New Zealand geckos (Diplodactylidae): Cryptic diversity in a post-Gondwanan lineage with trans-Tasman affinities

We used a multi-gene approach to assess the phylogenetic relationships of New Zealand diplodactylid geckos to their Australian and New Caledonian relatives and to one another. Data from nuclear (RAG-1, PDC) and mitochondrial (ND2, 16S) genes from >180 specimens representing all 19 recognized New Zealand taxa and all but two of 20 putatively new species suggested by previous studies were analyzed using Maximum Parsimony, Maximum Likelihood and Bayesian inference. All analyses retrieved a monophyletic New Zealand clade, most closely related to the Australian Diplodactylidae exclusive of Pseudothecadactylus. Hoplodactylus is paraphyletic and composed of two morphological groups: a broad-toed clade, consisting of the island-restricted, largest extant species, Hoplodactylus duvaucelii, and the species-rich, wide-ranging Hoplodactylus maculatus clade; and a narrow-toed clade, comprising five monophyletic subgroups: Naultinus, the Hoplodactylus pacificus and Hoplodactylus granulatus clades, and the distinctive species Hoplodactylus rakiurae and Hoplodactylus stephensi. Each of these lineages is here recognized at the generic level. Our data support recognition of 16 new species (36 total), and five new or resurrected genera (seven total). The New Zealand diplodactylid radiation split from its Australian relatives 40.2mya (95% highest posterior density estimate 28.9-53.5), after the opening of the Tasman Sea. Their distribution cannot, therefore, be regarded as derived as a result of Gondwanana vicariance. The age of the New Zealand crown group, 24.4mya (95% highest posterior density estimate 15.5-33.8), encompasses the period of the 'Oligocene drowning' of New Zealand and is consistent with the hypothesis that New Zealand was not completely inundated during this period. Major lineages within New Zealand geckos diverged chiefly during the mid- to late Miocene, probably in association with a suite of geological and climatological factors that have characterized the region's complex history.     

Corticosterone treatment has subtle effects on thermoregulatory behavior and raises metabolic rate in the New Zealand common gecko, Hoplodactylus maculatus

Baseline concentrations of adrenal glucocorticoids often vary substantially in wild vertebrates in the field. In at least one ectotherm, females of the New Zealand common gecko, Hoplodactylus maculatus, this variation in baseline (not stress-induced) corticosterone appears to be correlated with variation in body temperature (T(b)). We tested the hypothesis that elevated corticosterone affects thermoregulatory behavior so as to raise T(b) and that, independently of an increase in T(b), corticosterone increases metabolic rate. Compared with geckos receiving placebo implants, those that received implants containing corticosterone displayed heat-seeking behaviors, had a higher mean T(b) in their home cages, and, at one time of day, selected a higher mean T(b) in a thermal gradient. At a constant T(b), corticosterone-treated geckos consumed oxygen at a rate approximately 50% higher than placebo geckos. This work has far-reaching implications for a variety of physiological and ecological processes in ectotherms and suggests that corticosterone should be considered as a variable influencing T(b) and metabolism in future studies.     

Redescription of Neotrombicula naultini (Dumbleton, 1947) and descriptions of two new species of chiggers from New Zealand (Acari: Trombiculidae)

Abstract

Neotrombicula naultini (Dumbleton, 1947) was redescribed from the type specimen and additional specimens collected off Hoplodactylus granulatus (= Dactylocnemus granulatus), Hoplodactylus maculatus, and Hoplodactylus pacificus in New Zealand. Neotrombicula sphenodonti and Microtrombicula hoplodactyla were described, as new species, from specimens collected from New Zealand reptiles.     

Sampling skinks and geckos in artificial cover objects in a dry mixed grassland-shrubland with mammalian predator control

Introduced mammalian predators threaten populations of endemic New Zealand lizards but their effects on lizard populations have not been quantified on the mainland. We trialled the use of artificial cover objects (ACOs) for sampling small terrestrial lizards (the skinks Oligosoma maccanni, O. nigriplantare polychroma and O. inconspicuum, and gecko Hoplodactylus maculatus) in three experimental mammal-management treatments: a mammal-proof fence, two sites in an intensive mammal-removal area, and an experimental control site with no mammal removal. These predator control regimes were established in 2005-2006 to protect endangered grand skinks (O. grande) and Otago skinks (O. otagense) at Macraes Flat, North Otago. We (1) counted skinks and geckos found under ACOs on a single day and compared these counts between treatments, and (2) estimated lizard population sizes (N) based on capture-mark-recapture (CMR) of lizards under ACOs in daily and weekly sampling sessions. Our results provide baseline data of the abundance of the small lizard species shortly after implementation of predator management. Single-day counts of skinks were significantly higher inside the mammal fence compared with the experimental control. No consistent differences were found between the other treatments. Significantly more skinks were counted in gully habitats than in ridge habitats. N?, counts of skinks from the first day of CMR, and the total number of individuals caught were correlated, but these relationships must be validated with independent data. Few geckos were caught unless ACOs were placed near rock outcrops. Only two skinks but 25% of geckos moved between adjacent ACOs (5-m spacing). The recapture rate of skinks was low; captures declined when ACOs were checked daily but not when they were checked weekly. Because of potential biases of these methods, we propose to compare counts in ACOs and N? based on CMR in ACOs with N? based on CMR in pitfall traps with 3-m spacing.     

Effects of reproductive condition, season, and site on selected temperatures of a viviparous gecko

The relationship between thermal and reproductive biology is complex and poorly understood. We measured selected body temperatures (T(sel)) for the viviparous gecko Hoplodactylus maculatus. T(sel) was compared among pregnant females, nonpregnant females, and males from two sites: a cool site with biennially reproducing geckos and a warm site with annually reproducing geckos. T(sel) was measured at five times of day during three seasons and compared with microhabitat temperature (T(top)) and field body temperature (T(b)). T(sel) varied with time of day in all comparisons, and the effect of reproductive condition on T(sel) differed between sites and seasons. At both sites, when T(sel) differed between reproductive conditions, pregnant females had higher T(sel) than nonpregnant females and males. Stage of pregnancy affected the degree of elevation of T(sel). Measurements of microhabitat temperature and field T(b) showed that, even in the warmest season, geckos rarely had the opportunity to achieve T(sel) at the cool site but were able to do so at the warm site. The elevation of T(sel) with pregnancy is extreme in this species (up to 8 degrees C), which suggests that an increase in T(b) is critical to successful reproduction. Interactions between the effects of time of day, season, and reproductive condition on T(sel) must be considered in the assessment of thermoregulation in reptiles.     

Extreme longevity of the common gecko (

The longevity of common geckos (Hoplodactylus maculatus) on predator-free Motunau Island, North Canterbury, was investigated. Sixteen of 133 individuals marked between 1967-75 were re-captured in the summer of 1996/97. A growth curve was generated to estimate the age of these geckos at first capture, and from this their age in 1996/97; 10 were estimated to be at least 36 years old. In this cool-temperate habitat, H. maculatus matures late and has a low annual reproductive output over an extended lifespan. This suggests that nearby mainland populations would be particularly slow to recover from the impacts of introduced mammalian predators.     

ACTH-induced stress response during pregnancy in a viviparous gecko: no observed effect on offspring quality

The typical stress response in reptiles involves the release of corticosterone from the adrenal glands. Elevated maternal concentrations of corticosterone in mammals during pregnancy may have deleterious effects on offspring fitness, and recent work has shown a suppression of the hormonal response to stress during pregnancy in rats. Little is known about the influence of reproductive state on the secretion of corticosterone in viviparous reptiles or on the effects of high levels of corticosterone during reproduction on the developing embryos. We examined whether New Zealand common geckos (Hoplodactylus maculatus), pregnant with embryos at stages 34-35 of development, secrete corticosterone in response to adrenocorticotrophic hormone (ACTH) and whether an ACTH-induced increase in maternal corticosterone affects the outcome of pregnancy. Corticosterone concentrations in pregnant lizards increased more than seven-fold over basal levels following injection of ACTH. However, there were no significant effects of elevated corticosterone on the duration or success of pregnancy, or on various morphological measures, growth, or sprint speed of the offspring. This may reflect a lack of sensitivity of relevant embryonic tissues to corticosterone under the conditions of the present experiment or an ability of the embryos to bind, degrade, or restrict placental transport of corticosterone. Future studies should investigate the possibility of corticosteroid effects on other offspring tissues, including effects in adult life.     

Using testis size to predict the mating systems of New Zealand geckos

Abstract

The mating system is unknown for the majority of New Zealand geckos (Family Gekkonidae). I investigated interspecific variation in relative testis volume across 19 New Zealand gecko taxa and 63 additional species of squamate reptiles from other countries to make predictions about the social mating system of the New Zealand geckos. Relative testis size varied greatly between species of New Zealand gecko, with testes ranging from 119% larger than expected to 75% smaller than expected. This variation was even greater across other squamates, with testes ranging from 55 to 152% of expected size. This variation could not be explained by seasonality of breeding, clutch size or the sex ratio of populations. As species subject to more intense sperm competition sport relatively larger testes in other vertebrate groups, it is likely that similar variation in gecko testis size is due to differences in mating systems between species. Based on testis volume, it is predicted that at least half of the New Zealand gecko taxa studied are likely to have polygynandrous mating systems.     

Skink predation by hedgehogs at Macraes Flat, Otago, New?Zealand

The stomach contents of 158 hedgehogs captured at Macraes Flat, Otago, New Zealand, over two summers in 2000 and 2001 were examined for the occurrence of lizards. The remains of at least 43 skinks (both Oligosoma nigriplantare polychroma and O.?maccanni) and one gecko (Hoplodactylus sp.) were found. Twenty-one percent (n?=?33; 8 males and 25 females) of the examined hedgehogs had fed on skinks. Female hedgehogs ate significantly more skinks than did males. Our results suggest that the presence of large numbers of hedgehogs can have a high impact on native reptile populations in New Zealand and therefore they should be targeted in future trapping programmes.     

Little and large: body size and genetic clines in a New Zealand gecko (Woodworthia maculata) along a coastal transect

Clinal variation can result from primary differentiation or secondary contact and determining which of these two processes is responsible for the existence of a cline is not a trivial problem. Samples from a coastal transect of New Zealand geckos (Woodworthia maculata) identified for the first time a body size cline 7-10 km wide. The larger geckos are almost twice the mass of the small adult geckos. Clines in allele and haplotype frequency were found at two of the four genetic loci examined. Estimated width of the morphological cline was concordant with neither the narrower mtDNA cline (3-7 m) nor the wider nuclear cline (RAG-2; 34-42 km), and cline centers were not coincident. Although the body size cline is narrow compared to the entire range of the species, it is 2-3 orders of magnitude greater than estimates of dispersal distance per generation for these geckos. No evidence of assortative mating, nor of hybrid disadvantage was identified, thus there is little evidence to infer that endogenous selection is maintaining a hybrid zone. We cannot distinguish secondary contact from primary origin of this body size cline but conclude that secondary contact is likely due to the occurrence of mtDNA haplotypes from three distinct clades within the coastal transect and the presence of two frequency clines within this region.     

Comparative fine structure of the axial skeleton inside the regenerated tail of some lizard species and the tuatara (Sphenodon punctatus)

The regenerated tail of the New Zealand gecko Hoplodactylus maculatus is equipped with an elastic cartilaginous tube as skeletal axis. Other lizard species and Sphenodon punctatus possess variably developed hyaline cartilaginous tubes. Moreover, H. maculatus enhances the functional performance of its tail by long elastic fibres, which are arranged all around the central regenerated spinal cord. The different characteristics of the regenerated skeleton could be related to the different environments that the species studied occupy in nature.     

Phylogeny recapitulates geography, or why New Zealand has so many species of skinks

The evolutionary history of 25 New Zealand scincid lizards in the endemic genera Oligosoma and Cyclodina was examined using 12S rRNA sequence data. Phylogenetic resolution was poor, despite there being up to 9% sequence divergence between taxa. Lack of resolution was not attributable to biases in the data, such as site saturation or differences in sites free to vary, so we infer that New Zealand skinks underwent two relatively rapid phases of divergence. The rate of substitution for the skink sequences appears to be similar to some bird and mammal groups for which times of divergence have been estimated. Using fhese calibrations diversification of Oligosoma skinks probably began at least 23 million years ago (Mya). The pattern of relationships and the timing of this diversification are interpreted as resulting from rapid allopatric speciation during the Oligocene (25–35 Mya) when New Zealand was fragmented into many low lying islands. A second major phase of speciation involving the Cyclodina seems to have occurred during the Miocene (15–24 Mya), probably as a consequence of increasing land area and habitat diversity. This pattern of skink evolution contrasts with the Oligocene 'environmental crisis' hypodiesis of Cooper & Cooper (Proc. R. Soc. Land. B. 261, 293–302), but can be attributed to differences in the ecology of different taxa. This can be tested by examination of other groups, such as land snails and geckos. The large number of lizard species in New Zealand can be considered a legacy both of past geography as well as the absence of small mammals which would have been both competitors and predators.     

Are viviparous lizards from cool climates ever exclusively nocturnal? Evidence for extensive basking in a New Zealand gecko

Viviparity has evolved numerous times among squamate reptiles; however, the combination of viviparity and nocturnality is apparently rare among lizards. We used time‐lapse photography to examine evidence for diurnal activity in a viviparous lizard often described as nocturnal, the gecko Woodworthia ‘Otago/Southland’ from southern New Zealand (family Diplodactylidae). Evidence for diurnal emergence was extensive. Females have a higher incidence of basking compared to males, although no difference was detected between females in different reproductive conditions. Temperature loggers inserted into calibrated copper models were used to compare the body temperatures available to geckos in two basking positions and in two retreat types. Models in basking positions reached higher mean temperatures than models in retreats, although there was no significant effect of basking position or retreat type on model temperatures. Collectively, our results indicate that pregnant geckos that bask consistently could reduce gestation length by at least 14 days compared with females that remain in retreats. Extensive basking in this species adds to the growing evidence of diurno‐nocturnality in many New Zealand lepidosaurs, including other viviparous geckos. Our results lead us to question whether viviparity in lizards is ever compatible with ‘pure’ nocturnality in a cool climate. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, ●● , ●●–●●.     

Low cost of locomotion in lizards that are active at low temperatures

The nocturnality hypothesis of K. Autumn and coworkers states that nocturnal geckos have evolved a low energetic cost of locomotion (C(min)). A low C(min) increases maximum aerobic speed and partially offsets the decrease in maximum oxygen consumption caused by activity at low nocturnal temperatures. We tested whether a low C(min) is unique to nocturnal geckos or represents a more general pattern of convergent evolution among lizards that enables nocturnality and/or cold-temperature activity. We measured C(min) in four carefully selected lizard species from New Zealand (two nocturnal and two diurnal; n=5-9 individuals per species), including a nocturnal and diurnal gecko (a low C(min) is a gecko trait and is not related to nocturnality), a nocturnal skink (a low C(min) is related to being nocturnal), and a diurnal skink active at low temperatures (a low C(min) is related to being active at low body temperatures). The C(min) values of the four species measured in this study (range=0.21-2.00 mL O(2) g(-1) km(-1)) are lower than those of diurnal lizards from elsewhere, and the values are within or below the 95% confidence limits previously published for nocturnal geckos. A low C(min) increases the range of locomotor speeds possible at low temperatures and provides an advantage for lizards active at these temperatures. We accepted the hypothesis that nocturnal lizards in general have a low C(min) and provide evidence for a low C(min) in lizards from cool-temperate environments. The low C(min) in lizards living at high latitudes may enable extension of their latitudinal range into otherwise thermally suboptimal habitats.     

Geographical differences in erythemally-weighted UV measured at mid-latitude USDA sites.

UV measurements from instruments maintained by USDA at 16 mid-latitude sites were analysed to investigate geographic differences. Fifteen of the sites are in North America, and one is in New Zealand. The instruments measure erythemally weighted UV radiation, and the results are presented in terms of UV Index (UVI). The focus of this work is on data from 2003, but the main results are also shown for years 2002 and 2004. In the North American sites, the peak UVI values increase by approximately 15% between latitudes 47 degrees N and 40 degrees N, and they show an increase with altitude of approximately 15% in the first kilometer, but much smaller rates of increase above that level. Peak UV intensities in the New Zealand site (45 degrees S, alt. 0.37 km) exceed those at comparable latitudes and altitudes in North America by 41 +/- 5%, and are more comparable with those over 1 km higher and 5 degrees closer to the equator. The number of observations on these days that exceeded various thresholds of UVI showed similar patterns. Furthermore, the number of days in which the peak values exceeded various thresholds also showed similar patterns, with the number of extreme values in New Zealand being anomalously high. For example, the only sites in North America where UVI exceeded 12 were at the high altitude sites in Colorado and Utah, for which there were 53 days, 6 days and 2 days respectively at the 3.2 km, 1.6 and 1.4 km sites. By contrast, the peak UVI at Lauder (0.37 km) exceeded 12 on 17 days. Lauder was the only site under 1 km altitude where the UVI exceeded 11 on a regular basis (48 days). The optical depths at Lauder were significantly lower than at all North American sites. These, together with the lower ozone amounts and the closer Earth-Sun separation in summer all contribute to the relatively high UV intensities at the New Zealand site. Other sites in New Zealand show similar increases compared with corresponding sites in North America, and the differences persist from year to year. The contrast in UV between New Zealand and North America is similar to that observed previously between New Zealand and Europe. During winter months, the UVI in New Zealand is not particularly high, giving a larger summer/winter contrast in UVI, which may be important from a health perspective.     

Distribution and abundance of endemic coelostomidiid scale insects (Hemiptera: Coelostomidiidae) in Auckland forests, New Zealand

Sap-feeding insects can excrete considerable quantities of sugar-rich honeydew. In New Zealand, South Island beech (Nothofagus spp.) forests are shaped by the extensive honeydew resource produced by two endemic coelostomidiid species (Ultracoelostoma assimile and U.?brittini) and geckos on northern islands are known to feed on the honeydew of a third endemic coelostomidiid, Coelostomidia zealandica. There are six other endemic coelostomidiid species in New Zealand that utilise a range of plant hosts but the ecological role of these species is poorly understood. A survey of mainland forests in the Auckland Ecological Region was conducted in February?April 2006 to investigate the distribution and abundance of coelostomidiids in this area. Three coelostomidiid species were detected in the survey (C.?zealandica, C.?pilosa and C.?wairoensis) and five new host?scale insect associations were identified. C.?zealandica was uncommon, C.?pilosa was widespread in broadleaved?podocarp forest but only formed light infestations, and C.?wairoensis was present in all teatree stands examined, often forming heavy infestations on k?nuka (Kunzea ericoides). Infested k?nuka trees had sooty moulds growing on them and exotic wasps were regularly seen feeding on C.?wairoensis honeydew. The extent and intensity of C. wairoensis infestation on k?nuka suggests it will have community-level impacts.     

Miocene skinks and geckos reveal long-term conservatism of New Zealand's lizard fauna

The New Zealand (NZ) lizard fossil record is currently limited to late Quaternary remains of modern taxa. The St Bathans Fauna (early Miocene, southern South Island) extends this record to 19–16 million years ago (Myr ago). Skull and postcranial elements are similar to extant Oligosoma (Lygosominae) skinks and Hoplodactylus (Diplodactylinae) geckos. There is no evidence of other squamate groups. These fossils, along with coeval sphenodontines, demonstrate a long conservative history for the NZ lepidosaurian fauna, provide new molecular clock calibrations and contradict inferences of a very recent (less than 8 Myr ago) arrival of skinks in NZ.     

Key innovations and island colonization as engines of evolutionary diversification: a comparative test with the Australasian diplodactyloid geckos

The acquisition of key innovations and the invasion of new areas constitute two major processes that facilitate ecological opportunity and subsequent evolutionary diversification. Using a major lizard radiation as a model, the Australasian diplodactyloid geckos, we explored the effects of two key innovations (adhesive toepads and a snake‐like phenotype) and the invasion of new environments (island colonization) in promoting the evolution of phenotypic and species diversity. We found no evidence that toepads had significantly increased evolutionary diversification, which challenges the common assumption that the evolution of toepads has been responsible for the extensive radiation of geckos. In contrast, a snakelike phenotype was associated with increased rates of body size evolution and, to a lesser extent, species diversification. However, the clearest impact on evolutionary diversification has been the colonization of New Zealand and New Caledonia, which were associated with increased rates of both body size evolution and species diversification. This highlights that colonizing new environments can drive adaptive diversification in conjunction or independently of the evolution of a key innovation. Studies wishing to confirm the putative link between a key innovation and subsequent evolutionary diversification must therefore show that it has been the acquisition of an innovation specifically, not the colonization of new areas more generally, that has prompted diversification.     

Breeding and survival of New Zealand Pigeons Hemiphaga novaeseelandiae

The breeding and survival of New Zealand Pigeons Hemiphaga novaeseelandiae were studied by radiotelemetry at three contrasting native forest sites in the North and South Islands of New Zealand. At each site, mean annual productivity was low (0-0.12 fledglings/adult) in relation to the mean annual rate of adult mortality (0.18-0.53). Losses of eggs and chicks to introduced mammals were the main identified causes of nest failure. Causes of adult mortality included episodic predation by introduced mammals and apparent starvation in spring at one site. At the most intensively-studied site (Pelorus Bridge), where 75 birds were radiotagged over 7 years, there was a marked annual variation in breeding success (0-0.3 fledglings/adult), including one season (1986–1987) when no breeding activity was detected at all. New Zealand Pigeons were legally hunted in the past, but our results indicate that harvesting is unlikely to be sustainable under current ecological conditions.     

A structural comparison of New Zealand and south-east Australian rain forests and their tropical affinities

An ecological comparison, with special reference to tropical affinities, is made between the rain forests of New Zealand and south-east Australia, based on the distribution of seventy physiognomic-structural attributes in mature forests at selected sites (ten in New Zealand, twenty in Australia, and four in New Guinea to represent authentic humid tropical lowland rain forest). The structural data were recorded in a standard pro forma and subjected to classification, ordination and two-parameter analysis. In the classification, the Australian and New Zealand sites, with two exceptions, separated at the four-group level. The more complex (cool subtropical) Australian types were the least related to the New Zealand forests, which are closest to Australian simple (submontane) types. There was a similar distinction in the ordination, in which the trend along the first two vectors was latitudinal, correlated with extremes of temperature and with moisture availability. The relative contributions of the structural attributes to the various site groupings in the classification and ordination are enumerated, and provide an objective scale of comparison of the forests. Structural attributes designated by analysis as exclusively or preferentially tropical by reference to the New Guinea sites are then used to assess degree of tropical affinity. The simplified cool temperate (montane) forests dominated by one species of Notho-fagus in New Zealand and Australia are closely related. The Australian forests of the sub-montane zone (mean annual temperature 12–15° C) which are typically dominated by Ceratopetalum apetalum, Nothofagus moorei or Doryphora sassafras, are similar to the podocarp-broadleaf forests, with or without kauri, of New Zealand. The Australian forests of the cool subtropical zone (mean annual temperature 15–17°C) which have mixed dominants, have some affinities with the kauri-podocarp-broadleaf forests of North Auckland. In New Zealand, a broadleaf type in which kauri is absent or rare on basalt in North Auckland (lat. 35° S) was the most complex forest sampled and is marginally subtropical.