Innate and Learned Predator Recognition Mediated by Chemical Signals in Eurycea nana

Effective and efficient predator recognition and avoidance are essential for the persistence of prey populations, especially in habitats where non-native predators have been introduced. Predator recognition studies are commonly couched within a learned or innate dichotomous framework; however, characteristics of some systems or species could favor innate recognition combined with the ability to alter avoidance responses based on experience with predators. Eurycea nana is a fully aquatic salamander inhabiting a system with a diverse, yet temporally stable, community of native and non-native opportunistically foraging fish predators. To examine predator recognition, we examined avoidance responses (decreased activity) of predator-naïve (first-generation, captive-reared) and predator-experienced (recently collected) E. nana to the chemical cues of a native predator, a non-native predator, a non-predator, and a blank control. Both predator-naïve and predator-experienced E. nana significantly lowered activity in response to the native fish predator when compared with a blank control. Interestingly, predator-naïve E. nana decreased activity in response to the non-native fish predator while predator-experienced E. nana did not. These results indicate that while there is an innate component to predator recognition in E. nana , experience and risk assessment may also be important.     

Evolving possibilities: postembryonic axial elongation in salamanders with biphasic (Eurcyea cirrigera,Eurycea longicauda,Eurycea quadridigitata) and paedomorphic life cycles (Eurycea nana and Ambystoma mexicanum)

Vaglia, JL., White, K, and Case, A. 2012. Evolving possibilities: postembryonic axial elongation in salamanders with biphasic (Eurcyea cirrigera, Eurycea longicauda, Eurycea quadridigitata) and paedomorphic life cycles (Eurycea nana and Ambystoma mexicanum). —Acta Zoologica (Stockholm) 93 : 2–13. Typically, the number of vertebrae an organism will have postembryonically is determined during embryogenesis via the development of paired somites. Our research investigates the phenomenon of postembryonic vertebral addition in salamander tails. We describe body and tail growth and patterns of postsacral vertebral addition and elongation in context with caudal morphology for four plethodontids (Eurycea) and one ambystomatid. Eurycea nana and Ambystoma mexicanum have paedomorphic life cycles; Eurcyea cirrigera, Eurycea longicauda and Eurycea quadridigitata are biphasic. Specimens were collected, borrowed and/or purchased, and cleared and stained for bone and cartilage. Data collected include snout‐vent length (SVL), tail length (TL), vertebral counts and centrum lengths. Eurycea species with biphasic life cycles had TLs that surpassed SVL following metamorphosis. Tails in paedomorphic species elongated but rarely exceeded body length. Larger TLs were associated with more vertebrae and longer vertebrae in all species. We observed that rates of postsacral vertebral addition varied little amongst species. Regional variation along the tail becomes prominent following metamorphosis in biphasic developers. In all species, vertebrae in the posterior one‐half of the tail taper towards the tip. We suggest that a developmental link might exist between the ability to continually add vertebrae and regeneration in salamanders.     

Computer-Assisted Photo Identification Outperforms Visible Implant Elastomers in an Endangered Salamander,Eurycea tonkawae

Despite recognition that nearly one-third of the 6300 amphibian species are threatened with extinction, our understanding of the general ecology and population status of many amphibians is relatively poor. A widely-used method for monitoring amphibians involves injecting captured individuals with unique combinations of colored visible implant elastomer (VIE). We compared VIE identification to a less-invasive method – computer-assisted photographic identification (photoID) – in endangered Jollyville Plateau salamanders (Eurycea tonkawae), a species with a known range limited to eight stream drainages in central Texas. We based photoID on the unique pigmentation patterns on the dorsal head region of 1215 individual salamanders using identification software Wild-ID. We compared the performance of photoID methods to VIEs using both ‘high-quality’ and ‘low-quality’ images, which were taken using two different camera types and technologies. For high-quality images, the photoID method had a false rejection rate of 0.76% compared to 1.90% for VIEs. Using a comparable dataset of lower-quality images, the false rejection rate was much higher (15.9%). Photo matching scores were negatively correlated with time between captures, suggesting that evolving natural marks could increase misidentification rates in longer term capture-recapture studies. Our study demonstrates the utility of large-scale capture-recapture using photo identification methods for Eurycea and other species with stable natural marks that can be reliably photographed.     

Prey Abundance, Intraguild Predators, Ants and the Optimal Egg-laying Strategy of a Furtive Predator

Larval performance can have a great influence on female oviposition choice, especially in insects where the newly hatched offspring are unable to move any great distance to find an appropriate food source. For furtive predators, like the predatory midge Aphidoletes aphidimyza which preys on aphids while simultaneously residing and remaining undetected within their colonies, oviposition behaviour is crucial because these slow moving offspring are restrained to their natal colony. Here we develop a new model for predicting the optimum number of eggs that a furtive predator should lay in an aphid colony, based on: (1) the number of available prey (aphids); (2) the protection from predation conferred by “hiding” in the colony and (3) the effects of interspecific and intraspecific competition. We also explore the effect of aphid attendance by ants on oviposition behavior. We compare model predictions with empirical field observations of the clutch sizes of A. aphidimyza in apple orchards. The simplest of the four models best fits the observed data and provides the first field evidence that a furtive predator adjusts its clutch size as a function of prey density. The slope of the relationship between clutch size and aphid number is quite close to that predicted by our models suggesting that intra-clutch competition is the main factor governing furtive aphid midge oviposition choice.     

Innate Predator Recognition and the Problem of Introduced Trout

Innate predator recognition typically only occurs when there is an evolutionary history between predator and prey. Predator introductions thus can pose a substantial threat to native fauna that rely heavily on inherent identification of predators. In permanent aquatic habitats prey often encounter a variety of predatory and non-predatory fish species, and the ability to distinguish between the two is essential to avoid wasted time and energy spent in unnecessary antipredatory efforts. Here, we present a study evaluating the ability of lab-reared larvae of an endangered fully aquatic salamander (hellbenders: Cryptobranchus alleganiensis ) to recognize chemical cues from native and introduced fish predators. We recorded responses of hellbender larvae to chemical stimuli from native and non-native predatory fishes, a non-predatory fish and a blank control. Eastern hellbender larvae ( C. a. alleganiensis ) significantly reduced activity in response to chemical stimuli from native predators ( Micropterus salmoides , Micropterus dolomieu , Ambloplites rupestris , Sander vitreus , and Cottus carolinae ), but responses to non-native rainbow ( Oncorhynchus mykiss ) and brown ( Salmo trutta ) trout were not significantly different from responses to the non-predatory control (redhorse sucker, Moxostoma spp.). Responses of larval Ozark hellbenders ( C. a. bishopi ) to brown trout were similar to that of the native fishes and different from the blank control, but responses to rainbow trout did not differ from the blank control. The generally weak responses of larval hellbenders to chemical cues from introduced predatory trout could lead to increased predation in the wild, which may have exacerbated the decline of hellbender populations.     

Managing the Effects of Introduced Predators on Hawaiian Endangered Seabirds

Introduced predators are one of the greatest threats facing seabirds worldwide. We investigated the effects of multiple introduced predators on 2 endangered seabirds, the Newell's shearwater (Puffinus newelli) and the Hawaiian petrel (Pterodroma sandwichensis), on the island of Kauaʻi, Hawaiʻi, USA. Between 2011 and 2017, we recorded 309 depredations of which 35.6% were by feral cats, 50.2% by black rats (Rattus rattus), 10.4% by pigs (Sus scrofa; feral pigs), and 3.9% by barn owls (Tyto alba). Cats were the most destructive of the predators because they killed more breeding adults than chicks, which had repercussions on breeding probability in following years. Cats and rats were also the most prevalent of all the predators, depredating birds at all of the sites under consideration regardless of how remote or inaccessible. We also considered the effectiveness of predator control over the study period. Reproductive success at all sites increased once predator control operations were in place and depredations by all species except barn owls decreased. Furthermore, we modeled population trajectories for all sites with and without predator control. Without predator control, population trajectories at all sites declined rapidly over 50 years. With predator control operations in place, populations at all sites increased; thus, controlling introduced predators at endangered seabird colonies is important for their management. © 2020 The Wildlife Society.     

Combined Effects of Virus, Pesticide, and Predator Cue on the Larval Tiger Salamander (Ambystoma tigrinum)

Emerging diseases and environmental contamination are two of the leading hypotheses for global amphibian declines. Yet few studies have examined the influence of contaminants on disease susceptibility, and even fewer have incorporated the role of natural stressors such as predation. We performed a factorial study investigating the interaction of the insecticide carbaryl, dragonfly predator cue, and the emerging pathogen Ambystoma tigrinum virus (ATV) on fitness correlates and disease susceptibility in tiger salamander larvae. Four week old larvae were exposed for 22 days in a 2 (0, 500 μg/l carbaryl) × 2 (control, predator cue water) × 2 (0, 1 × 10⁴ pfu ATV) factorial designed laboratory study. Results show significant impacts to survival of larvae for both virus and predator cue treatments, as well as an interactive effect between the two, in which predator cue strongly exacerbated disease-driven mortality. There was a clear pattern of reduced survival with the addition of stressors, with those where all three stressors were present exhibiting the worst effects (a decrease in survival from 93 to 60%). On those that survived, we also detected several sub-lethal impacts in mass, SVL, and development. Predator cue and pesticide treatments significantly reduced both SVL and mass. Virus and predator treatments significantly slowed development. Stressors also exhibited opposing effects on activity. Predator cue caused a significant reduction in activity, whereas virus caused a significant increase in activity over time. These results highlight the importance of examining combined natural and introduced stressors to understand potential impacts on amphibian species. Such stressors may contribute to the emergence of ATV in particular regions, raising concerns about the influence of pesticides on disease emergence in general.     

Eurycea bislineata (Green), the Two-Lined Salamander, a New Host of Myxidium serotinum Kudo & Sprague, 1940 (Myxosporida, Myxidiidae)

SYNOPSIS. Myxidium serotinum was found in 51 of 58 (87.9%) specimens of the two-lined salamander, Eurycea bislineata , from West Virginia. This constitutes a new host record. No specimens of the order Salientia, or other species of the order Caudata were infected. Eurycea bislineata appears to be the normal host of M. serotinum , which is specific for the gallbladder in a variety of amphibian hosts. Apparently, larval E. bislineata becomes infected with M. serotinum , and the parasite does not become a mature trophozoite until after the tadpoles metamorphose to the adult salamander. Certain host hormonal factors may be important to the maturation of M. serotinum.     

Generalization of Mimics Imperfect in Colour Patterns: The Point of View of Wild Avian Predators

Current research of imperfect mimicry brings ambiguous results. Experiments simulating more natural conditions rather than laboratory experiments show lower willingness of avian predators to attack less perfect mimics. We decided to simulate a natural situation by testing responses of wild‐caught adult avian predators (Great tit – Parus major) to variously perfect mimics of the red firebug (Pyrrhocoris apterus), which were in previous studies shown to elicit avoidance in Great tits. Presented mimics were perfect in all traits (firebug with its own colour pattern), imperfect in colour pattern (firebug with modified colour pattern), perfect in colour pattern, but imperfect in other visual traits (cockroach with firebug colour pattern), and imperfect in colour pattern as well as in other visual traits (cockroach with modified colour patterns). Modification of the pattern focused on the rounded spots on firebug's hemielytra, which is a conspicuous trait within the pattern. The pattern modification had no influence on the number of birds attacking the prey; nevertheless, birds spent more time observing the cockroaches that displayed the perfect firebug colour pattern than in the case of any other prey. Moreover, firebugs that displayed the perfect firebug colour pattern were observed for the shortest time (equal to that of the model – unmodified firebug). Cockroaches were attacked more often than firebugs, which suggest that birds were able to use additional visual cues (shape of legs and antennae) in prey recognition. Given these result, we conclude that differences in morphological traits characteristic for used prey taxa (true bugs, cockroaches) seem to be more important in the prey's protection than its colour pattern.     

Effect of Plant Growth Regulators on Agronomic Characteristics,Lint Quality,Pests, and Predators in Cotton

Field experiments were conducted with some commercial plant growth regulators (PGRs) to determine their effects on agronomic characteristics, pest densities, and predators when administered as a foliar spay on cotton at Adnan Menderes University Agricultural Research Center located in Aydin, Turkey, during the 2006 and 2007 cotton-growing seasons. The three commercial PGRs, Pix, Tonic, and Turbo pamuk, were sprayed at recommended doses and application time during the study. Application of PGRs significantly positively affected the yield, plant height, average number of open bolls, and predators, and significantly decreased the population densities of some economically important cotton pests. However, lint quality, ginning turnout, and average of seed cotton weight were not affected by the treatments. More yield was obtained in Pix- and Turbo pamuk-treated plots. The lowest densities of Bemisia tabaci, Frankliniella spp., and leaves infested with Liriomyza trifolii were recorded in Pix-treated plots. Although Turbo pamuk and Tonic numerically lowered the pest population densities compared to the control, the changes were not significant and these PGRs were not as effective as Pix. Furthermore, Empoasca spp. was not affected by the treatments. Populations of predators were not affected by the PGRs in Aranea orders, but were affected in Heteroptera, Neuroptera, Coleoptera, and Thysanoptera. Pix proved more suitable than others to producing resistance against pests and increasing the yields. PGRs neither enhanced any insect attack nor reduced predators in the study. Therefore, PGRs may be considered a component of Integrated Pest Management to provide higher yields in cotton.     

Sperm storage and degradation in the spermathecae of the salamander Eurycea Cirrigera

Spermathecae are exocrine glands in the roof of the female cloaca that store sperm. Cytological and histochemical data indicate that the one type of secretion into the lumen is a glycoprotein. After a period of stasis in the summer, production of the secretion is initiated in the fall, coincident with an increase in ovarian follicular size. By the time of maximal follicular development and most intense mating activity in March and April, the spermathecal epithelium is filled with secretory granules. The secretory material is released into the lumen, enveloping the sperm. Many sperm remain in the spermathecae after oviposition, and most of these sperm are degraded in the spermathecal epithelium or pass through interruptions in the spermathecal walls caused by desquamation. Sperm in contact with the stromal environment are phagocytized by leukocytes. Some sperm, however, may survive in the lumen until at least the following fall. These sperm retain normal cytology, but whether or not they remain fertile and intact until a subsequent ovipository cycle is unknown.     

Effect of Predators of Juvenile Rodents on the Spread of the Hantavirus Epidemic

Effects of predators of juvenile mice on the spread of the Hantavirus are analyzed in the context of a recently proposed model. Two critical values of the predation probability are identified. When the smaller of them is exceeded, the hantavirus infection vanishes without extinguishing the mice population. When the larger is exceeded, the entire mice population vanishes. These results suggest the possibility of control of the spread of the epidemic by introducing predators in areas of mice colonies in a suitable way so that such control does not kill all the mice but lowers the epidemic spread.     

Predator avoidance behaviour in the buffy-headed marmoset,Callithrix flaviceps

The predator avoidance behaviour of a free-ranging group of buffy-headed marmosets,Callithrix flaviceps, was recorded in detail during the course of a long-term study of behavioural ecology at the Fazenda Montes Claros, southeastern Brazil. Four distinct patterns of predator avoidance behaviour, each with specific vocalisations, were recognised and are described here. The selection and use of sleeping sites by the study group are also described. An analysis of the records indicates that these small monkeys are generally most vulnerable to predation by aerial raptors. Variations in the frequency of alarm calls also indicate that the marmosets tend to be more vigilant at higher levels in the forest and when the leaf cover is less extensive. The implications of group size and social structure for both the evolution and the efficacy of the anti-predator behaviour of marmosets are also discussed.     

Modification of genital kidney nephrons for sperm transport in a plethodontid salamander,Eurycea longicauda

Salamanders possess kidneys with two distinct regions: a caudal pelvic portion and cranial genital portion. Nephrons of the pelvic region are responsible for urine formation and transport. Nephrons of the genital region transport sperm from testes to Wolffian ducts; however, nephrons of the genital region possess all the same functional regions found in pelvic kidney nephrons that are involved with urine formation and transport (renal corpuscles, proximal tubules, distal tubules, and collecting ducts). Morphological similarities between pelvic and genital regions stimulated past researchers to hypothesize that nephrons of genital kidneys possess dual function; that is, sperm transport and urine formation/transport. Considering size of glomeruli is directly related to the total amount of blood plasma filtered into the Bowman's space, we tested the hypothesis that nephrons of genital kidneys have reduced urine formation function by comparing glomerular size between nephrons of pelvic and genital kidney regions in Eurycea longicauda with general histological techniques. Light microscopy analysis revealed that glomeruli of pelvic kidneys were significantly larger than those measured from genital kidneys. Transmission electron microscopy analysis also revealed modifications in genital kidney nephrons when compared to pelvic kidney nephrons that suggested a decrease in urine formation function in genital kidneys. Such modifications included a decrease in basal and lateral plasma membrane folding in genital kidney proximal and distal tubules compared to that of pelvic kidney proximal and distal tubules. Genital kidney proximal tubules were also ciliated, which was not observed in pelvic kidney proximal tubules. In conclusion, although structurally similar at the histological level, it appears that nephrons of genital kidneys have decreased urine formation function based on glomerular size comparison and nephron ultrastructure.