Molluscs in Temporary Waters: Adaptations

Molluscs. Both gastropods and bivalves are represented in temporary waters. The bivalve fauna of North America, to take an example, is the most species-rich in the world, with most of them belonging to a single superfamily, the Unionacea (227 native species), which contains many endemics. Typical habitats include permanent lakes and river systems. In contrast, the family Sphaer- iidae contains only 33 native (plus 4 introduced) species, but many of these are found in small, frequently temporary, ponds, lakes, and streams (McMahon 1991). Further, most sphaeriids have broad distributions, often extending from the Atlantic to the Pacific coasts. These result from effective dispersal mechanisms that include: juveniles clamping their shells onto the limbs of aquatic insects and salamanders, and onto the feathers of waterfowl; and survival of some individuals ingested and regurgitated by ducks, which feed on them. In addition, sphaeriids are selffertilizing hermaphrodites which enables a single individual to found a new population—a property favouring successful colonization of isolated drainage systems and temporary ponds. Sphaeriid genera appear to have different substrate preferences that are perhaps associated with different organic matter contents. There are also physiological differences with, for example, the genera Sphaerium and Musculium being relatively intolerant of low oxygen levels, but many species of Pisidium surviving well under hypoxia (Burky 1983). Many sphaeriids (and a few unionaceans) are very tolerant of exposure to air and are thus able to exist at the margins of fluctuating permanent waters, or in truly temporary waters.

The adaptations that allow sphaeriids to survive exposure for periods of up to several months have been studied in some detail, and to some extent seem to be stage-specific (e.g. adults versus newly hatched individuals). Individuals frequently burrow into the basin sediments during the last part of the hydroperiod, and oxygen consumption and rate of metabolism drop. For Sphaerium occidentale, Collins (1967) showed that, in air, oxygen requirement was 20% of that in water, exchange in air taking place across specialized pyramidal cells that extended through minute pores in the shell. The latter allows gas exchange while keeping the valves closed to conserve water. The problem of dealing with metabolite detoxification while exposed appears to be solved through suspension of protein catabolism combined with greater dependence on carbohydrates. McKee and Mackie (1980) showed that tolerance of desiccation may involve prior physiological and biochemical adjustments, in that individuals of both S. occidentale and M. securis taken from populations aestivating in an already dry pond were more tolerant than individuals taken from a permanent pond.

The gastropod fauna of temporary waters comprises species belonging to two of the molluscan subclasses. The Prosobranchia (which are gill- breathers) are primarily marine and only a few species, from the order Mesogastropoda, are able to live in moist, semi-terrestrial habitats. On the other hand, the Pulmonata contains many species that have successfully adapted to live in both permanent and temporary freshwaters, and on land—in fact the freshwater forms are descendants of species that returned to water during the Mesozoic era (~70-250 million years ago) (Kozloff 1990). Foremost among these adaptations is possession of a lung-like structure formed from part of the mantle and which communicates with the outside environment through a closable aperture known as the pneumostome. The lung has spongy walls and a rich blood supply which, along with a slight positive pressure when the pneumostome closes, facilitate gas exchange when the lung is filled. Carbon dioxide-rich air is expelled when the pneumostome opens and the lung floor is raised. Some pulmonates fill their lungs with water and use them as gills.

Other adaptations to living in variable environments include the shell (and also the closable operculum in prosobranchs), production of slime to prevent drying (including production of a mucous epiphragm to seal the shell aperture in pulmonates), and direct development, which eliminates free-living larval stages in the life cycle. Alongside these largely morphological adaptations are a number of physiological ones such as extreme temperature tolerance (0-40^oC for the group as a whole), and excretion of nitrogen as urea, a relatively non-toxic form that can be safely stored in the blood during drought hibernation.

Pulmonates are also capable of withstanding low oxygen tension by means of breathing at the water surface and switching to anaerobic respiration (McMahon 1983; Brown 1991). The fact that many pulmonate species successfully survive being passively dispersed on plants, birds, and insects (as eggs or adults), enables them to colonize new and isolated habitats, and results in broad distributions (e.g. Lymnaea stagnalis, Physa gyrina, P. integra, Gyraulus parvus). A measure of this success has been provided by Davis (1982) who recorded immigration rates to ponds as high as nine species in a single year. Successful establishment in new locations may require habitat features known to influence gastropod populations, such as suitable substratum particle sizes, the presence of macrophytes, moderate-to-high water hardness and pH, and the absence of molluscivorous fishes.

Although pulmonates tend to dominate shallow and temporary waters, a number of prosobranch families are also found in these habitats, for example, Hydrobiidae, Viviparidae, Valvatidae, and Pomatiopsidae. The most abundant pulmon- ates in similar habitats belong to the Lymnaeidae, Physidae, and Planorbidae. Apart from the adaptations already listed, pulmonates also exhibit considerable adaptive plasticity in their life cycles. For example, Thomas and McClintock (1996) found that the physid Physella cubensis survived habitat drying in warm-water temporary ponds in Alabama by burrowing into the bed sediments. In addition, when water was present, it exhibited several 'opportunistic' strategies, such as rapid juvenile growth and attainment of maturity, high fecundity, and continuous reproduction. Other, temperate, pulmonate species have been observed reproducing in cold water, allowing early breeding in the spring followed by rapid maturation before the hydroperiod ends.