Taxonomy, distribution, and conservation status of a rare arboreal lizard, Bronchocela celebensis Gray, 1845 (Reptilia: Agamidae) endemic to Sulawesi, Indonesia.

Bronchocela celebensis Gray, 1845 is one of the rarest species of the genus, known only from less than 20 museum specimens collected from northern Sulawesi. It is often confused with its similar congener, B. cristatella, which occurs widely throughout the Indonesian Archipelago and Peninsular Malaysia, except on the Sulawesi mainland. Here, we examine the morphology of B. celebensis based on 46 museum specimens including freshly collected individuals, and redescribe the species based on the holotype (by monotypy). We studied the characters of B. celebensis with morphometric comparison to its allopatric congener B. cristatella from the adjacent islands of southern Sulawesi in Indonesia. Based on the current distribution pattern and the apparent threats, we update the conservation status of B. celebensis using the IUCN Red List Criteria and propose that it be considered as a Vulnerable (VU) species endemic to Sulawesi.

Species Delimitation, Phylogenomics, and Biogeography of Sulawesi Flying Lizards: A Diversification History Complicated by Ancient Hybridization, Cryptic Species, and Arrested Speciation.

The biota of Sulawesi is noted for its high degree of endemism and for its substantial levels of in situ biological diversification. While the island's long period of isolation and dynamic tectonic history have been implicated as drivers of the regional diversification, this has rarely been tested in the context of an explicit geological framework. Here, we provide a tectonically informed biogeographical framework that we use to explore the diversification history of Sulawesi flying lizards (the Draco lineatus Group), a radiation that is endemic to Sulawesi and its surrounding islands. We employ a framework for inferring cryptic speciation that involves phylogeographic and genetic clustering analyses as a means of identifying potential species followed by population demographic assessment of divergence-timing and rates of bi-directional migration as means of confirming lineage independence (and thus species status). Using this approach, phylogenetic and population genetic analyses of mitochondrial sequence data obtained for 613 samples, a 50-SNP data set for 370 samples, and a 1249-locus exon-capture data set for 106 samples indicate that the current taxonomy substantially understates the true number of Sulawesi Draco species, that both cryptic and arrested speciations have taken place, and that ancient hybridization confounds phylogenetic analyses that do not explicitly account for reticulation. The Draco lineatus Group appears to comprise 15 species-9 on Sulawesi proper and 6 on peripheral islands. The common ancestor of this group colonized Sulawesi ~11 Ma when proto-Sulawesi was likely composed of two ancestral islands, and began to radiate ~6 Ma as new islands formed and were colonized via overwater dispersal. The enlargement and amalgamation of many of these proto-islands into modern Sulawesi, especially during the past 3 Ma, set in motion dynamic species interactions as once-isolated lineages came into secondary contact, some of which resulted in lineage merger, and others surviving to the present. [Genomics; Indonesia; introgression; mitochondria; phylogenetics; phylogeography; population genetics; reptiles.].

Taxonomy and distribution of a common arboreal lizard, Bronchocela jubata Dumril amp; Bibron, 1837 (Reptilia: Agamidae), with designation of its lectotype from Java, Indonesia.

Bronchocela jubata Dumril and Bibron, 1837 is one of the commonest species of the genus, known mostly from Java Island and southern parts of Sumatra. It is rare in Bali and Borneo. The juveniles are often confused with its morphologically similar congener, B. cristatella, which occurs widely throughout the Indonesian Archipelago and Peninsular Malaysia. We examined the morphology of B. jubata based on museum specimens including its two available syntypes, and redescribed the species based on the lectotype designated herein. We highlight the characters of B. jubata with a morphometric comparison to its sympatric congener B. cristatella from Java Island, Indonesia. Based on the current distribution pattern and the apparent threats, we update the conservation status of B. jubata using IUCN Red List Criteria, and propose that it be considered as a species of Least Concern (LC), endemic to the Greater Sundaic Islands.

A set of principles and practical suggestions for equitable fieldwork in biology.

Field biology is an area of research that involves working directly with living organisms in situ through a practice known as "fieldwork." Conducting fieldwork often requires complex logistical planning within multiregional or multinational teams, interacting with local communities at field sites, and collaborative research led by one or a few of the core team members. However, existing power imbalances stemming from geopolitical history, discrimination, and professional position, among other factors, perpetuate inequities when conducting these research endeavors. After reflecting on our own research programs, we propose four general principles to guide equitable, inclusive, ethical, and safe practices in field biology: be collaborative, be respectful, be legal, and be safe. Although many biologists already structure their field programs around these principles or similar values, executing equitable research practices can prove challenging and requires careful consideration, especially by those in positions with relatively greater privilege. Based on experiences and input from a diverse group of global collaborators, we provide suggestions for action-oriented approaches to make field biology more equitable, with particular attention to how those with greater privilege can contribute. While we acknowledge that not all suggestions will be applicable to every institution or program, we hope that they will generate discussions and provide a baseline for training in proactive, equitable fieldwork practices.

Taxonomy, distribution, and conservation status of a rare arboreal lizard, Bronchocela hayeki (Mller, 1928) (Reptilia: Agamidae) from northern Sumatra, Indonesia.

Bronchocela hayeki (Mller, 1928) is one of the rarest species of the genus, known only from a handful of museum specimens from five locations in North Sumatra, and often confused with its similar congener, B. cristatella, which occurs widely throughout the Indonesian Archipelago and Peninsular Malaysia. Here, we examined the morphology of B. hayeki based on museum specimens, and redescribe the species based on a freshly collected series near the type locality, as the condition of its neotype is not in a good state. We studied the characters of B. hayeki with a morphometric comparison to its sympatric congener B. cristatella and allopatric congener, B. jubata from Sumatra Island, Indonesia. Based on the current distribution pattern and the apparent threats, we update the conservation status of B. hayeki using IUCN Red List Criteria and propose that it be considered as an Endangered (EN) species endemic of northern Sumatra including Aceh. We also provide a key to the recognized Bronchocela species, based on examined material and literature.

Mitonuclear interactions and introgression genomics of macaque monkeys (Macaca) highlight the influence of behaviour on genome evolution.

In most macaques, females are philopatric and males migrate from their natal ranges, which results in pronounced divergence of mitochondrial genomes within and among species. We therefore predicted that some nuclear genes would have to acquire compensatory mutations to preserve compatibility with diverged interaction partners from the mitochondria. We additionally expected that these sex-differences would have distinctive effects on gene flow in the X and autosomes. Using new genomic data from 29 individuals from eight species of Southeast Asian macaque, we identified evidence of natural selection associated with mitonuclear interactions, including extreme outliers of interspecies differentiation and metrics of positive selection, low intraspecies polymorphism and atypically long runs of homozygosity associated with nuclear-encoded genes that interact with mitochondria-encoded genes. In one individual with introgressed mitochondria, we detected a small but significant enrichment of autosomal introgression blocks from the source species of her mitochondria that contained genes which interact with mitochondria-encoded loci. Our analyses also demonstrate that sex-specific demography sculpts genetic exchange across multiple species boundaries. These findings show that behaviour can have profound but indirect effects on genome evolution by influencing how interacting components of different genomic compartments (mitochondria, the autosomes and the sex chromosomes) move through time and space.

Genetic connectivity of the scalloped hammerhead shark Sphyrna lewini across Indonesia and the Western Indian Ocean.

Scalloped Hammerhead shark (Sphyrna lewini) is an endangered species which its populations have been declining globally including in Indonesia, the world's top shark fishing country. However, there is a lack of information on the recent population structure of this species to promote proper management and its conservation status. This study aimed to investigate the genetic diversity, population structure, and connectivity of the S. lewini population, in three major shark landing sites: Aceh (n = 41), Balikpapan (n = 30), and Lombok (n = 29). Meanwhile, additional sequences were retrieved from West Papua (n = 14) and the Western Indian Ocean (n = 65) populations. From the analyses of the mitochondrial CO1 gene, a total of 179 sequences of S. lewini, with an average size of 594 bp, and 40 polymorphic loci in four and eight haplotypes for the Indonesian population and the Western Indian Ocean population were identified. The overall values of genetic diversity were high (h = 0.717; π = 0.013), with the highest values recorded in Aceh (h = 0.668; π = 0.002) and the lowest in Papua (h = 0.143; π = 0.000). On the contrary, the overall value was fairly low in the Western Indian Ocean (h = 0.232; π = 0.001). Furthermore, AMOVA and FST showed three significant subdivisions in Indonesia (FST = 0.442; P < 0.001), with separated populations for Aceh and West Papua, and mixed between Balikpapan and Lombok (FST = 0.044; P = 0.091). In contrast, genetic homogeneity was observed within the population of the Western Indian Ocean (FST = -0.013; P = 0.612). The establishment of a haplotype network provided evidence of a significantly different population and a limited genetic distribution between the Indonesian and the Western Indian Ocean populations (FST = 0.740; P < 0.001). This study showed the presence of a complex population of S. lewini with limited connectivity only in Indonesia separated from the Western Indian Ocean and requiring specific management measures based on the population structure at the regional level.

Abrupt Decline in a Protected Population of Siamangs (Symphalangus syndactylus) in Southern Sumatra.

Between 2011 and 2016, approximately 50% of siamangs in the Way Canguk Research Area disappeared, including members of 7 of 12 habituated groups. Demographic data from 1998 to 2015 confirm that the population decline in the habituated groups reflects a larger trend in the local population. There was no evidence of hunting of primates in the area, and ecological data do not suggest substantial changes in food availability or predation pressure during this period. From 2011 to 2014, we monitored the habituated groups only intermittently, and most deaths or disappearances were not observed. However, in 2014-2016, we monitored some groups more intensively, and observed 2 individuals with symptoms including whitened skin on the face, hands, and abdomen, hair loss, swelling of the face, frequent scratching, and lethargy. One affected individual disappeared days after this observation, while the other survived. The spatiotemporal pattern of disappearances in the habituated groups was consistent with that expected if the deaths resulted from disease transmission among neighbouring groups. Thus, the available evidence, while preliminary, suggests that a local disease epizootic may have been a factor driving the population decline. We recommend that researchers establish monitoring protocols to better understand primate disease epidemiology and to guide conservation management.

Rhinos in the Parks: An Island-Wide Survey of the Last Wild Population of the Sumatran Rhinoceros.

In the 200 years since the Sumatran rhinoceros was first scientifically described (Fisher 1814), the range of the species has contracted from a broad region in Southeast Asia to three areas on the island of Sumatra and one in Kalimantan, Indonesia. Assessing population and spatial distribution of this very rare species is challenging because of their elusiveness and very low population number. Using an occupancy model with spatial dependency, we assessed the fraction of the total landscape occupied by Sumatran rhinos over a 30,345-km2 survey area and the effects of covariates in the areas where they are known to occur. In the Leuser Landscape (surveyed in 2007), the model averaging result of conditional occupancy estimate was ψ(SE[ψ]) = 0.151(0.109) or 2,371.47 km2, and the model averaging result of replicated level detection probability p(SE[p]) = 0.252(0.267); in Way Kambas National Park--2008: ψ(SE[ψ]) = 0.468(0.165) or 634.18 km2, and p(SE[p]) = 0.138(0.571); and in Bukit Barisan Selatan National Park--2010: ψ(SE[ψ]) = 0.322(0.049) or 819.67 km2, and p(SE[p]) = 0.365(0.42). In the Leuser Landscape, rhino occurrence was positively associated with primary dry land forest and rivers, and negatively associated with the presence of a road. In Way Kambas, occurrence was negatively associated with the presence of a road. In Bukit Barisan Selatan, occurrence was negatively associated with presence of primary dryland forest and rivers. Using the probabilities of site occupancy, we developed spatially explicit maps that can be used to outline intensive protection zones for in-situ conservation efforts, and provide a detailed assessment of conserving Sumatran rhinos in the wild. We summarize our core recommendation in four points: consolidate small population, strong protection, determine the percentage of breeding females, and recognize the cost of doing nothing. To reduce the probability of poaching, here we present only the randomized location of site level occupancy in our result while retaining the overall estimation of occupancy for a given area. ψ

Quantifying killing of orangutans and human-orangutan conflict in Kalimantan, Indonesia.

Human-orangutan conflict and hunting are thought to pose a serious threat to orangutan existence in Kalimantan, the Indonesian part of Borneo. No data existed prior to the present study to substantiate these threats. We investigated the rates, spatial distribution and causes of conflict and hunting through an interview-based survey in the orangutan's range in Kalimantan, Indonesia. Between April 2008 and September 2009, we interviewed 6983 respondents in 687 villages to obtain socio-economic information, assess knowledge of local wildlife in general and orangutan encounters specifically, and to query respondents about their knowledge on orangutan conflicts and killing, and relevant laws. This survey revealed estimated killing rates of between 750 and 1800 animals killed in the last year, and between 1950 and 3100 animals killed per year on average within the lifetime of the survey respondents. These killing rates are higher than previously thought and are high enough to pose a serious threat to the continued existence of orangutans in Kalimantan. Importantly, the study contributes to our understanding of the spatial variation in threats, and the underlying causes of those threats, which can be used to facilitate the development of targeted conservation management.

Adaptive radiation and ecological opportunity in Sulawesi and Philippine fanged frog (Limnonectes) communities.

Because island communities are derived from mainland communities, they are often less diverse by comparison. However, reduced complexity of island communities can also present ecological opportunities. For example, amphibian diversity on Sulawesi Island is lower than it is in the Philippines, but Sulawesi supports a surprising diversity of Sulawesi fanged frogs (Limnonectes). Here we examine molecular, morphological, and geographical variation of fanged frogs from these two regions. Using genealogical concordance, morphology, and a Bayesian approach to species delimitation, we identified 13 species on Sulawesi, only four of which have been previously described. After evolutionary history is accounted for, a model with multiple body size optima in sympatric species is favored over a "random-walk" model of body size evolution. Additionally, morphological variation is higher among sympatric than nonsympatric species on Sulawesi but not in the Philippines. These findings suggest that adaptive radiation of fanged frogs on Sulawesi was driven by natural selection to infiltrate ecological niches occupied by other frog lineages in the Philippines. This supports a role of ecological opportunity in community assembly: diversification in mature communities, such as the Philippines, is limited by a dearth of unoccupied ecological niches. On Sulawesi, evolutionary novelties originated in a predictable and replicated fashion in response to opportunities presented by a depauperate ancestral community.

Phylogeography and historical demography of Polypedates leucomystax in the islands of Indonesia and the Philippines: evidence for recent human-mediated range expansion?

Southeast Asia's widespread species offer unique opportunities to explore the effects of geographical barriers to dispersal on patterns of vertebrate lineage diversification. We analyzed mitochondrial gene sequences (16S rDNA) from a geographically widespread sample of 266 Southeast Asian tree frogs, including 244 individuals of Polypedates leucomystax and its close relatives. Our expectation was that lineages on island archipelagos would exhibit more substantial geographic structure, corresponding to the geological history of terrestrial connectivity in this region, compared to the Asian mainland. Contrary to predictions, we found evidence of numerous highly divergent lineages from a limited area on the Asian mainland, but fewer lineages with shallower divergences throughout oceanic islands of the Philippines and Indonesia. Surprisingly and in numerous instances, lineages in the archipelagos span distinct biogeographical provinces. Phylogeographic analyses identified four major haplotype clades; summary statistics, mismatch distributions, and Bayesian coalescent inference of demography provide support for recent range expansion, population growth, and/or admixture in the Philippine and some Sulawesi populations. We speculate that the current range of P. leucomystax in Southeast Asia is much larger now than in the recent past. Conversion of forested areas to monoculture agriculture and transportation of agricultural products between islands may have facilitated unprecedented population and range expansion in P. leucomystax throughout thousands of islands in the Philippine and Indonesian archipelagos.

A coalescent framework for comparing alternative models of population structure with genetic data: evolution of Celebes toads.

Isolation of populations eventually leads to divergence by genetic drift, but if connectivity varies over time, its impact on diversification may be difficult to discern. Even when the habitat patches of multiple species overlap, differences in their demographic parameters, molecular evolution and stochastic events contribute to differences in the magnitude and distribution of their genetic variation. The Indonesian island of Sulawesi, for example, harbours a suite of endemic species whose intraspecific differentiation or interspecific divergence may have been catalysed by habitat fragmentation. To further test this hypothesis, we have performed phylogenetic and coalescent-based analyses on molecular variation in mitochondrial and nuclear DNA of the Celebes toad (Bufo celebensis). Results support a role for habitat fragmentation that led to a population structure in these toads that closely matches distributions of Sulawesi macaque monkeys. Habitat fragmentation, therefore, may also have affected other groups on this island.

Phylogenetics of fanged frogs: testing biogeographical hypotheses at the interface of the asian and Australian faunal zones.

The interface of the Asian and Australian faunal zones is defined by a network of deep ocean trenches that separate intervening islands of the Philippines and Wallacea (Sulawesi, the Lesser Sundas, and the Moluccas). Studies of this region by Wallace marked the genesis of the field of biogeography, yet few workers have used molecular methods to investigate the biogeography of taxa whose distribution spans this interface. Some taxa, such as the fanged frogs of the ranid genus Limnonectes, have distributions on either side of the zoogeographical lines of Wallace and Huxley, offering an opportunity to ask how frequently these purported barriers were crossed and by what paths. To examine diversification of Limnonectes in Southeast Asia, the Philippines, and Wallacea, we estimated a phylogeny from mitochondrial DNA sequences obtained from a robust geographic sample. Our analyses suggest that these frogs dispersed from Borneo to the Philippines at least twice, from Borneo to Sulawesi once or twice, from Sulawesi to the Philippines once, and from the Philippines to Sulawesi once. Dispersal to the Moluccas occurred from Sulawesi and to the Lesser Sundas from Java/Bali. Species distributions are generally concordant with Pleistocene aggregate island complexes of the Philippines and with areas of endemism on Sulawesi. We conclude that the recognition of zoogeographic lines, though insightful, may oversimplify the biogeography of widespread taxa in this region.

Diversification of Sulawesi macaque monkeys: decoupled evolution of mitochondrial and autosomal DNA.

In macaque monkeys, females are philopatric and males are obligate dispersers. This social system is expected to differently affect evolution of genetic elements depending on their mode of inheritance. Because of this, the geographic structure of molecular variation may differ considerably in mitochondrial DNA (mtDNA) and in autosomal DNA (aDNA) in the same individuals, even though these genomes are partially co-inherited. On the Indonesian island of Sulawesi, macaque monkeys underwent an explosive diversification as a result of range fragmentation. Today, barriers to dispersal have receded and fertile hybrid individuals can be found at contact zones between parapatric species. In this study, we examine the impact of range fragmentation on Sulawesi macaque mtDNA and aDNA by comparing evolution, phylogeography, and population subdivision of each genome. Our results suggest that mtDNA is paraphyletic in some species, and that mtDNA phylogeography is largely consistent with a pattern of isolation by distance. Autosomal DNA, however, is suggestive of fragmentation, in that interspecific differentiation across most contact zones is significant but intraspecific differentiation between contact zones is not. Furthermore, in mtDNA, most molecular variation is partitioned between populations within species but in aDNA most variation is partitioned within populations. That mtDNA has a different geographic structure than aDNA (and morphology) in these primates is a probable consequence of (1) a high level of ancestral polymorphism in mtDNA, (2) differences between patterns of ancestral dispersal of matrilines and contemporary dispersal of males, and (3) the fact that female philopatry impedes gene flow of macaque mtDNA.

Monkeys and toads define areas of endemism on Sulawesi.

Ecological or geological phenomena can impose limits on geographic diversification that cause biogeographical patterns of distantly related but sympatrically occurring taxa to be similar. Concordant patterns of diversity facilitate conservation management because strategic designation of protected areas can capture complementary rather than redundant components of variation. Here we demonstrate that on the biodiverse Indonesian island of Sulawesi, seemingly idiosyncratic distributions of diversity in endemic monkeys (Macaca species) and toads (Bufo celebensis) are actually virtually identical on a fine geographic scale. It appears that range fragmentation has generated seven multi-taxon areas of genetic endemism, each of which should be targeted for conservation. Joint consideration of molecular phylogeography, morphology, and demography helps resolve apparent contradictions in paraphyletic macaque mitochondrial DNA and in undifferentiated toad morphology, and facilitates an understanding of biogeography and conservation genetics of Sulawesi fauna.