Endemic Geckos in Tropical Biodiversity Hot Spots: A Case Study of Phyllodactylus martini (Squamata: Phyllodactylidae) along an Urban Gradient in Curaçao

Abstract Predicting the response of endemic species to urbanization has emerged as a fundamental challenge in 21st century conservation biology. The factors that underlie population declines of reptiles are particularly nebulous, as these are often the least understood class of vertebrates in a given community. In this study, we assess correlations between feeding ecology and phenotypic traits of the Lesser Antillean endemic Dutch leaf-toed gecko, Phyllodactylus martini, along an urban gradient in the Caribbean island of Curaçao. There has been a marked decline of this species in developed habitats associated with the invasive tropical house gecko Hemidactylus mabouia. We find a correlation between aspects of locomotor morphology and prey in undeveloped habitats that is absent in developed habitats. Analyses of stomach contents further suggest that Phyllodactylus martini alters primary prey items in developed areas. However, changes in prey promote the overlap in foraging niches between Phyllodactylus martini and Hemidactylus mabouia, suggesting that direct resource competition is contributing to the decline of Phyllodactylus martini. In addition to competitive exclusion, we suggest that the urban extirpation of Phyllodactylus martini could also be attributed to a top-down control on population growth by Hemidactylus mabouia. Colonizations of walls put Phyllodactylus martini in direct contact with Hemidactylus mabouia increasing the chances for predation events, as evidenced by our observation of a predation event on a Phyllodactylus martini juvenile by an adult Hemidactylus mabuoia. In total, our results add to a growing body of literature demonstrating the threat that invasive synanthropic reptiles pose to endemics that might otherwise be able to cope with increased urbanization pressures.

Reconciling species diversity in a tropical plant clade (Canarium, Burseraceae)

The challenges associated with sampling rare species or populations can limit our ability to make accurate and informed estimates of biodiversity for clades or ecosystems. This may be particularly true for tropical trees, which tend to be poorly sampled, and are thought to harbor extensive cryptic diversity. Here, we integrate genomics, morphology, and geography to estimate the number of species in a clade of dioecious tropical trees (Canarium L.; Burseraceae) endemic to Madagascar, for which previous taxonomic treatments have recognized between one and 33 species. By sampling genomic data from even a limited number of individuals per taxon, we were able to clearly reject both previous hypotheses, and support instead an intermediate number of taxa. We recognize at least six distinct clades based on genetic structure and species delimitation analyses that correspond clearly with geographic and discrete morphological differences. Two widespread clades co-occur broadly throughout eastern wet forests, one clade is endemic to western dry forests, and several slightly admixed clades are more narrowly distributed in mountainous regions in the north. Multiple previously described taxa were recovered as paraphyletic in our analyses, some of which were associated with admixed individuals, suggesting that hybridization contributes to taxonomic difficulties in Canarium. An improved understanding of Canarium species diversity has important implications for conservation efforts and understanding the origins of diversity in Madagascar. Our study shows that even limited genomic sampling, when combined with geography and morphology, can greatly improve estimates of species diversity for difficult tropical clades.