Differences between two physid species (Gastropoda: Physidae) in antipredator behaviour induced by leeches

Differences between two physid species (Gastropoda: Physidae) in antipredator behaviour induced... Abstract The occurrence and the intensity of specific behavioural defensive reactions were investigated in freshwater snails of the family Physidae, which vigorously shake their shells when attacked by invertebrate predators. Physella acuta and Physa fontinalis were exposed to two species of leeches with different hunting strategies—the molluscivorous Glossiphonia complanata and the opportunistic predator Erpobdella octoculata. Parameters of reaction were measured and compared between snails and leeches. Significant differences were found in the reactions of both snail species in 10 out of 11 measured parameters. Physa fontinalis reacted more intensively, with a higher number of shell movements triggered by both leech species. The study showed possible recognition by the prey of the predator species, followed by a specific defensive reaction. In general, G. complanata elicited more intensive reactions, especially in treatment with P. fontinalis. INTRODUCTION For most animals, the ability to recognize predators as a potential danger is of fundamental importance. This ability can be either innate or acquired and is considered to be the first stage of defence (Vermeij & Covich, 1978; Lima & Dill, 1990). Early recognition of danger gives animals the opportunity to respond with a suitable strategy and is significant because different threats require different defensive reactions. Induction of these responses in freshwater snails is a good example of phenotypic plasticity, which can refer to induced changes in behaviour, anatomy or even life history (Petterson, Nilsson & Brönmark, 2000; Kishida & Nishimura, 2005). Animals have basically two defensive strategies to choose from, in different time perspectives: the first is to avoid a predator’s attack (e.g. upon sensing a chemical signal; this can be considered an early response) and the second is to repulse a direct attack when it occurs (late response; Lima & Dill, 1990). In freshwater snails, both early and late responses are evident in changes of behaviour, shell morphology and life history (e.g. Crowl, 1990; Langerhans & DeWitt, 2002; Covich, 2010). Changes in shell morphology and life history traits can only occur over a longer time perspective, due to the ontogenetic nature of such changes (Langerhans & DeWitt, 2002; Dalesman, Rundle & Cotton, 2009) and are often expressed no sooner than the subsequent generation (Dybdahl & Kane, 2005). Changes in behaviour, however, can occur at any time throughout the animal’s life. There are often specialized defence mechanisms that are particularly effective during encounters with particular types of predators. A defence mechanism can be a risky strategy, but on the other hand they may have positive effects, e.g. by allowing longer foraging time. Caenogastropod snails can effectively defend against direct attack by shell-invading predators by closing the operculum, whereas pulmonates do not have this option, generally lacking an operculum. Moreover, defence against direct attack is not common among pulmonates (Brönmark & Malmqvist, 1986). An exception is the family Physidae, in which there is a characteristic muscle group (‘physid muscles’) that are considered to be responsible for a specific defensive reaction (SDR), which is the main defence mechanism against predatory, shell-invading leeches (Townsend & McCarthy, 1980; Dillon, 2000; Taylor, 2003; Naranjo-García & Appleton, 2009). Upon physical contact of a predator with the sensitive, finger-like extensions of its mantle, the snail starts vigorous shell-shaking movements or leaping (Degner, 1921). This reaction is still not fully understood, including its use in defence against shell-invaders and the differences in its expression between snail species and against various threats (Townsend & McCarthy, 1980; Wilken & Appleton, 1991; Taylor, 2003). Notably, the precise parameters of the SDR in response to direct contact with the predator have been little studied. In the natural environment, snails are exposed to various predators including those that are not specialized in hunting for snails (Dillon, 2000) and numerous studies have dealt with general predator–prey interactions, assuming various defensive strategies (e.g. Eggers, 1978; Peckarsky, 1980; Pierce, 1988; Alexander & Covich, 1991; Boeing, Ramcharan & Riessen, 2006; Squires et al., 2008; Lehtonen, McCrary & Meyer, 2012). Such interactions always involve tradeoffs between predator and prey (Covich, 2010). Moreover, an SDR that evolved against particular predators can also be exhibited against species closely related to such predators, even when they are harmless (Langerhans & DeWitt, 2002). Such an unnecessary reaction was described for Physa fontinalis in response to stimuli from leeches and triclads; the reaction was observed whether the predators were molluscivorous or non-molluscivorous (Langerhans & DeWitt, 2002). On the other hand, certain species show more discrimination in their response strength, depending on the degree of potential threat from predators. Such differentiation is especially important when a snail is threatened simultaneously by specialized and generalist predators. Thus, the correct recognition of signals from predators allows snails to avoid the energetic cost of an unnecessary reaction. In their study of this phenomenon, Townsend & McCarthy (1980) used tissue only from the anterior (sucker) of the leech’s body, so their results do not provide a complete account. Exposure of snails to a direct threat from actively hunting leeches that differ in diet should provide information about the effectiveness of the SDR (Brönmark & Malmqvist, 1986). Differences between closely related snail species in predator recognition and avoidance should also be informative, yet remain poorly understood (Alexander & Covich, 1991). For instance, while it is known that P. fontinalis exhibits a very intensive and efficient defensive reaction at least against shell-invading leeches (Townsend & McCarthy, 1980; Brönmark & Malmqvist, 1986; Taylor, 2003), less is known about the response of Physella acuta, which shows a less intensive reaction to molluscivorous leeches than that of Aplexa marmorata (Wilken & Appleton, 1991). Therefore, the nature of the SDR in closely related species depending on the type of threat remains a matter of speculation. Perhaps even a less intensive reaction is sufficient to escape a predator. It is worth noting that P. acuta is the most widespread freshwater snail globally; furthermore, its range is expanding in Europe, where it has been considered an alien species (Turner & Montgomery, 2009; Covich, 2010; Strzelec, 2011). Some authors have attributed the success of the species to, among other attributes, the physid SDR (Naranjo-García & Appleton, 2009). The aim of this study was to compare an induced behavioural SDR and its effectiveness between two physid species, one native to Europe (Physa fontinalis) and the other alien (Physella acuta). We described and compared the reaction of these species against direct threat from a molluscivorous leech (Glossiphonia complanata) and an opportunistic species (Erpobdella octoculata). MATERIAL AND METHODS Subject Physella acuta and Physa fontinalis were exposed to two species of freshwater predatory leeches, Erpobdella octoculata and Glossiphonia complanata. Specimens of P. acuta were obtained from the longterm culture (started in 2006) at the Department of Hydrobiology, University of Warsaw. Specimens of P. fontinalis, E. octoculata and G. complanata, on the other hand, were collected in the field, from Lake Łaśmiady (Masurian Lakeland District, Poland; GPS: 53°56′04.2″N 22°17′09.3″E), the small rivers of Wilanówka, Potok Służewiecki (Warsaw, Poland; GPS: 52°09′00.4″N 21°07′04.8″E and 52°10′03.9″N 21°01′35.7″E, respectively) and Ciemięga (Sadurki, Poland; GPS: 51°17′59.9″N 22°19′15.2″E), as well as small ponds in the valley of the Potok Służewiecki river (Warsaw, Poland; GPS: 52°10′11.8″N 21°02′14.9″E). In order for the animals to acclimate, all species were kept separately in four aerated aquaria filled with filtered tap water (20 l each, 16:8 h light:dark, 22 °C) for several weeks prior to the experiment. All animals were fed ad libitum, snails with commercial fish food (Tropical® ‘Vitabin’) and leeches with P. acuta. In the case of E. octoculata, the snails were crushed before being administered. Leeches were not fed also with P. fontinalis, because insufficient individuals were available for both experimentation and feeding. Apparatus A stereoscopic Nikon C-BD230 microscope and NIS Elements D 4.00.01 software were used to measure the animals. The aquaria (dimensions 15 × 5 × 5 cm) were filled with tap water filtered through a carbon filter. Two video cameras (VIDEOLINE ViDi-500S) were mounted to record each of the aquaria from the front and top. Procedure One week before the experiment, 60 individuals of each snail species were randomly selected from the aquaria and placed separately in 100 ml plastic containers (summer photoperiod 16:8 h light:dark, 22 °C). Thirty specimens of E. octoculata and 18 specimens of G. complanata were used in each treatment (exposing prey to predator). The leeches were starved for 1 week prior to the experiment. All animals were weighed (ranges: P. acuta 0.021–0.081 g, P. fontinalis 0.017–0.130 g, G. complanata, 0.013–0.169 g, E. octoculata 0.030–0.384 g) before the experiment. Each trial comprised the following steps. First, 30 min before predator exposure, a single snail was placed in the aquarium to acclimate. After this time a leech was put into the aquarium and recording was started. After every exposure, the snail (if still alive) and the leech were taken out, the aquarium was cleaned and refilled with new water. Each recording was up to 2 h long, but was stopped if the snail was eaten earlier. This procedure was conducted separately for all selected individuals of both snail species (30 per treatment). Because of the low number of collected individuals of G. complanata, individuals of this leech had to be used in the experiment more than once (specimens being randomly selected each time). While investigating the behavioural response of the snails, we focused on the physid SDR (Degner, 1921). The SDR was identified as a vigorous shell-shaking reaction (first described by Degner, 1921, and in detail by Townsend & McCarthy, 1980), sometimes also followed by leaps, but also detachment from the substrate, considered a less intensive reaction (Townsend & McCarthy, 1980; Wilken & Appleton, 1991). In order to obtain a more detailed description of the SDR, 11 parameters were chosen and measured based on analysis of the recordings (Table 1). Table 1. Selected parameters used to describe the SDR of Physella acuta and Physa fontinalis.   Parameter  Scale  A  Occurrence of SDR  0, no reaction; 1, reaction  B  Occurrence of SDR in response to chemical cue  0, no reaction; 1, reaction (only if snail reacted without direct contact with leech)  C  Intensity of first occurrence of SDR  0, no reaction; 1, shell-shaking without leaps or only vertical movement in aquarium; 2, strong shell-shaking with leaps  D  Effectiveness of first occurrence of SDR  0, leech remained attached to snail after SDR; 1, SDR resulted in failure of leech attack  E  Snail sensitivity  0, no reaction or reaction to attachment by leech sucker to shell; 1, reaction to leech touch or chemical cue  F  Number of events of SDR during predator exposure  Number (defensive reactions treated as separate reactions if intervals between shell movements were longer than 5 s)  G  Number of events of SDR induced by direct contact with predator  Number  H  Average number of shell movements in a single SDR  Number  I  Number of events of direct contact with predator during exposure  Number  J  Number of SDR with leaps only during exposure  Number  K  Mortality upon first direct contact with predator  0, snail not consumed; 1, snail consumed    Parameter  Scale  A  Occurrence of SDR  0, no reaction; 1, reaction  B  Occurrence of SDR in response to chemical cue  0, no reaction; 1, reaction (only if snail reacted without direct contact with leech)  C  Intensity of first occurrence of SDR  0, no reaction; 1, shell-shaking without leaps or only vertical movement in aquarium; 2, strong shell-shaking with leaps  D  Effectiveness of first occurrence of SDR  0, leech remained attached to snail after SDR; 1, SDR resulted in failure of leech attack  E  Snail sensitivity  0, no reaction or reaction to attachment by leech sucker to shell; 1, reaction to leech touch or chemical cue  F  Number of events of SDR during predator exposure  Number (defensive reactions treated as separate reactions if intervals between shell movements were longer than 5 s)  G  Number of events of SDR induced by direct contact with predator  Number  H  Average number of shell movements in a single SDR  Number  I  Number of events of direct contact with predator during exposure  Number  J  Number of SDR with leaps only during exposure  Number  K  Mortality upon first direct contact with predator  0, snail not consumed; 1, snail consumed  The experiment was carried out in four treatments: P. acuta exposed to G. complanata, P. acuta exposed to E. octoculata, P. fontinalis exposed to G. complanata and P. fontinalis exposed to E. octoculata. Data and statistical analysis Treatments were analysed with regard to snail species, leech species and the interaction between them, using generalized linear models (GLMs), with binomial errors and a logit link function for parameters A, D and E, Poisson errors and a log link function for parameters B, C, J and K, and gamma errors and a log link function for parameters F, G, H and I (Table 1). The correlations of length and weight of snails and leeches with all parameters were investigated (Spearman correlation) in order to determine any possible influence of animal body mass and size on the success of both hunting leeches and snail defensive strategies. Statistical analysis was carried out using SPSS software (v. 23). RESULTS Significant differences between snail species were found for 10 of 11 analysed parameters and between leech species in seven of 11 analysed parameters. Occurrence of SDR Occurrence of SDR differed significantly between the snail species (Wald χ2 = 9.93, P = 0.002) and when exposed to different predators (Wald χ2 = 6.00, P = 0.014) (Fig. 1A). There was no significant interaction between snail species and leech species in occurrence of SDR (Wald χ2 = 0.01, P = 0.978). The reaction was more frequently noted in treatments with Physa fontinalis, but both snail species reacted more often when exposed to Glossiphonia complanata than Erpobdella octoculata. Figure 1. View largeDownload slide Estimated marginal means of measured parameters. Panels A–K and their scales correspond to parameters from Table 1. Solid and broken lines represent Physella acuta and Physa fontinalis, respectively. Figure 1. View largeDownload slide Estimated marginal means of measured parameters. Panels A–K and their scales correspond to parameters from Table 1. Solid and broken lines represent Physella acuta and Physa fontinalis, respectively. Occurrence of SDR in response to chemical cue Occurrence of SDR in response to chemical cue was observed in 12 cases of exposure P. fontinalis to G. complanata and in only one case of exposure of P. fontinalis to E. octoculata (Fig. 1B). No SDR response to chemical cue was observed in Physella acuta. Due to low numbers of SDR responses to chemical cue, full model results were unavailable. Intensity of first occurrence of SDR The intensity of the first occurrence of SDR was significantly higher for both snail species in treatments with G. complanata than in treatments with E. octoculata (Wald χ2 = 10.99, P = 0.001) (Fig. 1C). However, P. fontinalis reacted significantly more intensively than P. acuta when exposed to G. complanata as well as E. octoculata (Wald χ2 = 7.62, P = 0.006). There was no significant interaction between snail species and leech species in intensity of the first SDR (Wald χ2 = 0.181, P = 0.670). Effectiveness of first occurrence of SDR There were significant differences between the two snail species in the effectiveness of the first occurrence of their SDR (Wald χ2 = 14.55, P < 0.001), being higher in P. fontinalis (Fig. 1D). Both snail species had similar effectiveness of SDR when exposed to G. complanata and E. octoculata, and the values of this parameter did not differ significantly (Wald χ2 = 3.33, P = 0.068). There was no significant interaction between snail species and leech species in effectiveness of first SDR (Wald χ2 = 0.45, P = 0.504). Snail sensitivity Significant differences in sensitivity between both snail species were found between snail species exposed to G. complanata and E. octoculata (Wald χ2 = 19.54, P < 0.001) (Fig. 1E). In both treatments, P. fontinalis showed higher sensitivity than P. acuta, but the differences were not significant (Wald χ2 = 0.52, P = 0.471). There was no significant interaction between snail species and leech species in snail sensitivity (Wald χ2 = 1.45, P = 0.229). Number of events of SDR during predator exposure The highest number of SDR (average = 5) was observed for the treatment of P. fontinalis with G. complanata. In general, P. fontinalis reacted more frequently than P. acuta (Wald χ2 = 22.54, P < 0.001), and both species had different numbers of SDR when exposed to different predators (Wald χ2 = 6.53, P = 0.011) (Fig. 1F). For P. fontinalis, values of this parameter were higher for the G. complanata treatment than for the E. octoculata treatment. There was no significant interaction between snail species and leech species (Wald χ2 = 2.26, P = 0.133). Number of events of SDR induced by direct contact with predator For P. fontinalis, there were more events of SDR induced by direct contact with G. complanata and E. octoculata than for P. acuta (Wald χ2 = 15.00, P < 0.001) (Fig. 1G). Direct contact with G. complanata induced higher numbers of SDR in both snails species that with E. octoculata (Wald χ2 = 6.09, P = 0.014). There was no significant interaction between snail species and leech species in number of events of SDR induced by direct contact (Wald χ2 = 0.11, P = 0.738). Average number of shell movements in single SDR The highest values were observed in treatments involving P. fontinalis and G. complanata (average = 2.5 per SDR), being significantly higher in treatments involving P. acuta and G. complanata (average = 1.5) (Wald χ2 = 4.05, P = 0.044) (Fig. 1H). Different species of leeches also influenced this parameter, higher values being observed for both snails exposed to G. complanata (Wald χ2 = 4.74, P = 0.029). Due to lack of SDR during exposure of P. acuta to E. octoculata, results of interaction of snail species and leech species were unavailable. Number of events of direct contact with predator during exposure There were differences for both snail species in the number of events of direct contact with G. complanata and E. octoculata (Wald χ2 = 86.03, P < 0.001), but no differences were observed between the snail species (Wald χ2 = 0.02, P = 0.896) (Fig. 1I). There was no significant interaction between snail species and leech species in number of direct contacts (Wald χ2 = 0.09, P = 0.759). Number of SDR with leaps only during exposure There were no significant differences in this parameter between the snail species (Wald χ2 = 3.62, P = 0.057) or between different leech species (Wald χ2 = 0.07, P = 0.789) (Fig. 1J). There was no significant interaction between snail species and leech species (Wald χ2 = 0.22, P = 0.638). Mortality upon first direct contact with predator Results of the full model were unavailable for this analysis. First contact with G. complanata caused mortality of P. acuta in six cases and of P. fontinalis in only one case (Fig. 1K). There were no cases where snails died after first contact with E. octoculata. No significant correlations of length and weight of snails and leeches with all SDR parameters were found; the observed Spearman correlation coefficients were all low (rho < 0.2, P > 0.05). DISCUSSION In general, the measured parameters of SDR indicated that, regardless of snail species examined, the defensive reaction was far less expressed in treatments with the generalist predator Erpobdella octoculata. For both snail species, Physa fontinalis and Physella acuta, the SDR occurred more often (c. 50% increase) in the presence of the molluscivorous leech Glossiphonia complanata. Similarly, the average number of shell-shaking movements in a single SDR and the intensity of the first SDR were lower in presence of E. octoculata. Furthermore, often the only reaction observed during exposure to E. octoculata was detachment and floating up to the water surface, especially in the case of P. acuta. This kind of defensive reaction is less elaborate than shell shaking (in terms of response categories described by Wilken & Appleton, 1991), but still allows escape from a potentially dangerous area. Rapidly escaping the leech would seem to be a good defensive strategy, provided there is no simultaneous threat from other types of predators (e.g. fish, as described by Ahlgren & Brönmark, 2012). In the experimental treatments, the snails encountered G. complanata less frequently than E. octoculata. This might suggest that the snails tended to avoid the more serious threat posed by G. complanata. On the other hand, this particular leech species is considered a less active hunter, which could result in fewer encounters with prey. This is so because E. octoculata feeds mainly on immobile prey such as the larvae of Chironomidae (Young, Martin & Seaby, 1993), in contrast to G. complanata, which prefers snails (Young & Ironmonger, 1980). Similar results were reported by Townsend & McCarthy (1980), in which the strongest reaction of P. fontinalis was induced, among others, by G. complanata. Such discrimination between the presence and absence of threat is profitable for any prey, because induced late defensive reactions increase the probability of prey survival, while simultaneously reducing unnecessary defensive reactions when the threat is not present (Turner, Fetterolf & Bernot, 1999). DeWitt (1998) hypothesized the putative cost of induced defensive strategies such as morphological and life history changes in Physa heterostropha (a synonym of P. acuta), although he was unable to confirm these proposed costs experimentally. In contrast, induced behavioural changes (e.g. shell-shaking behaviour) would seem to have a low potential energetic cost to snails, especially when taking into account the energetic costs of early and late responses. A late-response SDR enables snails to react only when direct threat is presented, avoiding unnecessary investment in morphological changes or less time spent on foraging (e.g. when snails crawl out of water to avoid predators) (DeWitt, 1998; Rigby & Jokela, 2000). Shell-shaking behaviour saves energy that can be allocated to growth or reproduction instead. Physa fontinalis showed a stronger behavioural reaction than P. acuta as an effect of direct exposure to the two leech species. The effectiveness of the SDR of P. acuta was lower than that of P. fontinalis during the first attack of G. complanata. Despite using shell-shaking movements, 7% of attacked P. acuta died, while another 10% were killed without having exhibited these movements; ultimately, after a 2 h exposure, 67% of P. acuta individuals had been killed against only 4% (1 individual) of P. fontinalis. The initial defensive reaction seems to play a crucial role in escaping from the danger zone; preventing attachment of the leech to the snail’s shell, followed by a rapid escape from the place of attack can save the prey. The more vigorous and numerous shell-shaking movements and detachment of P. fontinalis allow it to escape its predator, while the reaction of P. acuta involved less shell-shaking movements without detachment from the substrate and mortality was consequently greater. In the latter species, should the leech fail to attach itself onto the shell of the hunted snail, it has no trouble repeating the attack. It is not only the strength of the SDR itself (as expressed by the number of shell-shaking movements) that limits the predator’s hunting success, but also the ability to repeat the reaction with a certain, effective frequency. Physa fontinalis exhibited defensive reactions more often over a period of 2 h, contributing to its low mortality. The overall stronger reaction and especially the sensitivity of P. fontinalis may be due to the finger-like mantle digitations that cover the outside of the shell. This touch-sensitive tissue is larger than in other physids, such as P. acuta (Piechocki, 1979). Thus, the reduced sensitivity of P. acuta may lie with the fact that a smaller area is covered by the mantle extensions, so that the leech sometimes manages to avoid stimulating the soft tissue on first encounter. In their laboratory experiment, Wilken & Appleton (1991) exposed two physids (P. acuta and Aplexa marmorata) to a molluscivorous leech species. Similarly to the observations reported in this paper, they found that A. marmorata, a species characterized by larger mantle digitations, exhibited a more complex and effective response to predators after direct contact than P. acuta, making the latter more vulnerable to predators. A complementary or alternative explanation could be connected with the quality or quantity of the ‘physid muscles’—present only in this particular family and considered to be responsible for the shell-shaking reaction (Naranjo-García & Appleton, 2009). Unfortunately, there are as yet insufficient data comparing these structures among physid species, so their contribution remains hypothetical. Physella acuta is also characterized by a low metabolic rate, allowing snails to remain under water for a longer period (Dillon, 2000), which could possibly also contribute to a weaker reaction strength. Another consideration is that in our experiment the leeches were fed only with P. acuta before experiment, so that they were more responsive towards P. acuta than P. fontinalis. However, all the leeches were collected from natural environments, where P. fontinalis and other possible prey species are present, and because the experiment was conducted shortly after collection, we consider any such bias towards P. acuta to be unlikely. Furthermore, every individual was starved for a week prior to the experiment, which should further decrease possible bias. A second possible reason for the significant differences in defensive reactions between the examined physids might be the origin of the animals used in the experiment. Individuals of P. fontinalis were collected in natural habitats, while those of P. acuta were supplied from a longterm culture (established in 2006) in which at least a few dozens of generations had experienced no contact with leeches. This could have led to a gradual weakening of defensive reactions and the ability to detect predators (e.g. Bernot & Whittinghill, 2003; Turner, Turner & Lappi, 2006). Turner et al. (2006) showed that the effects of the experience of P. acuta of fish predators were significant but rather small, suggesting that the behavioural reaction against fish is innate. However, the laboratory-reared generation used by these authors was the first generation from wild-caught specimens, whereas the snails in our experiment were reared without leech predators for many generations. Salice & Plautz (2011) also found some differences between wild-caught and laboratory-reared (for 3–4 generations) individuals of Physa pomilia in avoidance behaviour in response to crayfish; offspring of newly caught snails decreased their predator avoidance behaviour over time, while the opposite was observed for laboratory-reared ones. However, over the 40 days of the experiment, offspring of newly caught and laboratory snails displayed similar predator-avoidance behaviour on average. Since we compared two species with different population histories, we cannot comment on the possible significance of past experience of predators within prey species and this should be the subject of future research. Physella acuta is a generalist species with a broad geographical range, which thereby encounters different types of predators. The adaptive evolutionary response to predators is probably less specialized when facing many levels of risk (McCarthy & Fisher, 2000). Investment in large mantle extensions or developing more rapid SDR may compromise the allocation of resources to other defensive mechanisms. McCarthy & Fisher (2000) suggested that surfacing is one of the least costly defensive behaviours and commonly found when only the chemical trait of a predator is present, without alarm cues from injured snails. Moreover, the probability of encounter with an actively hunting predator is higher than with opportunistic ones. Thus, allocation of resources to different defensive strategies, such as altered shell morphology or life history traits, might be preferable when other kinds of predators are detected (Young & Procter, 1986). Even though laboratory breeding of P. acuta may have affected the results of this study, the simultaneous threats from other predators (such as fish or crayfish) common in natural environment may sometimes cause changes in behaviour or morphology of the shell in contrary directions. In such situations prey might be predicted to respond to the most dangerous predator and the overall adaptational change may be a trade-off (Lakowitz, Brönmark & Nyström, 2008; Bourdeau, 2009). Despite the higher mortality of P. acuta than P. fontinalis found in our study, the former species has the faster growth rate and thus might be more competitive than P. fontinalis, which appears to be crucial in the multipredatory environment (Früh, Haase & Stoll, 2017). Physa fontinalis seems to be better adapted to resist direct attacks from molluscivorous leeches, which may be the result of a more efficient discrimination between species that pose a threat and those that do not. Generally, the values of the response parameters in the two predator treatments differed more strongly in case of P. fontinalis than P. acuta. Physella acuta did not always react to G. complanata upon first encounter and the number of encounters needed to trigger the first defensive reaction was high, when exposed to either leech species; it was less discriminating in its response to the two leech species and slower to react at all. The reaction of Lymnaea stagnalis was found to be faster when the snail was pre-exposed to the chemical cue of a predator (Dalesman et al., 2006). In our experiment, P. fontinalis reacted to G. complanata upon first encounter or even when it had only detected leech odour. The opposite was observed on treatment with E. octoculata, when the reaction occurred much later, suggesting that the reaction was induced only after the snail had been disturbed for a longer period of time. Furthermore, P. fontinalis reacted not only to the touch or attack of the molluscivorous leech, but also to its chemical signal (kairomone) if the leech was in close proximity where it presented a high, direct threat. In other words, as found by Bourdeau (2009), the defensive reaction was strongest and most appropriate to the most dangerous predator present at time. The efficient defensive reaction of P. fontinalis allows the snail to react only if a leech is in close proximity or attacking. Thus, no escape strategy (e.g. crawling to the surface) is required when a chemical cue is detected (Brönmark & Malmqvist, 1986). In our experiment, the number of encounters with G. complanata was the same for both snail species, regardless of the efficacy of their defenses. Therefore, it can be assumed that P. acuta does not use escape strategies as often as P. fontinalis to avoid attack from leeches. Physella acuta is among the most ubiquitous macroinvertebrates in the world, inhabiting a wide spectrum of fresh waters (Dillon et al., 2002; Turner & Montgomery, 2009; Covich, 2010). Naranjo-García & Appleton (2009) claim that the physid SDR has been key to the spread of P. acuta. On the other hand, this theory is less convincing when considering the fact that the snail is very susceptible to predation by shell-invading invertebrates such as leeches, triclads and insects (Turner & Chislock, 2007; Lombardo et al., 2012). Apparently its behavioural defence mechanisms against these predators are not efficient and are only auxiliary to other antipredator adaptations. Instead, successful colonization of new areas seems to be associated with early maturation, high reproductive potential, relatively long life and high phenotypic plasticity in life history (Blandenier & Perrin, 1989; Turner & Montgomery, 2009; Covich, 2010; Núñez, 2011). ACKNOWLEDGEMENTS We would like to thank Ludmiła Rycielska, Piotr Rycielski and Associate Editor Prof. Yoichi Yusa for advice on statistical analysis. FUNDING This research was partially supported by funds from the National Science Centre of Poland B/NZ8/04670 and carried out in the Biological and Chemical Research Centre, University of Warsaw. REFERENCES Ahlgren, J. & Brönmark, C. 2012. Fleeing towards death—leech-induced behavioural defences increase freshwater snail susceptibility to predatory fish. Oikos , 121: 1501– 1506. 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Competitive interactions between the lake-dwelling leeches Glossiphonia complanata and Helobdella stagnalis an experimental investigation of the significance of a food refuge. Oecologia , 93: 156– 161. Google Scholar CrossRef Search ADS PubMed  Young, J.O. & Procter, R.M. 1986. Are the lake‐dwelling leeches, Glossiphonia complanata (L.) and Helobdella stagnalis (L.), opportunistic predators on molluscs and do they partition this food resource? Freshwater Biology , 16: 561– 566. Google Scholar CrossRef Search ADS   © The Author(s) 2017. Published by Oxford University Press on behalf of The Malacological Society of London, all rights reserved. For Permissions, please email: journals.permissions@oup.com http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Journal of Molluscan Studies Oxford University Press

Differences between two physid species (Gastropoda: Physidae) in antipredator behaviour induced by leeches

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Abstract

Abstract The occurrence and the intensity of specific behavioural defensive reactions were investigated in freshwater snails of the family Physidae, which vigorously shake their shells when attacked by invertebrate predators. Physella acuta and Physa fontinalis were exposed to two species of leeches with different hunting strategies—the molluscivorous Glossiphonia complanata and the opportunistic predator Erpobdella octoculata. Parameters of reaction were measured and compared between snails and leeches. Significant differences were found in the reactions of both snail species in 10 out of 11 measured parameters. Physa fontinalis reacted more intensively, with a higher number of shell movements triggered by both leech species. The study showed possible recognition by the prey of the predator species, followed by a specific defensive reaction. In general, G. complanata elicited more intensive reactions, especially in treatment with P. fontinalis. INTRODUCTION For most animals, the ability to recognize predators as a potential danger is of fundamental importance. This ability can be either innate or acquired and is considered to be the first stage of defence (Vermeij & Covich, 1978; Lima & Dill, 1990). Early recognition of danger gives animals the opportunity to respond with a suitable strategy and is significant because different threats require different defensive reactions. Induction of these responses in freshwater snails is a good example of phenotypic plasticity, which can refer to induced changes in behaviour, anatomy or even life history (Petterson, Nilsson & Brönmark, 2000; Kishida & Nishimura, 2005). Animals have basically two defensive strategies to choose from, in different time perspectives: the first is to avoid a predator’s attack (e.g. upon sensing a chemical signal; this can be considered an early response) and the second is to repulse a direct attack when it occurs (late response; Lima & Dill, 1990). In freshwater snails, both early and late responses are evident in changes of behaviour, shell morphology and life history (e.g. Crowl, 1990; Langerhans & DeWitt, 2002; Covich, 2010). Changes in shell morphology and life history traits can only occur over a longer time perspective, due to the ontogenetic nature of such changes (Langerhans & DeWitt, 2002; Dalesman, Rundle & Cotton, 2009) and are often expressed no sooner than the subsequent generation (Dybdahl & Kane, 2005). Changes in behaviour, however, can occur at any time throughout the animal’s life. There are often specialized defence mechanisms that are particularly effective during encounters with particular types of predators. A defence mechanism can be a risky strategy, but on the other hand they may have positive effects, e.g. by allowing longer foraging time. Caenogastropod snails can effectively defend against direct attack by shell-invading predators by closing the operculum, whereas pulmonates do not have this option, generally lacking an operculum. Moreover, defence against direct attack is not common among pulmonates (Brönmark & Malmqvist, 1986). An exception is the family Physidae, in which there is a characteristic muscle group (‘physid muscles’) that are considered to be responsible for a specific defensive reaction (SDR), which is the main defence mechanism against predatory, shell-invading leeches (Townsend & McCarthy, 1980; Dillon, 2000; Taylor, 2003; Naranjo-García & Appleton, 2009). Upon physical contact of a predator with the sensitive, finger-like extensions of its mantle, the snail starts vigorous shell-shaking movements or leaping (Degner, 1921). This reaction is still not fully understood, including its use in defence against shell-invaders and the differences in its expression between snail species and against various threats (Townsend & McCarthy, 1980; Wilken & Appleton, 1991; Taylor, 2003). Notably, the precise parameters of the SDR in response to direct contact with the predator have been little studied. In the natural environment, snails are exposed to various predators including those that are not specialized in hunting for snails (Dillon, 2000) and numerous studies have dealt with general predator–prey interactions, assuming various defensive strategies (e.g. Eggers, 1978; Peckarsky, 1980; Pierce, 1988; Alexander & Covich, 1991; Boeing, Ramcharan & Riessen, 2006; Squires et al., 2008; Lehtonen, McCrary & Meyer, 2012). Such interactions always involve tradeoffs between predator and prey (Covich, 2010). Moreover, an SDR that evolved against particular predators can also be exhibited against species closely related to such predators, even when they are harmless (Langerhans & DeWitt, 2002). Such an unnecessary reaction was described for Physa fontinalis in response to stimuli from leeches and triclads; the reaction was observed whether the predators were molluscivorous or non-molluscivorous (Langerhans & DeWitt, 2002). On the other hand, certain species show more discrimination in their response strength, depending on the degree of potential threat from predators. Such differentiation is especially important when a snail is threatened simultaneously by specialized and generalist predators. Thus, the correct recognition of signals from predators allows snails to avoid the energetic cost of an unnecessary reaction. In their study of this phenomenon, Townsend & McCarthy (1980) used tissue only from the anterior (sucker) of the leech’s body, so their results do not provide a complete account. Exposure of snails to a direct threat from actively hunting leeches that differ in diet should provide information about the effectiveness of the SDR (Brönmark & Malmqvist, 1986). Differences between closely related snail species in predator recognition and avoidance should also be informative, yet remain poorly understood (Alexander & Covich, 1991). For instance, while it is known that P. fontinalis exhibits a very intensive and efficient defensive reaction at least against shell-invading leeches (Townsend & McCarthy, 1980; Brönmark & Malmqvist, 1986; Taylor, 2003), less is known about the response of Physella acuta, which shows a less intensive reaction to molluscivorous leeches than that of Aplexa marmorata (Wilken & Appleton, 1991). Therefore, the nature of the SDR in closely related species depending on the type of threat remains a matter of speculation. Perhaps even a less intensive reaction is sufficient to escape a predator. It is worth noting that P. acuta is the most widespread freshwater snail globally; furthermore, its range is expanding in Europe, where it has been considered an alien species (Turner & Montgomery, 2009; Covich, 2010; Strzelec, 2011). Some authors have attributed the success of the species to, among other attributes, the physid SDR (Naranjo-García & Appleton, 2009). The aim of this study was to compare an induced behavioural SDR and its effectiveness between two physid species, one native to Europe (Physa fontinalis) and the other alien (Physella acuta). We described and compared the reaction of these species against direct threat from a molluscivorous leech (Glossiphonia complanata) and an opportunistic species (Erpobdella octoculata). MATERIAL AND METHODS Subject Physella acuta and Physa fontinalis were exposed to two species of freshwater predatory leeches, Erpobdella octoculata and Glossiphonia complanata. Specimens of P. acuta were obtained from the longterm culture (started in 2006) at the Department of Hydrobiology, University of Warsaw. Specimens of P. fontinalis, E. octoculata and G. complanata, on the other hand, were collected in the field, from Lake Łaśmiady (Masurian Lakeland District, Poland; GPS: 53°56′04.2″N 22°17′09.3″E), the small rivers of Wilanówka, Potok Służewiecki (Warsaw, Poland; GPS: 52°09′00.4″N 21°07′04.8″E and 52°10′03.9″N 21°01′35.7″E, respectively) and Ciemięga (Sadurki, Poland; GPS: 51°17′59.9″N 22°19′15.2″E), as well as small ponds in the valley of the Potok Służewiecki river (Warsaw, Poland; GPS: 52°10′11.8″N 21°02′14.9″E). In order for the animals to acclimate, all species were kept separately in four aerated aquaria filled with filtered tap water (20 l each, 16:8 h light:dark, 22 °C) for several weeks prior to the experiment. All animals were fed ad libitum, snails with commercial fish food (Tropical® ‘Vitabin’) and leeches with P. acuta. In the case of E. octoculata, the snails were crushed before being administered. Leeches were not fed also with P. fontinalis, because insufficient individuals were available for both experimentation and feeding. Apparatus A stereoscopic Nikon C-BD230 microscope and NIS Elements D 4.00.01 software were used to measure the animals. The aquaria (dimensions 15 × 5 × 5 cm) were filled with tap water filtered through a carbon filter. Two video cameras (VIDEOLINE ViDi-500S) were mounted to record each of the aquaria from the front and top. Procedure One week before the experiment, 60 individuals of each snail species were randomly selected from the aquaria and placed separately in 100 ml plastic containers (summer photoperiod 16:8 h light:dark, 22 °C). Thirty specimens of E. octoculata and 18 specimens of G. complanata were used in each treatment (exposing prey to predator). The leeches were starved for 1 week prior to the experiment. All animals were weighed (ranges: P. acuta 0.021–0.081 g, P. fontinalis 0.017–0.130 g, G. complanata, 0.013–0.169 g, E. octoculata 0.030–0.384 g) before the experiment. Each trial comprised the following steps. First, 30 min before predator exposure, a single snail was placed in the aquarium to acclimate. After this time a leech was put into the aquarium and recording was started. After every exposure, the snail (if still alive) and the leech were taken out, the aquarium was cleaned and refilled with new water. Each recording was up to 2 h long, but was stopped if the snail was eaten earlier. This procedure was conducted separately for all selected individuals of both snail species (30 per treatment). Because of the low number of collected individuals of G. complanata, individuals of this leech had to be used in the experiment more than once (specimens being randomly selected each time). While investigating the behavioural response of the snails, we focused on the physid SDR (Degner, 1921). The SDR was identified as a vigorous shell-shaking reaction (first described by Degner, 1921, and in detail by Townsend & McCarthy, 1980), sometimes also followed by leaps, but also detachment from the substrate, considered a less intensive reaction (Townsend & McCarthy, 1980; Wilken & Appleton, 1991). In order to obtain a more detailed description of the SDR, 11 parameters were chosen and measured based on analysis of the recordings (Table 1). Table 1. Selected parameters used to describe the SDR of Physella acuta and Physa fontinalis.   Parameter  Scale  A  Occurrence of SDR  0, no reaction; 1, reaction  B  Occurrence of SDR in response to chemical cue  0, no reaction; 1, reaction (only if snail reacted without direct contact with leech)  C  Intensity of first occurrence of SDR  0, no reaction; 1, shell-shaking without leaps or only vertical movement in aquarium; 2, strong shell-shaking with leaps  D  Effectiveness of first occurrence of SDR  0, leech remained attached to snail after SDR; 1, SDR resulted in failure of leech attack  E  Snail sensitivity  0, no reaction or reaction to attachment by leech sucker to shell; 1, reaction to leech touch or chemical cue  F  Number of events of SDR during predator exposure  Number (defensive reactions treated as separate reactions if intervals between shell movements were longer than 5 s)  G  Number of events of SDR induced by direct contact with predator  Number  H  Average number of shell movements in a single SDR  Number  I  Number of events of direct contact with predator during exposure  Number  J  Number of SDR with leaps only during exposure  Number  K  Mortality upon first direct contact with predator  0, snail not consumed; 1, snail consumed    Parameter  Scale  A  Occurrence of SDR  0, no reaction; 1, reaction  B  Occurrence of SDR in response to chemical cue  0, no reaction; 1, reaction (only if snail reacted without direct contact with leech)  C  Intensity of first occurrence of SDR  0, no reaction; 1, shell-shaking without leaps or only vertical movement in aquarium; 2, strong shell-shaking with leaps  D  Effectiveness of first occurrence of SDR  0, leech remained attached to snail after SDR; 1, SDR resulted in failure of leech attack  E  Snail sensitivity  0, no reaction or reaction to attachment by leech sucker to shell; 1, reaction to leech touch or chemical cue  F  Number of events of SDR during predator exposure  Number (defensive reactions treated as separate reactions if intervals between shell movements were longer than 5 s)  G  Number of events of SDR induced by direct contact with predator  Number  H  Average number of shell movements in a single SDR  Number  I  Number of events of direct contact with predator during exposure  Number  J  Number of SDR with leaps only during exposure  Number  K  Mortality upon first direct contact with predator  0, snail not consumed; 1, snail consumed  The experiment was carried out in four treatments: P. acuta exposed to G. complanata, P. acuta exposed to E. octoculata, P. fontinalis exposed to G. complanata and P. fontinalis exposed to E. octoculata. Data and statistical analysis Treatments were analysed with regard to snail species, leech species and the interaction between them, using generalized linear models (GLMs), with binomial errors and a logit link function for parameters A, D and E, Poisson errors and a log link function for parameters B, C, J and K, and gamma errors and a log link function for parameters F, G, H and I (Table 1). The correlations of length and weight of snails and leeches with all parameters were investigated (Spearman correlation) in order to determine any possible influence of animal body mass and size on the success of both hunting leeches and snail defensive strategies. Statistical analysis was carried out using SPSS software (v. 23). RESULTS Significant differences between snail species were found for 10 of 11 analysed parameters and between leech species in seven of 11 analysed parameters. Occurrence of SDR Occurrence of SDR differed significantly between the snail species (Wald χ2 = 9.93, P = 0.002) and when exposed to different predators (Wald χ2 = 6.00, P = 0.014) (Fig. 1A). There was no significant interaction between snail species and leech species in occurrence of SDR (Wald χ2 = 0.01, P = 0.978). The reaction was more frequently noted in treatments with Physa fontinalis, but both snail species reacted more often when exposed to Glossiphonia complanata than Erpobdella octoculata. Figure 1. View largeDownload slide Estimated marginal means of measured parameters. Panels A–K and their scales correspond to parameters from Table 1. Solid and broken lines represent Physella acuta and Physa fontinalis, respectively. Figure 1. View largeDownload slide Estimated marginal means of measured parameters. Panels A–K and their scales correspond to parameters from Table 1. Solid and broken lines represent Physella acuta and Physa fontinalis, respectively. Occurrence of SDR in response to chemical cue Occurrence of SDR in response to chemical cue was observed in 12 cases of exposure P. fontinalis to G. complanata and in only one case of exposure of P. fontinalis to E. octoculata (Fig. 1B). No SDR response to chemical cue was observed in Physella acuta. Due to low numbers of SDR responses to chemical cue, full model results were unavailable. Intensity of first occurrence of SDR The intensity of the first occurrence of SDR was significantly higher for both snail species in treatments with G. complanata than in treatments with E. octoculata (Wald χ2 = 10.99, P = 0.001) (Fig. 1C). However, P. fontinalis reacted significantly more intensively than P. acuta when exposed to G. complanata as well as E. octoculata (Wald χ2 = 7.62, P = 0.006). There was no significant interaction between snail species and leech species in intensity of the first SDR (Wald χ2 = 0.181, P = 0.670). Effectiveness of first occurrence of SDR There were significant differences between the two snail species in the effectiveness of the first occurrence of their SDR (Wald χ2 = 14.55, P < 0.001), being higher in P. fontinalis (Fig. 1D). Both snail species had similar effectiveness of SDR when exposed to G. complanata and E. octoculata, and the values of this parameter did not differ significantly (Wald χ2 = 3.33, P = 0.068). There was no significant interaction between snail species and leech species in effectiveness of first SDR (Wald χ2 = 0.45, P = 0.504). Snail sensitivity Significant differences in sensitivity between both snail species were found between snail species exposed to G. complanata and E. octoculata (Wald χ2 = 19.54, P < 0.001) (Fig. 1E). In both treatments, P. fontinalis showed higher sensitivity than P. acuta, but the differences were not significant (Wald χ2 = 0.52, P = 0.471). There was no significant interaction between snail species and leech species in snail sensitivity (Wald χ2 = 1.45, P = 0.229). Number of events of SDR during predator exposure The highest number of SDR (average = 5) was observed for the treatment of P. fontinalis with G. complanata. In general, P. fontinalis reacted more frequently than P. acuta (Wald χ2 = 22.54, P < 0.001), and both species had different numbers of SDR when exposed to different predators (Wald χ2 = 6.53, P = 0.011) (Fig. 1F). For P. fontinalis, values of this parameter were higher for the G. complanata treatment than for the E. octoculata treatment. There was no significant interaction between snail species and leech species (Wald χ2 = 2.26, P = 0.133). Number of events of SDR induced by direct contact with predator For P. fontinalis, there were more events of SDR induced by direct contact with G. complanata and E. octoculata than for P. acuta (Wald χ2 = 15.00, P < 0.001) (Fig. 1G). Direct contact with G. complanata induced higher numbers of SDR in both snails species that with E. octoculata (Wald χ2 = 6.09, P = 0.014). There was no significant interaction between snail species and leech species in number of events of SDR induced by direct contact (Wald χ2 = 0.11, P = 0.738). Average number of shell movements in single SDR The highest values were observed in treatments involving P. fontinalis and G. complanata (average = 2.5 per SDR), being significantly higher in treatments involving P. acuta and G. complanata (average = 1.5) (Wald χ2 = 4.05, P = 0.044) (Fig. 1H). Different species of leeches also influenced this parameter, higher values being observed for both snails exposed to G. complanata (Wald χ2 = 4.74, P = 0.029). Due to lack of SDR during exposure of P. acuta to E. octoculata, results of interaction of snail species and leech species were unavailable. Number of events of direct contact with predator during exposure There were differences for both snail species in the number of events of direct contact with G. complanata and E. octoculata (Wald χ2 = 86.03, P < 0.001), but no differences were observed between the snail species (Wald χ2 = 0.02, P = 0.896) (Fig. 1I). There was no significant interaction between snail species and leech species in number of direct contacts (Wald χ2 = 0.09, P = 0.759). Number of SDR with leaps only during exposure There were no significant differences in this parameter between the snail species (Wald χ2 = 3.62, P = 0.057) or between different leech species (Wald χ2 = 0.07, P = 0.789) (Fig. 1J). There was no significant interaction between snail species and leech species (Wald χ2 = 0.22, P = 0.638). Mortality upon first direct contact with predator Results of the full model were unavailable for this analysis. First contact with G. complanata caused mortality of P. acuta in six cases and of P. fontinalis in only one case (Fig. 1K). There were no cases where snails died after first contact with E. octoculata. No significant correlations of length and weight of snails and leeches with all SDR parameters were found; the observed Spearman correlation coefficients were all low (rho < 0.2, P > 0.05). DISCUSSION In general, the measured parameters of SDR indicated that, regardless of snail species examined, the defensive reaction was far less expressed in treatments with the generalist predator Erpobdella octoculata. For both snail species, Physa fontinalis and Physella acuta, the SDR occurred more often (c. 50% increase) in the presence of the molluscivorous leech Glossiphonia complanata. Similarly, the average number of shell-shaking movements in a single SDR and the intensity of the first SDR were lower in presence of E. octoculata. Furthermore, often the only reaction observed during exposure to E. octoculata was detachment and floating up to the water surface, especially in the case of P. acuta. This kind of defensive reaction is less elaborate than shell shaking (in terms of response categories described by Wilken & Appleton, 1991), but still allows escape from a potentially dangerous area. Rapidly escaping the leech would seem to be a good defensive strategy, provided there is no simultaneous threat from other types of predators (e.g. fish, as described by Ahlgren & Brönmark, 2012). In the experimental treatments, the snails encountered G. complanata less frequently than E. octoculata. This might suggest that the snails tended to avoid the more serious threat posed by G. complanata. On the other hand, this particular leech species is considered a less active hunter, which could result in fewer encounters with prey. This is so because E. octoculata feeds mainly on immobile prey such as the larvae of Chironomidae (Young, Martin & Seaby, 1993), in contrast to G. complanata, which prefers snails (Young & Ironmonger, 1980). Similar results were reported by Townsend & McCarthy (1980), in which the strongest reaction of P. fontinalis was induced, among others, by G. complanata. Such discrimination between the presence and absence of threat is profitable for any prey, because induced late defensive reactions increase the probability of prey survival, while simultaneously reducing unnecessary defensive reactions when the threat is not present (Turner, Fetterolf & Bernot, 1999). DeWitt (1998) hypothesized the putative cost of induced defensive strategies such as morphological and life history changes in Physa heterostropha (a synonym of P. acuta), although he was unable to confirm these proposed costs experimentally. In contrast, induced behavioural changes (e.g. shell-shaking behaviour) would seem to have a low potential energetic cost to snails, especially when taking into account the energetic costs of early and late responses. A late-response SDR enables snails to react only when direct threat is presented, avoiding unnecessary investment in morphological changes or less time spent on foraging (e.g. when snails crawl out of water to avoid predators) (DeWitt, 1998; Rigby & Jokela, 2000). Shell-shaking behaviour saves energy that can be allocated to growth or reproduction instead. Physa fontinalis showed a stronger behavioural reaction than P. acuta as an effect of direct exposure to the two leech species. The effectiveness of the SDR of P. acuta was lower than that of P. fontinalis during the first attack of G. complanata. Despite using shell-shaking movements, 7% of attacked P. acuta died, while another 10% were killed without having exhibited these movements; ultimately, after a 2 h exposure, 67% of P. acuta individuals had been killed against only 4% (1 individual) of P. fontinalis. The initial defensive reaction seems to play a crucial role in escaping from the danger zone; preventing attachment of the leech to the snail’s shell, followed by a rapid escape from the place of attack can save the prey. The more vigorous and numerous shell-shaking movements and detachment of P. fontinalis allow it to escape its predator, while the reaction of P. acuta involved less shell-shaking movements without detachment from the substrate and mortality was consequently greater. In the latter species, should the leech fail to attach itself onto the shell of the hunted snail, it has no trouble repeating the attack. It is not only the strength of the SDR itself (as expressed by the number of shell-shaking movements) that limits the predator’s hunting success, but also the ability to repeat the reaction with a certain, effective frequency. Physa fontinalis exhibited defensive reactions more often over a period of 2 h, contributing to its low mortality. The overall stronger reaction and especially the sensitivity of P. fontinalis may be due to the finger-like mantle digitations that cover the outside of the shell. This touch-sensitive tissue is larger than in other physids, such as P. acuta (Piechocki, 1979). Thus, the reduced sensitivity of P. acuta may lie with the fact that a smaller area is covered by the mantle extensions, so that the leech sometimes manages to avoid stimulating the soft tissue on first encounter. In their laboratory experiment, Wilken & Appleton (1991) exposed two physids (P. acuta and Aplexa marmorata) to a molluscivorous leech species. Similarly to the observations reported in this paper, they found that A. marmorata, a species characterized by larger mantle digitations, exhibited a more complex and effective response to predators after direct contact than P. acuta, making the latter more vulnerable to predators. A complementary or alternative explanation could be connected with the quality or quantity of the ‘physid muscles’—present only in this particular family and considered to be responsible for the shell-shaking reaction (Naranjo-García & Appleton, 2009). Unfortunately, there are as yet insufficient data comparing these structures among physid species, so their contribution remains hypothetical. Physella acuta is also characterized by a low metabolic rate, allowing snails to remain under water for a longer period (Dillon, 2000), which could possibly also contribute to a weaker reaction strength. Another consideration is that in our experiment the leeches were fed only with P. acuta before experiment, so that they were more responsive towards P. acuta than P. fontinalis. However, all the leeches were collected from natural environments, where P. fontinalis and other possible prey species are present, and because the experiment was conducted shortly after collection, we consider any such bias towards P. acuta to be unlikely. Furthermore, every individual was starved for a week prior to the experiment, which should further decrease possible bias. A second possible reason for the significant differences in defensive reactions between the examined physids might be the origin of the animals used in the experiment. Individuals of P. fontinalis were collected in natural habitats, while those of P. acuta were supplied from a longterm culture (established in 2006) in which at least a few dozens of generations had experienced no contact with leeches. This could have led to a gradual weakening of defensive reactions and the ability to detect predators (e.g. Bernot & Whittinghill, 2003; Turner, Turner & Lappi, 2006). Turner et al. (2006) showed that the effects of the experience of P. acuta of fish predators were significant but rather small, suggesting that the behavioural reaction against fish is innate. However, the laboratory-reared generation used by these authors was the first generation from wild-caught specimens, whereas the snails in our experiment were reared without leech predators for many generations. Salice & Plautz (2011) also found some differences between wild-caught and laboratory-reared (for 3–4 generations) individuals of Physa pomilia in avoidance behaviour in response to crayfish; offspring of newly caught snails decreased their predator avoidance behaviour over time, while the opposite was observed for laboratory-reared ones. However, over the 40 days of the experiment, offspring of newly caught and laboratory snails displayed similar predator-avoidance behaviour on average. Since we compared two species with different population histories, we cannot comment on the possible significance of past experience of predators within prey species and this should be the subject of future research. Physella acuta is a generalist species with a broad geographical range, which thereby encounters different types of predators. The adaptive evolutionary response to predators is probably less specialized when facing many levels of risk (McCarthy & Fisher, 2000). Investment in large mantle extensions or developing more rapid SDR may compromise the allocation of resources to other defensive mechanisms. McCarthy & Fisher (2000) suggested that surfacing is one of the least costly defensive behaviours and commonly found when only the chemical trait of a predator is present, without alarm cues from injured snails. Moreover, the probability of encounter with an actively hunting predator is higher than with opportunistic ones. Thus, allocation of resources to different defensive strategies, such as altered shell morphology or life history traits, might be preferable when other kinds of predators are detected (Young & Procter, 1986). Even though laboratory breeding of P. acuta may have affected the results of this study, the simultaneous threats from other predators (such as fish or crayfish) common in natural environment may sometimes cause changes in behaviour or morphology of the shell in contrary directions. In such situations prey might be predicted to respond to the most dangerous predator and the overall adaptational change may be a trade-off (Lakowitz, Brönmark & Nyström, 2008; Bourdeau, 2009). Despite the higher mortality of P. acuta than P. fontinalis found in our study, the former species has the faster growth rate and thus might be more competitive than P. fontinalis, which appears to be crucial in the multipredatory environment (Früh, Haase & Stoll, 2017). Physa fontinalis seems to be better adapted to resist direct attacks from molluscivorous leeches, which may be the result of a more efficient discrimination between species that pose a threat and those that do not. Generally, the values of the response parameters in the two predator treatments differed more strongly in case of P. fontinalis than P. acuta. Physella acuta did not always react to G. complanata upon first encounter and the number of encounters needed to trigger the first defensive reaction was high, when exposed to either leech species; it was less discriminating in its response to the two leech species and slower to react at all. The reaction of Lymnaea stagnalis was found to be faster when the snail was pre-exposed to the chemical cue of a predator (Dalesman et al., 2006). In our experiment, P. fontinalis reacted to G. complanata upon first encounter or even when it had only detected leech odour. The opposite was observed on treatment with E. octoculata, when the reaction occurred much later, suggesting that the reaction was induced only after the snail had been disturbed for a longer period of time. Furthermore, P. fontinalis reacted not only to the touch or attack of the molluscivorous leech, but also to its chemical signal (kairomone) if the leech was in close proximity where it presented a high, direct threat. In other words, as found by Bourdeau (2009), the defensive reaction was strongest and most appropriate to the most dangerous predator present at time. The efficient defensive reaction of P. fontinalis allows the snail to react only if a leech is in close proximity or attacking. Thus, no escape strategy (e.g. crawling to the surface) is required when a chemical cue is detected (Brönmark & Malmqvist, 1986). In our experiment, the number of encounters with G. complanata was the same for both snail species, regardless of the efficacy of their defenses. Therefore, it can be assumed that P. acuta does not use escape strategies as often as P. fontinalis to avoid attack from leeches. Physella acuta is among the most ubiquitous macroinvertebrates in the world, inhabiting a wide spectrum of fresh waters (Dillon et al., 2002; Turner & Montgomery, 2009; Covich, 2010). Naranjo-García & Appleton (2009) claim that the physid SDR has been key to the spread of P. acuta. On the other hand, this theory is less convincing when considering the fact that the snail is very susceptible to predation by shell-invading invertebrates such as leeches, triclads and insects (Turner & Chislock, 2007; Lombardo et al., 2012). 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Journal of Molluscan StudiesOxford University Press

Published: Feb 1, 2018

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