Chlorophyll fluorometry sheds light on the role of desiccation resistance for vegetative overland dispersal of aquatic plants

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Resistance to desiccation and distribution patterns in bush-dwelling land snails

Bush-dwelling land snails are exposed to desiccating conditions that are more severe than those of snails that seek the shelter of rock crevices, litter or the upper layers of the soil. We studied the resistance to desiccation in four bush-dwelling species of Israeli snails to evaluate a possible relation between their water economy and their distribution pattern. The resistance to desiccation decreased in the following order: Xeropicta vestalis (a widely distributed Mediterranean species), Trochoidea simulata (a desert species), Theba pisana (a Mediterranean species from the sand dunes of the coastal plain), and Monacha haifaensis (a Mediterranean species). Xeropicta vestalis also had the quickest response to the desiccating conditions. It is probably prevented from establishing itself in the desert, in spite of its superior water economy, because it is an annual, semelparous species, and the desert is a highly unpredictable environment. An immediate response to desiccating conditions may be a key factor in the success of desert-inhabiting land snails. Snails from more humid regions take several days to recruit their water preserving mechanisms, a delay which may be crucial to their water balance. The conchiometrics of X. vestalis and T. simulata suggest that the main water preserving mechanisms of these species are located in the mantle, rather than in the shell and epiphragm.     

A potential role for overland dispersal in shaping aquatic invertebrate communities in arid regions

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Water balance and resistance to desiccation in rock-dwelling snails

We have examined the resistance to desiccation among rock-dwelling land snails of various phylogenetic groups:Cristataria genezarethana (Clausiliidae),Rupestrella rhodia (Chondrinidae) andLevantina caesareana (Helicidae), all from the same location in Israel.L. caesareana was the most resistant andR. rhodia the least resistant to desiccation andC. genezarethana was of intermediate resistance. Differences in the rates of water loss during desiccation were determined mainly by rate of water loss during the first 2 days of desiccation. The high rates of water loss in rock-dwelling species exceed those of other snails in the Mediterranean habitat of Israel. However, snails collected in the field at the end of aestivation were in only a mild state of dehydration, suggesting that the rocky habitat protects its occupants against desiccation. We also suggest that among the rock-dwelling species, the protective role of the rock is more important in the more evolutionarily primitive genera (the chondrinidRupestrella and the clausiliidCristataria) and that physiological capacities are more effective in the more highly evolved helicidLevantina.     

Heat shock proteins and resistance to desiccation in congeneric land snails

Land snails are subject to daily and seasonal variations in temperature and in water availability and depend on a range of behavioral and physiological adaptations for coping with problems of maintaining water, ionic, and thermal balance. Heat shock proteins (HSPs) are a multigene family of proteins whose expression is induced by a variety of stress agents. We used experimental desiccation to test whether adaptation to different habitats affects HSP expression in two closely related Sphincterochila snail species, a desiccation-resistant, desert species Sphincterochila zonata, and a Mediterranean-type, desiccation-sensitive species Sphincterochila cariosa. We examined the HSP response in the foot, hepatopancreas, and kidney tissues of snails exposed to normothermic desiccation. Our findings show variations in the HSP response in both timing and magnitude between the two species. The levels of endogenous Hsp72 in S. cariosa were higher in all the examined tissues, and the induction of Hsp72, Hsp74, and Hsp90 developed earlier than in S. zonata. In contrary, the induction of sHSPs (Hsp25 and Hsp30) was more pronounced in S. zonata compared to S. cariosa. Our results suggest that land snails use HSPs as part of their survival strategy during desiccation and as important components of the aestivation mechanism in the transition from activity to dormancy. Our study underscores the distinct strategy of HSP expression in response to desiccation, namely the delayed induction of Hsp70 and Hsp90 together with enhanced induction of sHSPs in the desert-dwelling species, and suggests that evolution in harsh environments will result in selection for reduced Hsp70 expression.     

The river Rhine: a global highway for dispersal of aquatic invasive species

The river Rhine is heavily influenced by human activities and suffers from a series of environmental constraints which hamper a complete recovery of biodiversity. These constraints comprise intensive navigation and habitat modification by hydraulic engineering. Improving water quality while these constraints remain in place has led to increased colonization by aquatic invasive species. This tendency has been accelerated by the construction of canals connecting river basins. Over the last two centuries, the total surface area of river catchments connected to the river Rhine via inland waterways has been increased by a factor 21.6. Six principal invasion corridors for aquatic species to the river Rhine are discerned. The extensive network of inland waterways has allowed macroinvertebrate species from different bio-geographical regions to mix, changing communities, affecting the food webs and forming new constraints on the recovery of the native biodiversity. From the eighteenth century onward, in the freshwater sections of the river Rhine, a total of 45 non-indigenous macroinvertebrate species have been recorded. The average number of invasions per decade shows a sharp increase from <1 to 13 species. Currently, the contribution of non-indigenous species to the total species richness of macroinvertebrates in the river Rhine is 11.3%. The Delta Rhine and Upper Rhine exhibit higher numbers of non-indigenous species than other river sections, because the sea ports in the Delta Rhine and the Main-Danube canal function as invasion gateways. Important donor areas are the Ponto-Caspian area and North America (44.4 and 26.7% of the non-indigenous macroinvertebrate species, respectively). Transport via shipping and dispersal via man made waterways are the most important dispersal vectors. Intentional and unintentional introductions are highest for the period 1950–1992. The cumulative number of non-indigenous species in time is significantly correlated with the increase in total surface area of other river catchments connected to the river Rhine by means of networks of canals. The species richness of non-indigenous macroinvertebrates is strongly dominated by crustaceans and molluscs. Invasive species often tolerate higher salt content, temperature, organic pollution and current flow than native species. Spatiotemporal analyses of distribution patterns reveal that average and maximum dispersal rates of six invasive species vary between 44–112 and 137–461 km year⁻¹, respectively. Species arriving in upstream sections first show a shorter time lag between colonisation of the Delta and Upper Rhine than species initially arriving in downstream areas. Temporal analyses of macroinvertebrate assemblages in the littoral zones indicate that native species are displaced by non-indigenous species. However, established non-indigenous species are also displaced by more recent mass invaders.     

Parallel variation among populations in the shell morphology between sympatric native and invasive aquatic snails

A phenotypic response, either plastic or evolved, is often required for successful invasion of novel environments. Populations of the invasive snail Potamopyrgus antipodarum have colonized a wide range of environments in the western U. S. since 1985, but the extent of plastic adjustment and evolved adaptation to local environments is largely unknown. We examined variation in shell morphology among four sites in the Snake River, Idaho, including both still-water and free-flowing river habitats and compared the variation to that of a native snail (Pyrgulopsis robusta) using geometric morphometric techniques. Using Generalized Procrustes analysis, we tested for phenotypic responses by determining (1) whether Po. antipodarum from the four locations differed in shell morphology, and (2) whether these snails exhibited corresponding shell shape variation with sympatric populations of a native snail. Both native and invasive snails exhibited similar variation in shell morphology across three of the four sites. The Canonical Variate assignment test grouped 85 % of both snail species to their rightful sample site. In addition, the Principal Component Analysis displayed similar patterns of shell variation across the four sites, indicating parallel variation in shell shape. For three of the four sites, both the native and invasive snails exhibited differences in shell shape consistent with water flow variation (still-water versus fast free-flowing river). Taken together, these results suggest that the shell shape of the invasive snail has changed either through plasticity or evolution, and that both native and invasive snail populations responded to local environmental conditions in a similar manner.     

Experimental quantification of long distance dispersal potential of aquatic snails in the gut of migratory birds

Many plant seeds and invertebrates can survive passage through the digestive system of birds, which may lead to long distance dispersal (endozoochory) in case of prolonged retention by moving vectors. Endozoochorous dispersal by waterbirds has nowadays been documented for many aquatic plant seeds, algae and dormant life stages of aquatic invertebrates. Anecdotal information indicates that endozoochory is also possible for fully functional, active aquatic organisms, a phenomenon that we here address experimentally using aquatic snails. We fed four species of aquatic snails to mallards (Anas platyrhynchos), and monitored snail retrieval and survival over time. One of the snail species tested was found to survive passage through the digestive tract of mallards as fully functional adults. Hydrobia (Peringia) ulvae survived up to five hours in the digestive tract. This suggests a maximum potential transport distance of up to 300 km may be possible if these snails are taken by flying birds, although the actual dispersal distance greatly depends on additional factors such as the behavior of the vectors. We put forward that more organisms that acquired traits for survival in stochastic environments such as wetlands, but not specifically adapted for endozoochory, may be sufficiently equipped to successfully pass a bird's digestive system. This may be explained by a digestive trade-off in birds, which maximize their net energy intake rate rather than digestive efficiency, since higher efficiency comes with the cost of prolonged retention times and hence reduces food intake. The resulting lower digestive efficiency allows species like aquatic snails, and potentially other fully functional organisms without obvious dispersal adaptations, to be transported internally. Adopting this view, endozoochorous dispersal may be more common than up to now thought.     

Prospecting and dispersal: their eco-evolutionary dynamics and implications for population patterns

Dispersal is not a blind process, and evidence is accumulating that individual dispersal strategies are informed in most, if not all, organisms. The acquisition and use of information are traits that may evolve across space and time as a function of the balance between costs and benefits of informed dispersal. If information is available, individuals can potentially use it in making better decisions, thereby increasing their fitness. However, prospecting for and using information probably entail costs that may constrain the evolution of informed dispersal, potentially with population-level consequences. By using individual-based, spatially explicit simulations, we detected clear coevolutionary dynamics between prospecting and dispersal movement strategies that differed in sign and magnitude depending on their respective costs. More specifically, we found that informed dispersal strategies evolve when the costs of information acquisition during prospecting are low but only if there are mortality costs associated with dispersal movements. That is, selection favours informed dispersal strategies when the acquisition and use processes themselves were not too expensive. When non-informed dispersal strategies evolve, they do so jointly with the evolution of long dispersal distance because this maximizes the sampling area. In some cases, selection produces dispersal rules different from those that would be ‘optimal’ (i.e. the best possible population performance—in our context quantitatively measured as population density and patch occupancy—among all possible individual movement rules) for the population. That is, on the one hand, informed dispersal strategies led to population performance below its highest possible level. On the other hand, un- and poorly informed individuals nearly optimized population performance, both in terms of density and patch occupancy.     

Reproduction and dispersal in aquatic hyphomycetes

The conidia of aquatic hyphomycetes were discovered by C.T. Ingold some 60 years ago. They are typically multiradiate or sigmoid, relatively fragile, and produced in enormous numbers. Their main function seems to be the rapid colonization of a periodic superabundance of leaves common in most streams. Conidia are unlikely to survive adverse conditions and to be responsible for the apparently worldwide distribution of many aquatic hyphomycete species. It has repeatedly been suggested that meiospores are responsible for long-distance dispersal; however, to date, only some 10% of described species have been connected to a teleomorph. To determine additional connections, and to document the potential role of meiospores in long-distance dispersal of aquatic hyphomycetes, the application of modern molecular methods is essential.     

Historical data reveal power‐law dispersal patterns of invasive aquatic species

Understanding how invasive species spread is of particular concern in the current era of globalisation and rapid environmental change. The occurrence of super‐diffusive movements within the context of Lévy flights has been discussed with respect to particle physics, human movements, microzooplankton, disease spread in global epidemiology and animal foraging behaviour. Super‐diffusive movements provide a theoretical explanation for the rapid spread of organisms and disease, but their applicability to empirical data on the historic spread of organisms has rarely been tested. This study focuses on the role of long‐distance dispersal in the invasion dynamics of aquatic invasive species across three contrasting areas and spatial scales: open ocean (north‐east Atlantic), enclosed sea (Mediterranean) and an island environment (Ireland). Study species included five freshwater plant species, Azolla filiculoides, Elodea canadensis, Lagarosiphon major, Elodea nuttallii and Lemna minuta; and ten species of marine algae, Asparagopsis armata, Antithamnionella elegans, Antithamnionella ternifolia, Codium fragile, Colpomenia peregrina, Caulerpa taxifolia, Dasysiphonia sp., Sargassum muticum, Undaria pinnatifida and Womersleyella setacea. A simulation model is constructed to show the validity of using historical data to reconstruct dispersal kernels. Lévy movement patterns similar to those previously observed in humans and wild animals are evident in the re‐constructed dispersal pattern of invasive aquatic species. Such patterns may be widespread among invasive species and could be exacerbated by further development of trade networks, human travel and environmental change. These findings have implications for our ability to predict and manage future invasions, and improve our understanding of the potential for spread of organisms including infectious diseases, plant pests and genetically modified organisms.     

Resistance to shell breaking in two intertidal snails

The ability of shells to withstand shell breaking forces has been examined in two intertidal prosobranchs, Nucella lapillus and Littorina littorea , using four methods: measuring shell strength on a compressive testing machine, measuring the shell to body mass ratio, measuring the shell thickness and measuring the ability of crabs to break shells in aquarium experiments. Nucella lapillus consistently showed a relationship between shell vulnerability and environmental variables: the shells were easier to break at sites where rock and boulder movement was the least. Although some between-site differences were found in L. littorea shells, these were less than in N. lapillus and did not relate to environment variables: the shells were easier to break at sites where exposure to wave action was the least. Although some between-site differences were found in L. littorea shells , these were less than in N. lapillus and did not relate to environmental factors. However, both species appear to grow into a size refuge in which they are secure from predation by shore crabs at the sites where these crabs are commonest.     

Complex interactions among fish, snails and macrophytes: implications for biological control of an invasive snail

The golden apple snail (Pomacea canaliculata), a native of freshwater wetlands of South America, has invaded many Asian countries and grazed heavily in agricultural and wild areas. Common carp (Cyprinus carpio) has been proposed as a biological control agent against this snail, but little is known about its impact on non-target aquatic plants and animals. In a 8-week enclosure experiment, we quantified the impact of common carp on three species of aquatic macrophytes and nine species of snails, including the apple snail, in a shallow pond. The results showed that the apple snail or carp alone significantly reduced the plant biomass, although the apple snail had a stronger overall herbivorous effect than the carp. The carp completely removed juvenile apple snails, but had only a weak predatory effect on larger apple snails and no effect on the adults’ oviposition frequency. Furthermore, the carp significantly reduced the populations of most species of other snails that occurred naturally in the pond. Our results thus indicate that common carp can be an effective biological control agent against the invasive apple snail, but caution should be taken about its potential to reduce wetland floral and faunal diversity.     

Individual boldness is linked to protective shell shape in aquatic snails

The existence of consistent individual differences in behaviour (‘animal personality’) has been well documented in recent years. However, how such individual variation in behaviour is maintained over evolutionary time is an ongoing conundrum. A well-studied axis of animal personality is individual variation along a bold–shy continuum, where individuals differ consistently in their propensity to take risks. A predation-risk cost to boldness is often assumed, but also that the reproductive benefits associated with boldness lead to equivalent fitness outcomes between bold and shy individuals over a lifetime. However, an alternative or complementary explanation may be that bold individuals phenotypically compensate for their risky lifestyle to reduce predation costs, for instance by investing in more pronounced morphological defences. Here, we investigate the ‘phenotypic compensation’ hypothesis, i.e. that bold individuals exhibit more pronounced anti-predator defences than shy individuals, by relating shell shape in the aquatic snail Radix balthica to an index of individual boldness. Our analyses find a strong relationship between risk-taking propensity and shell shape in this species, with bolder individuals exhibiting a more defended shell shape than shy individuals. We suggest that this supports the ‘phenotypic compensation’ hypothesis and sheds light on a previously poorly studied mechanism to promote the maintenance of personality variation among animals.