Mechanism of a Plastic Phenotypic Response: Predator-Induced Shell Thickening in the Intertidal Gastropod Littorina Obtusata
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doi:10.1111/j.1420-9101.2007.01299.x Mechanism of a plastic phenotypic response: predator-induced shell thickening in the intertidal gastropod Littorina obtusata J. I. BROOKES & RE´ MY ROCHETTE University of New Brunswick, Saint John, NB, Canada Keywords: Abstract phenotypic plasticity; Phenotypic plasticity has been the object of considerable interest over the past evolutionary potential; several decades, but in few cases are mechanisms underlying plastic responses predation risk; well understood. For example, it is unclear whether predator-induced changes induced defences; in gastropod shell morphology represent an active physiological response or a mechanisms; by-product of reduced feeding. We address this question by manipulating shell morphology; feeding and growth of intertidal snails, Littorina obtusata, using two approa- gastropod; ches: (i) exposure to predation cues from green crabs Carcinus maenas and (ii) green crab; reduced food availability, and quantifying growth in shell length, shell mass, Littorina obtusata; and body mass, as well as production of faecal material and shell micro- Carcinus maenas. structural characteristics (mineralogy and organic fraction) after 96 days. We demonstrate that L. obtusata actively increases calcification rate in response to predation threat, and that this response entails energetic and developmental costs. That this induced response is not strictly tied to the animal’s behaviour should enhance its evolutionary potential. physiological modifications generally induced by ‘pred- Introduction ator cues’, and which increase resistance to predatory Phenotypic plasticity, i.e. the ability of a particular attacks (see review by Harvell, 1990). Examples of genotype to produce different phenotypes in response induced defences among animals in response to chemical to environmental variation (West-Eberhard, 1989; cues released by a predator, or predatory event, include Thompson, 1991; Via et al., 1995; Zhivotovsky et al., the production of larger spines in the colonial marine 1996; DeWitt et al., 1998; Pigliucci, 2005), has been the bryozoan Membranipora membranacea (Harvell, 1992), object of considerable interest and debate over the past bending of the lateral plates of the barnacle Chthamalus two decades; recent reviews can be found in DeWitt & anisopoma (Lively et al., 2000), production of neckteeth Scheiner (2004a), Pigliucci & Preston (2004), and by water fleas, Dapnia spp. (Tollrian, 1995), production of Pigliucci (2005). However, plasticity was not part of the thicker and/or more ornamental shells by different neo-Darwinian synthesis, and it has only recently been species of mollusc (Appleton & Palmer, 1988; Palmer, incorporated into theoretical models of evolutionary 1990; Trussell, 1996; Cheung et al., 2004), changes in tail potentials and trajectories (see Sarkar, 2004 for an and body colour and shape of amphibian tadpoles insightful historical overview). Furthermore, rigorous (McCollum & Leimberger, 1997; Van Buskirk & McCol- empirical tests concerning the adaptive value of plasticity lum, 2000; Teplitsky et al., 2003; LaFiandra & Babbitt, remain rare (DeWitt & Scheiner, 2004b), and in very few 2004; Morre et al., 2004), and development of deeper cases are the mechanisms underlying plastic responses bodies in crucian carp, Carassius carassius (Vøllestad et al., well understood (Windig et al., 2004). 2004). Inducible defences are amongst the best-documented Predator-induced morphological defences have been and most taxonomically widespread examples of phen- documented in several species of intertidal gastropods otypic plasticity; they are behavioural, morphological, or (Nucella lamellose: Appleton & Palmer, 1988; Nucella lapillus: Palmer, 1990; Littorina obtusata: Trussell, 1996; Littorina subrotundata: Dalziel & Boulding, 2005). The Correspondence: Dr. Re´my Rochette, Biology Department, University of New Brunswick (Saint John), 100 Tucker Park Road, P.O. Box 5050, specific cues responsible for these phenotypic changes are Saint John, NB, E2L 4L5 Canada. Tel.: 506 648-5988; fax: 506 648-5811; not known, but they are chemical in nature and related e-mail: [email protected] to the foraging activity of predators. In particular, ª 2007 THE AUTHORS JOURNAL COMPILATION ª 2007 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY 1 2 J. I. BROOKES AND R. ROCHETTE experiments have shown that gastropods exposed to two different approaches: (i) exposure to predation cues effluents from predatory crabs fed conspecific snails (effluents from C. maenas feeding on L. obtusata snails) develop thicker, or more ornamented shells than those and (ii) varying food availability, and we compared exposed to crabs that are starved or fed alternative types patterns of linear shell growth and shell mass growth of food, which in turn develop better-defended shells with patterns predicted (see Materials and methods) by than snails not exposed to any type of predation effluent the three different mechanisms of predator-enhanced (Appleton & Palmer, 1988; Palmer, 1990; Trussell & shell thickening outlined above. We also quantified snail Nicklin, 2002). Similar phenotypically plastic responses body mass growth, production of faecal material, as well have been documented in numerous species of inverte- as shell aperture area and micro-structural characteristics brates and vertebrates (Kats & Dill, 1998). (mineralogy and organic fraction) to further investigate Very little empirical work has been done to elucidate the benefits, costs and evolutionary significance of this the proximate control of induced defences in gastropod plastic response. We demonstrate that L. obtusata actively molluscs, or any other animal for that matter. One increases its rate of shell material deposition in response outstanding question, which has significant implications to predation threat, and that this response entails both for the costs and evolutionary potential of this plastic energetic and developmental costs. That this induced response, is whether predator-enhanced shell thickness response is not strictly tied to, and hence constrained by, and ornamentation is an active physiological response to the animal’s behaviour should enhance its potential to predation risk, or a developmental by-product of a evolve by natural selection. behavioural change induced by predation cues (Palmer, 1990; Trussell, 1996; Trussell & Etter, 2001; Trussell & Materials and methods Nicklin, 2002). More specifically, perhaps predation cues cause an active increase in the rate at which calcium Collection and initial morphological measurements carbonate is deposited by the mantle into the gastropod’s shell; if the rate of linear shell translation (i.e. increase of Small L. obtusata were randomly collected at mid-tide shell length along the axis of coiling) is unchanged, then level (3.86 m above mean low water) from St Andrews this increased calcification rate will result in the produc- (45°04¢08.45¢¢N, 67°02¢14.59¢¢W), NB, until 400 snails tion of a relatively thicker shell. Alternatively, predation 4.5–6.0 mm in shell length (see Trussell, 1996) were cues may cause snails to reduce feeding activity, which in obtained. In the lab, we measured shell length of all turn could cause a reduction in the rate of body growth experimental animals using digital callipers (±0.01 mm), and linear shell translation (e.g. Behrens Yamada et al., and then shell mass and body tissue mass using a 1998; Trussell et al., 2003); if calcification rate remains nondestructive weighing technique developed by Palmer unchanged, then this reduced shell elongation will cause (1982). This technique, which is based on the fact that more calcium carbonate to be deposited in any area of the specific gravity of a snail’s body tissue is similar to the shell parallel to the axis of translation. In support of that of sea water, involves weighing each snail sub- this latter hypothesis, studies have shown that predation merged in seawater and also in air, and then using cues can reduce both snail grazing activity and linear regression equations, developed separately with sacri- shell translation (e.g. Behrens Yamada et al., 1998; ficed animals, to estimate their dry shell and body tissue Trussell et al., 2003), and that growth rate is intrinsically masses, respectively, from these whole-snail mass meas- related to the shape (Kemp & Bertness, 1984; Boulding & urements (Palmer, 1982). To obtain submerged masses, a Hay, 1993; DeWitt, 1998; Yeap et al., 2001) and mass Mettler AE240 balance (±0.00001 g) was placed above (Kemp & Bertness, 1984; Boulding & Hay, 1993) of an aquarium filled with seawater maintained at approxi- gastropod shells. A third possibility is that both these mately 18 °C, and a small weighting boat was suspended mechanisms contribute to predation-induced increases in by a fine copper wire from the underside of the balance. gastropod shell thickness. Before being transferred to the weighing boat, each snail The main objective of this study was to determine was chased into its shell while still underwater to remove which of these mechanisms was responsible for the any air bubbles that might be present within the shell, production of thicker and heavier shells by L. obtusata which would have affected the submerged mass estimate; snails raised in the presence of effluents from green crabs, we ensured the aperture remained full of water during C. maenas, feeding on conspecific snails (Trussell, 1996; transfer to the weighing boat, so no new air bubbles Trussell & Nicklin, 2002). There is evidence that this