Many scientists argue that our planet is undergoing a mass extinction event that is largely due to human influences. In this context, rediscoveries of species presumed to be extinct are encouraging and of great potential interest. During a 2003 expedition to New Caledonia, Bocourt’s terrific skink, Phoboscincus bocourti, was unexpectedly rediscovered on a small islet by one of us. This skink species had been described from a single specimen collected around 1872 in New Caledonia. Since that time, however, no data on the species’ biology, trophic interactions, or role in the ecosystem have been collected, making it difficult to follow the established conservation plan. In this study, we used a multidisciplinary approach involving natural history, anatomy, morphology, genetics, and stable isotopes to elucidate the ecology of Bocourt’s terrific skink. Over the course of three different expeditions to the islet (total of 55 days across 2005 and 2012), we captured 4 individuals and observed another 4 individuals. The species’ dentition and trophic ecology suggest that it is a top predator in its ecosystem and a major consumer of small terrestrial reptiles. Its high degree of genetic relatedness to another New Caledonian skink, which has a broad distribution, suggests that P. bocourti underwent genetic isolation at a geographical remote location, where dispersal or colonization was highly improbable. Moreover, the lack of genetic variation among the four individuals we captured may imply that a unique lineage, characterized by few inter-island exchanges, exists on the islet. Bocourt’s terrific skink may be the largest terrestrial squamate predator alive in New Caledonia today. As a result, it is likely vulnerable to habitat modifications and especially the invasive rodents found on this islet. Further information is necessary to assess the conservation plans and practices in place as no concrete changes have been made since the species’ rediscovery almost 10 years ago.

Introduction

“There is no doubt that the terrific skink ruled over the smaller reptiles of New Caledonia as effectively as Tyrannosaurus rex did over the lesser dinosaurs of its era, or the lion does on Africa’s Serengeti today.” ([1]; speculation made ten years before Phoboscincus bocourti’s rediscovery)

While the human population continues to increase exponentially, 30% of amphibians, 12% of birds, and 21% of mammals are either threatened or already extinct [2]. Many scientists argue that our planet is undergoing a mass higher extinction event, mostly due to anthropogenic factors such as the overexploitation of natural resources, habitat fragmentation, urbanization, the wildlife trade, the introduction of invasive species, pollution, and/or global warning [3-6]. Reptiles seem to be especially vulnerable. A recent study conducted by over 200 world-renowned experts assessed the extinction risk of 1,500 randomly selected reptiles from across the globe; it revealed that almost one in five reptiles is struggling to survive [7]. It is thus not surprising that at least 19% of the world’s reptiles are threatened and in danger of extinction.

Rediscoveries of species that are presumed to be extinct are encouraging and generate both great interest and concern for conservationists and biogeographers [8-11]. Over the past 122 years, at least 351 species have been rediscovered, a number that continues to increase over time. In most cases, the rediscovery represents the first opportunity to collect data on the species since it was first described [12]. For example, many species have been described from just one or a few museum specimens that were collected decades or even centuries earlier. For instance, the snake species Eirenis africana, identified from a single museum specimen described in 1914, was rediscovered in Djibouti in 1999 [13], and the crested gecko of New Caledonia, Correlophus ciliatus, considered to be extinct for more than a century, was rediscovered in 1994 [14]. Once their habitats are better characterized, some species are more commonly encountered and found to be no more threatened than other species in the same genus.

The rediscovery of an extinct species may present a variety of regulatory challenges and raise the question of the direction future conservation efforts should take [15]. Although species rediscovery can draw media attention, promote conservation efforts, and encourage research aimed at understanding population declines [9,16], it may also spur unsupported optimism for the survival of the species [12]. Many rediscovered species remain seriously threatened with extinction and could go extinct if concerted efforts are not directed to their conservation [12]. Thus, the rediscovery of a species is the first of many steps, especially if the species’ ecology is poorly characterized or unknown.

The lizard fauna of New Caledonia (~120 species) is among the most diverse of the South Pacific; it is probably the richest in the world if land surface area is taken into account. Moreover, it is characterized by an exceptionally high level of endemism at both the genus (~75%) and species (~95%) levels [17,18]. The high speciation rate of New Caledonian lizard fauna is most likely a consequence of restricted species distributions: fine-scale microendemism is associated with local geological features that generate unique habitats [18].

Before the arrival of humans in New Caledonia, the archipelago was dominated by the gigantic, herbivorous Meiolania horned tortoise [1,19] and two top predators: a goanna, similar to Australia’s varanids [1,20], and an ancient member of an extinct pygmy crocodile group discovered in 1980 (Mekosuchus inexpectatus; see [20,21]) and that probably originated in Australia. Unfortunately, only two moderately-sized groups of lizards survived in New Caledonia: the Gekkota, which are represented by the regionally endemic Diplodactylidae and the more widely distributed Gekkonidae, and the Scincidae or the skinks (however, it should be noted that some authors suggest Scincidae is not a single family, but rather several). Among the skinks, the gigantic skink (Phoboscincus bocourti Brocchi, 1876), previously considered to be extinct, is among the most emblematic [17]. Prior to 2003, the lizard species had been described from a single specimen (holotype by monotypy) collected around 1872 by the French botanist Benjamin Balansa at an unknown location in New Caledonia. The species was rediscovered by Ivan Ineich more than 130 years later, in December 2003, during an expedition devoted to the study of sea snakes on a small islet off the Isle of Pines. The specimen was captured by hand and later released after tissue samples and pictures were taken [22]. P. bocourti is remarkable because of its large size and pronounced dentition; its elongated, curved, and sharp teeth suggest it is a predator, an unusual trophic position since larger skink species are generally herbivorous and/or frugivorous. Its diet has been hypothesized to include larger invertebrates (crabs, mollusks, worms, insects, and spiders), other lizards, young birds, and different kinds of eggs [17,23,24]. Those teeth and its historical characters give that lizard its common name “Bocourt’s terrific skink” in relation with its generic name (Phoboscincus): “The name Phoboscincus combines the Greek noun for “fear” (phobos) with the Latin noun for “skink” (scincus) to give a name that should emphasize the awe-inspiring aspect imparted to these skinks by their large size and sharply pointed teeth” [25]. Indeed, its total length is about 50 cm, making it the second largest lizard species in New Caledonia (the first largest being the extinct goanna species mentioned above) and the largest predator lizard in the archipelago.

In 2005, researchers returned to the islet where P. bocourti was rediscovered to study the species and obtain the first information on its natural history. At the request of the environmental authorities of the Southern Province of New Caledonia, a conservation plan was established that included several recommendations [24]. Since that time, no additional data on the biology, trophic interactions, and role of the species in the ecosystem have been obtained that would allow the established conservation plan to be followed. As a potential top predator, P. bocourti could have a significant impact on the island’s lower trophic levels (e.g. [1,24,26]), but more importantly, from a conservation point of view, it may also be very vulnerable to changes or disturbances in the ecosystem, thus making it a prime candidate for extinction. Such disturbances may include habitat fragmentation, tourism-related development, invasive species (rats and ants), environmental pollution, diseases, climate change, wildfire and prey availability [27]. Species vulnerability seems to be higher in general in island ecosystems; human-induced extinction rates are much higher on islands than on continents. Invasive species in particular are responsible for a large number of the documented extinctions of island vertebrates [28,29].

Basic biological information on P. bocourti is scarce; specifically, its population size, trophic interactions, and biological adaptations remain uncharacterized. Such data are essential to the identification of a species’ future risk of extinction and the establishment of clear conservation guidelines. Yet obtaining these data can be extremely challenging, particularly when population size is small or individuals are cryptic, making it difficult to capture or monitor the species [30,31]. Our study aims to elucidate the trophic ecology of P. bocourti using a multidisciplinary approach involving natural history, anatomy, morphology, genetics, and stable isotopes. In addition to the 2003 and 2005 expeditions, two additional trips were made to the islet in 2012 to collect more biological data on this elusive species. The goal was to observe the lizard in its natural habitat (feeding, reproduction, distribution, etc.), characterize potential threats to its well-being, and sample its tissues. We were able to amplify a small fragment of the mitochondrial 12S rDNA gene from the sole museum specimen of P. bocourti, the adult holotype collected around 1872 and deposited in the collection of Paris Natural History Museum (MNHN 3029). We compared the holotype’s sequence with those obtained from four individuals sampled during the 2005 and 2012 expeditions. We were also able to amplify larger fragments of the 12S rDNA and 16S rDNA genes from the four more recently sampled individuals, thus allowing us to examine genetic variability among them. We used x-ray microtomography to visualize the holotype’s skull and dentition. We employed stable isotopes to determine P. bocourti’s trophic position in the islet’s food web and thus test the hypothesis that it preys upon sympatric terrestrial vertebrates such as rodents, birds, and other reptiles. Because traditional trophic analysis techniques, e.g. stomach content sampling and stomach flushing, should not be used on endangered species, the development of indirect biochemical approaches such as analyzing the stable isotope ratios of animal tissues has been a boon in conservation studies. Finally, we discuss the importance of our different results in the context of the lizard’s rediscovery and the urgent need to establish clear conservation perspectives and priorities.