Terrestrial Salamanders Research Articles

Revisiting Burton and Likens (1975): Nutrient Standing Stock and Biomass of a Terrestrial Salamander in the Midwestern United States

Animals found in high densities can have significant influence in nutrient cycles of ecosystems. For example, frogs have been known to influence nutrient cycles in tropical forests. However, research understanding the influence of vertebrates in nutrient cycles of North American forest is limited. It has been found that the biomass of terrestrial salamanders (family Plethodontidae) is higher than that of birds, small mammals, and deer in a New Hampshire forest, and recent studies have found prior estimates of terrestrial salamander densities are likely lower than current estimates using sampling and analysis frameworks to account for imperfect detection. A re-evaluation of the impact plethodontid salamanders could have on forest nutrient cycles is therefore justified. We quantified the degree to which a completely terrestrial, lungless salamander (Plethodon albagula; Western Slimy Salamander) constitutes a standing stock of limiting nutrients in a Missouri, USA forest ecosystem. We utilized values of whol...

Male terrestrial salamanders demonstrate sequential mate choice based on female gravidity and size

In many vertebrate mating systems, mate choice evolves when signalling via visual, chemical or auditory traits is an energetically costly process. Selection may favour individuals that can discriminate among potential mates and invest in signalling to mates with particular characteristics. Most commonly, females with costly gametes are thought to be the more selective sex; however, runaway sexual selection can produce elaborate male ornaments and behaviours that are similarly costly to produce, which can lead to male mate choice. In this study, we used behavioural trials to experimentally test male mate choice in a terrestrial salamander, Plethodon shermani. We investigated whether males altered the proportion of time they spent performing a potentially costly courtship display, ‘foot dancing’, in the presence of females. Specifically, we explored male mate choice in two experiments: (1) measuring how males modified the time they invested in courtship based solely on female reproductive value, and (2) determining whether males varied the amount of time they invested in courting females of varying sizes but similar reproductive value. In the first experiment, we quantified the duration of male courtship displays when males were paired with females of differing levels of fecundity (nongravid, weakly gravid and strongly gravid). Males displayed longest for females of high reproductive value (strongly gravid females) and less for weakly gravid and nongravid females. In the second experiment, we showed that males paired sequentially with different-sized females of similar reproductive values displayed significantly more often to larger females (i.e. male effort positively correlated with female size). In conclusion, male P. shermani are one of the few vertebrates known to modify their display behaviour based on female mate quality, and visual signs, such as size, may provide honest indicators of fitness.

Prescribed fire alters surface activity and movement behavior of a terrestrial salamander

AbstractPrescribed fire has become a commonly used forest management tool for reducing the occurrence of severe wildfires, decreasing fuel loads and reestablishing the historic ecological influences of fire. Investigating population‐level wildlife responses to prescribed fire is important for evaluating the effects of fire management on animals, but in order to predict and simulate wildlife responses to potential management actions, mechanistic studies that elucidate individual‐level responses are also necessary. We used radio‐frequency identification to investigate individual‐level responses of western slimy salamanders Plethodon albagula to prescribed fire. We compared the salamander home‐range sizes [minimum convex polygons (MCP)], movement behaviors, and activity levels before and after prescribed fire using a randomized block experiment. We initiated the study at three plots in 2011, and added two new plots in 2012. We captured, tagged and released ≥38 salamanders at each plot from May 2011–May 2012 (total N = 205). We recorded 918 total recaptures of 142 unique salamanders; 31% of tagged salamanders were never recaptured. Across all years and treatments, only 14% of relocations were surface‐active (i.e. visually confirmed) salamanders; the others were underground. Following prescribed fire, the surface‐active proportion of recaptures was nearly seven times greater in control versus burned areas, which indicates that P. albagula respond to post‐prescribed fire conditions by spending more time belowground. We did not find evidence of direct mortality of salamanders from fires; the proportion of known‐alive individuals did not differ between treatments. Maximum daily displacement was 43.3% higher among burn‐area than control‐area salamanders, and MCP varied in a similar pattern; this may indicate salamanders were attempting to find more hospitable microenvironments or other resources, such as prey. Together, these individual‐level observations corroborate our findings from a population‐level study of a congeneric terrestrial salamander and contribute to our understanding of the behavioral mechanisms underlying population dynamics.

A test of scent-trailing as a contributing factor in the climbing behaviour of the redback salamander (Plethodon cinereus)

Terrestrial salamanders of the family Plethodontidae are common predators of invertebrates in deciduous forest communities of eastern North America. While normally residing and foraging in forest-floor microhabitats, many species facultatively climb vegetation. Different hypotheses have been proffered to explain this behaviour including optimal-foraging strategies and predator avoidance. Using laboratory-based trials, we tested the hypothesis that the terrestrial salamander Plethodon cinereus climbs in response to scent trails left by insect prey. We found that salamanders climbed significantly higher and spent significantly more time climbing on wooden dowel rods that had been treated with prey residue than they did on control rods. Scent trailing possibly interacts with other factors such as optimal-foraging opportunities and predation risk in influencing climbing behaviour in these salamanders.

Thermal Sensitivity of Aggression in Two Terrestrial Salamanders, Plethodon cylindraceus and P. montanus

Understanding the abiotic and biotic mechanisms regulating species distributions is an important area of study for ecologists. Increasingly, studies have begun to focus on the influence of abiotic conditions on biotic interactions. Numerous examples of interspecific aggression exist within the terrestrial salamander genus Plethodon and many occur between montane endemics and lowland conspecifics. Here, we explore how variation in temperature might influence aggressive interactions between two Plethodon species that have relatively broad elevational overlap, P. cylindraceus and P. montanus. We found that both species increased aggressive acts with increasing temperatures. We also found that the pattern of variation in aggression across test temperatures differed between species. Interestingly, we found that the lowland congener, P. cylindraceus, was more aggressive than the montane endemic, P. montanus, a pattern opposite of previous observations within Plethodon. The large range of sympatry observed between these species may be a result of a reverse of what is expected based on previous research with congeners in similar systems and not the result of temperature-specific outcomes.

Salamander diversity of reforested abandoned surface coal mines in the Appalachian Region, U.S.A.

Surface coal mining is a pervasive form of land use and leading cause of deforestation in the Appalachian Region of the United States. Contemporary reclamation practices tend to produce strongly altered landscapes that inhibit forest succession, so there is a need for the development of alternative methods. Surface coal mines that preceded modern reclamation laws, known as abandoned mine lands, have become reforested in many locations and may serve as a model for improving the restoration of forests in postmining landscapes. I compared salamander diversity between 5 forests growing atop abandoned surface coal mines to 5 similar aged reference forests in southeastern Ohio using time constrained transect searches in autumn 2012 and spring 2013. The survey revealed 1,480 salamander individuals, representing 11 different species from 3 different families. The vast majority of salamanders (93%) were from the family Plethodontidae. Salamander species richness was significantly higher in reference forests than in mined forests, but this difference was contingent on the presence of stream‐dependent species in the reference forests. Salamander relative abundance was not significantly different between reference and mined forests. This survey demonstrates that reforested abandoned surface coal mines can provide suitable habitat for many forest‐dependent, terrestrial salamander species, but impaired water quality of headwater streams may limit the colonization of these forests by stream‐dependent species.

Advancing Terrestrial Salamander Population Ecology: The Central Role of Imperfect Detection

Abstract Terrestrial salamanders (Plethodontidae) are increasingly cited as important surrogates for monitoring forest ecosystem health and biodiversity. To accurately assess the ecological role of salamanders, total abundance is more relevant than the population subset available for sampling. Therefore, estimating detectability is important for generating unbiased population metrics, as abundance estimates average an order of magnitude greater than surface counts. The past two decades have seen a tremendous increase in analytical methods that account for imperfect detection. Terrestrial salamanders have unique physiological requirements and surface activity patterns that contribute to their inherently low detection levels, and variable terminology makes it difficult to compare detectability parameter values across species, regions, methods, and studies. It is important to use consistent terminology and explicitly state what specific components of detectability are being reported in a study. Availability ...

Effective Use of Trails for Assessing Terrestrial Salamander Abundance and Detection: A Case Study at Great Smoky Mountains National Park

ABSTRACT: The conservation and management of wildlife species is contingent on estimating distribution and abundance. Sampling of wildlife requires repeated visits to accurately determine species occurrence and to quantify abundance across temporal and spatial scales. The use of trails to sample wildlife populations is increasing and offers opportunities to potentially sample more frequently, with increased ease of access, and less disturbance to habitats, which can be important in sensitive natural areas. We examined capture data of terrestrial salamanders within Great Smoky Mountains National Park to determine if detection and abundance estimates from trail and non-trail transects were significantly different. Across two, 3-week periods during June and July 2012, we sampled 195 transects (70 along trails and 125 within non-trail habitat) on multiple occasions. We found that most microhabitat variables associated with salamander detection and abundance did not differ between trail and non-trail transects...

Lagged influence of North Atlantic Oscillation on population dynamics of a Mediterranean terrestrial salamander.

The North Atlantic Oscillation (NAO) is a large-scale climatic pattern that strongly influences the atmospheric circulation in the northern Hemisphere and by consequence the long-term variability of marine and terrestrial ecosystem over great part of northern Europe and western Mediterranean. In the Mediterranean, the effects of the NAO on vertebrates has been studied mainly on bird populations but was rarely analysed in ectothermic animals, and in particular in amphibians. In this study, we investigated the relationships between winter, spring and summer NAO indexes and the long-term population dynamics of the plethodontid salamander Speleomantes strinatii. This terrestrial salamander was monitored inside an artificial cave in NW Italy for 24 consecutive years. The relationships between seasonal NAO indexes and the salamander dynamics were assessed by cross-correlation function (CCF) analysis, after prewhitening the time series by autoregressive moving average statistical modelling. Results of CCF analyses indicated that the salamander abundance varied in relation to the one-year ahead winter NAO (P = 0.018), while no relationships were found with spring and summer indexes. These results strengthen some previous findings that suggested a high sensitivity of temperate terrestrial amphibians to wintertime climatic conditions.

A multistate mark–recapture approach to estimating survival ofPIT‐tagged salamanders following timber harvest

SummarySurvival is a critical component of individual fitness, population dynamics and the landscape ecology of organisms. Survival in animal populations is frequently estimated from capture–mark–recapture studies, yet these estimates are biased low when the permanent emigration of individuals is confounded with mortality. This systematic bias can limit the value of demographic information available for conservation and management efforts.We developed a novel multistate mark–recapture model for survival estimation in fossorial organisms that incorporates auxiliary passive integrated transponder (PIT‐tag) detection data to account for the possibility of permanent emigration from our study area as well as the imperfect detection of individuals. Our study provides a direct comparison of mortality, emigration and reduced ground surface activity as explanations for declines in terrestrial salamander counts which are commonly reported following timber harvest.Reduced ground surface activity was not supported as a likely cause for reduced counts of plethodontid salamanders after timber harvest. Instead, ground surface activity was predicted to be considerably higher after timber harvest, suggesting that surface counts would under‐represent the extent of population losses relative to control areas.Controlling for multiple causes for non‐detection of salamanders, we found evidence that survival probability was reduced while permanent emigration rates may also be elevated in the initial months after timber harvest. However, a substantial majority of salamanders were known to survive the process of initial forest stand entry and timber removal.Synthesis and applications. Our analysis of passive integrated transponder (PIT‐tag) detection data with a novel multistate mark–recapture model indicated that mortality and emigration are both potential causes for short‐term reductions in salamander abundance following timber harvest. We suggest that salamander mortality is likely tied to habitat or microclimate conditions in early successional timber cuts, rather than the physical process of timber removal.

Thriving in the Cold: Glacial Expansion and Post-Glacial Contraction of a Temperate Terrestrial Salamander (Plethodon serratus).

The dynamic geologic history of the southeastern United States has played a major role in shaping the geographic distributions of amphibians in the region. In the phylogeographic literature, the predominant pattern of distribution shifts through time of temperate species is one of contraction during glacial maxima and persistence in refugia. However, the diverse biology and ecology of amphibian species suggest that a “one-size-fits-all” model may be inappropriate. Nearly 10% of amphibian species in the region have a current distribution comprised of multiple disjunct, restricted areas that resemble the shape of Pleistocene refugia identified for other temperate taxa in the literature. Here, we apply genetics and spatially explicit climate analyses to test the hypothesis that the disjunct regions of these species ranges are climatic refugia for species that were more broadly distributed during glacial maxima. We use the salamander Plethodon serratus as a model, as its range consists of four disjunct regions in the Southeast. Phylogenetic results show that P. serratus is comprised of multiple genetic lineages, and the four regions are not reciprocally monophyletic. The Appalachian salamanders form a clade sister to all other P. serratus. Niche and paleodistribution modeling results suggest that P. serratus expanded from the Appalachians during the cooler Last Glacial Maximum and has since been restricted to its current disjunct distribution by a warming climate. These data reject the universal applicability of the glacial contraction model to temperate taxa and reiterate the importance of considering the natural history of individual species.

Prescribed fire and timber harvest effects on terrestrial salamander abundance, detectability, and microhabitat use

Prescribed fire and timber harvest are anthropogenic disturbances that modify resource availability and ecosystem structure, and can affect wildlife both directly and indirectly. Terrestrial salamanders are effective indicators of forest health due to their high abundance and sensitivity to microclimatic conditions. Given their ecological importance, it is critical to understand how forest salamanders respond to management-related disturbances. We predicted that timber harvest and prescribed fire would decrease salamander abundance and availability, and increase salamander cover object use. We surveyed for southern red-backed salamanders (Plethodon serratus) over 9 sampling periods from 2010 to 2014 in a Missouri Ozark (USA) forest, and used binomial mixture models to estimate abundance and detectability in a large-scale Before-After, Control-Impact (BACI) experiment. Five replicate 5-ha units were randomly assigned to each treatment (prescribed burn, shelterwood harvest, midstory herbicide) and control. We compared abundance, surface activity, detectability, and microhabitat use among treatments. Abundance and surface activity decreased post-treatment in shelterwood, midstory, and burn units. Abundance estimates in midstory and burn units rebounded in the second post-treatment year but declined further in shelterwood harvest units. Overall, treatments had stronger effects on salamander availability than on actual abundance. We also found a higher proportion of salamanders under cover objects after prescribed fire, further illustrating the importance of accounting for imperfect detectability. Our findings foster a more robust understanding of the mechanisms underlying population-level responses to management practices, ultimately increasing our ability to manage terrestrial salamanders effectively.

3D bite modeling and feeding mechanics of the largest living amphibian, the Chinese giant salamander Andrias davidianus (Amphibia:Urodela).

Biting is an integral feature of the feeding mechanism for aquatic and terrestrial salamanders to capture, fix or immobilize elusive or struggling prey. However, little information is available on how it works and the functional implications of this biting system in amphibians although such approaches might be essential to understand feeding systems performed by early tetrapods. Herein, the skull biomechanics of the Chinese giant salamander, Andrias davidianus is investigated using 3D finite element analysis. The results reveal that the prey contact position is crucial for the structural performance of the skull, which is probably related to the lack of a bony bridge between the posterior end of the maxilla and the anterior quadrato-squamosal region. Giant salamanders perform asymmetrical strikes. These strikes are unusual and specialized behavior but might indeed be beneficial in such sit-and-wait or ambush-predators to capture laterally approaching prey. However, once captured by an asymmetrical strike, large, elusive and struggling prey have to be brought to the anterior jaw region to be subdued by a strong bite. Given their basal position within extant salamanders and their “conservative” morphology, cryptobranchids may be useful models to reconstruct the feeding ecology and biomechanics of different members of early tetrapods and amphibians, with similar osteological and myological constraints.

Effects of Buffering Key Habitat for Terrestrial Salamanders: Implications for the Management of the Federally Threatened Red Hills Salamander (Phaeognathus hubrichti) and Other Imperiled Plethodontids

Forestry practices are placing ever increasing emphasis on sustainability and the maintenance of ecological processes, biodiversity, and endangered species or populations. Balancing timber harvest and the management of imperiled species presents a particularly difficult challenge during this shift, as we often know very little about these species’ natural history and how and why silviculture practices affect their populations. Accordingly, investigation of and improvement on current management practices for threatened species is imperative. We investigated the effectiveness of habitat buffers as a management technique for the imperiled Red Hills salamander (Phaeognathus hubrichti) by combining genetic, transect, and body-condition data. We found that populations where habitat buffers have been employed have higher genetic diversity and higher population densities, and individuals have better overall body condition. These results indicate that buffering the habitat of imperiled species can be an effective management tool for terrestrial salamanders. Additionally, they provide further evidence that leaving the habitat of imperiled salamanders unbuffered can have both immediate and long-term negative impacts on populations.

Partitioning detectability components in populations subject to within-season temporary emigration using binomial mixture models.

Detectability of individual animals is highly variable and nearly always < 1; imperfect detection must be accounted for to reliably estimate population sizes and trends. Hierarchical models can simultaneously estimate abundance and effective detection probability, but there are several different mechanisms that cause variation in detectability. Neglecting temporary emigration can lead to biased population estimates because availability and conditional detection probability are confounded. In this study, we extend previous hierarchical binomial mixture models to account for multiple sources of variation in detectability. The state process of the hierarchical model describes ecological mechanisms that generate spatial and temporal patterns in abundance, while the observation model accounts for the imperfect nature of counting individuals due to temporary emigration and false absences. We illustrate our model’s potential advantages, including the allowance of temporary emigration between sampling periods, with a case study of southern red-backed salamanders Plethodon serratus. We fit our model and a standard binomial mixture model to counts of terrestrial salamanders surveyed at 40 sites during 3–5 surveys each spring and fall 2010–2012. Our models generated similar parameter estimates to standard binomial mixture models. Aspect was the best predictor of salamander abundance in our case study; abundance increased as aspect became more northeasterly. Increased time-since-rainfall strongly decreased salamander surface activity (i.e. availability for sampling), while higher amounts of woody cover objects and rocks increased conditional detection probability (i.e. probability of capture, given an animal is exposed to sampling). By explicitly accounting for both components of detectability, we increased congruence between our statistical modeling and our ecological understanding of the system. We stress the importance of choosing survey locations and protocols that maximize species availability and conditional detection probability to increase population parameter estimate reliability.

Antifungal isolates database of amphibian skin‐associated bacteria and function against emerging fungal pathogens

Microbial symbionts of vertebrate skin have an important function in defense of the host against pathogens. In particular, the emerging chytrid fungus Batrachochytrium dendrobatidis, causes widespread disease in amphibians but can be inhibited via secondary metabolites produced by many different skin‐associated bacteria. Similarly, the fungal pathogens of terrestrial salamander eggs Mariannaea elegans and Rhizomucor variabilis are also inhibited by a variety of skin‐associated bacteria. Indeed, probiotic therapy against fungal diseases is a recent approach in conservation medicine with growing experimental support. We present a comprehensive Antifungal Isolates Database of amphibian skin‐associated bacteria that have been cultured, isolated, and tested for antifungal properties. At the start, this database includes nearly 2000 cultured bacterial isolates from 37 amphibian host species across 18 studies on five continents: Africa, Oceania, Europe, and North and South America. As the research community gathers information on additional isolates, the database will be updated periodically. The resulting database can serve as a conservation tool for amphibians and other organisms, and provides empirical data for comparative and bioinformatic studies. The database consists of a FASTA file containing 16S rRNA gene sequences of the bacterial isolates, and a metadata file containing information on the host species, life‐stage, geographic region, and antifungal capacity and taxonomic identity of the isolate.

Effects of timber harvests and silvicultural edges on terrestrial salamanders.

Balancing timber production and conservation in forest management requires an understanding of how timber harvests affect wildlife species. Terrestrial salamanders are useful indicators of mature forest ecosystem health due to their importance to ecosystem processes and sensitivity to environmental change. However, the effects of timber harvests on salamanders, though often researched, are still not well understood. To further this understanding, we used artificial cover objects to monitor the relative abundance of terrestrial salamanders for two seasons (fall and spring) pre-harvest and five seasons post-harvest in six forest management treatments, and for three seasons post-harvest across the edge gradients of six recent clearcuts. In total, we recorded 19,048 encounters representing nine species of salamanders. We observed declines in mean encounters of eastern red-backed salamanders (Plethodon cinereus) and northern slimy salamanders (P. glutinosus) from pre- to post-harvest in group selection cuts and in clearcuts. However, we found no evidence of salamander declines at shelterwoods and forested sites adjacent to harvests. Edge effects induced by recent clearcuts influenced salamanders for approximately 20 m into the forest, but edge influence varied by slope orientation. Temperature, soil moisture, and canopy cover were all correlated with salamander counts. Our results suggest silvicultural techniques that remove the forest canopy negatively affect salamander relative abundance on the local scale during the years immediately following harvest, and that the depth of edge influence of clearcuts on terrestrial salamanders is relatively shallow (<20 m). Small harvests (<4 ha) and techniques that leave the forest canopy intact may be compatible with maintaining terrestrial salamander populations across a forested landscape. Our results demonstrate the importance of examining species-specific responses and monitoring salamanders across multiple seasons and years. Long-term monitoring will be necessary to understand the full impacts of forest management on terrestrial salamanders.

Abundance, biomass production, nutrient content, and the possible role of terrestrial salamanders in Missouri Ozark forest ecosystems

The transfer of energy and nutrients largely depends on the role of animals in the movement of biomass between trophic levels and ecosystems. Despite the historical recognition that amphibians could play an important role in the movement of biomass and nutrients, very few studies have provided reliable estimates of abundance and density of amphibians to reveal their true importance. Here, we provide robust estimates of abundance and density of a dominant species, the Southern Redback Salamander (Plethodon serratus Grobman, 1944), in the oak forest ecosystem of the Ozark Highlands in Missouri. We then use the abundance and density estimates to calculate biomass and nutrient content of salamanders at our study sites in the Ozark forests. Salamanders at the Sinkin Experimental Forest comprise a large amount of protein, energy, and nutrients that greatly exceed estimates derived some 35 years ago in the Hubbard Brook Experimental Forest, New Hampshire. Our estimates (7 300 – 12 900 salamanders·ha−1) are 2–4 times greater than the values reported by Burton and Likens (1975a, Ecology, 56: 1068–1080; 1975b, Copeia, 1975: 541–546). Furthermore, we show that density estimates of other small plethodontid species reported in the literature are nearly an order of magnitude greater than that reported by Burton and Likens. We believe this indicates that previous results have underestimated the importance of salamander biomass, nutrient, and energy flux, and their functional role in regulating invertebrates and carbon retention in forest ecosystems.

Potential reduction in terrestrial salamander ranges associated with Marcellus shale development

Natural gas production from the Marcellus shale is rapidly increasing in the northeastern United States. Most of the endemic terrestrial salamander species in the region are classified as ‘globally secure’ by the IUCN, primarily because much of their ranges include state- and federally protected lands, which have been presumed to be free from habitat loss. However, the proposed and ongoing development of the Marcellus gas resources may result in significant range restrictions for these and other terrestrial forest salamanders. To begin to address the gaps in our knowledge of the direct impacts of shale gas development, we developed occurrence models for five species of terrestrial plethodontid salamanders found largely within the Marcellus shale play. We predicted future Marcellus shale development under several scenarios. Under scenarios of 10,000, 20,000, and 50,000 new gas wells, we predict 4%, 8%, and 20% forest loss, respectively, within the play. Predictions of habitat loss vary among species, but in general, Plethodon electromorphus and Plethodonwehrlei are predicted to lose the greatest proportion of forested habitat within their ranges if future Marcellus development is based on characteristics of the shale play. If development is based on current well locations, Plethodonrichmondi is predicted to lose the greatest proportion of habitat. Models showed high uncertainty in species’ ranges and emphasize the need for distribution data collected by widespread and repeated, randomized surveys.

Proteins and peptides as pheromone signals and chemical signatures

Proteins and peptides are used as pheromones by many invertebrates and vertebrates, on land as well as underwater. These molecules are used as pheromones by aquatic animals such as squid, sea hares, and newts. Males in some terrestrial salamander species use high molecular weight glycopeptide pheromones transferred directly to the nostrils of the female. In Drosophila fruit flies, sex peptides in the male's seminal fluid change the female's behaviour so that after mating she rejects other males and starts to lay eggs. The rapid evolution of Drosophila sex peptides and salamander peptide pheromones suggests that sexual conflict may be involved. In mice, exocrine gland-secreting peptide 1 (ESP1) secreted from the male's tear glands is transferred to the female's nose through physical contact during investigation of the facial areas during courtship. ESP1 activates a narrowly specific vomeronasal receptor, leading to receptive behaviour in the female. The urine marks of male territorial house mice contain high concentrations of highly variable major urinary proteins (MUPs). The MUPs bind small molecule pheromones and other odorants, slowly releasing them and thus greatly prolonging the attractive volatile lifetime of the signal. One of the MUPs, darcin, is the same in all male house mice: it is a pheromone in itself. When the female comes into contact with darcin in a scent mark it prompts a learned attraction to both the male's individual chemical signature mixture and the location of the scent mark. Proteins and peptides may also contribute to the highly variable chemical profiles that differ between individual mammals, for example, and that are used as cues to allow individuals to be distinguished.