Conspecific Trails Research Articles

Testing presence of directionality information in female spider silk trails through male trail-following behavior

Mate search is challenging for solitary species. Trails represent a particularly potent, target-oriented means for finding mates, as trail-following increases encounter rates between individuals compared to random search. Embedding directionality information into the trail allows individuals to follow trails correctly to the source. Yet, directionality remains poorly understood. Spiders deposit trails during locomotion consisting of silk lines and substrate-borne chemicals. We conducted multiple experiments to test whether female silk trails convey directionality information, whether directionality is chemically or structurally encoded and depends on female phenotype. We also examined whether males interact with silk in a way that suggests information gathering. We exposed males of the cursorial spider Pisaura mirabilis to female trails deposited unidirectionally and scored their trail-following direction (i.e., same as or opposite to the females’). Tests were repeated after washing trails with a solvent to remove putative chemicals and by sourcing silk from females of different feeding regimes. While we found little evidence for male directional trail-following, we did find that unwashed trails were more likely to be followed than washed trails. Similarly, trails of relatively larger females were more likely to be followed correctly than those of smaller females. Males extensively probed and pulled on silk lines with their appendages, suggesting the gathering of chemical and tactile information. Taken together, results suggest that directional trail-following is selected only under specific contexts in this species. Chemical attributes of trails may convey information on female quality, with directional trail-following reflecting male mate choice in a system characterized by costly male nuptial gifts.Significance statementIn the context of male mate search, following conspecific trails increases the chances of encountering a mating partner, especially if trails provide information about the direction the conspecific went. Yet, trail directionality remains poorly understood. Female spiders deposit silk trails as they walk. We overall show that males follow trails directionally only under a specific context. Males were more likely to follow correctly when trails were unmanipulated (compared to being washed with solvents to remove chemicals) and when they were deposited by relatively larger females (compared to smaller ones). Chemical attributes of trails may potentially indicate directionality, while decoding movement direction from trails of larger females may reflect male preferences for females of higher reproductive value.

How fast is a snail’s pace? The influences of size and substrate on gastropod speed of locomotion

AbstractTerrestrial gastropods display monotaxic direct crawling. During locomotion, smooth muscle contraction stimulates a series of pedal waves that move along the ventral surface of the foot. These waves interact with a thin layer of mucus produced by the foot, propelling the animal forward. Although the mechanism by which this process occurs has been well studied, less is known about how morphological or environmental factors affect this process, and ultimately how they may alter the speed of propulsion. In this study, we tested the influences of body size, substrate type, and substrate orientation on crawling speed in the terrestrial snail Cornu aspersum. We found that substrate texture and orientation had a strong effect on speed, whereas snail body size and the presence of a conspecific trail did not. Crawling speed across rough sandpaper was the most striking, showing a clear inversely proportional relationship between the size of abrasive particle and speed. We suggest that this may be the result of substrate attributes interfering with mucus adhesion or mucus production, subsequently affecting locomotion, although gait choice or the frequency and length of each pedal wave may also play a role.

Conspecific chemical cues facilitate mate trailing by invasive Argentine black and white tegus.

Squamate reptiles (snakes and lizards) rely on chemical cues from conspecifics to search the environment for potential mates. How such cues are used by invasive species to facilitate reproduction, especially seasonally, is a key question that can inform management practices. The Argentine black and white tegu (Salvator merianae) is an invasive reptile species in south Florida threatening native fauna in biodiverse regions such as Everglades National Park. While some information exists on the reproductive ecology of this species in its native range in South America, the chemical ecology of S. merianae is unclear especially in its invasive range. By testing both male (n = 7) and female (n = 7) tegus in a Y-maze apparatus, we assessed if either sex follows chemical trails left by conspecifics and if behaviors were sex- or season-specific. We conducted three types of trials where conspecifics created odor trails: Male-only (male scent only in base and one arm of Y), Female-only, and Male vs. female. Males did not preferentially follow scent trails from either sex, but they did differentially investigate conspecific scent from both sexes. Seasonally, males showed increased rates of chemosensory sampling (rates of tongue-flicking) during the spring (breeding season; March-May) compared to fall (non-breeding season; September-November). Males also had reduced turning and pausing behavior while trailing in the spring. Female tegus exhibited stronger conspecific trailing abilities than males, following both male and female scent trails, and they explored the maze less before making an arm choice. Females also investigated the scent trails intensely compared to males (more passes in scented arms, more time with scent trails). Our results demonstrate for the first time that females of an invasive reptile species can follow conspecific scent trails. Given the strong female responses to odor, sex-specific targeting of tegus via application of a conspecific chemical cue in traps could enhance removal rates of females during the breeding season.

Strangers in the dark: behavioral and biochemical evidence for trail pheromones in Hawaiian tree snails

AbstractThe importance of pheromones in insect and mammal social systems is well documented, but few studies have addressed the role of pheromones in land snail behavior. In this investigation, we used a series of behavioral trials and direct analysis in real time mass spectrometry (MS) to test the hypothesis that land snails use mucous trails in orientation and chemical communication. We worked with six endemic Hawaiian land snail species in four genera, three subfamilies, and two families. We tested conspecific trail following in five of these species, and trail following occurred at a statistically significant frequency for each of the species tested (n=181, p‐values ranged <0.0001–0.0494). Percentage of conspecific trials that showed trail following ranged 66.7–94.1%. None of the interspecific tests revealed evidence of trail following among species (n=105, with p‐values of 0.0577–0.5000). Juvenile achatinelline snails did not follow trails of conspecific juveniles (n=30, p=0.5722) or adults (n=30, p=0.4278), nor did adults follow juvenile trails (n=30, p=0.5722). Comparative MS analysis of adult and juvenile trails showed distinct chemical signatures in the two groups. Signals corresponding to medium‐ and long‐chain fatty acids and other unidentified small molecules were present in adult but not in juvenile trails. Considered together, these results support the hypotheses that trail following could serve an important social and reproductive function. This discovery provides evidence for the presence of an ephemeral tree snail pheromone, which could have important implications for the conservation of these increasingly rare and threatened species.

Feeding Behavior of the Wrinkled Dove SnailAmphissa columbiana

The wrinkled dove snail (Amphissa columbiana) is a columbellid gastropod common in marine waters along the west coast of North America. This species has long been anecdotally described as an opportunistic scavenger, but little is known about its diet or scavenging behaviors. A. columbiana were observed at subtidal sites within the San Juan Islands, Washington to document associations with potential food items. Laboratory experiments were done to determine what this species eats and how it finds food. In the field, A. columbiana were often found on dead or damaged organisms, frequently in aggregations. In the laboratory, the snails consumed a broad range of dead or damaged invertebrate prey, showing little discrimination. They appear to locate food resources primarily through chemosensory cues, often following conspecific mucus trails and sometimes congregating around actively feeding sea stars. The chemical cues that draw A. columbiana to food act as feeding stimulants; the addition of scent from a damaged animal induced the snails to feed on healthy prey. The ability to sense chemical cues from damaged animals, including those being consumed by feeding sea stars, creates scavenging opportunities other gastropods may be unable to exploit.

Snails and their trails: the multiple functions of trail‐following in gastropods

Snails are highly unusual among multicellular animals in that they move on a layer of costly mucus, leaving behind a trail that can be followed and utilized for various purposes by themselves or by other animals. Here we review more than 40 years of experimental and theoretical research to try to understand the ecological and evolutionary rationales for trail-following in gastropods. Data from over 30 genera are currently available, representing a broad taxonomic range living in both aquatic and terrestrial environments. The emerging picture is that the production of mucus trails, which initially was an adaptation to facilitate locomotion and/or habitat extension, has evolved to facilitate a multitude of additional functions. Trail-following supports homing behaviours, and provides simple mechanisms for self-organisation in groups of snails, promoting aggregation and thus relieving desiccation and predation pressures. In gastropods that copulate, trail-following is an important component in mate-searching, either as an alternative, or in addition to the release of water- or air-borne pheromones. In some species, this includes a capacity of males not only to identify trails of conspecifics but also to discriminate between trails laid by females and males. Notably, trail discrimination seems important as a pre-zygotic barrier to mating in some snail species. As production of a mucus trail is the most costly component of snail locomotion, it is also tempting to speculate that evolution has given rise to various ways to compensate for energy losses. Some snails, for example, increase energy intake by eating particles attached to the mucus of trails that they follow, whereas others save energy through reducing the production of their own mucus by moving over previously laid mucus trails. Trail-following to locate a prey item or a mate is also a way to save energy. While the rationale for trail-following in many cases appears clear, the basic mechanisms of trail discrimination, including the mechanisms by which many snails determine the polarity of the trail, are yet to be experimentally determined. Given the multiple functions of trail-following we propose that future studies should adopt an integrated approach, taking into account the possibility of the simultaneous occurrence of many selectively advantageous roles of trail-following behaviour in gastropods. We also believe that future opportunities to link phenotypic and genotypic traits will make possible a new generation of research projects in which gastropod trail-following, its multitude of functions and evolutionary trade-offs can be further elucidated.

Conspecific pheromone trailing and pheromone trail longevity in the African Colubrid Boaedon fuliginosus

In snakes, pheromone trailing is a strategy used for long-distance location of conspecifics. The two existing hypotheses for this behaviour are: a) to locate individuals for reproductive purposes; and b) to form aggregations during the winter/dry season. Pheromone trailing for reproductive purposes has been observed in over 20 snake species representing four different families. The ability of adult male African brown house snakes (Boaedon fuliginosus) to track a sexually attractive female (assumed to be producing pheromones), as well as a conspecific male, was tested using a standard Y-maze. The length of time a female's pheromone remained distinguishable to a male was also tested using the same methodology. Male B. fuliginosus showed a strong ability to trail females both immediately after the trail was left by a female (100%; n=14) and seven days after a female left a trail (100%; n=14). After 14 days, however, only 71.4% (n=14) of males chose the same arm as the female, demonstrating that the pheromone trail degraded over time. Males also trailed other males in 77.8% (n=18) of trials, which suggests that males may use other male trails to locate females, or navigate through unfamiliar territories.

Trail Marking by Caterpillars of the Silverspot ButterflyDione Juno Huascuma

A pheromone is implicated in the trail marking behavior of caterpillars of the nymphalid silverspot butterfly, Dione juno huascuma (Reakirt) (Lepidoptera: Heliconiinae) that feed gregariously on Passiflora (Malpighiales: Passifloraceae) vines in Mexico. Although they mark pathways leading from one feeding site to another with silk, this study shows that the silk was neither adequate nor necessary to elicit trail following behavior. Caterpillars marked trails with a long-lived pheromone that was deposited when they brushed the ventral surfaces of the tips of their abdomens along branch pathways. The caterpillars distinguished between pathways deposited by different numbers of siblings and between trails of different ages. Caterpillars also preferentially followed the trails of conspecifics over those of another nymphalid, Nymphalis antiopa L., the mourning cloak butterfly.

Social behavior and pheromonal communication in reptiles

The role of pheromones in orchestrating social behaviors in reptiles is reviewed. Although all reptile orders are examined, the vast majority of the literature has dealt only with squamates, primarily snakes and lizards. The literature is surprisingly large, but most studies have explored relatively few behaviors. The evolution of chemical signaling in reptiles is discussed along with behaviors governed by pheromones including conspecific trailing, male-male agonistic interactions, sex recognition and sex pheromones, and reptilian predator recognition. Nonreptilian prey recognition by chemical cues was not reviewed. The recent literature has focused on two model systems where extensive chemical ecology studies have been conducted: the reproductive ecology of garter snakes and the behavioral ecology of Iberian lacertid lizards. In these two systems, enough is known about the chemical constituents that mediate behaviors to explore the evolution of chemical signaling mechanisms that affect life history patterns. In addition, these models illuminate natural and sexual selection processes which have lead to complex chemical signals whose different components and concentrations provide essential information about individuals to conspecifics. Reptiles provide excellent candidates for further studies in this regard not only in squamates, but also in the orders where little experimental work has been conducted to date.

Perceptual differences in trail-following leaf-cutting ants relate to body size

Leaf-cutting ants of the genus Atta have highly size-polymorphic workers, and size is related to division of labor. We studied trail-following behavior of different-sized workers in a laboratory colony of Atta vollenweideri. For small and large workers, we measured responsiveness and preference to artificial conspecific and heterospecific pheromone trails made from poison gland extracts of A. vollenweideri and A. sexdens. Responsiveness was measured as the probability of trail-following, and preference was measured by testing the discrimination between one conspecific and one heterospecific trail. Minute amounts of the releaser component methyl-4-methylpyrrole-2-carboxylate (0.4 pg/1 m), present in both, conspecific and heterospecific trails, suffice to elicit trail-following behavior. Workers followed heterospecific trails, and these trails (after normalizing their concentration) were as effective as conspecific trails. Small workers were less likely to follow a trail of a given concentration than large workers. In the discrimination test, small workers preferred the conspecific trail over the heterospecific trail, whereas large workers showed no significant preference. It is suggested that large workers primarily respond to the releaser component present in both trails, whereas small workers focus more on the conspecific traits provided by the blend of components contained in the trail pheromone.

Investigation in the laboratory of mucous trail detection in the terrestrial pulmonate snail Mesodon thyroidus (Say, 1817) (Mollusca: Gastropoda: Polygyridae)*

Many gastropods, including limpets, periwinkles, and mud snails, detect and follow mucous trails. The stylommatophoran pulmonate snail Mesodon thyroidus follow conspecific trails in the field, potentially following in the direction they were laid, as has been demonstrated for other pulmonates. This study investigated whether individuals of M. thyroidus directionally follows conspecific trails, and whether substrate type or incline influences trail following. Trail following was quantified on plexiglas and glass surfaces at horizontal, vertical, and 45° inclines. On horizontal plexiglas surfaces, 36% of M. thyroidus followed a marker trail made by a conspecific (n = 11). On horizontal glass surfaces, 45% of the snails followed a marker trail (n = 20). On glass (all inclines combined) 75% of snails that followed a conspecific trail followed it in the same direction it was laid (n = 60). On plexiglas (all inclines combined) 86% of trail-following proceeded in the direction the trail was laid (n = 33). The di...

Initial Den Location Behavior in a Litter of Neonate Crotalus horridus (Timber Rattlesnakes)

Abstract In September 2003, we monitored the movements of a postpartum Crotalus horridus (Timber Rattlesnake) and her four neonates via radiotelemetry. Upon dispersal, two neonates maintained a close association with the mother, but within one week they were making independent movements. Total movement distance by all five snakes during the first 10 days varied considerably (mother: 22 m; neonates: 3, 21, 49, and 154 m). Continued movements by neonates were independent and sporadic, with individuals staying several days in single locations. Excluding one neonate, all individuals converged to a single wooded, rocky hillside for hibernation (320 m from birth site). During their movements to the hibernaculum, one neonate was found with a subadult female and another neonate was found again with its mother. Our observations support the hypothesis that conspecific trails may be used by neonates during their initial den location.

A predatory snail distinguishes between conspecific and heterospecific snails and trails based on chemical cues in slime

The rosy wolfsnail, Euglandina rosea, is a predatory snail native to the southeastern United States. It eats other snails and slugs, tracking them by following their mucus trails. Although wolfsnails follow mucus trails of both prey and conspecifics, they rarely eat conspecifics, and only conspecific trails are followed directionally. We investigated how wolfsnails distinguish conspecifics from prey snails (Helix aspersa) and how they determine directionality of conspecific mucus trails. We found that wolfsnails used chemical cues present in mucus to distinguish conspecifics from prey, and were less likely to attack a snail covered with wolfsnail mucus than one covered with prey mucus (experiment 1). Juvenile wolfsnails that were isolated from conspecifics before hatching recognized conspecifics as nonprey (experiment 2), and adult wolfsnails learned to follow trails of novel substances associated with exposure to other wolfsnails (experiment 3). Wolfsnails were equally attracted to both soluble and insoluble components of conspecific mucus (experiment 4) and followed conspecific mucus trails directionality even after the trails had been washed (experiment 5). We also examined whether a structural or chemical asymmetry in conspecific mucus allowed wolfsnails to determine directionality of conspecific trails. Although results of scanning electron microscopy provided no support for directionality using a structural asymmetry, manipulations of wolfsnail trails (experiments 6, 7) indicated that wolfsnails use a right/left chemical asymmetry in mucus trails to orient themselves on conspecific trails in the same direction as the trail-layer snail, independent of the trail layer's direction of movement.

Why Did the Snake Cross the Road? Effects of Roads on Movement and Location of Mates by Garter Snakes (Thamnophis sirtalis parietalis)

Shine, R., M. Lemaster, M. Wall, T. Langkilde and R. Mason 2004. Why Did the Snake Cross the Road? Effects of Roads on Movement and Location of Mates by Garter Snakes (Thamnophis sirtalis parietalis). Ecology and Society 9(1):9. https://doi.org/10.5751/ES-00624-090109

Comparative analysis of food‐finding behavior of an herbivorous and a carnivorous land snail

Abstract. Although the olfactory capabilities of land snail tentacles have been tested by lesion studies and unilateral exposure of tentacles to specific odors, studies of a carnivorous species suggest that the anatomical similarities of herbivorous and carnivorous land snails may belie a fundamental difference in the way these structures are used to find food. Therefore, we challenged the herbivore, Anguispira alternata, and the carnivore, Haplotrema concavum, to find a stationary food source (carrot and caged young prey snail, respectively) under identical still air conditions. The herbivore traveled a significantly shorter distance to the food, even negotiating a barrier placed halfway between the snail and its food. The carnivore, on the other hand, followed a circuitous, apparently random, path to the food. Subsequent tests revealed that H. concavum readily follows prey slime trails while A. alternata seldom follows conspecific slime trails when a distant food source is available. These results are consistent with what might be expected as adaptations to the usually mobile nature of carnivore prey and the stationary nature of herbivore food plants. The ability of A. alternata to exhibit typical detour behavior is noted.

Evidence for a female sex pheromone mediating male trailing behavior in the red-sided garter snake, Thamnophis sirtalis parietalis

Male garter snakes locate females during the breeding season utilizing conspecific trailing behavior. It has been hypothesized that the female-derived chemical cue responsible for mediating male reproductive trailing behavior is the sexual attractiveness pheromone, a previously characterized contact pheromone responsible for releasing male courtship behavior. To examine this hypothesis, we tested the response of male red-sided garter snakes, Thamnophis sirtalis parietalis, to pheromone trails produced by males, females and ‘she-males’. She-males are a small subset of males in the natural population that are morphologically and behaviorally similar to other males except that they produce and express the sexual attractiveness pheromone during the breeding season. When tested on a Y-maze, males were found to detect and follow the skin lipid trails of females and she-males, but displayed no behavioral responses to male trails. In addition, males were unable to discriminate between she-male and female trails when given a choice. These results are consistent with the hypothesis that the sexual attractiveness pheromone is the chemical cue primarily utilized by males to mediate reproductive trailing behavior.

Effects of trematode parasitism on the behaviour and ecology of a common marine snail (Littorina littorea (L.)).

Cryptocotyle lingua (Creplin) is a digenean trematode parasite of the littoral prosobranch gastropod Littorina littorea (L.). The literature suggests the snails become infected by grazing guano of the final host, the herring gull, Larus argentatus Pontoppidan. The parasite emerges from the snail as free-swimming cercariae. Interactions between the snail and the parasite at cellular and life-history levels are well established, but little is known of the influences the interaction has on the behaviour and the ecology of the snail. We tested the response of the snail to encounters with cercariae, examined the longevity of the guano on-shore and tested the responses of the snail to encounters with guano. Over half the L. littorea tested were able to detect both cercariae and a filtered homogenate of cercariae in conspecific mucus trails, approximately one-third of animals refusing to cross the treatments. Chemoreception by the mouth or foot is considered the most likely means of detection. Guano samples (mean weight 3.22 g) naturally deposited at approximately mid-tide level were completely washed away by one tidal inundation. We consider this period too brief to allow for ingestion of eggs in guano by the snail. Further, snails would not cross guano placed in conspecific trails. Most snails would not cross guano diluted by 10(3)x(10 mg ml(-1)) and some snails could still detect guano diluted by 10(6)x(10 &mgr;g ml(-1)), though all were prepared to cross it. Detection of guano is again believed to be by chemoreception by the mouth or foot. These results are discussed in terms of the mating and aggregating behaviour of L. littorea. Ingestion of the parasite by L. littorea is likely to take place once the guano has washed away as the eggs are negatively buoyant in seawater and may adhere to rock (biofilm) or algal fronds which may be grazed by the snail.

Conspecific trailing behaviour of red-sided garter snakes, Thamnophis sirtalis parietalis, in the natural environment

The ability of animals to orient based on pheromonal cues in the environment can have significant consequences to their reproductive success and survival. For example, it is hypothesized that snakes use pheromone trails to locate potential mates during the breeding season and to locate winter hibernacula. Numerous studies have demonstrated that snakes are capable of detecting and following pheromone trails in the laboratory, but it has yet to be shown experimentally whether snakes use such behaviour in their natural environment. In this study, we conducted trailing experiments to test the response of adult red-sided garter snakes to pheromone trails on the natural substrate under naturally occurring conditions during two periods, the spring breeding season and the autumn migration back to the hibernacula. Male snakes detected and followed female trails in the spring, while neither sex displayed trailing behaviour during the period of autumn migration. Our results suggest that adult garter snakes use pheromone trails for locating potential mates during the breeding season and most likely rely on other mechanisms (e.g. visual cues) for navigation to overwintering hibernacula.

Sperm delivery and egg production of the simultaneously hermaphroditic land snail Arianta arbustorum exposed to an increased sperm competition risk

Summary Sperm competition theory predicts that males exposed to an increased risk of sperm competition should maximize fertilization prospects by inseminating more sperm per ejaculate. We designed a laboratory experiment to examine the effect of increased sperm competition risk on male and female reproductive traits in individuals of the simultaneously hermaphroditic land snail Arianta arbustorum. Courtship behaviour, spermatophore size and number of sperm delivered were not influenced by a higher sperm competition risk. However, snails constantly exposed to mucous trails of conspecifics deposited more egg batches than snails denied any cues from conspecific mucous trails. On the individual level, the number of sperm delivered was positively correlated with the number of eggs produced. This finding contradicts the basic prediction of sex allocation theory that there is a trade-off between resources allocated to male and female function in simultaneous hermaphrodites. Most probably this trade-off may only occur if resources are limited.

Role of mucus trails and trail-following in the behaviour and nutrition of the periwinkle Littorina littorea

Gastropod locomotion typically involves the deposition of a mucus trail. This trail can be energetically costly, and its producer could defray this cost if the trail were to perform some post-deposition function. Here we report laboratory experiments aimed at assessing the potential role in nutrition of the mucus trail of the common intertidal periwinkle Littorina littorea (L.). Mucus trails bound more microalgal cells from suspension than did a glass substratum, microalgal densities increasing with period of exposure to the suspension up to ∼5-8 h. After this time adhesion was less (but still greater than to glass). Amphora coffeaeformis (pennate diatom) adhered in greater densities than did Tetraselmis suecica (flagellate prasinophyte). Mucus trails containing microalgae of both species (∼ 50 to 100 cells mm -2 ; approximatly the conditions on-shore) induced a greater degree of trail-following than did bare trails. Individuals followed conspecific trails longer than they did their own trails. Winkles moved significantly slower on bare mucus trails (mean = 0.35 mm s -1 ) than on glass (0.68 mm s -1 ), though the addition of microalgae to mucus increased the speed of the winkles, A. coffeaeformis significantly so. Feeding rate (rate of radular rasping) was also significantly increased on trails containing A. coffeaeformis (mean = 17.8 bites min - 1 ) and T. suecica (12.9 bites min -1 ) in comparison to control trails (4.3 bites min -1 ), where a form of searching behaviour occurred. Microalgae embedded in mucus were seen to enter the mouth. Only 3 out of 40 periwinkles showed any radular activity on glass. Following the passage of a winkle, the density of A. coffeaeformis was reduced by ∼38% and that of T. suecica by 43%. Winkles can clearly exploit food (microalgae) in conspecific mucus trails and in doing so modify their trail-following and feeding behaviour. Thus trail-following seems inextricably linked to nutrition. Since much of the intertidal is likely to be covered with a layer of mucus - or its degradation products - those experiments on trail-following that used 'clean' substrata were not representative of the field. Distribution patterns of both L. littorea and benthic microalgae might be shaped by the ability of mucus trails to bind microalgae and by their subsequent exploitation by the grazer.