Fluctuating Asymmetry as an Indicator of Environmental Stress From Off-Highway Vehicles

Abstract: With human activities increasingly impacting natural resources in relatively remote locations, there is a need for simple and efficient methods to explore the ecological consequences of these activities. Little is understood about the influences of off-highway vehicle (OHV) use on wildlife populations. We examined the effect of OHV activity on developmental instability in a phrynosomatid lizard (i.e., western fence lizard [Sceloporus occidentalis]) in the western Great Basin, USA. We measured fluctuating asymmetry (FA) of bilateral head-scale patterns in populations of lizards at 3 OHV and 3 non-OHV sites. Fluctuating asymmetry was higher at OHV sites relative to non-OHV sites, supporting the idea that OHV activity can stress wildlife populations. We found FA to be a good tool for uncovering responses to stress in natural populations, and we recommend exploring FA as a means of uncovering developmental instability in other systems that merit conservation interest.     

The effect of prey availability on offspring survival depends on maternal food resources

Maternal nutrition can strongly influence embryo development and offspring fitness. The environmental matching hypothesis posits that developmental conditions affect offspring in ways that enable them to appropriately deal with similar post‐developmental conditions, although mismatches between developmental and post‐developmental environments will reduce fitness. To test this hypothesis, reproductive lizards (Anolis sagrei) were reared in environments with high versus low prey availability. The resultant offspring were then reared reciprocally under the same two prey conditions that their mothers experienced. High levels of prey available to mothers increased egg production, although the survival of eggs was low compared to those produced by mothers in the low‐prey treatment. Low prey availability to offspring reduced growth, regardless of the amount of prey available to their mothers. Low prey availability also compromised offspring survival, although this negative effect was only present when mothers experienced high‐prey conditions, whereas matching of low‐prey conditions in maternal and offspring stages resulted in high survival. However, because the mismatch of low maternal and high offspring prey availability resulted in similar offspring survival to the matched treatments, our results do not fully support the environmental matching hypothesis. Nevertheless, the present study highlights the interactive role of maternal and post‐hatching environments in generating variation in offspring fitness. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 115 , 437–447.     

The ultrastructure of spermatid development during spermiogenesis within the rosebelly lizard,Sceloporus variabilis (Reptilia,Squamata, Phrynosomatidae)

Several recent studies have mapped out the characters of spermiogenesis within several species of squamates. Many of these data have shown both conserved and possibly apomorphic morphological traits that could be important in future phylogenetic analysis within Reptilia. There, however, has not been a recent study that compares spermiogenesis and its similarities or differences between two species of reptile that reside in the same genus. Thus, the present analysis details the changes to spermiogenesis in Sceloporus variabilis and then compares spermatid morphologies to that of Sceloporus bicanthalis. Many of the morphological changes that the spermatids undergo in these two species are similar or conserved, which is similar to what has been reported in other squamates. There are six main character differences that can be observed during the development of the spermatids between these two sceloporid lizards. They include the presence (S. variabilis) or absence (S. bicanthalis) of a mitochondrial/endoplasmic reticulum complex near the Golgi apparatus during acrosome development, a shallow (S. variabilis) or deep (S. bicanthalis) nuclear indentation that accommodates the acrosomal vesicle, filamentous (S. variabilis) or granular (S. bicanthalis) chromatin condensation, no spiraling (S. variabilis) or spiraling (S. bicanthalis) of chromatin during condensation, absence (S. variabilis) or presence (S. bicanthalis) of the longitudinal manchette microtubules, and the lack of (S. variabilis) or presence (S. bicanthalis) of nuclear lacunae. This is the first study that compares spermiogenic ultrastructural characters between species within the same genus. The significance of the six character differences between two distantly related species within Sceloporus is still unknown, but these data do suggest that spermiogenesis might be a good model to study the hypothesis that spermatid ontogeny is species specific. J. Morphol. 275:258–268, 2014. © 2013 Wiley Periodicals, Inc.     

Microhabitat relationships among five lizard species associated with granite outcrops in fragmented agricultural landscapes of south‐eastern Australia

A fundamental part of developing effective biodiversity conservation is to understand what factors affect the distribution and abundance of particular species. However, there is a paucity of data on ecological requirements and habitat relationships for many species, especially for groups such as reptiles. Furthermore, it is not clear whether habitat relationships for particular species in a given environment are transferable to other environments within their geographical range. This has implications for the type of ‘landscape model’ used to guide management decisions in different environments worldwide. To test the hypothesis that species‐specific habitat relationships are transferable to other environments, we present microhabitat models for five common lizard species from a poorly studied habitat – insular granite outcrops, and then compared these relationships with studies from other environments in south‐eastern Australia. We recorded twelve species from five families, representing 699 individuals, from 44 outcrops in the south‐west slopes of New South Wales. Five lizard species were abundant and accounted for 95% of all observations: Egernia striolata, Ctenotus robustus, Cryptoblepharus carnabyi, Morethia boulengeri and Carlia tetradactyla (Scincidae). Linear regression modelling revealed suites of different variables related to the abundance patterns of individual species, some of which were broadly congruent with those measured for each species in other environments. However, additional variables, particular to rocky environments, were found to relate to reptile abundance in this environment. This finding means that species' habitat relationships in one habitat may not be readily transferable to other environments, even those relatively close by. Based on these data, management decisions targeting reptile conservation in agricultural landscapes, which contain rocky outcrops, will be best guided by landscape models that not only recognize gradients in habitat suitability, but are also flexible enough to incorporate intraspecies habitat variability.     

Sexual dimorphism in histological characteristics and contractility of the iliofibularis muscle in the lizard Sceloporus torquatus

The iliofibularis is a hindlimb muscle used in lizard locomotion that is composed of at least three types of fibres: fast‐twitch‐glycolytic (FG), fast‐twitch‐oxidative‐glycolytic fibre (FOG) and slow‐twitch‐oxidative (SO). The striated skeletal muscle is a highly plastic tissue undergoing phenotypic change in response to activity. The lizard Sceloporus torquatus has sexual differences associated with microhabitat use, which can be reflected in the physiology and anatomy of the muscle, and thus, in our study, we analysed the morphological and contractile characteristics of the iliofibularis muscle (IF) of S. torquatus males and females. We found a larger prevalence of FOG compared with FG and SO fibres in the muscle of both sexes. We also found that males show larger areas of the three types of fibres, develop greater strength but also faster fatigue than females, suggesting that strength is a key functional feature that enables males to perform faster movements (but for shorter periods), associated with the demands of territoriality.     

Population augmentation had no effect on the abundance or body condition of conspecifics and co‐occurring lizard species in a native grassland community

Wildlife translocations have been historically plagued by failure. As more species gain endangered status, we must increase the success rate through use of pre‐emptive empirical, evidence‐based research. The main ecological risk is the potential for the relocated individuals to have competitive advantage at the recipient site, acting invasively and, potentially, outcompeting the native fauna for food, shelter or other resources. Here we investigated the ecological risk of increased population density, following a population augmentation of the pygmy bluetongue lizard (Tiliqua adelaidensis) an endangered lizard, endemic to South Australia. We experimentally increased T. adelaidensis density to ascertain if a sudden increase in T. adelaidensis density would negatively affect the abundance or body condition of the resident conspecifics and co‐existing lizard species found at the recipient site. Twenty‐four individuals, from two populations, were relocated into previously built enclosures at a recipient site in grassland habitat, north of Adelaide, South Australia. For one activity‐season pre and post the augmentation, co‐existing lizard species were sampled in an effort to detect any changes inabundance or body condition. Comparisons were also made between experimental enclosures, containing residents and translocated individuals and control enclosures, containing only residents. Using Menetia greyii as a proxy for all of the competing species, our results show there was no reduction in abundance or body condition post augmentation. Our lack of evidence indicating a negative impact of the T. adelaidensis translocation on the body condition and abundance of the resident lizard species is a positive outcome for future conservation of this species. This study provides a new way of approaching wildlife movements, through identification of potential risks using small‐scale translocations in an enclosed area before conducting large‐scale releases into unfenced areas; the results are intended to facilitate higher translocation success rates and limit the negative effects upon the wider ecological community at recipient sites.     

Seasonal effects on circulating leptin in the lizard Sceloporus undulatus from two populations

Characterizing leptin's structure and function in mammals has been the subject of thousands of studies since 1994. Recently, the study of leptin has expanded to include its distribution in non-mammalian taxa, and the role that leptin plays in the reproductive axis. We demonstrated in a previous study that Sceloporus undulatus, fence lizards (ectotherms), express a leptin-like protein. In the current study we quantified seasonal variation in this putative leptin among free-ranging fence lizards from two populations characterized by early and late reproductive maturation (after one or two years, respectively). Immunoblots were performed on whole blood samples to detect leptin and estimate its titer. Leptin titers were higher in the reproductive population of S. undulatus (early maturing: 2.5 ± 0.2 μg/mL; late-maturing 2.2 ± 0.3 μg/mL; mean ± 2 S.E.), but both populations showed the same seasonal pattern. Leptin titers were lowest in fall when fat stores are expected to be highest (spring: 2.6 ± 0.3 μg/mL; summer: 2.6 ± 0.3; μg/mL; fall: 1.8 ± 0.3 μg/mL), consistent with findings of seasonal variation in free-ranging mammals. Our data support previous work asserting that lizards express leptin and that it has a similar physiological function in endotherms and ectotherms. Our long-term goal is to use leptin to manipulate age at maturity and to test fundamental questions in the evolution of life-history strategies.     

Density effects on life-history traits of an island lizard population

Long-term monitoring of life-history traits and the effects of density upon them were studied in an island population of the lizardEumeces okadae. Although life-history traits such as clutch size, egg size and the proportion of mature reproductive females varied little over 7 years in the intact population, manipulation of density to simulate decreased population density enhanced juvenile growth rate, age at first reproduction, frequency of female reproduction and size-specific clutch mass. In particular, the proportion of mature females reproducing annually increased almost 10 times from 5.6% to 53.8% after the removal of some lizards. However, body size at first reproduction and egg size were almost identical under both high and low density conditions. This study suggests that there were strong density-dependent effects on several life-history traits and thatE. okadae attained a density close to the carrying capacity of the environment.     

Fire severity influences the post-fire habitat structure and abundance of a cool climate lizard

In the spring and summer of 2019–2020, the ‘Black Summer’ bushfires burned more than 97 000 km² of predominantly Eucalyptus dominated forest habitat in eastern Australia. The Black Summer bushfires prompted great concern that many species had been imperilled by the fires. Here, we investigate the effects that fire severity had on the habitat and abundance of a cool climate lizard Eulamprus tympanum that was identified as a species of concern because 37% of its habitat was burnt in the Black Summer bushfires. We quantified habitat structure and the abundance of E. tympanum at sites which were unburnt, burnt at low severity and at high severity 10, 15 and 23 months after the fires. Our classification of fire severity based on scorch height and canopy status corresponded well with the Australian Government Google Earth Engine Burnt Area Map (AUS GEEBAM) fire severity layer. Ten months after the fires, sites burnt at high severity had less canopy cover, more bare ground and less fine fuel than sites burnt at low severity or unburnt sites. The abundance of E. tympanum varied with survey occasion and was greatest during the warmest sampling period and lowest during the coolest sampling period. The abundance of E. tympanum was consistently lower on sites burnt at high severity than sites burnt at low severity or unburnt sites. Our findings show that higher severity fires had a greater effect on E. tympanum than low severity fires. Our results suggest that E. tympanum were likely to have persisted in burnt sites, with populations in low severity and unburnt sites facilitating population recovery in areas burnt at high severity. Our results also suggest that wildfire impacts on E. tympanum populations will increase because the frequency and extent of severe fires are expected to increase due to climate change.     

Context-dependent effects of glucocorticoids on the lizard gut microbiome

The vertebrate gut microbiota (bacterial, archaeal and fungal communities of the gastrointestinal tract) can have profound effects on the physiological processes of their hosts. Although relatively stable, changes in microbiome structure and composition occur due to changes in the environment, including exposure to stressors and associated increases in glucocorticoid hormones. Although a growing number of studies have linked stressor exposure to microbiome changes, few studies have experimentally explored the specific influence of glucocorticoids on the microbiome in wild animals, or across ecologically important processes (e.g., reproductive stages). Here we tested the response of the gut microbiota of adult female Sceloporus undulatus across gestation to ecologically relevant elevations of a stress-relevant glucocorticoid hormone (CORT) in order to determine (i) how experimentally elevated CORT influenced microbiome characteristics, and (ii) whether this relationship was dependent on reproductive context (i.e., whether females were gravid or not, and, in those that were gravid, gestational stage). We show that the effects of CORT on gut microbiota are complex and depend on both gestational state and stage. CORT treatment altered microbial community membership and resulted in an increase in microbiome diversity in late-gestation females, and microbial community membership varied according to treatment. In nongravid females, CORT treatment decreased interindividual variation in microbial communities, but this effect was not observed in late-gestation females. Our results highlight the need for a more holistic understanding of the downstream physiological effects of glucocorticoids, as well as the importance of context (here, gestational state and stage) in interpreting stress effects in ecology.     

Comparison of growth and nutritional status of juvenile Komodo monitors (Varanus komodoensis) maintained on rodent or poultry‐based diets

Nutrition and growth data were collected on six juvenile Komodo monitors (Varanus komodoensis) over 20 months. The animals were captive‐bred from two separate clutches, laid 6 months apart. Three animals were fed a rodent diet, and the other three were fed a poultry‐based diet. The animals were all weighed and measured weekly. Blood samples were collected monthly. Blood samples were analyzed for sodium (Na), potassium (K), calcium (Ca), phosphorus (P), magnesium (Mg), 25‐OH‐D, and cholesterol. Significant differences (P<0.05) were observed in dry matter intake (DMI) (1.12 vs. 0.90 %BW) and gross energy intake (GEI) (182.3 vs. 143.0 kcal GE/d), between rodent and poultry‐based diets, respectively. However, there were no differences in growth (average daily gain=6.13 vs. 6.33 g BW/d) between the two dietary treatments. Blood Na, K, Ca, P, Mg, and 25‐OH‐D concentrations were similar across treatments, while cholesterol levels were higher in the animals maintained on the rodent‐based diet. Zoo Biol 23:239–252, 2004. © 2004 Wiley‐Liss, Inc.     

Effects of long‐term fox baiting on species composition and abundance in an Australian lizard community

Abstract We report on the effects of almost a decade of 1080‐fox baiting on a lizard community in a mosaic Australian habitat. Replicated comparisons of baited versus non‐baited control areas with near‐identical histories of bush fires, grazing and climate showed a higher density of red fox tracks (Canis vulpes) in the non‐baited areas. Furthermore, the fox‐baited areas showed a more than five times higher density of sand goannas (Varanus gouldii), a species that strongly overlaps the red fox in food niche breadth and is itself a direct target of fox predation, in particular its eggs and young. Exclusion of predators from a natural habitat led to significant increases in the density of small lizards, suggesting that predation can drive lizard population dynamics in this ecosystem. Replicated pitfall‐trapping in three habitats in the control areas (with high fox and low goanna density) versus the baited areas (with low fox and high goanna density) showed that fox baiting had positive effects on the density of diurnal scincid lizards in open grassland, whereas the control areas showed higher density of nocturnal gecko lizards. Our interpretation is that fox removal may result in a shift in the top predator towards the sand goanna. Historically, this indigenous, endemic species was the natural top predator. It has co‐evolved with its prey and that may have moulded it into a more efficient lizard predator per encounter than the introduced fox.     

Metabolically similar cohorts of bacteria exhibit strong cooccurrence patterns with diet items and eukaryotic microbes in lizard guts

Gut microbiomes perform essential services for their hosts, including helping them to digest food and manage pathogens and parasites. Performing these services requires a diverse and constantly changing set of metabolic functions from the bacteria in the microbiome. The metabolic repertoire of the microbiome is ultimately dependent on the outcomes of the ecological interactions of its member microbes, as these interactions in part determine the taxonomic composition of the microbiome. The ecological processes that underpin the microbiome's ability to handle a variety of metabolic challenges might involve rapid turnover of the gut microbiome in response to new metabolic challenges, or it might entail maintaining sufficient diversity in the microbiome that any new metabolic demands can be met from an existing set of bacteria. To differentiate between these scenarios, we examine the gut bacteria and resident eukaryotes of two generalist‐insectivore lizards, while simultaneously identifying the arthropod prey each lizard was digesting at the time of sampling. We find that the cohorts of bacteria that occur significantly more or less often than expected with arthropod diet items or eukaryotes include bacterial species that are highly similar to each other metabolically. This pattern in the bacterial microbiome could represent an early step in the taxonomic shifts in bacterial microbiome that occur when host lineages change their diet niche over evolutionary timescales.     

Countergradient variation in growth and food conversion efficiency of juvenile turbot

Growth performance of a high latitude (Norway) population of juvenile turbot Scophthalmus maximus , was superior to that of two other lower latitude populations (Scotland, France) especially at 18° and 22° C. Overall these results lend some support to the hypothesis of countergradient variation in growth. The Norwegian population had the highest estimated temperature optimum for growth ( T _opt.G, ±S.E.) (23·0±0·9°C) and food conversion efficiency ( T _opt.Ec) (17·5±0·3), followed by the French ( T _opt.G 21·1±1·0; T _opt.Ec, 16·7±0·1) population, whereas the Scottish population had the lowest optimum ( T _opt.G, 19·6±0·6; T _{opt Ec}, 16·5±0·1°C). These results have two major implications: firstly, for turbot culture, particularly in selection work focusing on growth performance; secondly, if countergradient variation in growth performance takes place within a species one cannot assume automatically that one set of physiological parameters, in this case growth-related parameters, is satisfactory to predict growth for a species throughout its range as different populations might show a difference in response towards different physiological parameters.     

Health food versus fast food: the effects of prey quality and mobility on prey selection by a generalist predator and indirect interactions among prey species

1. In order to understand the relative importance of prey quality and mobility in indirect interactions among alternative prey that are mediated by a shared natural enemy, the nutritional quality of two common prey for a generalist insect predator along with the predator's relative preference for these prey was determined. 2. Eggs of the corn earworm Helicoverpa zea (Lepidoptera: Noctuidae) were nutritionally superior to pea aphids Acyrthosiphum pisum (Homoptera: Aphididae) as prey for big‐eyed bugs Geocoris punctipes (Heteroptera: Geocoridae). Big‐eyed bugs survived four times as long when fed corn earworm eggs than when fed pea aphids. Furthermore, only big‐eyed bugs fed corn earworm eggs completed development and reached adulthood. 3. In two separate choice experiments, however, big‐eyed bugs consistently attacked the nutritionally inferior prey, pea aphids, more frequently than the nutritionally superior prey, corn earworm eggs. 4. Prey mobility, not prey nutritional quality, seems to be the most important criterion used by big‐eyed bugs to select prey. Big‐eyed bugs attacked mobile aphids preferentially when given a choice between mobile and immobilised aphids. 5. Prey behaviour also mediated indirect interactions between these two prey species. The presence of mobile pea aphids as alternative prey benefited corn earworms indirectly by reducing the consumption of corn earworm eggs by big‐eyed bugs. The presence of immobilised pea aphids, however, did not benefit corn earworms indirectly because the consumption of corn earworm eggs by big‐eyed bugs was not reduced when they were present. 6. These results suggest that the prey preferences of generalist insect predators mediate indirect interactions among prey species and ultimately affect the population dynamics of the predator and prey species. Understanding the prey preferences of generalist insect predators is essential to predict accurately the efficacy of these insects as biological control agents.     

On caudal prehensility and phylogenetic constraint in lizards: The influence of ancestral anatomy on function in Corucia and Furcifer

We examined caudal anatomy in two species of prehensile‐tailed lizards, Furcifer pardalis and Corucia zebrata. Although both species use their tails to grasp, each relies on a strikingly different anatomy to do so. The underlying anatomies appear to reflect phylogenetic constraints on the consequent functional mechanisms. Caudal autotomy is presumably the ancestral condition for lizards and is allowed by a complex system of interdigitating muscle segments. The immediate ancestor of chameleons was nonautotomous and did not possess this specialized anatomy; consequently, the derived arrangement in the chameleon tail is unique among lizards. The limb functions as an articulated linkage system with long tendinous bands originating from longitudinal muscles to directly manipulate vertebrae. Corucia is incapable of autotomy, but it is immediately derived from autotomous ancestors. As such, it has evolved a biomechanical system for prehension quite different from that of chameleons. The caudal anatomy in Corucia is very similar to that of lizards with autotomous tails, yet distinct differences in the ancestral pattern and its relationship to the subdermal tunic are derived. Instead of the functional unit being individual autotomy segments, the interdigitating prongs of muscle have become fused with an emphasis on longitudinal stacks of muscular cones. The muscles originate from the vertebral column and a subdermal collagenous tunic and insert within the adjacent cone. However, there is remarkably little direct connection with the bones. The muscles have origins more associated with the tunic and muscular septa. Like the axial musculature of some fish, the tail of Corucia utilizes a design in which these collagenous elements serve as an integral skeletal component. This arrangement provides Corucia with an elegantly designed system capable of a remarkable variety of bending movements not evident in chameleon tails. J. Morphol. 239:143–155, 1999. © 1999 Wiley‐Liss, Inc.     

Seasonal and ontological variation in diet and age‐related differences in prey choice,by an insectivorous songbird

The diet of an individual animal is subject to change over time, both in response to short‐term food fluctuations and over longer time scales as an individual ages and meets different challenges over its life cycle. A metabarcoding approach was used to elucidate the diet of different life stages of a migratory songbird, the Eurasian reed warbler (Acrocephalus scirpaceus) over the 2017 summer breeding season in Somerset, the United Kingdom. The feces of adult, juvenile, and nestling warblers were screened for invertebrate DNA, enabling the identification of prey species. Dietary analysis was coupled with monitoring of Diptera in the field using yellow sticky traps. Seasonal changes in warbler diet were subtle, whereas age class had a greater influence on overall diet composition. Age classes showed high dietary overlap, but significant dietary differences were mediated through the selection of prey; (i) from different taxonomic groups, (ii) with different habitat origins (aquatic vs. terrestrial), and (iii) of different average approximate sizes. Our results highlight the value of metabarcoding data for enhancing ecological studies of insectivores in dynamic environments.     

Hybridization between two insectivorous bird species and the effect on prey-handling efficiency

Gene flow between closely related species is not always impeded by hybrid inviability or sterility but may be limited by behavioural or ecological factors. European common redstarts, Phoenicurus phoenicurus, and black redstarts, P. ochruros, are insectivorous passerine bird species which regularly interbreed in the wild and produce viable and fertile progeny. Yet, the isolation barriers, which prevent extensive gene flow between these distinct species, are unknown. I studied prey-handling time and efficiency in both species and the F₁-hybrids in captivity. All birds changed prey-handling mode from a single pick to more complex behaviour with increasing prey length and their handling time was a positive function of prey length. Common redstarts tended to handle their prey quicker than black redstarts. Hybrids appeared to be intermediate. However, individual differences were significant, but group membership was not. Handling efficiency decreased with increasing prey length and was determined by individual and family effects. Hybrid females handled their prey as efficient as hybrid males. Small differences in beak morphology could not explain individual differences in prey-handling behaviour. The results of this study suggest that prey-handling in F₁-hybrids is not a postzygotic barrier which prevent gene flow between common and black redstarts in the wild.