Joseph Heller

A desert migration indicator — oxygen isotopic composition of land snail shells

Abstract The oxygen isotopic compositions of land snail shell carbonate may be used as environmental indicators. A study of a single species, Levantina caesareana , shows that modern snails from an arid zone (less than 300 mm rain) are enriched in 18 O by 2‰ compared to the snail carbonate from a moderate climate zone. These measurements combined with those of the mean diameter of the shell are indicative of the climatic zone in which the snail lives. A comparison of the data on ancient populations with those on the modern one shows that the desert migrated northward in the early Holocene in Israel.

Spatial and temporal patterns of parthenogenesis and parasitism in the freshwater snail Melanoides tuberculata

The Red Queen hypothesis predicts that sex should be more common in populations heavily infested with parasites, than in those without. This hypothesis was investigated in the aquatic snail Melanoides tuberculata, in which both sexual and parthenogenetic individuals exist in natural populations, and some populations are heavily infested by trematodes. The presence of fertile males and the higher genetic diversity of bisexual populations are indicative of sexual reproduction. We compared sites in 1990, 1999, and 2001, and we looked for a positive correlation between male and parasite frequencies. Male frequency was not correlated with the frequency of individuals infected by trematodes. This lack of correlation was reconfirmed in a retrospective power analysis. In a period of 9 years, male frequencies decreased but infection levels increased. These results do not support the Red Queen hypothesis. In samples with high male frequency the number of embryos was low, perhaps indicating that males may have a negative effect on embryo numbers. This effect of males on fitness could perhaps suggest that the cost of sex is fewer embryos. The reduction in embryo numbers may also represent a trade‐off between mating and egg production costs.

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.

Natural annual cycle of heat shock protein expression in land snails: desert versus Mediterranean species of Sphincterochila.

SUMMARY Land snails are subject to daily and seasonal variations in temperature and in water availability, and have evolved annual cycles of activity and aestivation as part of their survival strategy. We tested in the field whether adaptation to different habitats affects the endogenous levels of heat shock proteins (HSPs) in two closely related Sphincterochila snail species, a desiccation-resistant desert species, Sphincterochila zonata, and a Mediterranean-type, desiccation-sensitive species, S. cariosa. We examined HSP levels in various tissues of snails during aestivation and after resumption of activity. Our study shows that, during aestivation, S. cariosa had higher standing stocks of Hsp70 in the foot and the hepatopancreas, and of small HSPs (sHSPs) in all the examined tissues, whereas S. zonata had higher stocks of Hsp70 in the kidney and of Hsp90 in the kidney and in the hepatopancreas. Arousal induced a general upregulation of HSPs, except for Hsp90, the expression of which in the foot was higher during aestivation. We suggest that the stress protein machinery is upregulated during arousal in anticipation of possible oxidative stress ensuing from the accelerating metabolic rate and the exit from the deep hypometabolic state. Our findings support the concept that, in land snails, aestivation and activity represent two distinct physiological states, and suggest that land snails use HSPs as important components of the aestivation mechanism, and as part of their survival strategy during and after arousal. Our study also indicates that adaptation to different habitats results in the development of distinct strategies of HSP expression with likely consequences for the ecology and distribution of land snails.

The Biogeography of Enid Landsnails on the Aegean Islands

The distribution in the Aegean archipelago of one family of landsnails, the Enidae, is described. The relationship between the number of species on an island and (i) the islands area, (ii) the islands distance from the nearest mainland, and (iii) mean size of each species, is examined. The number of species per island is not correlated significantly with any of these three factors. There is a good correlation between the distribution of landsnails and the topography beneath sea level around the island. Some species are found only off the coasts of Turkey or of Greece, on islands included within the 100 fathom isobath; one subspecies is found on twenty-four islands, all within the area included within the 200 fathom (364 m) isobath; and other species are found on those islands which lie beyond the 200 fathom (364 m) isobath. This suggests that, rather than representing island biogeography in its dynamic sense (recent dispersal over a hostile habitat), the recent Enid fauna represents a relict continental biogeography (past dispersal over a continuous, non-hostile habitat), and that such continental dispersal occurred in periodY when, as the relative level of the sea dropped as compared to that of today, isolation between certain islands, was abolished. The known geological history of the Aegean archipelago agrees well with such an hypothesis. From the recent distribution pattern it appears that the Enidae invaded the Aegean in three distinct waves, corresponding to three different past sea-levels. The fact that over 800% of the sixty-three islands, regardless of each islands area or proximity to mainland, have only one species of Enid each, whereas Turkey is inhabited by fifty-five Enids, suggests that today there is almost no immigration from the Turkish mainland. There also appears to be no immigration from Greece. The fact, on the other hand, that almost every Aegean island, down to the most remote and minute of these, is inhabited by Enidae of one species or another, suggests that the rate of extinction is very low. The number of species on an island thus appears to be the combined result of almost no immigration and almost no extinction.

SPERMATOGENESIS AND SPERM STRUCTURE OF THE NORMALLY PARTHENOGENETIC FRESHWATER SNAIL MELANOIDES TUBERCOLATA

ABSTRACT The freshwater snail Melanoides tuberculata ranges throughout Asia and Africa, and throughout much of its range it reproduces parthenogenetically. In Israel, however, males have been found. These males produce two types of spermatozoa, euspermatozoa and paraspermatozoa. The euspermatozoa are filiform (about 230 μ m in length) with a head comprising a nucleus and conical acrosome, a mid-piece (98 μ m long) of four equal-sized mitochondria, and a tail. Unlike in other cerithiaceans, the nucleus is unusually elongate (31 μ m long × 1 μ m diameter) and the axoneme is housed within an intranuclear canal. The paraspermatozoa consists of a head of electron-dense blocks (up to 25 μ m long) which surround up to 15 axonemes, a mid-piece of elongate mitochondria and a tail tuft, as in other cerithiaceans. Structural changes during spermatogenesis resemble those described for other gastropods with dimorphic spermatozoa.

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.

Intraspecific variation in resistance to desiccation in the land snailTheba pisana

Theba pisana is a bush-dwelling snail with a circum-Mediterranean distribution. In Israel it is limited to a narrow coastal strip, along which there is a north-to-south gradient in mean annual rainfall (700–300 mm per year). In this study we found significant intraspecific differences among populations ofT. pisana in resistance to desiccation along this gradient, and in a population from Greece, which may be grossly correlated with the climatic gradient. The Greek population was the least resistant to desiccation with an extremely high rate of water loss. The differences in total mass loss were mainly determined by the rate of water loss during the first 4 days of desiccation. A general phenomenon during desiccation was the close regulation of the soft body water content at the expense of the extra-pallial fluid compartment.

Heat shock proteins and survival strategies in congeneric land snails (Sphincterochila) from different habitats

Polmunate land snails are subject to stress conditions in their terrestrial habitat, and depend on a range of behavioural, physiological and biochemical adaptations for coping with problems of maintaining water, ionic and thermal balance. The involvement of the heat shock protein (HSP) machinery in land snails was demonstrated following short-term experimental aestivation and heat stress, suggesting that land snails use HSPs as part of their survival strategy. As climatic variation was found to be associated with HSP expression, we tested whether adaptation of land snails to different habitats affects HSP expression in two closely related Sphincterochila snail species, a desert species Sphincterochila zonata and a Mediterranean-type species Sphincterochila cariosa. Our study suggests that Sphincterochila species use HSPs as part of their survival strategy following desiccation and heat stress, and as part of the natural annual cycle of activity and aestivation. Our studies also indicate that adaptation to different habitats results in the development of distinct strategies of HSP expression in response to stress, namely the reduced expression of HSPs in the desert-inhabiting species. We suggest that these different strategies reflect the difference in heat and aridity encountered in the natural habitats, and that the desert species S. zonata relies on mechanisms and adaptations other than HSP induction thus avoiding the fitness consequences of continuous HSP upregulation.

Terrestrial snails use predator-diet to assess danger

Some aquatic snails are able to use chemical cues (kairomones) to differentiate between predators that have fed on snails and predators that have eaten other prey. However, it is unknown if terrestrial snails are able to differentiate between snail-fed predators and predators that have not recently consumed snails. Here we document diet-based chemical discrimination of a predator, the ground beetle Carabus carabus, by a terrestrial snail Theba pisana. When exposed to the feces of snail-fed beetles, snails initially stopped all movements and then increased climbing speed. The snails also decreased the time to deposition of their egg clutch. The snails did not react to an extract of crushed snails. Snails had only a partial reaction to the feces of beetles that had fed on chicken (Gallus domesticus) livers—they decreased climbing speed but did not alter egg laying times. These responses may be adaptive in that they allow snails to differentiate between individual beetles that may pose an immediate threat and beetles that may not. This is one of only a few studies to examine predator-diet effects on reproductive behavior.