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Physiological Differences Between Coexisting Congeneric Species of Snails in a Subarctic Lake

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Physiological Differences Between Coexisting Congeneric Species of Snails in a Subarctic Lake Vol. 5: 209–217, 2009 AQUATIC BIOLOGY Printed June 2009 doi: 10.3354/ab00150 Aquat Biol Published online May 12, 2009 OPEN ACCESS Physiological differences between coexisting congeneric species of snails in a subarctic lake Katherine S. Arakelova1,*, Ellinor Michel2 1Zoological Institute of RAS, 1 Universitetskaya emb., St. Petersburg 199034, Russia 2Department of Zoology, The Natural History Museum, Cromwell Road, London SW7 5BD, UK ABSTRACT: Quantitative measures of feeding, respiration, growth and reproduction were brought together to achieve an overview of differences in physiology between 2 sympatric species of Anisus (Gastropoda, Planorbidae) in subarctic Lake Krivoye, northwestern Russia. This is a resource-limited lake with a short summer growing season where one might expect intense competition for resources among the numerous snails. Because coexistence is a multidimensional process, we have aimed to quantify bioenergetic variables related to several different major physiological functions. Using experiments that manipulated detritus and periphyton, we showed that both species consume detri- tus in combination with algae, but used different feeding strategies. Anisus contortus has a steeper growth allometry, greater specific growth rate and faster reproductive cycle. Anisus acronicus, how- ever, has a faster absolute growth rate and longer life cycle, which results in its dominance in biomass and numbers. Although bioenergetics in general cannot be used to test directly for competition between closely related species, we have shown alternative growth and energy-metabolism strate- gies used by different species in a common habitat. Indicators of niche partitioning, maintained by balance calculations, included differences in preferences, quality and consumption rate of consumed food. We expect that these differences are not only important in proximal coexistence, but may also present alternatives for surviving long-term changes in the lake’s productivity and habitat types. KEY WORDS: Anisus contortus · Anisus acronicus · Coexistence · Subarctic lake · Respiration · Growth · Feeding · P/B coefficients Resale or republication not permitted without written consent of the publisher INTRODUCTION We tested hypotheses of trophic and metabolic sepa- ration for the snails Anisus (Bathyomphalus) contortus Freshwater communities commonly include coexist- (Linnaeus, 1758) and A. (Gyraulus) acronicus (Férus- ing congeneric species. When resources are limiting sac, 1807) (=Gyraulus gredleri [Bielz] Gredler, 1853) and competition plays a role, coexistence requires lim- (Gastropoda, Planorbidae) which co-exist in Lake iting similarity with neighboring species to ensure eco- Krivoye in northwestern Russia. This is a resource- logical separation (Tilman 1994). This can happen limited lake with a short growing season where one through partitioning of food and habitat resources by might expect intense competition for resources. The selective feeding, habitat specificity or staggered life snails are broadly sympatric in habitat occurrence. cycles (Townsend & Hildrew 1979, Williams 1994) and Because coexistence is a multidimensional process, should be reflected in differences in the species aute- connected with spatial distribution, demographics, cology. A number of classic ecological studies are external resources and specific ecological differences devoted to determining how resources are partitioned between species, we have aimed to quantify major along niche axes among coexisting species (Under- bioenergetic variables with a focus on feeding, but also wood 1984, Fletcher & Creese 1985, Schmitt 1996, Yu address respiration, growth and fecundity. et al. 2003), guilds (Hines 1982), or populations (Wenn- Feeding, ingestion, absorption and egestion rates are gren & Ólafsson 2002). the central variables determining the input and output *Email: [email protected] © Inter-Research 2009 · www.int-res.com 210 Aquat Biol 5: 209–217, 2009 of an animal’s bioenergetics. Selectivity in feeding fecundity. Quantitative descriptions of growth curves can result in resource partitioning (Schoener 1974) are generally focused on changes in mass through and results from either adaptive specializations that time, but should also include ontogenetic events such are species- or population-specific, or from behavioral as attainment of reproductive maturity, onset of senes- plasticity that allows animals to cope with variation in cence and total life span. The aim of the present study food types in space and time. Several studies have was to measure the rates of the main physiological quantified ingestion rates and absorption efficiencies processes in 2 freshwater planorbid snails. We bring in freshwater gastropods, such as Calow’s (1975) work together quantitative measures of respiration, growth on differences between the grazers Ancylus fluviatilis and feeding to achieve an overview of potential bio- (Müller, 1774) and detritivores Planorbis (Anisus) con- energetic differences between 2 sympatric Anisus spe- tortus (Linnaeus, 1758), Eleutheriadis & Lazaridou- cies. We use these results to assess whether coexis- Dimitriadou’s (1996) work on Bithynia graeca (Wester- tence is mediated by quantitative differences in life lund 1879), Brendelberger’s (1997) work on Radix history and physiology, especially feeding, among spe- peregra (Müller, 1774) and B. tentaculata (Linnaeus, cies. 1758) and Lombardo & Cooke’s (2004) study of con- sumption rates in 2 co-occuring species, Physa sp. and Helisoma trivolvis (Say, 1817). MATERIALS AND METHODS The rate of food consumption in detritus-feeding invertebrates is controlled by the animal’s energetic Study site and species size. This research was car- needs and is generally inversely proportional to the ried out in the oligotrophic Lake Krivoye situated in the food quality (Cammen 1979, McIntyre et al. 2005). In basin of the White Sea, northwestern Russia. The sur- snails considered to be algivores, the relative con- face area of this lake does not exceed 0.5 km2, the max- sumption of periphyton and detritus material has sel- imal depth is ~30 m and mean depth is 11.8 m. Ice cov- dom been compared directly (Lombardo & Cooke ers the surface from October to late May and mean 2002). Absorption, the most significant quantitative temperatures range from 16 to 17°C during the growing indicator of nutrition, allows us to trace the transforma- season. The aquatic macrophytes Potamogeton crispus tion of utilized food and to characterize distinctive fea- L., Phragmites communis Trin., the sedge Carex lepo- tures of the ecology of coexisting species. As for other rina L. and other reeds occur, but only rarely, in the physiological functions, the absorption rate depends narrow strip of littoral zone. primarily on the animal’s mass. Quantitative data on Anisus contortus and A. acronicus (Fig. 1) samples absorption rates are comparatively limited to the well- were collected in a single sampling effort from 2 shal- documented relationships between respiration, growth low littoral sites where they are broadly sympatric at rate and animal size. Food absorption of target species depths of 0 to 0.5 m. The sites were 1 km apart and and the biomass of competitors may be used as a mea- chosen to differ in flow regime and substrates. Site 1 sure of competitive advantage (Basset 1997). There are (66° 20’ 16.96’’ N; 33° 38’ 50.42’’ E) had continuous water currently sufficient published data related to growth flow as it was situated at the head of an out-flowing and metabolism of macroinvertebrates providing us stream and snails occurred on stones and pebbles, with a common notion about the mean rate of absorp- the preferred substrate for both species. Potamogeton tion. sp. occurred at Site 1, but only rarely. Site 2 (66° 20’ Life history differences among species are com- monly explained as a balance between the demands for growth and reproduction (Stearns 1992). Differ- ences in growth rates are common among closely related species that divide ecological space. For exam- ple, 2 closely related sympatric Heleobia species showed different growth rates along a gradient of estu- arine conditions (De Francesco & Isla 2004). Lymnaea peregra and L. ovata have convergent adult forms despite differing genetics; however, when grown under the same conditions they differed in juvenile growth rate and reproductive schedule (Wullschleger & Jokela 2002). Differences in size among closely Fig. 1. Anisus acronicus and A. contortus. (a) A. acronicus related species that share a habitat may be evidence apical and apertural views (redrawn from Starobogatov 1977, of genetic differences that determine alternative life Fig. 414a,b). (b) Anisus contortus apical (left), basal and history strategies, i.e. different balances of growth and apertural views (redrawn from Zhadin 1952, Fig. 93) Arakelova & Michel: Physiological differences between coexisting subarctic snails 211 38.21’’ N; 33°38’ 00.03’’ E) had still water, and the snail matched for shell size and mass (Table 1). Container substrate included the common reed Phragmites com- volume was large compared to biomass and unlikely munis. To quantify the relative abundances and bio- to have inhibited growth. Food was added in excess to mass of snails at each site, we sampled with a 25 × prevent negative effects of grouping on growth rate. In a 25 cm square frame placed randomly over 4 sections of parallel experiment, single snails (n = 20) were put in the the bottom at each site. The sampling frame was beakers of
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