Testing an ecophysiological mechanism of morphological plasticity in pupfish and its relevance to conservation efforts for endangered Devils Hole pupfish

Imperiled species that have been translocated or established in captivity can show rapid alterations in morphology and behavior, but the proximate mechanisms of such phenotypic changes are rarely known. Devils Hole pupfish (Cyprinodon diabolis) are endemic to a single desert pool and are characterized by a small body, large head and eyes, and lack of pelvic fins. To lessen the risk of extinction, additional populations of C. diabolis were established in artificial refuges. Yet, pupfish in these refuges rapidly shifted to a larger body, smaller head and eyes, and greater body depth. Here we examined how food availability and temperature, which differ between these habitats, influence morphological development in closely related Amargosa River pupfish (Cyprinodon nevadensis amargosae). We were interested in knowing whether these environmental factors could developmentally shift Amargosa River pupfish toward the morphology typical of pupfish in Devil\u27s Hole. By regulating food ration, we created groups of pupfish with low, medium and high growth rates. Pupfish with low growth showed proportionally larger head and eyes, smaller body depth, and reduction in pelvic fin development. Elevated temperature further inhibited pelvic fin development in all treatments. Pupfish in the low growth group also showed reduced levels of thyroid hormone, suggesting a possible physiological mechanism underlying these morphological changes. To test this mechanism further, pupfish were reared with goitrogens to pharmacologically inhibit endogenous thyroid hormone production. Pupfish given goitrogens developed larger heads and eyes, shallower bodies, and reduced pelvic fins. Taken together, our results suggest that changes in environmental factors affecting the growth and thyroid hormone status of juvenile pupfish may play a developmental role in generating the morphological differences between C. diabolis in Devil\u27s Hole and the refuges. These findings illustrate the need to incorporate a mechanistic understanding of phenotypic plasticity into conservation strategies to preserve imperiled fishes

Evidence for olfactory learning in procellariiform seabird chicks

Burrow nesting procellariiform seabirds use olfactory cues for both foraging and nest recognition. As chicks, burrow nesters develop in the dark, but are exposed to both prey-related and individual-specific scents through contact with their parents. This exposure suggests that chicks may have the opportunity to learn odors while still in the nest. In this study, we examined whether exposure to odorants during development might influence olfactory search behavior expressed later in life. To test this idea, we exposed eggs of thin-billed prions Pachyptila belcheri to a rosy-scented novel odor (phenyl ethyl alcohol, PEA) or a control (water) just before hatching; chicks were then tested with these odors in a simple wind tunnel. Prior to fledgling, subjects who had received pre-exposure to PEA displayed head sweeps nearly twice as frequently as control birds did when presented with PEA. This study demonstrates that under natural rearing conditions, procellariiforms learn odor characteristics of their rearing environment in the nest

Marine plastic debris emits a keystone infochemical for olfactory foraging seabirds.

Plastic debris is ingested by hundreds of species of organisms, from zooplankton to baleen whales, but how such a diversity of consumers can mistake plastic for their natural prey is largely unknown. The sensory mechanisms underlying plastic detection and consumption have rarely been examined within the context of sensory signals driving marine food web dynamics. We demonstrate experimentally that marine-seasoned microplastics produce a dimethyl sulfide (DMS) signature that is also a keystone odorant for natural trophic interactions. We further demonstrate a positive relationship between DMS responsiveness and plastic ingestion frequency using procellariiform seabirds as a model taxonomic group. Together, these results suggest that plastic debris emits the scent of a marine infochemical, creating an olfactory trap for susceptible marine wildlife

Phenotype management: a new approach to habitat restoration

The goal of habitat restoration is to provide environmental conditions that promote the maintenance and growth of target populations. But rarely is it considered how the allocation of resources influences the diversity of phenotypes in these populations. Here we present a framework for considering how habitat restoration can shape the development and expression of phenotypes. We call this approach phenotype management as it entails restoring the resources in a habitat to manage phenotypic diversity. Phenotype management is achieved by manipulating the spatial and temporal distribution of resources to alter the degree of competition among individuals. Differences in competition, in turn, lead to changes in phenotypic and life history expression that affect population parameters including demography and effective population size (Ne). To illustrate how phenotype management can be applied, we explore how resource distributions shape variation in phenotypes in two imperiled fishes, Pacific salmon and desert pupfish. In both examples, modulating male reproductive phenotypes changes the allocation of reproductive success among population members to subsequently affect Ne. These examples further demonstrate that whether to increase or decrease phenotypic diversity depends on the primary conservation pressures faced by the species

Tuning a nose to forage: Evidence for olfactory learning in a procellariiform seabird chicks

Burrow nesting procellariiform seabirds use olfactory cues for both foraging and nest recognition. As chicks, burrow nesters develop in the dark, but are exposed to both prey-related and individual-specific scents through contact with their parents. This exposure suggests that chicks may have the opportunity to learn odours while still in the nest. In this study, we examined whether exposure to odourants during development might influence olfactory search behaviour expressed later in life. To test this idea, we exposed eggs of thin-billed prions Pachyptila belcheri to a rosy-scented novel odour (phenyl ethyl alcohol, PEA) or a control (water) just before hatching; chicks were then tested with these odours in a simple wind tunnel. Prior to fledging, subjects who had received pre-exposure to PEA displayed head sweeps nearly twice as frequently as control birds did when presented with PEA. This study demonstrates that under natural rearing conditions, procellariiforms learn odour characteristics of their rearing environment in the nest

Responses of common diving petrel chicks (Pelecanoides urinatrix) to burrow and colony specific odours in a simple wind tunnel

Researchers have previously assumed that common diving petrels (Pelecanoides urinatrix) have a limited sense of smell since they have relatively small olfactory bulbs. A recent study, however, showed that adult diving petrels prefer the scent of their own burrow compared to burrows of other diving petrels, implying that personal scents contribute to the burrow’s odour signature. Because diving petrels appear to be adapted to use olfaction in social contexts, they could be a useful model for investigating how chemically mediated social recognition develops in birds. A first step is to determine whether diving petrel chicks can detect familiar and unfamiliar odours. We compared behavioural responses of chicks to three natural stimuli in a wind tunnel: soil collected from their burrow or colony, and a blank control. During portions of the experiment, chicks turned the least and walked the shortest distances in response to odours from the nest, which is consistent with their sedentary behaviour within the burrow. By contrast, behaviours linked to olfactory search increased when chicks were exposed to blank controls. These results suggest that common diving petrel chicks can detect natural olfactory stimuli before fledging, and lay the foundation for future studies on the role of olfaction in social contexts for this species

Evidence for hydrodynamic orientation by spiny lobsters in a patch reef environment

Western Atlantic spiny lobsters (Panulirus argus) are superb underwater navigators. Spiny lobsters perform dramatic seasonal offshore migrations and have also been shown to locate and home to specific den sites within the elaborate coral reef environment in which they live. How these animals perform such complex orientation tasks is not known. The study reported here was designed to explore the sensory mechanisms that spiny lobsters use to orient in and around a familiar patch reef environment. Our results show that, in the absence of visual cues, lobsters displaced a short (50 m) distance off the reef do not initially (i.e. within 20 min) travel towards their dens or return to the patch reef where their dens are located. Instead, the headings lobsters follow are significantly correlated to the direction of local hydrodynamic cues and, specifically, to the direction of approaching wave surge. Results from ultrasonic tracking experiments over longer periods (24 h) suggest that displaced lobsters are able to relocate the reef where they were captured, even without visual cues. These results suggest that hydrodynamic cues may provide useful and immediate directional information to lobsters within the local environment of the home reef

Exogenous vasotocin alters aggression during agonistic exchanges in male Amargosa River pupfish \u3cem\u3e(Cyprinodon nevadensis amargosae)\u3c/em\u3e

Pupfishes in the Death Valley region have rapidly differentiated in social behaviors since their isolation in a series of desert streams, springs, and marshes less than 20,000 years ago. These habitats can show dramatic fluctuations in ecological conditions, and pupfish must cope with the changes by plastic physiological and behavioral responses. Recently, we showed differences among some Death Valley populations in brain expression of arginine vasotocin (AVT). As AVT regulates both hydromineral balance and social behaviors in other taxa, these population differences may indicate adaptive changes in osmoregulatory and/or behavioral processes. To test whether AVT is relevant for behavioral shifts in these fish, here we examined how manipulations to the AVT system affect agonistic and reproductive behaviors in Amargosa River pupfish (Cyprinodon nevadensis amargosae). We administered exogenous AVT (0.1, 1, and 10 Ag/g body weight) and an AVP V1 receptor antagonist (Manning compound, 2.5 μg/g body weight) intraperitoneally to males in mixed-sex groups in the laboratory. We found that AVT reduced the initiation of aggressive social interactions with other pupfish but had no effect on courtship. The effects of AVT were confirmed in males in the wild where AVT (1 Ag/g body weight) reduced the aggressive initiation of social interactions and decreased aggressive responses to the behavior of other males. Combined, these results show that AVT can modulate agonistic behaviors in male pupfish and support the idea that variation in AVT activity may underlie differences in aggression among Death Valley populations

Evidence that thyroid hormone induces olfactory cellular proliferation in salmon during a sensitive period for imprinting

Salmon have long been known to imprint and home to natal stream odors, yet the mechanisms driving olfactory imprinting remain obscure. The timing of imprinting is associated with elevations in plasma thyroid hormone levels, with possible effects on growth and proliferation of the peripheral olfactory system. Here, we begin to test this idea by determining whether experimentally elevated plasma levels of 3,5,3′-triiodothyronine (T3) influence cell proliferation as detected by the 5-bromo-2′-deoxyuridine (BrdU) cell birth-dating technique in the olfactory epithelium of juvenile coho salmon (Oncorhynchus kisutch). We also explore how natural fluctuations in thyroxine (T4) relate to proliferation in the epithelium during the parr–smolt transformation. In both studies, we found that BrdU labeled both single and clusters of mitotic cells. The total number of BrdU-labeled cells in the olfactory epithelium was significantly greater in fish with artificially elevated T3 compared with placebo controls. This difference in proliferation was restricted to the basal region of the olfactory epithelium, where multipotent progenitor cells differentiate into olfactory receptor neurons. The distributions of mitotic cluster sizes differed significantly from a Poisson distribution for both T3 and placebo treatments, suggesting that proliferation tends to be non-random. Over the course of the parr–smolt transformation, changes in the density of BrdU cells showed a positive relationship with natural fluctuations in plasma T4. This relationship suggests that even small changes in thyroid activity can stimulate the proliferation of neural progenitor cells in the salmon epithelium. Taken together, our results establish a link between the thyroid hormone axis and measurable anatomical changes in the peripheral olfactory system