Gray A. Williams

Plant-Animal Interactions in the Marine Benthos

List of contributors Habitats and regional perspectives: S.J. Hawkins, R.G. Hartnoll, J.M. Kain, & T.A. Norton: Plant-animal interactions on hard substrata in the Northeast Atlantic R.L. Vadas & R.W. Elner: Plants-animal interactions in the Northwest Atlantic M.S. Foster: Plant animal interactions in the Northeast Pacific: the importance of grazing to seaweed evolution and assemblage structure D.M. John, J.H. Price, & G.W. Lawson: Tropical East Atlantic and islands: plant-animal interactions on tropical shores free of biotic reefs Deborah M. Brosnan: Ecology of tropical rocky shores: plant-animal interactions in tropical and temperate latitudes K. Reise: Grazing on sediment shores R.J. Orth: A perspective on plant-animal interactions in seagrasses: physical and biological determinants influencing plant and animal abundance L. Mazzella, M.C. Buia, M.C. Gambi, M. Lorenti, G.F. Russo, M.B. Scipione, & V. Zupo: Plant-animal trophic relationships in the posidonia oceanica ecosystem of the Mediterranean Sea: a review G.A. Williams & R. Seed: Interactions between macrofaunal epiphytes and their host algae N.V.C. Polunin & D.W. Klumpp: A trophodynamic model of fish production on a windward reef tract Processes and types of plant-animal interaction: Susan H. Brawley: Mesograzers B.L. Bayne & A.J.S. Hawkins: Herbivory in benthic suspension-feeding molluscs M.G. Chapman & A.J. Underwood: Foraging behaviour of marine benthic grazers M.E. Hay & W. Fenical: Chemical mediation of seaweed-herbivore interactions M.H. Horn: Herbivorous fish: feeding and digestion mechanisms B. Santelices: Digestion survival of algae: an overview A.N.C. Morse: Role of algae in the recruitment of marine invertebrate G.M. Branch, J.M. Harris, C. Parkins, R.H. Bustamente, & S. Eckhout: Algal gardening by marine grazers: a comparison of the ecological effects of territorial fish and limpets W.P. Sousa & J.H. Connell: Grazing and succession A.J. Underwood: Competition and marine plant-animal interactions R.S. Steneck: Plant-herbivore coevolution: a reappraisal from the marine realm and its fossil record T. Spencer: Bioerosion and biogeomorphology Endosymbiosis: P.S. Spencer-Davies: Endosymbiosis in marine cnidarians Summary and future view: A.J. Underwood: Summary and future prospects for plant-animal interactions Index List of Systematics Association Publications.

The relationship between shade and molluscan grazing in structuring communities on a moderately-exposed tropical rocky shore

Abstract The relationship between physical factors (principally temperature) and biological factors (herbivory) in structuring mid and low shore communities were investigated on a moderately-exposed tropical rocky shore. Physical stress, as measured by rock surface temperature and evaporation of distilled water, was greatest higher on the shore as a result of increased exposure time. Exclusion of herbivores (by caging) and alteration of physical factors (by shading) caused little visible change in community structure in the mid shore. There was also no difference in community structure between open rock areas and control treatments for experimental manipulations at either shore level. Chlorophyll levels increased in rock chips from treatments at both shore levels that excluded herbivores, but still allowed access to sunlight, indicating a developing biofilm. In the low shore, however, treatments that provided refuge from herbivores and direct sunlight were colonized by barnacles ( Balanus amphitrite ) and an encrusting alga, Hildenbrandia . There appeared to be an interaction between these factors in structuring the community, removal of herbivores allowed the settlement of barnacles which was greatest in shaded treatments. On Hong Kong shores during the summer months biological interactions are important low on the shore in combination with physical factors. In the mid shore, however, physical factors appear the major structuring agent. Community structure on Hong Kong shores is dictated by seasonal variation in physical factors which mediate the effect of biological factors such as herbivory.

Distribution of algae on tropical rocky shores: spatial and temporal patterns of non-coralline encrusting algae in Hong Kong

Encrusting algae have been described as dominant space occupying species on rocky shores around the world. Despite their abundance, however, most studies classify species under generic names (e.g. Ralfsia sp.) or as a functional group (e.g. encrusting algae), thereby underestimating the number of species present and their ecological importance. Studies on six rocky shores of varying exposure, in Hong Kong, recorded eight common species of encrusting algae. The greatest abundance of encrusting algae was recorded on shores of intermediate exposure, where four distinct zonation bands could be identified; a cyanobacterial “Kyrtuthrix-Zone” in the upper midlittoral, a “Bare-Zone” below this, a “Mixed-Zone” in the lower midlittoral and a “Coralline-Zone” in the infralittoral fringe. Abundance declined on shores of greater and lower exposure to wave action, where bivalves and barnacles were competitively dominant. Certain species were found in greater abundance on exposed shores (e.g. Dermocarpa sp. and Hildenbrandia occidentalis), while others preferred more sheltered shores (e.g. Hildenbrandia prototypus and Kyrtuthrix maculans). With the exception of some cyanobacterial crusts, the abundance of encrusting algae was always greatest towards the low shore, an area of decreased physical stress and increased herbivore density. Zonation patterns showed seasonal variation associated with the monsoonal climate of Hong Kong. Most species increased in abundance during the cool season, while during the summer months the cover and vertical extent of encrusting algae decreased in relation to summer temperatures, although K. maculans increased in abundance during the summer. On Hong Kong shores, encrusting algae have a high species richness and exhibit within-functional group spatial and temporal variation which is mediated by herbivory and seasonal, physical stresses.

Non-climatic thermal adaptation: implications for species' responses to climate warming.

There is considerable interest in understanding how ectothermic animals may physiologically and behaviourally buffer the effects of climate warming. Much less consideration is being given to how organisms might adapt to non-climatic heat sources in ways that could confound predictions for responses of species and communities to climate warming. Although adaptation to non-climatic heat sources (solar and geothermal) seems likely in some marine species, climate warming predictions for marine ectotherms are largely based on adaptation to climatically relevant heat sources (air or surface sea water temperature). Here, we show that non-climatic solar heating underlies thermal resistance adaptation in a rocky–eulittoral-fringe snail. Comparisons of the maximum temperatures of the air, the snails body and the rock substratum with solar irradiance and physiological performance show that the highest body temperature is primarily controlled by solar heating and re-radiation, and that the snails upper lethal temperature exceeds the highest climatically relevant regional air temperature by approximately 22°C. Non-climatic thermal adaptation probably features widely among marine and terrestrial ectotherms and because it could enable species to tolerate climatic rises in air temperature, it deserves more consideration in general and for inclusion into climate warming models.

Thermal adaptation in the intertidal snail Echinolittorina malaccana contradicts current theory by revealing the crucial roles of resting metabolism

SUMMARY Contemporary theory for thermal adaptation of ectothermic metazoans focuses on the maximization of energy gain and performance (locomotion and foraging). Little consideration is given to the selection for mechanisms that minimize resting energy loss in organisms whose energy gain is severely constrained. We tested a hypothetical framework for thermal performance of locomotor activity (a proxy for energy gain) and resting metabolism (a proxy for energy loss) in energetically compromised snails in the littoral fringe zone, comparing this with existing theory. In contrast to theory, the thermal ranges and optima for locomotor performance and metabolic performance of Echinolittorina malaccana are mismatched, and energy gain is only possible at relatively cool temperatures. To overcome thermal and temporal constraints on energy gain while experiencing high body temperatures (23–50°C), these snails depress resting metabolism between 35 and 46°C (thermally insensitive zone). The resulting bimodal relationship for metabolism against temperature contrasts with the unimodal or exponential relationships of most ectotherms. Elevation of metabolism above the breakpoint temperature for thermal insensitivity (46°C) coincides with the induction of a heat shock response, and has implications for energy expenditure and natural selection. Time-dependent mortality is initiated at this breakpoint temperature, suggesting a threshold above which the rate of energy demand exceeds the capacity for cellular energy generation (rate of ATP turnover). Mortality in a thermal range that elevates rather than limits aerobic metabolism contrasts with the hypothesis that cellular oxygen deficiency underlies temperature-related mortality. The findings of this study point to the need to incorporate aspects of resting metabolism and energy conservation into theories of thermal adaptation.

Seasonal variation in algal species richness and abundance in the presence of molluscan herbivores on a tropical rocky shore

Abstract Seasonal variation in species and percentage cover of macroalgae was investigated over a 15-month period on a semi-exposed tropical rocky shore. Cages were used to manipulate herbivore access in mid and low shore areas. Algal species richness and abundance showed a marked seasonal pattern, peaking during the winter months and decreasing in the summer. At both mid and low shore the number of species and abundance of algae was greatest in herbivore exclusion treatments and the effect was more pronounced in the low shore where there was a consistent difference between treatments throughout the year. In the mid shore there was a difference in the cover of algae between treatments in the winter months only; for the remaining period there was little difference. Algal abundance and species numbers declined dramatically in all treatments as the temperature increased with the onset of summer, although the decline was less pronounced in the lower shore treatments. The results indicate that at higher tidal levels physical factors influence algal abundance to a greater extent than lower on the shore where herbivory is important, although lower on the shore the physical extremes of a tropical summer are also strong limiting factors.

Beyond long-term averages: making biological sense of a rapidly changing world

Biological responses to climate change are typically communicated in generalized terms such as poleward and altitudinal range shifts, but adaptation efforts relevant to management decisions often require forecasts that incorporate the interaction of multiple climatic and nonclimatic stressors at far smaller spatiotemporal scales. We argue that the desire for generalizations has, ironically, contributed to the frequent conflation of weather with climate, even within the scientific community. As a result, current predictions of ecological responses to climate change, and the design of experiments to understand underlying mechanisms, are too often based on broad-scale trends and averages that at a proximate level may have very little to do with the vulnerability of organisms and ecosystems. The creation of biologically relevant metrics of environmental change that incorporate the physical mechanisms by which climate trains patterns of weather, coupled with knowledge of how organisms and ecosystems respond to these changes, can offer insight into which aspects of climate change may be most important to monitor and predict. This approach also has the potential to enhance our ability to communicate impacts of climate change to nonscientists and especially to stakeholders attempting to enact climate change adaptation policies.

The Impact of Yangtze River Discharge, Ocean Currents and Historical Events on the Biogeographic Pattern of Cellana toreuma along the China Coast

Aim Genetic data were used to measure the phylogeographic distribution of the limpet, Cellana toreuma along the China coast in order to acsertain impacts of historic events, ocean currents and especially freshwater discharge from the Yangtze River on the connectivity of intertidal species with limited larval dispersal capability. Methodology/Principal Findings Genetic variation in 15 populations of C. toreuma (n = 418), ranging from the Yellow Sea (YS), East China Sea (ECS) and South China Sea (SCS), were determined from partial mitochondrial cytochrome c oxidase subunit I gene. Genetic diversity and divergence based on haplotype frequencies were analyzed using CONTRIB, and AMOVA was used to examine genetic population structure. Historic demographic expansions were evaluated from both neutrality tests and mismatch distribution tests. Among the 30 haplotypes identified, a dominant haplotype No. 1 (H1) existed in all the populations, and a relatively abundant private haplotype (H2) in YS. Pairwise FST values between YS and the other two groups were relatively high and the percentage of variation among groups was 10.9%. Conclusions The high nucleotide and gene diversity in the YS, with large pairwise genetic distances and relatively high percentages of variation among groups, suggests that this group was relatively isolated from ECS and SCS. This is likely driven by historic events, ocean currents, and demographic expansion. We propose that freshwater discharge from the Yangtze River, which may act as physical barrier limiting the southward dispersal of larvae from northern populations, is especially important in determining the separation of the YS group from the rest of the Chinese populations of C. toreuma.

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.

Littorinids control high intertidal biofilm abundance on tropical, Hong Kong rocky shores

Biotic interactions in the high shore are assumed to be of little importance as compared to the role of adverse physical factors, despite the fact that these shore levels support dense numbers of grazing littorinids worldwide. In Hong Kong, three species, Nodilittorina trochoides, N. radiata and N. vidua, are abundant in the high shore and graze the epilithic biofilm, which is primarily composed of cyanobacteria (mostly Gloeocapsa and Dermocarpa species). When littorinids were excluded from the high shore (2.00–2.25 m above C.D.) using gum barriers, growth of the biofilm as measured by chlorophyll a levels was enhanced after 42 days at three different sites. Whilst the overall pattern of increasing chlorophyll a levels in exclusion areas was the same for all three sites, there was between-site variation possibly due to different littorinid densities and/or rock types. Exclusion of grazers, however, revealed that even at high shore levels on tropical shores biotic factors can control biofilm development. It is suggested that this influence acts in synergy with physical factors such as tidal inundation and frequency of wave splash and storms which can directly control littorinid grazing activity and presumably biofilm growth.