Behavioral repertoire of high-shore littorinid snails reveals novel adaptations to an extreme environment.

Species that inhabit high-shore environments on rocky shores survive prolonged periods of emersion and thermal stress. Using two Hong Kong high-shore littorinids (Echinolittorina malaccana and E. radiata) as models, we examined their behavioral repertoire to survive these variable and extreme conditions. Environmental temperatures ranged from 4°C in the cool season to 55.5°C in the hot season, with strong seasonal and daily fluctuations. In the hot season, both species allocated >35% of their activity budgets to stress-mitigating thermoregulatory behaviors (e.g. standing, towering) and relatively small proportions to foraging (<20%) and reproduction (<10%). In the assumedly benign cool season, greater proportions (>70%) of activity budgets were allocated to stress mitigation behaviors (crevice occupation, aggregation formation). Both species exhibited multifunctional behaviors that optimized time use during their tidally-constrained activity window in the hot season. Females mated while foraging when awash by the rising tide, and some males crawled on top of females prior to ceasing movement to form 'towers', which have both thermoregulatory benefits and reduce searching time for mates during subsequent activity. The function of such behaviors varies in a state-dependent manner, for example, the function of trail following changes over an activity cycle from mate searching on rising tides, to stress mitigation on falling tides (aiding aggregation formation), and to both functions through tower formation just before movement stops. Many of these behavioral responses are, therefore, multifunctional and can vary according to local conditions, allowing snails in this family to successfully colonize the extreme high-shore environment.

Provision of refugia and seeding with native bivalves can enhance biodiversity on vertical seawalls.

Recent studies have suggested that increasing habitat complexity of artificial seawalls by modifying surface heterogeneity could enhance exploitable habitat and therefore species richness and abundance. We tested the effects of adding complex tiles (with crevices/ledges) of different heterogeneity (i.e., flat tiles resembling the seawall vs. tiles with crevices of 2.5 cm or 5.0 cm depth) and seeding with native rock oysters, Saccostrea cuccullata (unseeded vs. seeded) on species richness and abundances of intertidal marine organisms on two vertical seawalls in Hong Kong. Tiles were affixed to the mid-intertidal zone of the seawalls for 12 months. The results showed that the tiles with crevices had greater species richness and cover of sessile epifauna than flat tiles. Seeding tiles with S. cuccullata also facilitated natural recruitment of the same species. Our results support the hypothesis that using eco-engineering to increase habitat complexity can enhance the biodiversity of intertidal marine organisms on seawalls.

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

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 Pearson's 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 (Crough and Cscaled) 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, Crough showed reasonable estimation properties and it was little affected by SCE, while Cscaled showed the best properties at infinite sample sizes and it was not affected by SCE but failed at biological sample sizes. We recommend using Crough combined with the r coefficient to infer mating preference in future empirical studies.

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.

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.