Chemosensory assessment of rival body size is based on chemosignal concentration in male Spanish terrapins

Assessment of the fighting ability of potential opponents is an essential skill to minimize the costs of agonistic interactions between males. Previous research showed that chemical cues released in the water by male turtles may convey information about body size, which is important for intrasexual competition. However, the mechanistic basis of such chemical signaling of body size remains poorly understood. Here, we aimed to experimentally examine whether the release of chemosignals is quantitatively or qualitatively dependent on body size in male Spanish terrapins Mauremys leprosa. We compared the time that turtles spent in a pool with clean water versus water containing chemical stimuli of conspecific males of different body sizes at two different concentrations (“diluted” or “undiluted”). Male terrapins avoided water with chemicals secreted by relatively larger males when these chemicals were undiluted, but not after the chemical stimuli were diluted. In contrast, male terrapins did not avoid chemicals of relatively smaller males in any treatment. Thus, male M. leprosa may assess the size of their rivals on the basis of the concentration or the amounts of their chemical cues released into the water and consequently avoid occupying these ponds with higher concentrations of chemicals. This study gives important hints about the mechanism of chemical signaling in freshwater turtles and demonstrates that male turtles may discriminate different concentrations of chemosignals of conspecifics and modify their behavior accordingly. Likewise, our results support the notion that relative body size is a key factor during male interactions in Spanish terrapins.     

Chemical rival recognition decreases aggression levels in male Iberian wall lizards, <Emphasis Type="Italic">Podarcis hispanica</Emphasis>

In an agonistic interaction, the assessment of the probable outcome of future encounters with the same individuals may be the best way of decreasing costs of fighting, but this may only be accomplished if animals are able to recognize individual conspecifics. We staged encounters between male lizards, Podarcis hispanica, to examine whether odoriferous cues are involved in rival recognition during agonistic interactions. We experimentally manipulated the odour of intruding males, creating familiar males with their own odour or bearing odours of unfamiliar males, and unfamiliar males bearing unfamiliar odours or odours of familiar males. The results showed that when familiar males were impregnated with scents from unfamiliar males, they elicited an aggressive response by resident unmanipulated males similar to that observed for a new unfamiliar male with unfamiliar odour. This suggests that resident males were unable to recognize familiar males when their own scents were removed. In contrast, responding males were less aggressive towards familiar males impregnated with their own odour and towards unfamiliar males impregnated with scents of familiar males, suggesting that when two males have already interacted, their scents become familiar for both males, and that the detection in successive encounters of the familiar scent suffices to reduce the aggressive response of territorial males. Therefore, recognition mechanisms based on chemical cues during agonistic encounters may contribute to reducing the intensity and the costs of fighting in P. hispanica and may play an important role in the organization of their social system.     

Chemosensory discrimination of familiar and unfamiliar conspecifics by lizards: implications of field spatial relationships between males

The ability of territorial lizards to discriminate between scents of neighbors and non-neighbors might contribute to decreasing the costs of aggressive interactions. To test this hypothesis, we conducted a field study to analyze the spatial relationships between male Iberian rock-lizards, Lacerta monticola. We then used the same individuals in a laboratory experiment to test whether male lizards can use chemical cues to discriminate between familiar conspecific males (those whose home ranges overlapped) and unfamiliar conspecific males (those whose home ranges did not overlap, and whose home range centers were at least 50 m apart). Differences in tongue-flick rates in the presence of chemical cues suggested that male L. monticola discriminated between odors of familiar and unfamiliar males. The behavioral responses were also dependent on relative differences in body size between the responding male and the unfamiliar male that donated the scent: There was a significant negative correlation between tongue-flick rates emitted in cages of unfamiliar males and the body size differences between males. In contrast, when the donor of the scent was a familiar male, the tongue-flick rate was not dependent on body size differences. These results are compatible with individual discrimination through chemical cues in male L. monticola.     

Chemical communication in green and golden bell frogs: do tadpoles respond to chemical cues from dead conspecifics?

Captive bred animals often lack the ability of predator recognition and predation is one of the strongest causes of failure of breed and release projects. Several tadpole and fish species respond defensively to chemical cues from injured or dead conspecifics, often referred to as alarm pheromones. In natural conditions and in species that school, the association of chemical cues from predators to alarm pheromones released by attacked conspecifics may lead to the learning of the predator-related danger without experiencing an attack. In the laboratory, this chemical communication can also be used in associative learning techniques to teach naïve tadpoles to avoid specific predators and improve survivorship of released animals. In our experimental trials, tadpoles of the threatened green and golden bell frog (Litoria aurea) did not avoid or decrease their activity when exposed to solutions of conspecific macerate, suggesting that the chemicals released into the water by dead/injured conspecifics do not function as an alarm pheromone. This non-avoidance of dead conspecific chemicals may explain why green and golden bell frog tadpoles have seemingly not developed any avoidance behaviour to the presence of introduced mosquito fish, and may render attempts to teach naïve tadpoles to avoid this novel predator more difficult.     

Field presentation of male secretions alters social display in Sceloporus virgatus but not S. undulatus lizards

Lizards have communicative displays involving primarily vision and chemicals, and recent work suggests trade-offs between these two modalities. In reptiles, little work assesses effects of conspecific chemicals on subsequent signaling behavior. Here, we studied responses to conspecific secretions in two Sceloporus species differing in visual signaling: male Sceloporus undulatus have blue abdominal patches used in aggressive territorial encounters, while Sceloporus virgatus males have evolutionarily lost the patches and have low rates of aggressive display. We measured behavior of free-ranging males following presentation of swabs with conspecific male chemicals from femoral glands and the cloaca, or of clean swabs. For male S. undulatus (blue), neither likelihoods nor rates of behavioral responses differed between swab treatments. In contrast, male S. virgatus (white) presented with secretions had significantly higher likelihood of performing head bob, push-up, and shudder displays, than males in control swab trials. Rates of behavior also differed for S. virgatus, with higher rates of push-up display and tongue flick in trials with conspecific chemicals, but rates of other displays, number of moves, and mean total distance moved did not differ between treatments. Male S. undulatus moved significantly greater distances than S. virgatus, independent of treatment. In sum, male S. virgatus responded to conspecific male chemicals by increasing their low rates of display behavior, whereas male S. undulatus did not alter their already high rates of display or movement following chemical exposure. Chemical signals may play a different role in social signaling in the species with the loss of the abdominal color signal.     

Kin recognition in the common lizard

The ability to recognize parents has never been reported in species in which parents do not provide care to their young; in such species, only sibling recognition has been found. However, there may be several advantages of parent recognition, even in the absence of parental care. We investigated the ability of neonates to recognize olfactory cues from both their mother and siblings in the common lizard, Lacerta vivipara, a species without parental care. Juveniles from 264 gravid females were reared for 2 days either with their mother, with another female, or separated from all other adults. Juveniles from some families were split into two or three groups so that each juvenile was unfamiliar with a subset of its siblings. After 2 days, we offered the juveniles a choice of two nocturnal shelters: one containing a lizard odor and the other without odor. The response to the odor of an unrelated and unfamiliar adult was influenced by both the sex of the adult and the sex of the juvenile. Juveniles of both sexes recognized the odor of their mother whether they were familiar with her or not (pre-natal determinism). Juveniles recognized familiar but not unfamiliar siblings (post-natal determinism). In the wild, spatial association with kin declines shortly after birth. Thus, recognition of the mother is likely to have biological relevance. Recognition of the mother may reduce competition and/or enhance juvenile establishment. Received: 15 May 1997 / Accepted after revision: 29 December 1997     

Binary individual recognition in hermit crabs

One mechanism that permits the maintenance of dominance hierarchies is individual recognition, defined as the ability of an animal to recognize a conspecific on the basis of one or more identifying cues, and to associate it with experiences of victories or defeats that the animal has gained from preceding encounters with that particular individual. We examined whether the long-clawed hermit crab, Pagurus longicarpus, could differentiate between unfamiliar and familiar opponents. The experimental protocol was designed to control in pairs of interacting individuals several factors together, such as status and relative size of the opponent, as well as species, quality, and fit of the inhabited shell. The hermit crabs were more reactive and their agonistic level was higher in unfamiliar than in familiar pairs; in addition, betas were more prone to initiate an interaction with unfamiliar than with familiar alphas. The alternative explanation—that the ability to discriminate between familiar and novel shells can explain our results per se— was tested following, in part, Jackson and Elwoods (1989) protocol for Pagurus bernhardus and was, at least for this species, rejected. This study did not determine whether a true individual recognition occurs, but demonstrated that P. longicarpus categorizes the individuals into two heterogeneous subgroups, thus being capable of a binary discrimination among opponents.Communicated by T. Czeschlik     

Herbicide exposure affects the chemical recognition of a non native predator in common toad tadpoles (<Emphasis Type="Italic">Bufo bufo</Emphasis>)

Summary. In amphibians and fishes, evidence is increasing that chemical cues from injured conspecifics can play a role in the chemical labelling and learned recognition of unfamiliar predators. In this laboratory study, we tested the prediction that prior chemical exposure to a non-native predator feeding on conspecific tadpoles will subsequently allow tadpoles of the common toad (Bufo bufo) to recognize the chemical cues specifically released by this starved predator. Furthermore, we investigated the vulnerability of this chemically-mediated process to herbicide contamination. With these aims in view, groups of tadpoles were kept either unexposed or exposed for ten days to chemical cues from Turkish crayfish (Astacus leptodactylus) previously fed on tadpoles, both in uncontaminated water and in the presence of four sublethal concentrations of amitrole (0.01, 0.1, 1 and 10 mg.l⁻¹). We then assessed the effects of the six conditioning treatments on general activity and behavioural response to chemical cues from starved crayfish. Larval treatments did not affect the general activity of the tadpoles. By contrast, the treatments had significant effects on the behavioural response to the test solution prepared form starved crayfish. The only tadpoles to show an antipredator behavioural response to the chemical stimulation from starved crayfish belonged to the groups derived from chemical exposure to tadpole-fed crayfish in uncontaminated water and in contaminated water with the lowest concentration of amitrole (0.01 mg.l⁻¹). Conversely, this chemical stimulation produced no behavioural change in the control group or in the groups derived from exposure to tadpole-fed crayfish in contaminated water containing 0.1, 1 and 10 mg.l⁻¹ of amitrole. This study demonstrates that chemical cues released during the predator’s feeding activity can subsequently be used by common toad tadpoles in the recognition of an unfamiliar predator. In addition, our results show that the presence of sublethal amitrole concentrations can impair this recognition process. Such a pesticide effect might be especially detrimental for amphibian populations threatened by invasive predators.     

Survival and remigration probabilities for loggerhead turtles (Caretta caretta) nesting in the eastern Gulf of Mexico

Few long-term mark-recapture tagging datasets exist to estimate population parameters for loggerhead sea turtle (Caretta caretta) recovery units. Using a two-state open robust design model, we analyzed a 20-year (1990–2009) mark-recapture dataset from the Keewaydin Island loggerhead nesting assemblage off the southwest coast of Florida (USA) in the eastern Gulf of Mexico. For this analysis, 2,292 turtle encounters were evaluated, representing 841 individual nesting turtles. Survival was estimated at 0.73 (95 % CI 0.69–0.76). This estimate is comparable with survival estimates elsewhere in the Peninsular Florida subpopulation and is among the lowest estimates for the Northwest Atlantic loggerhead population. We documented no changes in remigration rates or clutch frequency over time. These are the first survival and remigration probabilities estimated for a loggerhead nesting assemblage in the eastern Gulf of Mexico.     

Effects of Roads on the Structure of Freshwater Turtle Populations

Abstract:  Road mortality has the potential to alter the structure of turtle populations because turtle populations are highly sensitive to additive sources of adult mortality. To address the issue, we captured painted turtles (   Chrysemys picta ; n = 174) and snapping turtles (   Chelydra serpentina ; n = 56) in 18 wetlands surrounded by low road density (≤1.5 km roads/km² of landscape) and 17 wetlands surrounded by high road density (>1.5 km/km²) in central New York in 2002. High road density was associated with male-biased sex ratios in painted turtles (74% vs. 54% males; p = 0.01) and snapping turtles (95% vs. 74% males; p = 0.08), whereas turtle morphology and abundance were not associated with road density. Disproportionate road mortality of females on nesting migrations is the most likely cause of skewed sex ratios.     

Habituation in the green frog, Rana clamitans

Habituation and its role in the dear enemy effect was investigated in a population of green frogs, Rana clamitans. Green frogs have a prolonged breeding season, and males defend territories centered around suitable oviposition sites. We tested the prediction that male green frogs will habituate to broadcasts of synthetic conspecific stimuli. Our results indicate that male green frogs can discriminate familiar from unfamiliar stimuli. We suggest that habituation helps to mediate the territorial interactions between male green frogs. Strangers present a greater threat than familiar neighbors. By habituating to the advertisement vocalizations of their near neighbors, males avoid costly interactions with individuals that are not a major threat to their territories. Received: 20 July 1998 / Accepted after revision: 6 September 1998     

Schooling decisions in guppies (Poecilia reticulata) are based on familiarity rather than kin recognition by phenotype matching

Evidence from a number of freshwater species indicates that fish prefer to school with familiar individuals. Do they also choose to associate with kin? Our experiment tested this idea using the Trinidadian guppy, Poecilia reticulata, a species whose reproductive biology favours the association of kin groups. Juveniles reared together were able to recognise one another on the basis of either visual or chemical cues, but showed no preference for schooling with unfamiliar kin. We therefore conclude that any naturally occurring kin groups in this species will occur as a result of familiarity rather than as a consequence of kin recognition based on phenotype matching.     

Bold minnows consistently approach danger in the field and lab in response to either chemical or visual indicators of predation risk

A behavioral syndrome is a suite of behaviors correlated across multiple social contexts. In this study, boldness in the face of predation risk was assessed twice in fish across two different sensory modalities in both the field and lab to ascertain the biological relevance and complexity of this attribute. Individual fathead minnows were captured from a natural field population using traps that either contained chemical alarm cues (conspecific skin extract) or control (well water) and their responses to the presence of predator behind a glass partition assessed in the laboratory. Although fewer fish were captured in alarm cue-labeled traps, these bold fish performed longer predator inspections than shy fish captured in control traps. Thus, a shy/bold behavioral syndrome was expressed consistently across field and lab settings in response to both chemical and visual indicators of danger. Shy and bold individuals did not differ in sex, body length, secondary sexual characteristics, or parasite load but were of more robust physical condition.     

When to come out from your own shell: risk-sensitive hiding decisions in terrapins

Animals should optimize the decision of when to come out from a refuge after a predators unsuccessful attack because hiding may be costly. Many prey run to hide in refuges in their habitat, whereas others are sessile and take refuge in a protective structure surrounding their body. An intermediate situation is when animals, such as turtles, have morphological structures that provide some partial protection, but they are also able to escape actively to safer refuges. This might complicate hiding decisions predicted by the theory of optimal-refuge use. We studied antipredatory tactics of Spanish terrapins (Mauremys leprosa) in response to simulated predatory attacks with different characteristics (i.e. combinations of several risk factors) and under different conditions (i.e. proximity to safe refuges), which should contribute to overall risk-level estimation. We specifically examined how risk level affected time spent withdrawn into the shell and time until turtles switched to an active escape tactic. The results showed that turtles were able to adjust their hiding behavior by assessing the risk of emerging before the predator had left the area. However, increasing hiding time may also increase the risk that the predator was able to injure or kill the turtle. Thus, the possibility of switching the antipredatory tactic to an alternative active escape to safer refuges (i.e. water) also influenced hiding times.Communicated by P. Bednekoff     

Detection of coastal mud odors by loggerhead sea turtles: a possible mechanism for sensing nearby land

For sea turtles, an ability to detect land masses from a considerable distance away, and to distinguish coastal areas from the open sea, might be adaptive. The loggerhead turtle, Caretta caretta, can detect airborne odorants associated with food. To investigate whether sea turtles can also detect odors associated with land, we studied the responses of juvenile loggerheads to odors from coastal mud. Turtles were tested in a water-filled arena in which odorants could be introduced to the air above the water surface. Turtles exposed to air that had passed over a cup containing mud spent more time with their noses out of the water than did control turtles exposed to air that had passed over a cup containing distilled water. The results demonstrate for the first time that loggerheads can detect airborne odorants associated with land, an ability that might play a role in foraging, navigation, or both.     

Ontogenetic differences in chemical alarm cue production determine antipredator responses and learned predator recognition

How individuals assess, respond and subsequently learn from alarm cues is crucial to their survival and future fitness. Yet this information is not constant through time; many individuals are exposed to different predators throughout their life as they outgrow some predators or move to habitats containing different predators. To maximise overall fitness, individuals should discriminate between different cues and respond and learn from only those that are relevant to their current ontogenetic stage. We tested whether juvenile spiny chromis, Acanthochromis polyacanthus, could distinguish between chemical alarm cues from conspecific donors of different ontogenetic stages and whether the cue ontogenetic stage of the cue donor affected the efficacy of learning about predators. Juveniles displayed a significant antipredator response when conditioned with juvenile chemical alarm cues paired with predator odour but failed to respond when conditioned with predator odour paired with either adult alarm cues or with saltwater. Subsequently, individuals only recognised the predator odour alone as a threat when conditioned with juvenile alarm cues. This demonstrates that prey may be highly specific in how they use information from conspecific alarm cues, selectively responding to and learning from only those cues that are relevant to their developmental stage.     

Modelling the fate of marine turtle hatchlings

The SLIM oceanographic model was used to examine the fate of hatchling flatback turtles (Natator depressus) in the first two weeks of their dispersal starting at Wild Duck Island, a major turtle-nesting site in the central Great Barrier Reef region of Australia. We ran simulations to investigate the effects of spring versus neap tides, hatchling's swimming behaviour during their first three days at sea, and the location of nesting beaches. The model predicted that up to 50% of the turtle hatchlings entering the sea from the windward, southern beach remained after 14 days in shallow, nearshore waters, irrespective of tides and swimming. These waters are turbid and may be inhospitable to hatchlings. In contrast >80% of hatchlings dispersing from the leeward, northern beach were dispersed to deeper water (10-40 m) in a quasi-stationary dispersion core centred around 10 km north of the nesting beach after 14 days and the offshore spread of the turtle plume was enhanced by the hatchling's seaward swimming during the first three days. This was due to the presence of a coastal boundary layer and a stagnation zone around the northern side of island, but not the southern side. The model confirmed that dispersal from eastern Queensland flatback turtle rookeries is restricted to the lagoons and coastal waters, and that water circulation and hatchling's swimming control dispersion. The model explains why more turtles nest on the northern than the southern side. This study highlights the usefulness of oceanographic models to increase knowledge about a cryptic life stage of marine turtles.     

Aversive and avoidance responses of female mice to the odors of males infected with an ectoparasite and the effects of prior familiarity

The detection and avoidance of parasitized males is a component of female mate choice. Here we show that female mice can distinguish between the odors of individual males infected with an ectoparasite, the murine louse, Polyplax serrata, and uninfected males. Female mice displayed aversive responses to, and avoided the odors of, parasitized males. A 15 min exposure to the urinary odors of infected males induced an endogenous opioid-peptide-mediated reduction in pain sensitivity or analgesia, while a brief 1 min exposure to the odors elicited a non-opioid-mediated analgesic response. These neuromodulatory mechanisms facilitate the expression of a variety of anxiety and stress associated responses of which pain inhibition is one component. Females further distinguished between novel and familiar infected males. Prior exposure to the odors of an infected males reduced the degree of analgesia expressed and the associated levels of anxiety and stress and their concomitant costs. In a Y-maze odor preference test females also displayed a marked overall preference for, and initial choice of, the odors of clean, uninfected males and an active discrimination against, and avoidance of, the odors of both familiar and novel infected males. These findings indicate that female mice can distinguish between males infected with an ectoparasite and clean uninfected males and display aversive and avoidance responses to infected males. They also show that females can discriminate between individual infected males and modulate their aversive responses to the odors of infected males on the basis of prior familiarity. This is likely part of the mechanisms whereby females can both reduce the transmission of ectoparasites, such as lice, to themselves and select for parasite-free males.     

Femoral secretions and copulatory plugs convey chemical information about male identity and dominance status in Iberian rock lizards (Lacerta monticola)

Socially dominant males often signal their status to rival males and/or females. We tested the hypotheses that Lacerta monticola femoral gland secretions and copulatory plugs convey chemical information about male identity and dominance status. We estimated male dominance status by staging male–male agonistic encounters in a neutral arena. We then conducted two experiments to compare male tongue-flick behavior toward chemical stimuli consisting of cotton swabs bearing (1) deionized water (control), the lizard’s own femoral secretions, and the femoral secretions of another male and (2) phosphate-buffered saline solution (control), the lizard’s own plug products, and the plug products of another male. Results indicate that males discriminated their own femoral secretions and plugs from those of other males. They also discriminated morphological attributes of other males that were associated with dominance status based on chemical cues arising from femoral secretions and discriminated the dominance status of other males based on chemical cues arising from the plugs. Femoral secretions that convey information about male identity and dominance status may be hypothesized to function in the establishment of L. monticola dominance hierarchies through scent-marking of territories. We suggest that copulatory plugs and femoral secretions may allow males to scent-mark the female body and postulate that this behavior may influence male and female reproductive decisions under selective pressures of sperm competition.     

Demonstration of sex pheromones in the predaceous diving beetle Rhantus suturalis (MacLeay 1825) (Dytiscidae)

Sex pheromones are used by a wide variety of species in terrestrial ecosystems. Much less is known about these pheromones in aquatic systems e.g., for diving beetles. To test the use of pheromones and visual signals for mate finding by the diving beetle Rhantus suturalis (MacLeay 1825), behavioral experiments were performed using three different types of vessels containing conspecific. In experiments with non-permeable glass flasks, which did not allow the diffusion of chemical substances, males and females did not stimulate any reaction by conspecific of either sex. In experiments with opaque but water permeable vessels, and in experiments with vessels made of finely woven steel, which allowed the perception of chemical as well as optical cues, male diving beetles were significantly attracted to females. Females were attracted to other females only in the last experiment, when simultaneously perceiving chemical and optical cues. These results indicate that R. suturalis females release sex pheromones to attract mating partners, which is the first experimental demonstration of pheromones in the Dytiscidae.