Attempting to Manage Complex Predator-Prey Interactions Fails to Avert Imminent Extinction of a Threatened New Zealand Skink Population

Abstract: The current primary threats to biodiversity on a global scale are species invasions and habitat modification. Management of vulnerable populations often involves a lengthy sequence of 1) research to identify threats and recommend management strategies, 2) active management, and 3) results monitoring to assess effectiveness of management. The last mainland population of the large, endemic New Zealand skink (Whitaker's skink [Cyclodina whitakeri]) provides an opportunity to test this process in a system where the synergistic effects between invasive species (introduced rodents and grasses) have predicted outcomes. A low abundance of Whitaker's skink at the Pukerua Bay Scientific Reserve in the 1980s prompted management recommendations to remove grazing stock and revegetate the site to simultaneously restore habitat and provide protection against introduced mammalian predators. Since Whitaker's skink have low detectability, it was recommended that sympatric copper skink (C. aenea) be used an indicator species of management effectiveness. Grazing stock were removed in 1987, but efforts to revegetate the site were ineffective. Long-term monitoring (1984-2006) of the Whitaker's skink population and 4 other sympatric lizard species within a 336-m² area at the site resulted in 1,693 lizard captures over 7,597 trap days. Whitaker's skink represented 2.8% of all captures in 1984-1988, but declined relative to other species to represent only 0.2% of captures in 2000-2006 (representing 2 individuals). Congeneric copper skink showed a similar decline with capture rates also approaching zero by 2006. Removing grazing stock did not result in an increased abundance of Whitaker's skink or copper skink through improved habitat quality, as was intended by the management recommendation. Instead, reduced grazing has allowed introduced seeding grasses to proliferate, which may have led to periodic rodent irruptions, supporting a guild of introduced mammalian predators and depleting populations of Whitaker's skink and copper skink. In this instance, attempted protection may have driven a vulnerable population towards extinction. We recommend investigating the feasibility of constructing a mammal-proof fence around the core Whitaker's skink habitat, as the last remaining management option to salvage the population.     

Monitoring the population status of a secretive lizard,the threatened heath skink Liopholis multiscutata,in south-eastern Australia using surrogate metrics: An update

Our recent study compared monitoring data collected using surrogate metrics during 2014–2018 inclusive with baseline data from 2007 to evaluate the trajectory of the population status of the threatened heath skink Liopholis multiscutata in Victoria. The heath skink is a secretive burrowing species that is a habitat specialist and exists in north-western Victoria as a few small and highly disjunct populations on large dunes in semi-arid heathland or mallee. We re-assessed the trajectories of the Victorian populations with additional monitoring data collected in 2021 and found continuing decline across all four Victorian heath skink populations. Urgent management intervention is required to arrest this decline, likely due to predation, reduced availability of habitat and life history and demographic traits that make this species susceptible to decline.     

Characterization of 21 microsatellite marker loci in the prehensile‐tailed skink (Corucia zebrata)

Twenty‐one polymorphic microsatellite loci were isolated and characterized from the genome of the prehensile‐tailed skink (Corucia zebrata). The markers were screened using a set of 16 individuals from the collection of the Philadelphia Zoo. The corresponding characterization indicated significant levels of heterozygosity and information potential for use in future studies. These markers will be a valuable tool in analysing the paternal contributions in twin birth questions and for population genetic studies in wild populations.     

Isolation of polymorphic tetranucleotide microsatellite markers for the skink Mabuya affinis

We isolated 10 polymorphic microsatellite markers for the skink Mabuya affinis from genomic libraries enriched for (AAGG)_n and (AAAG)_n repetitive elements. The number of alleles ranged from eight to 13 per locus with the observed heterozygosity ranging from 0.60 to 0.92. These markers will be useful for analysis of questions concerning population genetic structure and models of speciation.     

Activity patterns and reproductive behavior of the Critically Endangered Bermuda skink (Plestiodon longirostris)

The study of rare or cryptic species in zoos can provide insights into natural history and behavior that would be difficult to obtain in the field. Such information can then be used to refine population assessment protocols and conservation management. The Bermuda skink (Plestiodon longirostris) is an endemic Critically Endangered lizard. Chester Zoo's successful conservation breeding program is working to safeguard, increase and reinforce skink populations in the wild. A key aim of this program is to develop our understanding of the behavior of this species. In this study, using 24 h video recordings, we examined the daily activity patterns, basking behavior and food preferences of four pairs of Bermuda skinks. The skinks displayed a bimodal pattern of activity and basking, which may have evolved to avoid the strength of the midday sun in exposed habitats in Bermuda. Captive Bermuda skinks appear to prefer a fruit-based diet to orthopteran prey. We also documented their reproductive behavior and compared it against two closely related species. Although there were many similarities between the courtship and mating behaviors of the three species, there was a significantly shorter period of cloacal contact in the Bermuda skink. Oophagia was also documented for the first time in this species. This knowledge has enabled the evaluation of the current ex-situ management practices of this species, filled gaps in knowledge that would be challenging to obtain in the field, and enabled the enhancement of both animal husbandry and reproductive success for the conservation breeding program.     

Chemical discrimination among predators by lizards: Responses of three skink species to the odours of high‐ and low‐threat varanid predators

Animals must balance the benefits of predator avoidance with costs. Costs of predator avoidance, such as being forced to spend long periods inactive, should select for careful discrimination among predator species. Although prey responses to multiple predators have been well researched across many taxa, no studies have tested whether lizards discriminate among larger lizard predators. We examined the responses of three species of skink to two species of predatory goanna, one that occasionally consumes skinks, and the other a skink specialist. Three litter‐dwelling, tropical skink species, Carlia rostralis, C. rubrigularis and C. storri, were given a choice between a retreat site treated with the odour of one of the goanna species, and an odourless control. The two goanna species used for stimulus scents were: Varanus tristis, a species that consumes skinks as a major proportion of its diet, and Varanus varius, a species that consumes skinks occasionally. Both goannas are broadly sympatric with all three skink species. Carlia rostralis and C. storri both avoided the scent of V. tristis, whereas C. rubrigularis did not. However, no skink species avoided the odour of V. varius. Prey are clearly able to avoid predators based on chemical cues, and can discriminate among similar predators that pose different levels of threat.     

Microhabitat use,seasonal activity and diet of the snake-eyed skink (<Emphasis Type="Italic">Ablepharus kitaibelii fitzingeri</Emphasis>) in comparison with sympatric lacertids in Hungary

Microhabitat selection and seasonal activity of the snake-eyed skink, Ablephaus kitaibelii fitzingeri, are compared to the two lacertid lizards (Lacerta viridis and Podarcis muralis) that co-occur in many of its habitats. The food composition of A. k. fitzingeri is also described. Significant differences in microhabitat selection and seasonal activity among the three species were found. The snake-eyed skink was associated with open grasslands, and with a low level of scrub, bare soil and rock cover. The microhabitat preference of L. viridis was quite similar to that of the skink, but with a higher preference for scrub. P. muralis occurred in places with greater rock and bare soil cover, and more scrub than A. k. fitzingeri. Activity of the snake-eyed skink decreased dramatically in summer, probably because of the reduced thermal inertia originating from the extremely small size of this species, but its seasonal activity overlapped with those of the lacertids. Stomach content analysis of the snake-eyed skink suggests that it is a generalist predator of small, mainly flightless arthropod prey. Competition with juvenile lacertids and predation by adult L. viridis are conceivable for the snake-eyed skink.     

Genetic diversity and gene flow in a rare New Zealand skink despite fragmented habitat in a volcanic landscape

Anthropogenic habitat fragmentation often restricts gene flow and results in small populations that are at risk of inbreeding. However, some endangered species naturally occupy patchy habitat where local population extinction and recolonization are normal. We investigated population fragmentation in the range‐restricted New Zealand small‐scaled skink (Oligosoma microlepis), documenting changes in habitat occupancy and analyzing mitochondrial, microsatellite, and morphological variation sampled across the geographical range of the species (approximately 100 km²). Small‐scaled skinks have a strong preference for rocky outcrops that exist in a mosaic of other habitat types. A metapopulation structure was indicated by both local extinction and colonization of new sites. We found relatively high mtDNA nucleotide site diversity within this narrow range (π = 0.004; 16S), evidence of inter‐patch gene flow, and no statistical support for inbreeding. Gene flow was limited by geographical distance, although the existence of pasture between habitat patches apparently has not prevented skink dispersal. Generalized linear models indicated an association between body size and location suggesting a local environmental influence on phenotype. Prior to human‐induced habitat modification, native forest probably separated preferred sites and, less than 2000 years ago, volcanic activity devastated much of the area currently occupied by O. microlepis. This skink appears able to re‐establish populations if other human‐linked factors such as agricultural intensification and introduced predators are limited. Although in contrast to expectations for a scarce and localized species living in a highly modified landscape, this lizard may have previously adapted to a dynamic, mosaic environment mediated by volcanism.     

At home with the birds: Kalahari tree skinks associate with sociable weaver nests despite African pygmy falcon presence

The way in which animals use habitat can affect their access to key resources or how they are buffered from environmental variables such as the extreme temperatures of deserts. One strategy of animals is to modify the environment or take advantage of structures constructed by other species. The sociable weaver bird (Philetairus socius) constructs enormous colonial nests in trees. These nests are frequented by Kalahari tree skinks (Trachylepis spilogaster) and the two species coexist over a large portion of the Kalahari Desert in South Africa. We tested whether skinks were more abundant in trees containing sociable weaver nests and asked whether the physical features of trees were important predictors of skink abundance. We then focused on potential costs of this association by examining the relationship between skink abundance and the presence of a potential predator, the pygmy falcon (Polihierax semitorquatus), which exclusively uses weaver nest colonies for roosting and nesting. Finally, we simulated a predatory threat to determine if skinks assess risk differently if a weaver nest is present. We found a significant positive association between the presence of weaver nests and skink abundance. In the absence of nests, the type of tree did not influence skink abundance. Skinks used weaver nests and were more likely to perch on the nest than the tree. When threatened with predation, skinks preferred to take refuge in nests. Surprisingly, the presence of nesting pygmy falcons in nests did not influence skink abundance, perhaps because of the abundance of nearby refuges within nests, tree crevices, or in debris at the tree base. We suggest that sociable weaver nests provide multiple benefits to skinks including lowered predation risk, thermal refuges and greater prey availability, although this requires experimental testing. In the current era of global climate change, sociable weaver nests may become a crucial resource for skinks seeking refuge as the Kalahari climate warms.     

Characterization of microsatellite markers in the threatened sand skink (Neoseps reynoldsi)

We characterized microsatellite loci for the sand skink (Neoseps reynoldsi) for future studies of genetic structure in this threatened taxon. We screened a partial genomic library enriched for microsatellites, designed primers for eight loci and assessed these markers for polymorphism across 11 populations in central Florida. Preliminary analyses indicate deviations from Hardy–Weinberg expectations for most loci, suggesting population genetic structure across the sampled populations; therefore, understanding genetic connectivity is critical for maintaining genetic variation in this species.     

Feeling the pressure at home: Predator activity at the burrow entrance of an endangered arid‐zone skink

Habitat modification and invasive species are among the most important contemporary drivers of biodiversity loss. These two threatening processes are often studied independently and few studies have focused on how they interact to influence species declines. Here we assess the predation pressure placed on the threatened great desert skink (Liopholis kintorei) and how this interacts with fire‐induced habitat modifications. We collected daily track data of potential predators for 1 month at 30 great desert skink burrow‐systems where vegetation cover varied significantly after experimental burns. We used these data to evaluate potential predation pressure at the burrow‐system and assess whether fire influenced predator pressure. We supplemented this analysis by documenting predation via the inspection of large mammalian predator scats collected from great desert skink habitat. The level of feral cat activity at a burrow‐system entrance was significantly higher than that of any other potential predator, however fire had no effect on the visitation rates of feral cats, dingoes or large snakes to great desert skink burrow‐systems. The remains of great desert skink were found significantly more frequently in feral cat scats, compared to fox and dingo scats. We provide the first direct evidence that feral cats are a significant predator for great desert skink, thus supporting the hypothesis that feral cat predation is a key threatening process. Feral cat activity was not influenced by small‐scale experimental burns, however, this does not preclude an effect of larger scale fires and we recommend further research exploring this possible interaction.     

Identifying a surrogate metric for monitoring the population status of a secretive habitat specialist,the heath skink Liopholis multiscutata,in south‐eastern Australia

Threatened species that exist in small isolated populations are vulnerable to extinction processes, so effectively monitoring the trajectory of such populations will help determine the most appropriate management actions to combat extinction threats. In this study, we aimed to track the population status of the fossorial heath skink Liopholis multiscutata that is listed as threatened in Victoria, south‐eastern Australia, and exists there as a few small and highly disjunct populations, by using an appropriate surrogate population monitoring metric. This secretive lizard is a habitat specialist, is highly localised in Victoria and lives in warrens in semi‐arid heathland or mallee on large dunes. Survey data, which included every warren and their constituent burrows, as well as an assessment of whether each burrow was ‘active’, were collected for the four known Victorian populations in 2007 and annually during 2014–2018 inclusive. We compared five population indices per monitoring site: number of active warrens (NAW), number of active burrows (NAB), population area for 80% of active warrens (PA80), percentage of warrens that were active (PAW) and average number of active burrows per active warren. The heath skink currently occurs in small populations (8–46 active warrens) and these populations have typically declined over recent years. NAW was the most robust metric; NAB and PA80 did not reveal strong temporal trends. PAW indicated that inactive warrens and burrows persist less than a year and hence may provide information about recent (within months) population changes. It is imperative to establish a material link between the effective monitoring of small, vulnerable populations and the implementation of management actions that benefit such populations. Here, NAW could be used as a long‐term monitoring tool to provide an estimate of the minimum population size of the heath skink at a site. Its use would also ensure continuity in monitoring approaches for the Victorian populations.     

Step on it: can footprints from tracking tunnels be used to identify lizard species?

There are few effective or efficient established methods for monitoring cryptic herpetofauna. Footprint tracking tunnels are routinely used to index small mammal populations, but also have potential for monitoring herpetofauna. We evaluated the utility of tracking tunnels for identification of New Zealand lizards using captive- and wild-sourced animals (four skink and eight gecko species). All skink prints that we obtained were indistinct or obscure, but we obtained relatively clear, measurable prints for all gecko species. We found that identification to species level was possible for the two gecko species for which we had a large sample—Naultinus gemmeus and Woodworthia ‘Otago large’—using linear discriminant analysis (the best model correctly assigned 96.1% of individuals). Our findings suggest that footprints from tracking tunnels may be used to distinguish between species of geckos. Additional research is needed to assess the ability to further discriminate intra- and inter-genera lizard footprints from tracking tunnels, and the utility of the technique for surveying and monitoring lizard populations.     

Polymorphic microsatellite markers for the gliding marsupials Petaurus australis and Petaurus breviceps

Habitat destruction is causing population decline of many hollow dependent species such as gliding marsupials of the Family Petauridae. Three petaurid species are now listed in some Australian states as either threatened, rare or vulnerable, precipitating a need for information on their basic biology and population structure. We isolated and characterized three polymorphic microsatellite loci from the yellow‐bellied glider (Petaurus australis) and six polymorphic microsatellite loci from the sugar glider (P. breviceps). Per‐locus heterozygosities range from 42%–92%, and cross‐species amplification studies show that between five and seven loci are polymorphic in the two target species as well as a related species P. norfolcensis.     

Mammals,reptiles and crabs on the Krakatau Islands: Their roles in the ecosystem

In 1982 I studied the changes which had taken place in the fauna of the Krakatau Islands over the last fifty years, and elucidated the roles of terrestrial consumers and reducers in the developing ecosystems of these islands. Only two species of rat were found (Rattus rattus andR. tiomanicus) as observed by Dammerman (1948) in 1933, butR. tiomanicus had newly established its population on Sertung. No rats were found on Anak Krakatau. Although many skinks (Mabuya multifasciata) were observed on R. Besar, this species was not found on the other islands. The rat and skink are considered strong competitors to the sand crab (Ocypode kuhli), because while the crab was restricted to the sandy beach on the three islands where rat and skink live it had expanded inland on Anak Krakatau where there are no rats and skinks. The two banded monitor (Varanus sarvator) was found on every island and it mainly fed on crabs (Gecarcoidea natalis andMetasesarma aubryi). Thus it is suggested that the crab plays an important role in the process of faunal succession on the Krakatau Islands.     

THE INTERPLAY BETWEEN LOCAL ECOLOGY,DIVERGENT SELECTION,AND GENETIC DRIFT IN POPULATION DIVERGENCE OF A SEXUALLY ANTAGONISTIC FEMALE TRAIT

Genetically polymorphic species offer the possibility to study maintenance of genetic variation and the potential role for genetic drift in population divergence. Indirect inference of the selection regimes operating on polymorphic traits can be achieved by comparing population divergence in neutral genetic markers with population divergence in trait frequencies. Such an approach could further be combined with ecological data to better understand agents of selection. Here, we infer the selective regimes acting on a polymorphic mating trait in an insect group; the dorsal structures (either rough or smooth) of female diving beetles. Our recent work suggests that the rough structures have a sexually antagonistic function in reducing male mating attempts. For two species (Dytiscus lapponicus and Graphoderus zonatus), we could not reject genetic drift as an explanation for population divergence in morph frequencies, whereas for the third (Hygrotus impressopunctatus) we found that divergent selection pulls morph frequencies apart across populations. Furthermore, population morph frequencies in H. impressopunctatus were significantly related to local bioclimatic factors, providing an additional line of evidence for local adaptation in this species. These data, therefore, suggest that local ecological factors and sexual conflict interact over larger spatial scales to shape population divergence in the polymorphism.     

Isolation and characterization of microsatellite loci from yellowtail Seriola quinqueradiata and cross‐species amplification within the genus Seriola

We developed five microsatellite primer pairs for the yellowtail Seriola quinqueradiata. The loci were highly polymorphic, with eight to 14 alleles per locus, and can be used to study kinship and/or population structure. Many of these primer pairs amplified polymorphic loci in cross‐species amplification tests for two other Seriola species (S. lalandi and S. dumerili).     

Taxonomic revision of the marbled skink (Cyclodina oliveri,Reptilia: Scincidae) species complex,with a description of a new species

Abstract

We have completed a taxonomic revision of the New Zealand marbled skink (Cyclodina oliveri) species complex. Morphological analyses and mitochondrial sequence data (ND2, ND4, Cytochrome b; Total 1933 bp) are used to describe a new taxon (commonly known as the “Mokohinau” skink) and redefine C. oliveri. The morphological and molecular data indicate that C. oliveri is distributed on the Poor Knights Islands, Mercury Islands and Aldermen Islands. The new species is restricted to the Mokohinau Islands, Hen and Chickens group, Little Barrier Island and Great Barrier Island. Our data demonstrate that there is no support for the separation of the Poor Knights Islands population of C. oliveri from those on the Mercury Islands and Aldermen Islands. The genetic data indicate that C. whitakeri is part of the C. oliveri species group. Divergence time estimates indicate that the C. oliveri species complex diverged during the late‐Miocene, with further divergences among island groups in C. oliveri including the origin of the new taxon during the late‐Pliocene and mid‐Pleistocene. We present a diagnostic key for Cyclodina.     

Characterization of microsatellite markers for snouted treefrogs in the Scinax perpusillus species group (Anura, Hylidae)

We characterized eight microsatellite loci for snouted treefrogs in the Scinax perpusillus species group, a group of hylid frogs endemic to the Atlantic Coastal Forest of Brazil, and tested their utility in mainland and island species of the complex. All eight loci were polymorphic in one population of S. perpusillus; four of the loci showed excess homozygosity and three of those deviated from Hardy–Weinberg expectations, possibly due to null alleles, inbreeding, or population structure in sampled individuals. Six loci amplified and were polymorphic in S. arduous, S. argyreornatus, and S. faivovichi, but only one in S. alcatraz. These markers will be useful for quantifying effects of habitat fragmentation on population genetic diversity and connectivity in coastal and island populations of this threatened species group.