Terence P. T. Ng

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.

Mucus trail following as a mate-searching strategy in mangrove littorinid snails

Mate searching often involves chemical cues and is a key process in determining fitness in most sexually reproducing animals. Effective mate-searching strategies are, therefore, essential for individuals to avoid wasting resources as a result of misrecognition of mating partners. Marine snails in the genus Littoraria are among the most successful molluscan groups that live closely associated with mangroves. Their population densities are often low, and finding a mate within the complex three-dimensional habitat of tree leaves, branches and trunks requires an effective searching strategy. We tested whether males of L. ardouiniana and L. melanostoma located females by following their mucus trails. In the laboratory, male tracker snails followed mucus trails laid by conspecific female marker snails at a higher intensity compared with other markeretracker sex combinations in the mating season, but not in the nonmating season, and this was more pronounced in L. ardouiniana. Male trackers did not move faster when following the trails of conspecific female markers compared with other sex combinations; however, tracker snails moved faster in the mating than in the nonmating season, although this might be related to temperature. In both species, males tracked females regardless of trail complexity, and the majority of male trackers were able to detect the direction (polarity) of the trails of conspecific females. Together with previous studies on rocky shore Littorina species, these findings suggest that sex pheromones are incorporated into mucus trails to facilitate the reproductive success of these snails. Mucus trail following is, therefore, an adaptive mate-searching strategy in intertidal gastropod molluscs, and potentially in other gastropod groups in which trail-following behaviour is prevalent.

Cheating the Locals: Invasive Mussels Steal and Benefit from the Cooling Effect of Indigenous Mussels.

The indigenous South African mussel Perna perna gapes during periods of aerial exposure to maintain aerobic respiration. This behaviour has no effect on the body temperatures of isolated individuals, but when surrounded by conspecifics, beneficial cooling effects of gaping emerge. It is uncertain, however, whether the presence of the invasive mussel Mytilus galloprovincialis limits the ability of P. perna for collective thermoregulation. We investigated whether varying densities of P. perna and M. galloprovincialis influences the thermal properties of both natural and artificial mussel beds during periods of emersion. Using infrared thermography, body temperatures of P. perna within mixed artificial beds were shown to increase faster and reach higher temperatures than individuals in conspecific beds, indicating that the presence of M. galloprovincialis limits the group cooling effects of gaping. In contrast, body temperatures of M. galloprovincialis within mixed artificial mussel beds increased slower and exhibited lower temperatures than for individuals in beds comprised entirely of M. galloprovincialis. Interestingly, differences in bed temperatures and heating rates were largely dependent on the size of mussels, with beds comprised of larger individuals experiencing less thermal stress irrespective of species composition. The small-scale patterns of thermal stress detected within manipulated beds were not observed within naturally occurring mixed mussel beds. We propose that small-scale differences in topography, size-structure, mussel bed size and the presence of organisms encrusting the mussel shells mask the effects of gaping behaviour within natural mussel beds. Nevertheless, the results from our manipulative experiment indicate that the invasive species M. galloprovincialis steals thermal properties as well as resources from the indigenous mussel P. perna. This may have significant implications for predicting how the co-existence of these two species may change as global temperatures continue to rise.

Enemies with benefits: parasitic endoliths protect mussels against heat stress.

Positive and negative aspects of species interactions can be context dependant and strongly affected by environmental conditions. We tested the hypothesis that, during periods of intense heat stress, parasitic phototrophic endoliths that fatally degrade mollusc shells can benefit their mussel hosts. Endolithic infestation significantly reduced body temperatures of sun-exposed mussels and, during unusually extreme heat stress, parasitised individuals suffered lower mortality rates than non-parasitised hosts. This beneficial effect was related to the white discolouration caused by the excavation activity of endoliths. Under climate warming, species relationships may be drastically realigned and conditional benefits of phototrophic endolithic parasites may become more important than the costs of infestation.

A biologically relevant rapid quantification of physical and biological stress profiles on rocky shores

Abstract Different combinations and intensities of physical (e.g. thermal) and biological (e.g. competition or predation) stress operate on organisms in different locations. Variation in these stresses can occur over small to medium spatial scales (cm to 10s of metres) in heterogeneous environments such as rocky shores, due to differences in sun and wave exposure, shore topography and/or recruitment. In this study we demonstrate how simple measurements can be taken that represent physical and biological stresses (stress profiles) in a given location. Using a bootstrapped principal component analysis, we identified significantly different stress profiles at four sites separated by only 10s to 100s of metres on the Shek O peninsula in Hong Kong. We then measured response to thermal stress, as determined by detachment temperature, in the limpet Cellana grata (which is known to be a sensitive indicator species to thermal stress) from each location. Significant differences in stress profile between locations were also seen in thermal stress tolerance of limpets from those locations. At locations where the major stresses are likely to be more physical or less biological in nature (e.g. southerly facing aspect or lower density of grazers), the mean detachment temperature was higher, whereas detachment temperature was lower at sites with more biological or less physical stress. This method is, therefore, able to determine biologically meaningful differences in stress profiles over small to medium spatial scales, and demonstrates that localised adaptation (i.e. post planktonic settlement) or acclimation of species may occur in response to these different stress profiles. The technique can be adapted to different environments and smaller or larger spatial scales as long as the stress experienced by the study species is relevant to these scales.

A novel method for estimating the strength of positive mating preference by similarity in the wild

Abstract Mating preference can be a driver of sexual selection and assortative mating and is, therefore, a key element in evolutionary dynamics. Positive mating preference by similarity is the tendency for the choosy individual to select a mate which possesses a similar variant of a trait. Such preference can be modelled using Gaussian‐like mathematical functions that describe the strength of preference, but such functions cannot be applied to empirical data collected from the field. As a result, traditionally, mating preference is indirectly estimated by the degree of assortative mating (using Pearsons correlation coefficient, r) in wild captured mating pairs. Unfortunately, r and similar coefficients are often biased due to the fact that different variants of a given trait are nonrandomly distributed in the wild, and pooling of mating pairs from such heterogeneous samples may lead to “false–positive” results, termed “the scale‐of‐choice effect” (SCE). Here we provide two new estimators of mating preference (C rough and C scaled) derived from Gaussian‐like functions which can be applied to empirical data. Computer simulations demonstrated that r coefficient showed robust estimations properties of mating preference but it was severely affected by SCE, C rough showed reasonable estimation properties and it was little affected by SCE, while C scaled showed the best properties at infinite sample sizes and it was not affected by SCE but failed at biological sample sizes. We recommend using C rough combined with the r coefficient to infer mating preference in future empirical studies.

A review of the thermal biology and ecology of molluscs, and of the use of infrared thermography in molluscan research

In an era of global change, thermal biology and ecology are becoming increasingly popular topics in invertebrate research, including molluscs. However, this area of research is still very limited, essentially due to the intrinsic spatial limitations of traditional single-point temperature measurements (e.g. thermocouples, iButtons and infrared thermometers). This is not the case, however, with infrared thermography, which has the desirable attribute of producing images that allow for simultaneous measurements of multiple molluscan individuals, species and communities. Infrared thermography allows for spatial and temporal monitoring of microclimates at scales relevant to individual organisms and hence may represent a first step to bridge the gap between field-based approaches (typically spanning from centimetres to tens of metres) to climatic scenarios (typically coarse-grained, i.e. 10 × 10 km). This review first provides a brief history of infrared thermography, followed by a description of the fundamental physical properties and quantities that bridge the gap between the physics of heat transfer and the physics of infrared thermography. We then thoroughly review the thermal biology and ecology of molluscs, and the previous biological and ecological applications of infrared thermography—including the very few in molluscan research. We provide detailed recommendations related to the proper use of infrared thermography. Finally, we discuss the potential applications of infrared thermography in molluscan research, based on case studies involving both terrestrial and intertidal molluscs, with emphasis on its use as a tool for monitoring impacts of climate