Salamander territoriality: pheromonal markers as advertisement by males

A laboratory experiment was performed to test the hypothesis that male red-backed salamanders (Plethodon cinereus) use pheromones contained in faecal pellets to identify male-marked territories. Each of 25 males was tested randomly under four conditions: (1) a burrow marked with its own faecal pellet versus one marked with a conspecific's pellet; (2) own-marked versus surrogate-marked burrows (the surrogate being a pellet of wadded paper); (3) conspecific-marked versus surrogate-marked burrows; and (4) a control of two surrogate-marked burrows. Males spent significantly more time in own-marked than in conspecific-marked burrows and significantly more time in surrogate-marked than in conspecific-marked burrows. Males favoured own-marked over surrogate-marked burrows. No position bias was found in the control. Males spent significantly more time nose-tapping (olfactory sampling) to a conspecific's pellet when it was paired with a surrogate but showed no differences in the other three tests. Significantly more time was spent in a submissive posture in front of the conspecific-marked burrow than in front of either their own-marked or the surrogate-marked burrows; no difference was found between own-marked versus surrogate-marked burrows or in the control. Time spent in the threat posture did not differ significantly between burrows in any condition. These data permit the inferences that males of P. cinereus use faecal pellets to mark and identify territories, avoid or display submissively toward burrows marked by conspecific males, and prefer own-marked shelters.     

Territorial Pheromones of Female Red-backed Salamanders

Pheromones provide an important source of communication during social interactions of caudate amphibians. To further examine their use in territorial defense, we performed a laboratory experiment to test the hypothesis that non-courting female red-backed salamanders (Plethodon cinereus) deposit pheromones in or on fecal pellets, as males are known to do during territorial advertisement. Four conditions were tested: (1) a burrow marked with a female's own pellet vs. a burrow marked by a conspecific female's pellet, (2) own vs. unmarked burrows, (3) conspecific vs. unmarked burrows, and (4) paired unmarked burrows as a control. Females nose-tapped (for olfactory cues) their own and conspecific pellets about equally. However, they spent significantly more time in both threat and submissive behavior toward the conspecific pellets and spent significantly more time in their own marked burrows. We infer that female P. cinereus do deposit pheromones in or on fecal pellets and that these pellets may be used to advertise territories. The behavioral responses of females toward pellets of other females were more aggressive than those of males (in a previous study) toward pellets of other males.     

Chemical Alarm Signalling in Terrestrial Salamanders: Intra- and Interspecific Responses

Chemical alarm cues are known to be important in mediating predator avoidance in a variety of taxonomic groups. The purpose of this study was to test whether three species of salamanders that co-occur in the coastal mountains of Oregon utilize chemical alarm cues in predator avoidance. In laboratory experiments, Western redback salamanders, Plethodon vehiculum, and Southern torrent salamanders, Rhyacotriton variegatus, exhibited an avoidance response to stimuli from injured conspecifics, while Dunn's salamanders, Plethodon dunni did not. Additional experiments demonstrated interspecific alarm responses. P. vehiculum and R. variegatus responded to each other's alarm cues but did not respond to the alarm cues of allotopic long-toed salamanders, Ambystoma macrodactylum. For R. variegatus, this is despite the fact that they are more closely related to the allotopic species (A. macrodactylum) than to the syntopic species (P. vehiculum). Thus phylogeny alone may not explain patterns of cross-species alarm responses. Instead, interspecific alarm responses may occur between syntopic species that belong to the same prey guild (i.e. those species that co-occur spatially and temporally and are exposed to the same suite of predators).     

Mate Choice by Chemical Cues in Western Redback (Plethodon vehiculum) and Dunn's (P. dunni) Salamanders

Western redback and Dunn's salamanders (Plethodon vehiculum and Plethodon dunni, respectively) can distinguish between potential mates by using chemical cues. In laboratory choice tests, adult males of both species showed significant discrimination between chemical cues of gravid females over non-gravid females of equal body size. Furthermore, males of both species differentiated the odour of paired gravid females that differed by ? 5 mm snout-vent length (SVL). Given that clutch size is related to female body size in these species, adult males may be able to distinguish between females via cues that signal potentially high female reproductive success. In choice tests, P. vehiculum females did not discriminate between two relatively large males that differed by ? 5 mm SVL. However, females of P. vehiculum did discriminate between two relatively small males that differed by the same amount. Apparently, P. vehiculum females ranked males by both absolute and relative body size using chemical cues. This pattern could reflect a female preference for large males or that females avoid mating with the smallest males.     

Iberian Rock Lizards (Lacerta monticola cyreni) Assess Conspecific Information Using Composite Signals from Faecal Pellets

A field and laboratory study was performed to analyse the role of excrement deposited on the substrate in intraspecific communication of the Iberian rock-lizard (Lacerta monticola cyreni). In the field, lizards selected specific sites on rocks to deposit faecal pellets, probably in order to facilitate visual location of pellets by conspecifics. Differential tongue flick rates to chemicals presented on cotton swabs demonstrated that male lizards can detect and discriminate between self-produced scents from faecal pellets and those of other conspecific males. In a subsequent experiment, male lizards were tested in a chamber with two platforms containing a faecal pellet of other male on one side and a control artificial pellet on the opposite side. Males spent significantly less time on the side containing the faecal pellet, suggesting that the decision of where to stay may depend on the presence of faecal pellets. Smaller males moved less than larger males on the experimental side whereas on the control side body size did not influence the proportion of time moving. The ability to discriminate chemicals from faeces, and the effects of faecal pellets on lizard behaviour, suggests that faeces might act as composite signals (visual and chemical) in the intraspecific communication of this lizard.     

Individual recognition in salamanders: Cloacal odours

Male red-backed salamanders (Plethodon cinereus) were studied to determine the origin of the chemical cues allowing for individual odour recognition between conspecifics. Individual males showed a preference for substrates with their own faecal and cloacal odours rather than those marked by unfamiliar conspecific males. This discriminatory ability did not depend on recent differences in food consumed. These scent marks might be used to define breeding territories in the field.     

Recognition of individual,sex and species odours by salamanders of the Plethodon glutinosus-P. Jordani complex

Salamanders of the Plethodon glutinosus-P. jordani complex were tested for the ability to distinguish conspecific, sex-specific, and heterospecific chemical cues. Male and female P. glutinosus preferred substrates previously occupied by conspecifics over their own, but randomly chose between substrates marked by male or female conspecifics. This suggests that while these salamanders are able to distinguish between their own and conspecific substrate odours, they are unable to identify sex by means of substrate odours. Experiments using an olfactometer showed that male P. jordani, male and female P. glutinosus, and an electrophoretically distinct and non-hybridizing sympatric phenotype in the P. glutinosus complex (here called species A), all preferred female airborne odours over male airborne odours. This demonstrates that these salamanders can identify sex by means of airborne odours. Male P. glutinosus and species A both preferred conspecific female odours over heterospecific female odours in olfactometer experiments. These results suggest an important role for olfaction in the sexual and social behaviour of these salamanders, particularly as a pre-mating isolating mechanism.     

Pheromonal markers as indicators of parasite load: parasite-mediated behavior in salamanders (Plethodon angusticlavius)

Assessment of parasite load of conspecifics may be important during social interactions such as courtship and aggressive encounters. We used a correlational study to test whether pheromonal markers can be used to assess parasite load of conspecifics, and whether the parasite load of the pheromone receivers affected their responses. We tested the responses of parasitized and nonparasitized Ozark zigzag salamanders, Plethodon angusticlavius, to territorial markers (fecal pellets) from conspecific males. Males and females were simultaneously exposed to fecal pellets placed in front of two artificial burrows located at the opposite ends of their chambers. The treatments were (1) fecal pellet of male with low parasite load versus fecal pellet of male with high parasite load, (2) fecal pellet of male with low parasite load versus control pellet (chemical blank), and (3) fecal pellet of male with high parasite load versus control pellet. Nonparasitized females spent significantly more time near fecal pellets of males with low parasite load in test condition 1, whereas the behavior of parasitized females was not significantly different from random in any test condition. Males responded differently to treatments only in condition 3; males with low parasite loads spent significantly more time near control pellets, whereas males with high parasite loads spent significantly more time near fecal pellets of males with high parasite loads. This study demonstrates that pheromonal markers may be used for assessment of parasite load of conspecifics and that responses by both males and females may be influenced by their own level of infection. Received: 21 January 1999 / Received in revised form: 17 March 2000 / Accepted: 13 November 2000     

Size-Dependent Chemosensory Responses to Familiar and Unfamiliar Conspecific Faecal Pellets by the Iberian Rock-Lizard, Lacerta monticola

We conducted a field study to analyse the social relationships between males of the Iberian rock lizard (Lacerta monticola). The degree of familiarity was determined based on the degree of overlap between their home ranges. We then designed a laboratory experiment to test whether the same males were able to discriminate between familiar and unfamiliar conspecifics using faecal pellet odours. Differential tongue‐flick rates suggest that large males (snout‐to‐vent length, SVL > 75 mm), at least, may discriminate between odours of familiar and unfamiliar males. The behavioural responses were dependent on relative differences in body size between the responding male and the male that donated the faecal pellet. Thus, as responding small males increased in size relative to their corresponding familiar male, their rate of tongue‐flicking significantly decreased; this was not the case in response to unfamiliar males. In contrast, there were no significant correlations between the response of large males to familiar or unfamiliar male stimuli, regardless of size differences. These results suggest that chemical cues contained in faecal pellets allow individual recognition in male L. monticola, and that the response depends on body size. We suggest that faecal pellets might be used to scent‐mark home ranges, which would contribute to lowering the costs of aggressive interactions.     

An alternative hypothesis for the primary function of a proposed mate assessment behaviour in red-backed salamanders

Using a laboratory experiment, we tested the hypothesis that faecal inspection and squashing behaviours by female red-backed salamanders, Plethodon cinereus, function in a context other than mate assessment, in this case foraging. Because only female P. cinereus squash faecal pellets, other studies have hypothesized that the faecal squashing is a mate assessment behaviour. During the courtship season, we exposed gravid female P. cinereus maintained on a ‘high-quality’ or ‘low-quality’ diet, to the faecal pellets of male and female conspecifics fed ‘high-quality’ diets. Female diet had no effect on activity level, and, overall, P. cinereus showed greater interest in male-marked substrates than female-marked substrates. However, female diet had a large effect on faecal inspection and squashing behaviours, and females showed similar inspection and squashing rates towards both male and female faecal pellets. These results suggest that faecal squashing does not function primarily in mate assessment, but rather as a means for female P. cinereus to gain information about prey availability. We propose that male P. cinereus have evolved to exploit female faecal inspection and squashing behaviours (sensory exploitation) to attract foraging females into areas to increase male encounter rates with females.     

On the role of olfaction in sexual and interspecies recognition in crickets (Acheta and Gryllus)

Crickets appear to rely less upon olfactory communication than do their non-acoustical relatives, but males and females of house (Acheta) and field (Gryllus) crickets can determine sex by odour, and males can distinguish odours of conspecific and heterospecific females. In the presence of female odours, female-deprived males groom more vigorously and are more aggressive.     

Earthworms, as ecosystem engineers, influence multiple aspects of a salamander��s ecology

Ecosystem engineers create habitat that can be used by other species in multiple ways, such as refuges from predators, places to breed, or areas with increased prey resources. I conducted a series of enclosure experiments to: (1) determine if salamanders use earthworm burrows, and (2) examine the potential influence of earthworm burrow use and indirect effects on salamander intra- and interspecific competition, predator avoidance, and seasonal performance. I found that one species of woodland salamander, Plethodon cinereus, used earthworm burrows 50% of the time when burrows were present. Neither adults nor juveniles of the congeneric P. glutinosus used earthworm burrows. Intraspecific, but not interspecific, competition by P. cinereus affected salamander behavior when earthworms were absent, with P. cinereus found under cover objects >70% of the time when alone or with a P. glutinosus, but only 40% of the time when with another P. cinereus. When earthworms were present, the behavior of P. cinereus was similar across salamander treatments. Earthworms decreased the amount of leaf litter and microinvertebrates, although this did not affect salamander mass. In subsequent experiments using only P. cinereus, the refuge provided by earthworm burrows increased the survival of P. cinereus over the winter and allowed P. cinereus to avoid being consumed by the common garter snake (Thamnophis sirtalis). Because earthworm burrows provide a refuge for P. cinereus during intraspecific encounters, in the presence of a predator and over the winter, they may serve as an important belowground?Caboveground linkage in eastern forests where salamanders are common.     

The effects of conspecifics on burrow selection in juvenile spotted salamanders (<Emphasis Type="Italic">Ambystoma maculatum)</Emphasis>

Spotted salamanders (Ambystoma maculatum) are pond-breeding amphibians that disperse into terrestrial habitat from natal wetlands after undergoing metamorphosis, relying on small-mammal burrows and coarse woody debris for refugia. The effect of conspecifics on burrow use in juvenile salamanders is poorly understood. Determining how the presence of conspecifics influences the settlement decisions of juvenile salamanders can increase our understanding of amphibian dispersal and our ability to predict population dynamics. We conducted behavioral laboratory trials using 58 recently metamorphosed salamanders to examine how salamanders selected burrows in the presence of conspecifics. Salamanders were more likely to settle in a burrow that was occupied by a conspecific versus an unoccupied burrow. Our results indicate that juvenile salamanders may show conspecific attraction and/or trailing behavior during the dispersal phase.     

Conspecific and heterospecific pheromone effects on female receptivity

Courtship pheromones play an important role in salamander reproductive behaviour. In salamanders of the family Plethodontidae, males deliver specialized pheromones to females during courtship interactions. These courtship pheromones increase female receptivity and may be involved in mate discrimination. In order to test hypotheses related to mate discrimination, we staged courtship encounters between male-female Plethodon shermani pairs in which the female received pheromones obtained from either conspecific (P. shermani) or heterospecific (P. yonahlossee orP. montanus ) males. Both conspecific and heterospecific pheromones increased female receptivity. Moreover, pheromones from both heterospecific species were as effective as the conspecific pheromone in increasing female receptivity inP. shermani females. Our results suggest that the courtship pheromone signal and function may be conserved across related species, with mate discrimination occurring before pheromone delivery. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.     

Responses of a plethodontid salamander to conspecific and congeneric intruders

After inhabiting their home sites for a few days, both males and females of the salamander Desmognathus monticola directed agonistic behaviour toward intruding salamanders. Resident D. monticola were significantly more aggressive toward D. fuscus intruders than toward conspecific ones, although both conspecific and congeneric intruders were frequently attacked. Responses of D. monticola residents were independent of sex, and no difference was found in the behaviour of residents toward conspecific male and female intruders. Small D. fuscus intruders were attacked and injured more frequently than similar-sized D. monticola intruders and, in general, smaller-sized salamanders were the victims of aggressive attacks more frequently than larger ones. The proportions of bites on the head and tail of intruders were similar, although injuries were much more frequent to the tail than to the head. This species-related and size-related agonistic behaviour may be functional in maintaining the spatial distribution of species in communities of Desmognathus salamanders.     

Periphyton responds differentially to nutrients recycled in dissolved or faecal pellet form by the snail grazer Theodoxus fluviatilis

1. We aimed to separate the effects of grazers on periphyton via grazing from that of nutrient recycling from their faecal pellets. 2. We set up three different experimental treatments (snails/no snails/faecal pellets) and sampled over 16 days. The ‘snail’ treatment contained a low density (snail biomass c. 14 g^?2) of the gastropod grazer Theodoxus fluviatilis and the ‘faecal pellet’ treatment received the same amount of faecal pellets as were produced in the ‘snail’ treatment. Whereas the ‘faecal pellet’ treatment provided extra nutrients to periphyton from the faeces, the ‘snail’ treatment provided nutrients in the form of both faeces and in excreta. There was also direct grazing on periphyton in the ‘snail’ treatment. The ‘no snail’ was not grazed and received no nutrients in faeces or excreta. 3. We measured periphyton C, N and P content, chlorophyll‐a (chl‐a), primary production, bacterial biomass, bacterial production and bacterial respiratory activity. In the water column we measured dissolved inorganic N and soluble reactive P. 4. Snails increased the amount of dissolved inorganic N in the water. On day 16, the periphyton N : P ratio in the ‘faecal pellet’ treatment was lower, and periphyton P content was higher, than in the other two treatments. N : P ratios decreased over time in the ‘faecal pellet’ treatment. Primary and bacterial production were positively correlated in all treatments. 5. Algal chl‐a and primary production of periphyton per unit area and periphyton chl‐a : C ratios increased over the 16 day in the ‘snail’ treatment, and thus excretion of dissolved N by snails had a stronger positive effect on the periphyton community than N and P in faecal pellets. 6. Our data show that excretion and egestion can have different effects on periphyton, probably because of the higher proportion of dissolved N in excreta and the higher proportion of P recycled in faecal pellets. The relative effect of nutrients recycled in egesta or in excretions, probably depends on the form of nutrient limitation of the periphyton. Further, the different components of the periphyton matrix could react differently to the different forms of nutrient recycling. 7. We conclude that direct grazing effects are less important than nutrient effects when nutrients are limiting and grazing pressure is low. Further, the spatial separation of different grazing effects can lead to differences in periphyton production and nutrient stoichiometry. This might be an explanation for the patchiness of periphyton in nature.     

Responses of Snow Voles, Chionomys nivalis, Towards Conspecific Cues Reflect Social Organization during Overwintering Periods

Among microtine rodents, reaction to chemical cues from conspecifics is assumed to reflect social and spatial relationships. Generally, strong attraction of particular odours correlates with non‐aggressive behaviour and high spatial tolerance towards odour donors, whereas weak attraction correlates with greater levels of aggression and spatial segregation. In the present study, we examined whether winter odour preferences of the snow vole Chionomys nivalis, a rock‐dwelling microtine principally found at high‐mountainous regions, differ from that of other vole species, owing to their different social organization during overwintering periods. The social structure of C. nivalis over the winter period is relatively unusual among vole species in that they become nomadic and solitary. In odour choice trials under laboratory conditions, we found that both males and females avoided zones with conspecific odours of both sexes in comparison with unscented control zones or own odours. These results are consistent with the elevated levels of intraspecific aggression and spatial isolation of C. nivalis during overwintering periods. Furthermore, scent‐elicited self‐grooming increased when their own odour was offered against conspecific cues. This, in combination with an active avoidance of conspecific odours, might functionally contribute to minimize direct confrontations between solitary individuals, thereby reducing the risks of aggressive encounters during overwintering periods.     

A tangerine-scented social odour in a monogamous seabird

Social odours, conspecific chemical signals, have been demonstrated in every class of vertebrate except birds. The apparent absence is surprising, as every bird examined has a functional olfactory system and many produce odours. The crested auklet (Aethia cristatella), a monogamous seabird, exhibits a distinctive tangerine-like scent closely associated with courtship. Using T-maze experiments, we tested whether auklets preferred conspecific odours and whether they distinguished between different types of scent, two prerequisites of chemical communication. Crested auklets exhibited: (i) an attraction to conspecific feather odour; (ii) a preference for two chemical components of feather scent (cis-4-decenal and octanal), which we identified as seasonally elevated; and (iii) differential responses to odours, as indicated by a preference for auklet odour, an aversion to mammalian musk, but no significant response to banana essence (amyl acetate). Our results suggest that crested auklets detect plumage odour and preferentially orientate towards this stimulus. The striking and well-described courtship display that involves the scented neck region, the 'ruff sniff', provides a conspicuous behavioural mechanism for odour transmission and the potential for scent assessment during sexual selection. Although the importance and full social function of chemical signals are just beginning to be understood in birds, including crested auklets, social odours promise to reveal a largely unexplored and possibly widespread means of avian communication.     

Tests of aggregative preferences of wandering salamanders (Aneides vagrans)

Plethodontid salamanders usually exhibit territorial spacing patterns and behaviors. Previous works suggest that plethodontids from Vancouver Island, Canada lack strong territoriality. In one Vancouver Island species, Aneides vagrans, salamanders may even be found in the field in small aggregations. We investigated preferences of A. vagrans for occupied vs unoccupied cover objects and for cover objects occupied by conspecifics of different age/size classes. We also tested A. vagrans preferences for conspecific vs heterospecific salamanders in an attempt to determine if the lack of territoriality by A. vagrans is species-specific and perhaps related to habitat segregation. A. vagrans did not avoid occupied cover objects or exhibit a preference for occupied vs unoccupied sites. Age class did not affect cover object choice. A. vagrans did not avoid heterospecifics that exhibit the highest degree of resource overlap (Plethodon vehiculum), which we believe might be attributable to a benign and resource-rich habitat, although alternative explanations exist. A. vagrans did avoid syntopic newts (Taricha granulosa), though this is probably due to toxic newt skin secretions.