Detection of Bemisia tabaci remains in predator guts using a sequence-characterized amplified region marker

Bemisia tabaci (Gennadius) (Homoptera: Aleyrodidae) B biotype is an invasive species (biotype) in China. In order to understand the role that native natural enemies might play in its control, techniques were developed for detecting B. tabaci DNA within the gut of predators. A species-specific DNA fragment, ca. 350 bp, was identified by random amplified polymorphic DNA analysis. This fragment was absent in other closely related or co-occurring prey species, cotton, and other select predator species. After cloning and sequencing the fragment, one pair of sequence-characterized amplified region (SCAR) primers was developed, which amplified a single band of 240 bp. Specificity tests performed with the primers showed the presence of the 240-bp band for B. tabaci in all developmental stages and both sexes, in adult Propylaea japonica (Thunberg) (Coleoptera: Coccinellidae) fed on B. tabaci nymphs in the laboratory, and in predators collected in cotton fields. Following consumption of a single red-eyed B. tabaci nymph, prey DNA was detectable in 100% of P. japonica at t = 0, decreasing to 20% after 12 h of digestion, and no B. tabaci DNA detected at t = 24 h. In total, we analyzed the gut contents of 185 field-collected predators, representing four different orders. All nine field-collected predator species (namely, P. japonica, Harmonia axyridis, Scymnus hoffmanni, Coccinella septempunctata, Orius sauteri, Chrysopa pallens, Chrysopa formosa, Erigonnidium graminicolum, and Neoscona doenitzi) contained DNA from B. tabaci and are assumed predators of this pest insect. Overall, the B. tabaci was eaten by more than 50% of field-collected predator individuals, including larvae of the coccinellids (P. japonica and H. axyridis) and lacewings (C. pallens and C. formosa) and adults of O. sauteri and the spiders (E. graminicolum and N. doenitzi). There was a trend of a higher percentage of larval than adult coccinellids and lacewings that preyed on B. tabaci in the field. This study provides a framework for the future use of molecular gut content analysis in arthropod conservation ecology and food web research, with considerable potential for quantifying threats to invasive or endemic pest species in China and elsewhere.     

Developmental temperatures and phenotypic plasticity in reptiles: a systematic review and meta‐analysis

Early environments can profoundly influence an organism in ways that persist over its life. In reptiles, early thermal environments (nest temperatures) can impact offspring phenotype and survival in important ways, yet we still lack an understanding of whether general trends exist and the magnitude of impact. Understanding these patterns is important in predicting how climate change will affect reptile populations and the role of phenotypic plasticity in buffering populations. We compiled data from 175 reptile studies to examine, and quantify, the effect of incubation temperature on phenotype and survival. Using meta‐analytic approaches (standardized mean difference between incubation treatments, Hedges' g), we show that across all trait types examined there is, on average, a moderate to large magnitude of effect of incubation temperatures (absolute effect: |g| = 0.75). Unsurprisingly, this influence was extremely large for incubation duration, as predicted, with warmer temperatures decreasing incubation time overall (g = −8.42). Other trait types, including behaviour, physiology, morphology, performance, and survival experienced reduced, but still mostly moderate to large effects, with particularly strong effects on survival. Moreover, the impact of incubation temperature persisted at least one‐year post‐hatching, suggesting that these effects have the potential to impact fitness in the long term. The magnitude of effect increased as the change in temperature increased (e.g. 6°C versus 2°C) in almost all cases, and tended to decrease when temperatures of the treatments fluctuated around a mean temperature compared to when they were constant. The effect also depended on the mid‐temperature of the comparison, but not in consistent ways, with some traits experiencing the greatest effects at extreme temperatures, while others did not. The highly heterogeneous nature of the effects we observe, along with a large amount of unexplained variability, indicates that the shape of reaction norms between phenotype and temperature, along with ecological and/or experimental factors, are important when considering general patterns. Our analyses provide new insights into the effects of incubation environments on reptile phenotype and survival and allow general, albeit coarse, predictions for taxa experiencing warming nest temperatures under climatic change.     

Utilization of granular solidification during terrestrial locomotion of hatchling sea turtles

Biological terrestrial locomotion occurs on substrate materials with a range of rheological behaviour, which can affect limb-ground interaction, locomotor mode and performance. Surfaces like sand, a granular medium, can display solid or fluid-like behaviour in response to stress. Based on our previous experiments and models of a robot moving on granular media, we hypothesize that solidification properties of granular media allow organisms to achieve performance on sand comparable to that on hard ground. We test this hypothesis by performing a field study examining locomotor performance (average speed) of an animal that can both swim aquatically and move on land, the hatchling Loggerhead sea turtle (Caretta caretta). Hatchlings were challenged to traverse a trackway with two surface treatments: hard ground (sandpaper) and loosely packed sand. On hard ground, the claw use enables no-slip locomotion. Comparable performance on sand was achieved by creation of a solid region behind the flipper that prevents slipping. Yielding forces measured in laboratory drag experiments were sufficient to support the inertial forces at each step, consistent with our solidification hypothesis.     

Direct and Indirect Effects of Fire on Eastern Box Turtles

Prescribed fire is an increasingly important management tool for eastern deciduous forests, but relativity little is known about the direct effects of fire on the eastern box turtle (Terrapene carolina carolina). We used very high frequency (VHF) transmitters to monitor mortality, movement, and spatial ecology of 118 box turtles in response to 17 prescribed fires across 4 seasons and 3 sites in east Tennessee, USA, during 2016–2018. Annual survival of box turtles that experienced a prescribed fire event was lower (0.87 ± 0.04 [SE]) than turtles that did not (0.98 ± 0.01) and was negatively correlated with fire intensity, fire temperature the turtle experienced, and litter depth. All prescribed fire-related mortalities occurred during the early (Apr–May, n = 5) or late growing season (Sep–Oct, n = 1). Fourteen percent of box turtles we captured exhibited damage to their carapace from previous fire events. Box turtles that survived prescribed fires were in microsites that did not burn, moved to unburned areas during the fire, or burrowed following ignition. Home range size was similar before and after burns and sinuosity of movements did not differ in burned or unburned areas. Our results indicate that though box turtles are susceptible to prescribed fire during their active season, they have behavioral and physical traits that reduce the direct effects of prescribed fire. Prescribed fire practitioners should be aware of the risks of fire, particularly during the active season. We suggest managers consider altering prescribed fire intensity, seasonality, and firing pattern to minimize risk of direct effects where box turtles are of concern. © 2020 The Wildlife Society.     

Performance in three shell functions predicts the phenotypic distribution of hard‐shelled turtles

Adaptive landscapes have served as fruitful guides to evolutionary research for nearly a century. Current methods guided by landscape frameworks mostly utilize evolutionary modeling (e.g., fitting data to Ornstein–Uhlenbeck models) to make inferences about adaptive peaks. Recent alternative methods utilize known relationships between phenotypes and functional performance to derive information about adaptive landscapes; this information can then help explain the distribution of species in phenotypic space and help infer the relative importance of various functions for guiding diversification. Here, data on performance for three turtle shell functions–strength, hydrodynamic efficiency, and self‐righting ability–are used to develop a set of predicted performance optima in shell shape space. The distribution of performance optima shows significant similarity to the distribution of existing turtle species and helps explain the absence of shells in otherwise anomalously empty regions of morphospace. The method outperforms a modeling‐based approach in inferring the location of reasonable adaptive peaks and in explaining the shape of the phenotypic distributions of turtle shells. Performance surface‐based methods allow researchers to more directly connect functional performance with macroevolutionary diversification, and to explain the distribution of species (including presences and absences) across phenotypic space.     

An experimental study of 226Ra and 45Ca accumulation from the aquatic medium by freshwater turtles (fam. Chelidae) under varying Ca and Mg water concentrations

Snapping turtles Elseya dentata (Gray) from Magela Creek, Northern Territory, were exposed under laboratory conditions for up to 30 days to waters resembling the inorganic composition of Magela Creek water during the Wet season, with background and elevated Ca and Mg concentrations, that were labelled with ²²⁶Ra and ⁴⁵Ca. The resulting concentrations of ⁴⁵Ca in muscle, skin, gut, liver, shell bone and leg bone of E. dentata equilibrated or approached equilibrium by 12–18 days. Among the experiments, the concentrations of ⁴⁵Ca in all six tissues were inversely related to turtle mass. An increase in the Ca water concentration by a factor of 15 increased the ⁴⁵Ca concentration in all six tissues. The arithmetic factors of increase in the concentration in each tissue were proportional or more than proportional to the factor of increase in Ca water concentration; this factor was highest for muscle tissue (26.6). An increase in the Mg water concentration by a factor of 48 reduced the ⁴⁵Ca concentration in all tissues except skin where it increased. The concentration of ²²⁶Ra in each tissue (except the gut) was positively related to its ⁴⁵Ca concentration and inversely related to turtle mass in muscle, skin and liver. With the exception of the skin, the increased Ca water concentration did not reduce the ²²⁶Ra in the tissues but increased the ²²⁶Ra concentration in bone and muscle. The increased Mg water concentration had an inverse effect on the ²²⁶Ra concentrations in all tissues except shell. With the exception of the skin the effects of increased Ca and Mg water concentrations and turtle size on ²²⁶Ra concentrations in the tissues of E. dentata were similar to their effects on ⁴⁵Ca tissue concentrations, indicating the similar metabolic behaviour of ²²⁶Ra and ⁴⁵Ca in E. dentata.Exposures of the species Elseya latisternum (Gray), Emydura signata (Ahl) and Chelodina longicollis (Shaw), which are the same or closely related to species reported to occur in Magela Creek, to ⁴⁵Ca-labelled Sydney tap water for 7 days demonstrated their ability to also accumulate ⁴⁵Ca from their aquatic medium. The patterns of ⁴⁵Ca concentrations in the tissues of these species indicated that they were inversely related to turtle mass, as demonstrated in E. dentata. The concentrations of ⁴⁵Ca accumulated in the tissues were also comparable to those found in single specimens of E. dentata and E. victoriae (Gray) that were exposed for 7 days to simulated Magela Creek water. The data also indicated the larger long-necked C. longicollis accumulated less ⁴⁵Ca per gram of tissue than similar-sized, short-necked species E. signata and E. latisternum, suggesting that long-necked turtles from Magela Creek would accumulate less ²²⁶Ra from their aquatic medium than similar-sized short-necked species.The capacity of E. dentata to accumulate ²²⁶Ra from the aquatic medium is about two orders of magnitude less than that of the tissue of the freshwater mussel Velesunio angasi (Sowerby) exposed under similar experimental conditions.     

Mixed-stock aging analysis reveals variable sea turtle maturity rates in a recovering population

Quantifying demographic parameters and variable vital rates, such as somatic growth rates, time to maturity, and reproductive longevity, is important for effective management of threatened and endangered populations such as sea turtles (Cheloniidae). To address these knowledge gaps, we applied skeletochronology to analyze and compare somatic growth rates and variation in life-history traits such as age and size at sexual maturity for 65 green turtles (Chelonia mydas) in the eastern Pacific Ocean (EP), along the west coast of the United States; turtles belonged to ≥2 nesting subpopulations that differed in body size (mean nesting size). Green turtles in the EP spend approximately 5 years in the oceanic stage before recruiting to nearshore habitats, males may be smaller and younger than females at maturation (x̅ = 17.7 ± 5.5 yr vs. 28.0 ± 8.2 yr), and younger age at sexual maturity was associated with smaller size at sexual maturity, suggesting that mean nesting body size may be reflective of maturation timing for subpopulations. Smaller body sizes for females nesting at Michoacán, Mexico (continental) rookeries, yielded a younger predicted age at sexual maturity (x̅ = ~17 yr) compared to females from Revillagigedo Islands, Mexico rookeries, which displayed larger body sizes and older age at sexual maturity (x̅ = ~30 yr). We consider possible mechanisms driving the observed divergence in life-history traits, including the possibility that earlier maturation (reduced generation length) for turtles in the Michoacán nesting subpopulation may be a response to intense harvesting in the past 50 years, and consideration of such anthropogenic impacts is warranted by population managers. Finally, our results indicate green turtles moved into nearshore neritic habitats at a young age (4–6 yr), emphasize the importance of protecting neritic habitats along the southwestern United States and northwestern Mexican coasts, and encourage the incorporation of variable maturation time in population recovery assessments.     

The olfactory receptor gene repertoires in secondary-adapted marine vertebrates: evidence for reduction of the functional proportions in cetaceans

An olfactory receptor (OR) multigene family is responsible for the well-developed sense of smell possessed by terrestrial tetrapods. Mammalian OR genes had diverged greatly in the terrestrial environment after the fish-tetrapod split, indicating their importance to land habitation. In this study, we analysed OR genes of marine tetrapods (minke whale Balaenoptera acutorostrata, dwarf sperm whale Kogia sima, Dall's porpoise Phocoenoides dalli, Steller's sea lion Eumetopias jubatus and loggerhead sea turtle Caretta caretta) and revealed that the pseudogene proportions of OR gene repertoires in whales were significantly higher than those in their terrestrial relative cattle and also in sea lion and sea turtle. On the other hand, the pseudogene proportion of OR sequences in sea lion was not significantly higher compared with that in their terrestrial relative (dog). It indicates that secondary perfectly adapted marine vertebrates (cetaceans) have lost large amount of their OR genes, whereas secondary-semi-adapted marine vertebrates (sea lions and sea turtles) still have maintained their OR genes, reflecting the importance of terrestrial environment for these animals.     

Experience pays: offspring survival increases with female age

Life-history theory predicts that, in long-lived organisms, effort towards reproduction will increase with age, and research from oviparous vertebrates largely supports this prediction. In reptiles, where parental care occurs primarily via provisioning of the egg, older females tend to produce larger eggs, which in turn produce larger hatchlings that have increased survival. We conducted an experimental release study and report that maternal age positively influences offspring survivorship in the painted turtle (Chrysemys picta) and predicts offspring survival at least as well as hatchling body size does. These data suggest that, although increasing hatchling size is a major component of reproductive success in older individuals, other factors also contribute.     

Reconstruction of paternal genotypes over multiple breeding seasons reveals male green turtles do not breed annually

For species of conservation concern, knowledge of key life-history and demographic components, such as the number and sex ratio of breeding adults, is essential for accurate assessments of population viability. Species with temperature-dependent sex determination can produce heavily biased primary sex ratios, and there is concern that adult sex ratios may be similarly skewed or will become so as a result of climate warming. Prediction and mitigation of such impacts are difficult when life-history information is lacking. In marine turtles, owing to the difficultly in observing males at sea, the breeding interval of males is unknown. It has been suggested that male breeding periodicity may be shorter than that of females, which could help to compensate for generally female-biased sex ratios. Here we outline how the use of molecular-based paternity analysis has allowed us, for the first time, to assess the breeding interval of male marine turtles across multiple breeding seasons. In our study rookery of green turtles (Chelonia mydas), 97% of males were assigned offspring in only one breeding season within the 3-year study period, strongly suggesting that male breeding intervals are frequently longer than 1year at this site. Our results also reveal a sex ratio of breeding adults of at least 1.3 males to each female. This study illustrates the utility of molecular-based parentage inference using reconstruction of parental genotypes as a method for monitoring the number and sex ratio of breeders in species where direct observations or capture are difficult.