Mucus trail following by the snail Biomphalaria glabrata (Say)

An experimental procedure involving time-lapse cinematography was used to investigate the responses of the freshwater pulmonate, Biomphalaria glabrata (Say), to their mucus trails. It has been shown that individuals of this species are capable of following their own trails and also those laid by other individuals of the same species. The capacity of mucus trails to influence snail behaviour is lost after a brief period of between 10 and 30 min. The snails tend to move in the direction the trail was laid with expectation greater than by chance. They do not follow mucus trails laid by another species, Limnaea stagnalis. The possible adaptive significance of trail following is discussed.     

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.     

Trail following behaviour in relation to pedal mucus production in the intertidal gastropod Monodonta labio (Linnaeus)

Trail following behaviour and pedal mucus production were investigated in the mid-shore topshell, Monodonta labio (Linnaeus) in Hong Kong. On the shore, individuals exhibited both conspecific and self trail following while awash on ebb and flood tides, although fidelity to resting sites during emersion on successive days was low. In the laboratory, animals that encountered trails that had been aged on the shore for different periods showed similar patterns of movement (distance moved, speed and tortuosity) suggesting that degradation of cues in the mucus that animals responded to did not occur until > 3 days post-deposition. Animals moved faster, with a lower rate of radular rasping, on freshly laid mucus trails than on a biofilm-covered substratum and did not change their speed when moving over aged (biofilm-covered) mucus compared to fresh mucus. Mucus production rates were similar when animals were crawling on vertical or horizontal surfaces, but significantly more mucus was produced when animals were emersed than when submerged. Mucus trail profiles were of variable thickness, but ‘double’ mucus trails (marker + tracker trails) did not contain significantly more mucus than ‘single’ trails (marker mucus only) and were considerably thinner than single trails suggesting tracker snails utilized mucus laid by marker snails, reducing their own deposition of mucus. Thus, while M. labio do not appear to utilize trails for orientation or refuge location, snails that follow trails have the potential to save energy through reducing mucus production or to gain energy through mucus ingestion. Given the role of pedal mucus production in the overall energy balance of gastropods, such energetic benefits are considerable and may have implications for the life history of the snail.     

The predatory snail Euglandina rosea successfully follows mucous trails of both native and non‐native prey snails

Mucous trail following is a primary means by which many predatory snails locate prey. I compared the ability of individuals of Euglandina rosea to follow mucous trails of two groups of gastropods: those found within its native habitat (southeastern USA), and those found outside its native range (Kansas). Members of E. rosea followed trails for both species found inside and outside its native range equally well. In contrast to previous studies, I found that the predatory snails consistently followed trails in the direction in which they were laid. I quantified the kinematics of trail‐following behavior using inter‐tentacle angle as the primary metric. In both prey groups, there were significant differences in the predator's inter‐tentacle angle when tracking a trail versus not, and when successfully following (in the direction the trail was laid) versus unsuccessfully following (opposite the direction that the trail was laid) trails. In addition, in both prey groups, there were significant differences in the predator's velocity when tracking a trail versus not, and when successfully versus unsuccessfully following trails. This study confirmed that members of E. rosea are robust generalist predators, capable of successfully tracking native and non‐native snails, and should not be introduced as biologic control agents. These results may be useful to managers, as they provide insight into how trail following could be used to trap members of this invasive species.     

A Laboratory study on the visual and chemical orientation of the gastropod Nerita Fulgurans Gmelin, 1791

Behavioural responses of the gastropod Nerita fulgurans Gmelin, 1791 to flat black rectangles and intraspecific mucus trails were measured in a circular arena. Snails were tested in water either in the presence or absence of chemicals generated from a predator gastropod, Chicoreus brevifrons (Lamarck, 1822). The test hypothesis was that this snail has different behavioural responses as result of visual and chemical cue integration. Nerita fulgurans has the capacity to orient to solid targets subtending angles larger than 10° and follow its own mucus trails. In water conditioned by the predator C . brevifrons, snails exhibited an avoidance response when 10°, 20° and 45° sectors were presented, demonstrating an integration of chemical and visual information. The simultaneous presentation of two orienting cues (black sectors and mucus trails) was tested to determine the nature of the interaction. When the two cues were oriented in the same direction there was no effect. When the two cues were presented from directions 180° apart a preference for visual cues over mucus trail cues was evident when the visual angle of the visual cue subtended angles greater than 90°. This result demonstrates a hierarchical usage of the orienting references.     

A Laboratory study on the visual and chemical orientation of the gastropod Nerita Fulgurans Gmelin, 1791

Behavioural responses of the gastropod Nerita fulgurans Gmelin, 1791 to flat black rectangles and intraspecific mucus trails were measured in a circular arena. Snails were tested in water either in the presence or absence of chemicals generated from a predator gastropod, Chicoreus brevifrons (Lamarck, 1822). The test hypothesis was that this snail has different behavioural responses as result of visual and chemical cue integration. Nerita fulgurans has the capacity to orient to solid targets subtending angles larger than 10° and follow its own mucus trails. In water conditioned by the predator C . brevifrons , snails exhibited an avoidance response when 10°, 20° and 45° sectors were presented, demonstrating an integration of chemical and visual information. The simultaneous presentation of two orienting cues (black sectors and mucus trails) was tested to determine the nature of the interaction. When the two cues were oriented in the same direction there was no effect. When the two cues were presented from directions 180° apart a preference for visual cues over mucus trail cues was evident when the visual angle of the visual cue subtended angles greater than 90°. This result demonstrates a hierarchical usage of the orienting references.     

Trail-Following Behaviour in the Malacophagous Larvae of the Aquatic Sciomyzid Flies <Emphasis Type="Italic">Sepedon spinipes spinipes</Emphasis> and <Emphasis Type="Italic">Dictya montana</Emphasis>

The ability of neonate larvae of the aquatic sciomyzids, Sepedon spinipes spinipes (Scopoli) and Dictya montana Steyskal (Diptera), to follow snail mucus trails was assessed using filter paper Y-mazes. On finding a mucus trail, larval behaviour of both species switched from unstimulated to stimulated searching behaviour, the latter being characterised by an increase in larval velocity and the frequency of lateral head taps. When fresh mucus trails were used, all of the neonates displayed a positive response and followed the mucus trail into the experimental arm. In addition, for S. s. spinipes and D. montana 80.00% and 86.67% of larvae respectively exhibited a strong response and followed the trail to its end. The stimulatory substance (s), however, appears to become inactive with time and after 45 minutes none of the tested larvae reached the trail end. These results are discussed in relation to the ability of aquatic species to forage outside of water for prey and the implications for their use in the biological control of nuisance snails.     

Influence of snail mucus trails and first snail meal on the behavior of malacophagous sciomyzid larvae

There has been considerable focus on the natural enemies of snails, particularly those of medical and veterinary significance. Much attention has focussed on members of the Family Sciomyzidae (Diptera), the majority of which feed on a range of mollusc species. However, little is known about the influence of first snail meal on subsequent prey choices, an important consideration in biocontrol. We examined neonate larval responses of Ilione albiseta to fresh and aged snail mucus trails of three snail species. Median neonate response rates to aged mucus trails for all three snail species tested were significantly (P < 0.001) weaker than for fresh mucus trails indicating a strategy which enhances the likelihood of reaching prey snail species without expending energy following “cold” trails. More than 78% of first instar larvae, fed on one snail species (Radix peregra or Stagnicola palustris) and subsequently offered a choice of these two snail species for the second snail meal, selected the snail species of the first snail meal suggesting that the first snail meal influences subsequent prey selection. However, the impact of the first snail meal on larval trail-following behavior is less clear-cut. While there may be some preference for the mucus trail of the snail species on which neonate larvae have fed, this does not exclude the larvae from following the mucus trails of other snail species. The results are discussed in the context of the potential use of I. albiseta as a biocontrol agent of vectors of snail borne diseases.     

Trail Communication During Foraging and Recruitment in the Subterranean Termite Reticulitermes santonensis De Feytaud (Isoptera, Rhinotermitidae)

The search for food in the French subterranean termite Reticulitermes santonensis De Feytaud is organized in part by chemical trails laid with the secretion of their abdominal sternal gland. Trail-laying and -following behavior of R. santonensis was investigated in bioassays. During foraging for food termites walk slowly (on average, 2.3 mm/s) and lay a dotted trail by dabbing the abdomen at intervals on the ground. When food is discovered they return at a quick pace (on average, 8.9 mm/s) to the nest, laying a trail for recruiting nestmates to the food source. While laying this recruitment trail the workers drag the abdomen continuously on the ground. The recruitment trail is highly attractive: it is followed within a few seconds, by more nestmates, and at a quicker pace (on average, 6.4 mm/s) than foraging trails (on average, 2.9 mm/s). The difference between foraging and recruitment trails in R. santonensis could be attributed to different quantities of trail pheromone. A caste-specific difference in trail pheromone thresholds, with workers of R. santonensis being more sensitive to trails than soldiers, was also documented: soldiers respond only to trails with a high concentration of trail pheromone.     

Size‐Dependent Male Mate Preference and its Association with Size‐Assortative Mating in a Mangrove Snail,Littoraria ardouiniana

In many animals, body size plays a crucial role in mating success in the context of competition and preference for mates. Increasing evidence has shown that male mate preference can be size‐dependent and, therefore, an important driver of size‐assortative mating. To test this theory, mate choice experiments were performed during the three consecutive stages of mating behaviour, namely trail following, shell mounting and copulation, in the dioecious mangrove snail, Littoraria ardouiniana. These experiments identified two possible forms of size‐dependent male mate preference which could contribute to the formation of size‐assortative mating in these snails. Firstly, whereas small males were unselective, large males were selective and preferred to follow mucus trails laid by large females. Alternatively, the results can also be interpreted as all males were selective and adopted a mating strategy of selecting females similar to, or larger than, their own sizes. Both small and large males also copulated for longer with large than with small females, and this was more pronounced in large males. When two males encountered a female, they engaged in physical aggression, with the larger male excluding the smaller male from copulating with the female. This study, therefore, demonstrated that size‐dependent male mate preference may, along with male–male competition, play an important role in driving size‐assortative mating in these mangrove snails, and this may also be the case in other species that exhibit male mate choice.     

The trail pheromone of the termite, Trinervitermes trinervoides

By using a T-junction choice assay workers of Trinervitermes trinervoides have been shown to lay and follow pheromone trails. The trials are not polarized and there is a quantitative relation between the number of termites laying the trail and the fraction of test termites which follw correctly. Workers reinforce trails whenever they follow them, and the degree of this reinforcement seems to be independent of trail strength. The trail pheromone is volatile and need not be perceived by contact chemoreception. Activity loss from filter paper is approximately exponential with a half-life of about 2 hr. Extracts of papers over which workers had laid trails were used to show a linear relationship, on a log-probit scale, between dose and response. Soldier termites also follow trails about as well as do workers, but workers lay trails that are about six to seven times as strong as soldier trails. No preference of either caste for their own trails could be demonstrated. Thin-layer chromatography indicated that the trail pheromone(s) is a fairly polar substance.     

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

The 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.     

Crystalline calcium in littorinid mucus trails

Previous work has shown that the feet of terrestrial and freshwater snails are important in calcium regulation, often secreting granules of CaCO₃. This phenomenon has not, until now, been observed in marine snails. Here we report the presence of CaCO₃ granules in the trail mucus of Littorina littorea (L.), L. saxatilis (Olivi) and L. obtusata (L.) Fixed mucus trails on plastic coverslips were examined by X-ray microanalysis under the SEM. Of the single-metal granules observed in the mucus trails the most abundant were of calcium (means: L. littorea, 440 mm⁻²; L. saxatilis, 401 mm⁻²; L. obtusata, 348 mm⁻²) followed for each species by silicon (maximum mean density: L. saxatilis, 120 mm⁻²) and iron (maximum mean density: L. saxatilis, 65 mm⁻²) granules. Single-metal granules of Al, Ti, Mg and P were also found but only in the mucus trails of L. obtusata, perhaps reflecting its different collection site from the other two species. The mean size of the calcium granules showed significant interspecific variation (L. littorea, 1.32 μm diameter±0 08 μm, n = 143; L. saxatilis, 1.80 μm±0.12, n = 113; L. obtusata, 2.14 μm±0.09, n = 167). Most calcium granules (L. littorea, 80%, n = 35; L. saxatilis, 57%, n = 113; L. obtusata, 69%, n = 167) were attached to, or embedded within, microthreads of mucus which tended to run parallel to the direction of locomotion. The significance of this is unknown although it may imply that the CaCO₃ granules are secreted with the mucus. It is concluded that calcium losses via this route are too small for pedal mucus to function significantly in ionoregulation of calcium. The calcium in the trail may therefore perform other functions, for example indicating trail polarity.     

Foraging dynamics in the group-hunting myrmicine ant,Pheidologeton diversus

Pheidologeton diversus workers group-hunt (that is, search for food in raiding groups) and are in this way remarkably convergent with army ants (Dorylinae and Ecitoninae). Raids appear usually to take independent courses and are capable of tracking areas of high food density. However, raid advance is not dependent on continual food discovery at the raid front, since raids can advance over areas without food. Most raids extend from trunk trails, which originate when the basal trail of a raid remains in use even after the original raid has ceased. Trunk trails can last at least as long as 10 weeks, with the terrain and the distance to the nest influencing the trail stability. Territories are limited to the trail systems, with rich food items in particular being vigorously defended. Group hunting permits P. diversus to quickly harvest booty, usurp foods from competing species, and capture large prey. This strategy is compared with the raiding strategies of other ants. I hypothesize that group hunting originated from an ancestor which hunted solitarily from trunk trails through the acceleration of trail production and reduction in worker autonomy.     

Male discrimination of female mucous trails permits assortative mating in a marine snail species

Recent research has shown the potential for nonallopatric speciation, but we lack an adequate understanding of the mechanisms of prezygotic barriers and how these evolve in the presence of gene flow. The marine snail Littorina saxatilis has distinct ecotypes in different shore microhabitats. Ecotypes hybridize in contact zones, but gene flow is impeded by assortative mating. Earlier studies have shown that males and females of the same ecotype copulate for longer than mates of different ecotype. Here we report a new mechanism that further contributes to reproductive isolation between ecotypes in the presence of gene flow. This mechanism is linked to the ability of males to track potential partners by following their mucous trail. We show that cliff ecotype males follow the trails of females of the same ecotype for longer than females of the alternate (boulder) ecotype. In addition, cliff males are more likely to follow the mucous trail in the correct direction if the trail is laid by a cliff-female. The capacity to discriminate the ecotype of female mucous trails combined with differential copulation times creates a strong prezygotic reproductive barrier between ecotypes of L. saxatilis that reduces gene flow from cliff to boulder ecotypes by >/=80%.     

Does trace density reflect tracemaker density? A test using intertidal gastropods on San Salvador Island,the Bahamas

Abstract

Trace densities may be a potential proxy for tracemaker densities, especially in settings where traces but not body fossils preserve well. The relationship between the density of the gastropod Batillaria minima and its trails was examined in a modern muddy intertidal zone of a lagoon on San Salvador Island, the Bahamas. The number of snails found within a quadrat was a moderately positive predictor of the number of trails that crossed the quadrat’s boundaries. This suggests in some modern ecological systems, trace density is a reasonable proxy for tracemaker density. However, in some cases, high densities of snails are found without correspondingly high trail densities, which may be driven by the snails clumping or moving little, perhaps to access shared resources. Observations of tagging individual snails and speed measurements also suggest that B. minima disperses around this type of mudflat habitat a few tens of centimeters a day.     

The predatory mite <Emphasis Type="Italic">Neoseiulus womersleyi</Emphasis> (Acari: Phytoseiidae) follows extracts of trails left by the two-spotted spider mite <Emphasis Type="Italic">Tetranychus urticae</Emphasis> (Acari: Tetranychidae)

As it walks, the two-spotted spider mite Tetranychus urticae Koch (Acari: Tetranychidae) spins a trail of silk threads, that is followed by the predatory mite, Neoseiulus womersleyi Schicha (Acari: Phytoseiidae). Starved adult female N. womersleyi followed T. urticae trails laid down by five T. urticae females but did not follow a trail of one T. urticae female, suggesting that the amount of spun threads and their chemical components should correlate positively with the number of T. urticae individuals. To examine whether chemical components of T. urticae trails are responsible for the predatory mite’s trail following, we collected separate T. urticae threads from the exuviae and eggs, and then washed the threads with methanol to separate chemical components from physical attributes of the threads. Female N. womersleyi did not follow T. urticae trails that had been washed with methanol but contained physical residues, but they did follow the direction to which the methanol extracts of the T. urticae trails was applied. These results suggest that the predatory mite follows chemical, not physical, attributes of T. urticae trails.     

On the mechanism of sperm release in three gobiid fishes (Teleostei: Gobiidae)

Synopsis In fish, gamete release is commonly assumed to be synchronous in externally inseminating fishes. By collecting and counting the number of sperm and eggs released during separate matings in three demersal spawners, the mediterranean gobies, Zosterisessor ophiocephalus, Gobius niger, and Knipowitschia panizzae, we observed that gametes are released asynchronously. Males release sperm before females start laying their eggs. Sperm is released in the form of sperm trails laid on the nest surface; subsequently active spermatozoa leave the trails and move in the water for several minutes. Sperm trails consist of bands of viscous material in which sperm is embedded. In most cases eggs are not laid directly over the sperm trail, suggesting that sperm may contact the eggs after the latter are released in the water. Male sperm duct glands, seminal vesicles, known to secrete mucosubstances, are likely involved in the production of sperm trails. The possible influence of this mode of insemination on the mating style of marine gobies is discussed.     

Trail‐sharing among tropical ants: interspecific use of trail pheromones?

1. Trail‐sharing between different ant species is rare and restricted to a small number of species pairs. Its underlying mechanisms are largely unknown. For trail‐sharing to occur, two factors are required: (i) one or both species must recognise the other species or its pheromone trails and (ii) both species must tolerate each other to a certain extent to allow joint use of the trail. A species that follows another's trails can efficiently exploit the other's information on food sources contained in the pheromone trails. Hence, food competition and thus aggressive interactions between a species following another's trail and the species being followed, seem likely. 2. In the present study, we investigated interspecific trail following and interspecific aggression in trail sharing associations (i) among Polyrhachis ypsilon, Camponotus saundersi, and Dolichoderus cuspidatus, and (ii) among Camponotus rufifemur and Crematogaster modiglianii. We tested whether trail‐sharing species follow each other's pheromone trails, and whether the ants tolerated or attacked their trail‐sharing partners. In both associations, we confronted workers with pheromone trails of their associated species, and, for the former association, measured interspecific aggression among the trail‐sharing species. 3. In our assays, D. cuspidatus and C. rufifemur regularly followed heterospecific pheromone trails of P. ypsilon and C. modiglianii, respectively. However, only few workers of the remaining species followed heterospecific pheromone trails. Thus, shared trails of P. ypsilon and C. saundersi cannot be explained by interspecific trail‐following. 4. Interspecific aggression among P. ypsilon, C. saundersi, and D. cuspidatus was strongly asymmetric, C. saundersi being submissive to the other two. All three species differentiated between heterospecific workers from the same or another site, suggesting habituation to the respective trail‐sharing partners. We therefore hypothesise that differential tolerance by dominant ant species may be mediated by selective habituation towards submissive species and this way determines the assembly of trail‐sharing associations.     

The Dynamics of Foraging Trails in the Tropical Arboreal Ant Cephalotes goniodontus

The foraging behavior of the arboreal turtle ant, Cephalotes goniodontus, was studied in the tropical dry forest of western Mexico. The ants collected mostly plant-derived food, including nectar and fluids collected from the edges of wounds on leaves, as well as caterpillar frass and lichen. Foraging trails are on small pieces of ephemeral vegetation, and persist in exactly the same place for 4–8 days, indicating that food sources may be used until they are depleted. The species is polydomous, occupying many nests which are abandoned cavities or ends of broken branches in dead wood. Foraging trails extend from trees with nests to trees with food sources. Observations of marked individuals show that each trail is travelled by a distinct group of foragers. This makes the entire foraging circuit more resilient if a path becomes impassable, since foraging in one trail can continue while a different group of ants forms a new trail. The colony’s trails move around the forest from month to month; from one year to the next, only one colony out of five was found in the same location. There is continual searching in the vicinity of trails: ants recruited to bait within 3 bifurcations of a main foraging trail within 4 hours. When bait was offered on one trail, to which ants recruited, foraging activity increased on a different trail, with no bait, connected to the same nest. This suggests that the allocation of foragers to different trails is regulated by interactions at the nest.