Responses to chemical cues indicative of predation risk by the freshwater shrimp Palaemon argentinus (Nobili, 1901) (Caridea: Palaemonidae)

Responses to chemical cues indicative of predation risk by the freshwater shrimp Palaemon... Abstract Many prey species detect predators through chemoreception, particularly in low-visibility aquatic environments. Moreover, injury-released chemical cues from conspecifics are often perceived as a reliable indicator of predation threat. We examined whether males of the freshwater caridean shrimp Palaemon argentinus (Nobili, 1901) react to different types of infochemicals associated with predation threat. Shrimp were exposed to chemical stimuli from starved individuals of a predatory fish (Australoheros facetus (Jenyns, 1842)) and from crushed conspecific shrimp. Our experiment showed that P. argentinus reacts to waterborne substances associated with predation threat, indicating that chemical cues mediate behavioural antipredator responses. Shrimp adopted an appropriate antipredator behaviour (reduced swimming activity) in response to chemical stimuli from A. facetus, and from crushed conspecifics, relative to a distilled-water control. The chemical stimuli from crushed conspecifics elicited the strongest reduction in swimming activity. Reduced movement, a common response in prey animals to the presence of predators, was not entirely consistent because shrimp increased their walking time in response to the chemical stimuli that were investigated. The ability to alter behaviour based on vision-independent perception of ambient risk would be highly useful for macroinvertebrate prey species such as P. argentinus living in eutrophic shallow lakes where visibility is often reduced. Our results demonstrated chemosensory recognition of predation risk highlighting the important role of chemical cues in the behavioural ecology of this shrimp, especially with regards to predator-prey interactions. INTRODUCTION There has been an increasing interest in understanding the importance of non-visual signals for communication and information in aquatic systems. Many studies have shown that aquatic animals use chemical cues to locate food, detect the presence of predators, find a partner or host, and for precise migration and navigation (Dodson et al., 1994; Brönmark & Hansson, 2012). Chemoreception depends primarily on the senses of taste and smell, and is probably one of the most common type of perception used by animals to exploit valuable resources and/or detect danger. Several crustacean groups have highly developed chemosensory systems (Hay, 2011), with chemical cues mediating numerous behavioural processes including foraging, reproduction, and antipredator responses (Dodson et al., 1994; Bauer 2011; Hay 2011; Hazlett, 2011; Brooker & Dixson, 2016, 2017). Among decapods, crabs, lobsters, and crayfishes have been shown to be capable of recognising and reacting to chemical substances indicative of predation risk (Dodson et al., 1994; Hazlett, 2011), and such responses have also been recently reported in some caridean shrimps (Huang et al., 2011; Brooker & Dixson 2016, 2017). In many aquatic animals, chemical cues from predators and cues from injured conspecifics have the potential to provide important information about the current risk of predation for prey (Tollrian & Harvell, 1999; Ferrari et al., 2010; Paterson et al., 2013; Wisenden, 2015). Chemical substances released by predators, defined as kairomones, can be important indicators of risk and elicit antipredatory responses in several aquatic taxa (Tollrian & Harvell, 1999; Wisenden, 2015). Moreover, when attacked by predators, diverse animals actively or passively release molecules that trigger alarm and related antipredatory behaviour by nearby conspecifics (Shabani et al., 2008; Derby & Zimmer, 2012). The actively released molecules are pheromones, whereas the passively released molecules are alarm cues (Shabani et al., 2008). It is believed that alarm cues which leak from injured or freshly killed preys warn conspecifics of an immediate danger (e.g., active predators) and elicit similar responses as predator odour when received by nearby conspecifics (Chivers & Smith, 1998; Shabani et al., 2008). After detecting these chemical cues, preys usually reduce their activity and/or their shelter-seeking. The reduction of overall activity and/or shelter-seeking may result in reduced foraging, mating activity or less investment in offspring (Holomuzki & Short, 1988; Lima & Dill, 1990). Therefore, prey species should be able to distinguish chemical cues as indicators of predation threats to ensure escape behaviour is not unnecessarily initiated, thus representing a cost in terms of decreased opportunities for foraging, mating activity, and other fitness-related behaviours (Åbjörnsson et al., 1997). The freshwater caridean shrimp Palaemon argentinus (Nobili, 1901) (= Palaemonetes argentinus, see DeGrave & Ashelby, 2013) inhabits shallow lakes and streams in southeastern South America, and breeds in spring and summer (from October to March). This shrimp is found sympatrically with predatory fishes such as cichlids, characids, and cyprinodonts in shallow lakes in the Pampa plains of Argentina (González Sagrario et al., 2009). Littoral fishes, such as the cichlid Australoheros facetus, are omnivores that feed on aquatic plants, zooplankton, smaller fishes, and macroinvertebrates such as P. argentinus (Yafé et al., 2002). Some shallow lakes in the Pampas are dominated by submersed macrophytes, have a relatively low phytoplankton biomass, and the water is clear, but in general, most water bodies exhibit high phytoplankton biomass and scarce macrophyte development, and are typically turbid (Allende et al., 2009). A third type of lake that can be encountered in this region corresponds to shallow lakes in which turbidity is mostly due to inorganic material, and in which both phytoplankton and macrophyte development is low (Allende et al., 2009). Nowadays, there is a gradual shift from clear to turbid-water conditions, which along with decreases in macrophyte abundance, has been shown to affect trophic interactions (Quirós, 1998; Quirós et al., 2002; Coops et al., 2003; González Sagrario et al., 2009; Sosnovsky et al., 2010). The prevailing low visibility during the turbid water condition suggests that macroinvertebrate prey species like P. argentinus probably rely almost completely on chemical senses to detect predators. Although P. argentinus is likely to play a key role in trophic interactions of these shallow lakes, chemosensory recognition of predation risk by adults of this shrimp has not yet been reported. We performed a short-term laboratory experiment to examine whether adults of P. argentinus can detect and react to chemical cues indicative of predation threat. We examined the ability of male shrimp to modify locomotor activities (swimming and walking) in response to chemical cues from starved individuals of a predatory fish (kairomones) and from crushed conspecific shrimp (alarm cues). We predicted that adults of P. argentinus will decrease their activity level when exposed to alarm cues, a reliable indicator of predation threat. Reduced movement to the presence of predators is a common response in prey taxa, including shrimps (e.g., Heck & Thoman, 1981). We exposed shrimp to chemical stimuli from the known predator (A. facetus) to verify that the response of shrimp to stimuli from crushed conspecifics represents antipredator behaviour. MATERIALS AND METHODS Sampling In March 2014, January and December 2015, mature individuals of P. argentinus and A. facetus were collected from La Brava Lake (37°52′52″S, 57°58′38″W), Buenos Aires province, Argentina. Both species co-occur in shallow lakes in the Pamapas, so the tested population of shrimp had previous experience with the experimental predator (Ituarte et al., 2014). Specimens were obtained from the littoral zone using a hand net (45 cm width, 30 cm deep; 1 mm mesh). In the laboratory, each group of animals was held in separate 50 l aerated aquaria (22 °C, 10:14 h light dark cycle) filled with dechlorinated tap water for at least five days before being included in experiments. During acclimation, shrimp and fish were fed daily on TetraMin Pro® (lipids 12%; proteins 46%) (Tetra GmbH, Melle, Germany). In order to avoid the possibility of sex differences in behavioural responses to predation risk during the breeding season, only males of P. argentinus were used for experimentation (Gancedo, 2015). As in many caridean shrimps, P. argentinus shows a ‘pure searching’ mating tactic, in which males are continually on the prowl for a receptive female (Bauer, 2004). In this type of mating, often referred to as promiscuous, males do not defend territories, are highly mobile, smaller than females, cryptic, and less obvious to visually oriented predators (Bauer, 2004). Male shrimp 4–6 mm carapace length were used in the experiments. Individuals were checked for the presence of metacercarial cysts of microphallid parasites (Trematoda, Microphallidae; Merlo et al., 2016), and only non-parasitized shrimp were used. Experimental procedure We tested the responses of male shrimp to chemical cues from three starved individuals of the fish A. facetus (collections made in March 2014, and January and December 2015; fork length = 14.1; 13.2 and 10.5 cm, respectively), and from crushed conspecific shrimp. Different male shrimp were used for each trial. Chemical stimuli from fish individuals were used as predator odour as suggested by Gelowitz et al. (1993), Wisenden et al. (1997), and Wudkevich et al. (1997) following the procedure described by Wisenden et al. (1997). During acclimation, approximately 12 h after the final feeding, each fish individual was placed in an aquarium (volume 3.5 l; 22 °C, 14:10 h light dark cycle) filled with dechlorinated tap water and was held there without food for three days. Specimens were then removed and the stimulus water was immediately used. The collection aquaria were well-aerated but contained no filtration system to avoid filtering active compounds. Chemical cues from conspecifics were prepared by crushing one adult shrimp using a mortar and pestle in 10 ml of distilled water; the stimulus preparation was immediately used. We tested the responses of male shrimp in an acrylic aquarium (10 × 10 × 10 cm) filled with 800 ml dechlorinated tap water. A video camera was installed on the side of the experimental aquaria to record shrimp behaviour. Each shrimp was left to acclimatise for 30 min before the beginning of each trial. Different male shrimp were used for each trial (N = 34 per trial). Shrimp behaviour (pre-stimulus activity) was recorded for 5 min before 3 ml of treatment water (Wisenden et al., 1997) were carefully introduced with a syringe into a corner of the aquarium. Twenty seconds after injection, behaviour was recorded for another 5 min (post-stimulus activity). Aquaria were thoroughly rinsed and cleaned between test trials to remove any trace of chemical stimuli from previous trials. All the recordings were randomly assigned to a video code and were blindly analysed by the same experimenter (BJG). From the recordings, we obtained the time in which each shrimp swam and walked in each of the two 5 min periods before and after adding a chemical stimulus to the water. Statistical analyses Shrimp response to a particular stimulus was defined as the difference between post- and pre-stimulus activity. All values were expressed as arithmetic mean ± standard error (SE). The effects of fish odour on changes in the swimming and walking time of shrimp were tested with mixed-model nested ANOVA with fish nested within control using InfoStat 2017 (Di Rienzo et al., 2017). Water treatment condition (distilled water and predator odour) was a fixed factor and fish identity was a random factor in the model. We compared behavioural changes in 34 male shrimp (8, 12, and 14 shrimp for each respective fish individual). The effects of the three treatment conditions (distilled water, predator odour, and crushed conspecifics) on the changes in time performing each activity were analysed by one-way ANOVA using SigmaStat v 4.0. Shrimp reactions to all three fish individuals tested were pooled as the predator odour treatment. We tested 102 male shrimp, 34 in each of the three treatment conditions. All ANOVAs were performed after checks for normal distribution and equality of variance (Shapiro-Wilk and Brown-Forsythe tests, respectively). When ANOVA indicated significant differences between treatments, they were tested with a post hoc Tukey test. RESULTS Basal behaviours of P. argentinus during the pre-stimulus period (before adding any water treatment) involved moving and stationary activities. Shrimp spent most of their time either swimming in the water column, motionless, or walking on the bottom of the aquarium. We focused our data analysis on the most frequently observed activities involving movement: swimming and walking. The two types of swim behaviour included slow forward motion by swimming through the water column with pereopods extended downward, and swimming up-side-down just below the surface of the water. To facilitate data recording, both types of swimming behaviour were grouped into a single activity category (“swimming”). Chemical cues from different fish individuals did not affect changes in swimming time of male shrimp relative to distilled water control (nested mixed-model ANOVA: F(1; 62) = 0.62; P = 0.48), whereas their walking time was affected (F(1; 62) = 25.44; P = 0.007). Shrimp increased their walking time in response to fish stimuli (P < 0.05). Data for all three fish were pooled as predator odour although variance for fish individuals differed from zero (swimming time: F(4; 62) = 34.4; P < 0.0001 and walking time: F(4; 62) = 2.52; P = 0.049). Changes in swimming time of male shrimp was affected by water treatment conditions (ANOVA: F(2; 101) = 46; P < 0.001). Male shrimp reduced their swimming time in response to chemical stimuli from predator odour (pooled data) and crushed conspecifics relative to distilled water, and the strongest reduction occurred in response to chemical stimuli from crushed conspecifics (Fig. 1A). Moreover, the amount of time that shrimp spent walking increased in response to both predator odour (pooled data) and conspecific stimuli relative to distilled water (ANOVA: F(2; 101) = 24; P < 0.001). Such increase was stronger in response to the predator odour treatment (Fig. 1B). Figure 1. View largeDownload slide Mean (± SE) change in time devoted to swimming (A), and walking (B) by males of Palaemon argentinus following exposure to a control of distilled water (DW), predator odour (PO, chemical stimuli from starved individuals of the predatory fish Australoheros facetus, or crushed conspecific shrimp (CC). For each behaviour, bars with different letters indicate significant differences (post-hoc Tukey test, α = 0.05); N = 34 in each treatment. Figure 1. View largeDownload slide Mean (± SE) change in time devoted to swimming (A), and walking (B) by males of Palaemon argentinus following exposure to a control of distilled water (DW), predator odour (PO, chemical stimuli from starved individuals of the predatory fish Australoheros facetus, or crushed conspecific shrimp (CC). For each behaviour, bars with different letters indicate significant differences (post-hoc Tukey test, α = 0.05); N = 34 in each treatment. DISCUSSION The ability to recognise and respond to a potential predator is an essential component of antipredator behaviour because failure to do so increases the probability of the predator capturing or injuring the prey (Lima & Dill, 1990). The importance of chemical cues in aquatic predator-prey systems is well known and chemical cues recognition has already been demonstrated in some caridean shrimps (e.g., Dunlop-Hayden & Rehage, 2011; Huang et al., 2011; Ocasio-Torres et al., 2014; Brooker & Dixson, 2016, 2017). Shrimps seem to have evolved a chemosensory ability that allows them to distinguish different organisms in their environment (Brooker & Dixson, 2016). Our experiment showed that the P. argentinus reacts to waterborne substances indicative of predation risk suggesting that chemical cues mediate behavioural antipredator responses in this species as well. Reduced swimming behaviour has been reported in palaemonids shrimps upon non-chemical detection of predatory fish (Heck & Thoman, 1981; Carson & Merchant, 2005; Kunz et al., 2006). By decreasing swimming activity, benthic prey such as P. argentinus can possibly be less vulnerable to predation by reducing the rate of encounter with potential predators (e.g., Wisenden et al., 1997; Chivers & Smith, 1998; Ferrari et al., 2010). Non-significant changes in the swimming behaviour of P. argentinus along with the high variability in shrimp behaviour when exposed to waterborne substances from each fish individual may be due to the small sample size for each fish. When data for all three fish were pooled, however, there was a clear reduction in the swimming time of shrimp. In turbid water and/or physically complex environments, preys able to detect predator odours will certainly be better suited to deal with predators than preys which solely rely on visual detection (Kats & Dill, 1998). Since many fishes feeding in light-limited environments locate their prey following hydrodynamic stimuli in the wake (e.g., Pohlmann et al., 2004; Schwalbe et al., 2012), a decrease in swimming activity will presumably be a good antipredatory response. Benthic invertebrate preys generally decrease their activities in response to predatory vertebrates (review by Wooster & Sih, 1995); however, some reports have shown an opposite response. Williams (1986) found in laboratory trials that larvae of the stonefly Paragnetina media (Walker, 1852) increase their movement when exposed to trout (Oncorhynchus mykiis (Walbaum, 1792)) odour. Moreover, response to predator odour is known to depend upon the presence or absence of a refuge (Sih & Kats, 1991). We found that male shrimp increased their walking time in response to predator odour and the crushed-conspecific treatment, suggesting that such reaction depends on the context of habitat (e.g., seeking for refuge). The increased walking time and the reduced swimming behaviour could provide protection against fish predators, but further experimental studies are needed to understand whether these observed reactions in males of P. argentinus are adaptive. The chemical characterization of predator-specific cues is still scarce (von Elert, 2012; Weiss et al., 2012), although faeces are often the source of predator odour (Kats & Dill, 1998). The fish in our experiments were starved for three days, indicating that shrimp reactions could be triggered by other metabolites of A. facetus rather than by faeces and/or by predator-associated bacteria that release specific metabolites (probably present in the mucus cover of fish; see Ringelberg & Van Gool, 1998). Almost every invertebrate species tested has shown an increase in antipredator behaviour when odours of crushed conspecifics were presented (e.g., Wisenden & Millard, 2001; Hazlett, 2011; Schaum et al., 2013), but the chemical identity of alarm cues has been determined in only a few species of sea anemones (Howe & Sheikh (1975) and ostariophysan fishes (e.g., Smith, 1992). There is no indication of specialized crustacean cells that could produce alarm cues (such as the epidermal club cells in ostariophysan fishes), but peptides found in the hemolymph have been suggested as alarm cues (Acquistapace et al., 2005; Shabani et al., 2008; Hazlett, 2011). Since multiple cues can act in an additive or synergistic fashion to provide additional information for risk assessment by prey (e.g., Schoeppner & Relyea, 2009), the observed reduction in swimming time of male P. argentinus could translate into a stronger learned response to the predator when the predator odour is paired with alarm cues. Future studies should test this hypothesis. The ability in small benthic species to identify other animals within proximity without visual cues would be highly useful (Brooker & Dixson, 2016). Since most of the shallow lakes in the Pampas are permanently limited by light (Quirós et al., 2002, Torremorell et al., 2007; Allende et al., 2009), macroinvertebrate prey such as P. argentinus, probably rely almost completely on chemical senses to detect the risk of predation. The fact that P. argentinus can distinguish between chemical exuded by a predatory fish and from crushed conspecifics highlights the important role of chemical cues in the behavioural ecology of caridean shrimps, especially with regards to predator-prey interactions (see Brooker & Dixson, 2016, 2017). ACKNOWLEDGEMENTS This article is based on work done by BJG in partial fulfilment of the bachelor’s degree at Universidad Nacional de Mar del Plata, Argentina, with the support of a fellowship from the Comisión de Investigaciones Científicas (CIC). We are also grateful to J. Nuñez and M.G. Vázquez for assistance with experiments, to E. Spivak, two anonymous reviewers for providing suggestions to improve previous drafts of the manuscript, and A. Cosulich for revising the English language. This research was supported by a grant from Consejo Nacional de Investigaciones Científicas y Técnicas, Argentina (PIP 112-201101-00830). REFERENCES Åbjörnsson, K., Wagner, B.M.A., Axelsson, A., Bjerselius, R. & Olsén, K.H. 1997. Responses of Acilius sulcatus (Coleoptera: Dytiscidae) to chemical cues from perch (Perca fluviatilis). Oecologia , 111: 166– 171. Google Scholar CrossRef Search ADS PubMed  Acquistapace, P., Calamai, L., Hazlett, B.A. & Gherardi, F. 2005. Source of alarm substances in crayfish and their preliminary chemical characterization. Canadian Journal of Zoology , 83: 1624– 1630. Google Scholar CrossRef Search ADS   Allende, L., Tell, G., Zagarese, H., Torremorell, A., Pérez, G., Bustingorry, J., Esaray, R. & Izaguirre, I. 2009. Phytoplankton and primary production in clear-vegetated, inorganic-turbid, and algal-turbid shallow lakes from the pampa plain (Argentina). Hydrobiologia , 624: 45– 60. Google Scholar CrossRef Search ADS   Bauer, R. 2004. Remarkable shrimps: adaptations and natural history of the carideans , Edn. 1. University of Oklahoma Press, Norman, OK, USA. Bauer, R. 2011. Chemical communication in decapod shrimps: the influence of mating and social systems on the relative importance of olfactory and contact pheromones. In: Chemical communication in crustaceans  ( T. Breithaupt & M. Thiel, eds.), pp. 277– 296. Springer, New York, USA. Google Scholar CrossRef Search ADS   Brönmark, C. & Hansson, L.-A. 2012. Chemical ecology in aquatic systems . Oxford, University Press, New York, USA. Google Scholar CrossRef Search ADS   Brooker, R.M. & Dixson, D.L. 2016. Comparable cross-taxa risk perception via chemical cues in marine and freshwater crustaceans. Marine and Freshwater Research , 68: 788– 792. Google Scholar CrossRef Search ADS   Brooker, R.M. & Dixson, D.L. 2017. Intertidal crustaceans use seaweed-derived chemical cues to mitigate predation risk. Behavioral Ecology and Sociobiology , 71: 47– 54. Google Scholar CrossRef Search ADS   Carson, M.L. & Merchant, H. 2005. A laboratory study of the behavior of two species of grass shrimp (Palaemonetes pugio Holthuis and Palaemonetes vulgaris Holthuis) and the killifish (Fundulus heteroclitus Linneaus). Journal of Experimental Marine Biology and Ecology , 314: 187– 201. Google Scholar CrossRef Search ADS   Chivers, D.P. & Smith, R.J.F. 1998. Chemical alarm signalling in aquatic predator-prey systems: a review and prospectus. Ecoscience , 5: 338– 352. Google Scholar CrossRef Search ADS   Coops, H., Beklioglu, M. & Crisman, T.L. 2003. The role of water-level fluctuations in shallow lake ecosystems – workshop conclusions. Hydrobiologia , 506: 23– 27. Google Scholar CrossRef Search ADS   DeGrave, S. & Ashelby, C.W. 2013. A re-appraisal of the systematic status of selected genera in Palaemoninae (Crustacea: Decapoda: Palaemonidae). Zootaxa , 3734: 331– 334. Google Scholar CrossRef Search ADS PubMed  Derby, C.D. & Zimmer, R.K. 2012. Neuroecology of predator-prey interactions. In: Chemical ecology in aquatic systems  ( C. Brönmark & L.-A. Hansson, eds.), pp. 158– 171. Oxford University Press, Oxford, UK. Di Rienzo, J.A., Casanoves, F., Balzarini, M.G., Gonzalez, L., Tablada, M. & Robledo, C.W. 2017. InfoStat versión . Grupo InfoStat, FCA, Universidad Nacional de Córdoba, Córdoba, Argentina. Dodson, S.I., Crowl, T.A., Peckarsky, B.L., Kats, L.B., Covich, A.P. & Culp, J.M. 1994. Non-visual communication in freshwater benthos: an overview. Journal of the North American Benthological Society , 13: 268– 282. Google Scholar CrossRef Search ADS   Dunlop-Hayden, K.L. & Rehage, J.S. 2011. Antipredator behavior and cue recognition by multiple Everglades prey to a novel cichlid predator. Behavior , 148: 795– 823. Google Scholar CrossRef Search ADS   Ferrari, M.C.O., Wisenden, B.D. & Chivers, D.P. 2010. Chemical ecology of predator-prey interactions in aquatic ecosystems: a review and prospectus. Canadian Journal of Zoology , 88: 698– 724. Google Scholar CrossRef Search ADS   Gancedo, B.J. 2015. Respuestas coportamentales inducidas por el riesgo de depredación en adultos del camarón Palaemontes argentinus . Undergraduate thesis, Universidad Nacional de Mar del Plata, Mar del Plata, Argentina. Gelowitz, C.M., Mathis, A. & Smith, R.J.F. 1993. Chemosensory recognition of northern pike (Esox lucius) by brook stickleback (Culaea inconstans): population differences and he influence predator diet. Behavior , 127: 105– 118. Google Scholar CrossRef Search ADS   González Sagrario, M.A., Balseiro, E., Ituarte, R.B. & Spivak, E.D. 2009. Macrophytes as refuge or risky area for zooplankton: a balance set by littoral predacious macroinvertebrates. Freshwater Biology , 54: 1042– 1053. Google Scholar CrossRef Search ADS   Hay, M.E. 2011. Crustaceans as powerful models in aquatic chemical ecology. In: Chemical communication in crustaceans  ( T. Breithaupt & M. Thiel, eds.), pp. 41– 63. Springer, New York, USA. Google Scholar CrossRef Search ADS   Hazlett, B.A. 2011. Chemical cues and reducing the risk of predation. In: Chemical communication in crustaceans  ( T. Breithaupt & M. Thiel, eds.), pp. 355– 370. Springer, New York, USA. Google Scholar CrossRef Search ADS   Heck, K.L., Jr. & Thoman, T.A. 1981. Experiments on predator-prey interactions in vegetated aquatic habitats. Journal of Experimental Marine Biology and Ecology , 53: 125– 134. Google Scholar CrossRef Search ADS   Holomuzki, J.R. & Short, T.M. 1988. Habitat use and fish avoidance behaviors by the stream-dwelling isopod Lirceus fontinalis. Oikos , 52: 79– 86. Google Scholar CrossRef Search ADS   Howe, N.R. & Sheikh, Y.M. 1975. Anthopleurine: a sea anemone alarm pheromone. Science , 189: 386– 388. Google Scholar CrossRef Search ADS PubMed  Huang, J., Wu, Z., Cai, F. & Liu, H. 2011. Responses of freshwater shrimp on alarm cues from injured-conspecific. In: International conference on remote sensing, environment and transportation engineering (RSETE), pp. 7078– 7082. Nanjing, China. Ituarte, R.B., Vázquez, M.G., González Sagrario, M.A. & Spivak, E.D. 2014. Carryover effects of predation risk on postembryonic life-history stages in a freshwater shrimp. Zoology , 117: 139– 145. Google Scholar CrossRef Search ADS PubMed  Kats, L.B. & Dill, L.M. 1998. The scent of death: chemosensory assessment of predation risk by prey animals. Ecoscience , 5: 361– 394. Google Scholar CrossRef Search ADS   Kunz, A.K., Ford, M. & Pung, O.J. 2006. Behavior of the grass shrimp Palaemonetes pugio and its response to the presence of the predatory fish Fundulus heteroclitus. American Naturalist , 155: 286– 294. Google Scholar CrossRef Search ADS   Lima, S.L. & Dill, L.M. 1990. Behavioral decisions made under the risk of predation: a review and prospectus. Canadian Journal of Zoology , 68: 619– 640. Google Scholar CrossRef Search ADS   Merlo, J.M., Parietti, M. & Ituarte, R.B. 2016. Influence of Microphallus szidatti Martorelli, 1986 (Trematoda) on the fecundity of the second intermediate host, Palaemonetes argentines Nobili, 1901 (Decapoda: Natantia). Journal of Crustacean Biology , 36: 94– 98. Google Scholar CrossRef Search ADS   Nobili, G. 1901. Decapodi raccolti dal Dr. Filipo Silvestri nell’America meridionale. Bolletino dei Musei di Zoologia ed Anatomia comparata della R. Università di Torino , 16: 1– 16. Ocasio-Torres, M., Crowl, T. & Sabat, A. 2014. Long rostrum in an amphidromous shrimp induced by chemical signals from a predatory fish. Freshwater Science , 33: 451– 458. Google Scholar CrossRef Search ADS   Paterson, R.A., Pritchard, D.W., Dick, J.T.A., Alexander, M.E., Hatcher, M.J. & Dunn, A.M. 2013. Predator cue studies reveal strong trait-mediated effects in communities despite variation in experimental designs. Animal Behavior , 86: 1301– 1313. Google Scholar CrossRef Search ADS   Pohlmann, K., Atema, J. & Breithaupt, T. 2004. The importance of the lateral line in nocturnal predation of piscivorous catfish. Journal of Experimental Biology , 207: 2971– 2978. Google Scholar CrossRef Search ADS PubMed  Quirós, R. 1998. Fish effects on trophic relationships in the pelagic zone of lakes. Hydrobiologia , 361: 101– 111. Google Scholar CrossRef Search ADS   Quirós, R., Rennella, A.M., Boveri, M.B., Rosso, J.J. & Sosnovsky, A. 2002. Factores que afectan la estructura y el funcionamiento de las lagunas pampeanas. Ecología Austral , 12: 175– 185. Ringelberg, J. & Van Gool, E. 1998. Do bacteria, not fish, produce ‘fish kairomone’? Journal of Plankton Research , 20: 1847– 1852. Google Scholar CrossRef Search ADS   Schaum, C.E., Batty, R. & Last, K.S. 2013. Smelling danger-alarm cue responses in the polychaete Nereis (Hediste) diversicolor (Müller, 1776) to potential fish predation. PlosOne , 8: e77431. Google Scholar CrossRef Search ADS   Schoeppner, N.M. & Relyea, R. 2009. Interpreting the smells of predation: how alarm cues and kairomones induce different prey defences. Functional Ecology, 23: 1114–1121. Schwalbe, M.A.B., Bassett, D.K. & Webb, J.F. 2012. Feeding in the dark: lateral line-mediated prey detection in the peacock cichlid Aulonocara stuartgranti. Journal of Experimental Biology , 215: 2060– 2071. Google Scholar CrossRef Search ADS PubMed  Shabani, S., Kamio, M. & Derby, D.D. 2008. Spiny lobsters detect conspecific blood-borne alarm cues exclusively through olfactory sensilla. Journal of Experimental Biology , 211: 2600– 2608. Google Scholar CrossRef Search ADS PubMed  Sih, A. & Kats, L.B. 1991. Effects of refuge availability on the response of salamander larvae to chemical cues from predatory green sunfish. Animal Behavior , 42: 330– 332. Google Scholar CrossRef Search ADS   Smith, R.J.F. 1992. Alarm signals in fishes. Reviews in Fish Biology and Fisheries , 2: 33– 63. Google Scholar CrossRef Search ADS   Sosnovsky, A., Rosso, J. J. & Quirós, R. 2010. Trophic interactions in shallow lakes of the Pampa Plain (Argentina) and their effects on water transparency during two cold seasons of contrasting fish abundance. Limnetica  29, 233– 246. Tollrian, R. & Harvell, C.D. 1999. The ecology and evolution of inducible defenses . Princeton University Press, Princeton, NJ, USA. Torremorell, A. Bustigorry, J. Escaray, R. & Zagarese, H.E. 2007. Seasonal dynamics of a large shallow lake, laguna Chascomús: the role of light limitation and other physical variables. Limnologica , 37: 100– 108. Google Scholar CrossRef Search ADS   von Elert, E. 2012. Information conveyed by chemical cues. In: Chemical ecology in aquatic systems  ( C. Brönmark & L.-A. Hansson, eds.), pp. 19– 38. Oxford University Press, Oxford, UK. Weiss, L., Laforsch, C. & Tollrian, R. 2012. The taste of predation and the defences of prey. In: Chemical ecology in aquatic systems  ( C. Brönmark & L.-A. Hansson, eds.), pp. 111– 126. Oxford University Press, Oxford, UK. Google Scholar CrossRef Search ADS   Williams, D.D. 1986. Factors influencing the microdistribution of two sympatric species of Plecoptera: an experiment al study. Canadian Journal of Fisheries and Aquatic Sciences , 43: 1005– 1009. Google Scholar CrossRef Search ADS   Wisenden, B.D. 2015. Chemical cues that indicate risk of predation. In: Fish pheromones and related cues  ( P.W. Sorensen & B.D. Wisenden, eds.), pp. 131– 148. John Wiley, Ames, IA, USA. Google Scholar CrossRef Search ADS   Wisenden, B.D., Chivers, D.P. & Smith, R.J.F. 1997. Learned recognition of predation risk by Enallagma damselfly larvae (Odonata, Zygoptera) on the basis of chemical cues. Journal of Chemical Ecology , 23: 137– 151. Google Scholar CrossRef Search ADS   Wisenden, B.D. & Millard, M.C. 2001. Aquatic flatworms use chemical cues from injured conspecifics to assess predation risk and to associate risk with novel cues. Animal Behavior , 62: 761– 766. Google Scholar CrossRef Search ADS   Wooster, D. & Sih, A. 1995. A review of the drift and activity responses of stream prey to predator presence. Oikos , 73: 3– 8. Google Scholar CrossRef Search ADS   Wudkevich, K. Wisenden, B.D., Chivers, D.P. & Smith, R.J.F. 1997. Reactions of Gammarus lacustris to chemical stimuli from natural predators and injured conspecifics. Journal of Chemical Ecology , 23: 1163– 1173. Google Scholar CrossRef Search ADS   Yafé, A., Loureiro, M., Scasso, F. & Quintans, F. 2002. Feeding of two cichlidae species (Perciformes) in an [sic] hypertrophic urban lake. Iheringia Serie Zoologica , 92: 73– 79. Google Scholar CrossRef Search ADS   © The Author(s) 2017. Published by Oxford University Press on behalf of The Crustacean Society. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png The Journal of Crustacean Biology Oxford University Press

Responses to chemical cues indicative of predation risk by the freshwater shrimp Palaemon argentinus (Nobili, 1901) (Caridea: Palaemonidae)

Loading next page...
 
/lp/ou_press/responses-to-chemical-cues-indicative-of-predation-risk-by-the-ulccjdqAat
Publisher
The Crustacean Society
Copyright
© The Author(s) 2017. Published by Oxford University Press on behalf of The Crustacean Society. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com
ISSN
0278-0372
eISSN
1937-240X
D.O.I.
10.1093/jcbiol/rux106
Publisher site
See Article on Publisher Site

Abstract

Abstract Many prey species detect predators through chemoreception, particularly in low-visibility aquatic environments. Moreover, injury-released chemical cues from conspecifics are often perceived as a reliable indicator of predation threat. We examined whether males of the freshwater caridean shrimp Palaemon argentinus (Nobili, 1901) react to different types of infochemicals associated with predation threat. Shrimp were exposed to chemical stimuli from starved individuals of a predatory fish (Australoheros facetus (Jenyns, 1842)) and from crushed conspecific shrimp. Our experiment showed that P. argentinus reacts to waterborne substances associated with predation threat, indicating that chemical cues mediate behavioural antipredator responses. Shrimp adopted an appropriate antipredator behaviour (reduced swimming activity) in response to chemical stimuli from A. facetus, and from crushed conspecifics, relative to a distilled-water control. The chemical stimuli from crushed conspecifics elicited the strongest reduction in swimming activity. Reduced movement, a common response in prey animals to the presence of predators, was not entirely consistent because shrimp increased their walking time in response to the chemical stimuli that were investigated. The ability to alter behaviour based on vision-independent perception of ambient risk would be highly useful for macroinvertebrate prey species such as P. argentinus living in eutrophic shallow lakes where visibility is often reduced. Our results demonstrated chemosensory recognition of predation risk highlighting the important role of chemical cues in the behavioural ecology of this shrimp, especially with regards to predator-prey interactions. INTRODUCTION There has been an increasing interest in understanding the importance of non-visual signals for communication and information in aquatic systems. Many studies have shown that aquatic animals use chemical cues to locate food, detect the presence of predators, find a partner or host, and for precise migration and navigation (Dodson et al., 1994; Brönmark & Hansson, 2012). Chemoreception depends primarily on the senses of taste and smell, and is probably one of the most common type of perception used by animals to exploit valuable resources and/or detect danger. Several crustacean groups have highly developed chemosensory systems (Hay, 2011), with chemical cues mediating numerous behavioural processes including foraging, reproduction, and antipredator responses (Dodson et al., 1994; Bauer 2011; Hay 2011; Hazlett, 2011; Brooker & Dixson, 2016, 2017). Among decapods, crabs, lobsters, and crayfishes have been shown to be capable of recognising and reacting to chemical substances indicative of predation risk (Dodson et al., 1994; Hazlett, 2011), and such responses have also been recently reported in some caridean shrimps (Huang et al., 2011; Brooker & Dixson 2016, 2017). In many aquatic animals, chemical cues from predators and cues from injured conspecifics have the potential to provide important information about the current risk of predation for prey (Tollrian & Harvell, 1999; Ferrari et al., 2010; Paterson et al., 2013; Wisenden, 2015). Chemical substances released by predators, defined as kairomones, can be important indicators of risk and elicit antipredatory responses in several aquatic taxa (Tollrian & Harvell, 1999; Wisenden, 2015). Moreover, when attacked by predators, diverse animals actively or passively release molecules that trigger alarm and related antipredatory behaviour by nearby conspecifics (Shabani et al., 2008; Derby & Zimmer, 2012). The actively released molecules are pheromones, whereas the passively released molecules are alarm cues (Shabani et al., 2008). It is believed that alarm cues which leak from injured or freshly killed preys warn conspecifics of an immediate danger (e.g., active predators) and elicit similar responses as predator odour when received by nearby conspecifics (Chivers & Smith, 1998; Shabani et al., 2008). After detecting these chemical cues, preys usually reduce their activity and/or their shelter-seeking. The reduction of overall activity and/or shelter-seeking may result in reduced foraging, mating activity or less investment in offspring (Holomuzki & Short, 1988; Lima & Dill, 1990). Therefore, prey species should be able to distinguish chemical cues as indicators of predation threats to ensure escape behaviour is not unnecessarily initiated, thus representing a cost in terms of decreased opportunities for foraging, mating activity, and other fitness-related behaviours (Åbjörnsson et al., 1997). The freshwater caridean shrimp Palaemon argentinus (Nobili, 1901) (= Palaemonetes argentinus, see DeGrave & Ashelby, 2013) inhabits shallow lakes and streams in southeastern South America, and breeds in spring and summer (from October to March). This shrimp is found sympatrically with predatory fishes such as cichlids, characids, and cyprinodonts in shallow lakes in the Pampa plains of Argentina (González Sagrario et al., 2009). Littoral fishes, such as the cichlid Australoheros facetus, are omnivores that feed on aquatic plants, zooplankton, smaller fishes, and macroinvertebrates such as P. argentinus (Yafé et al., 2002). Some shallow lakes in the Pampas are dominated by submersed macrophytes, have a relatively low phytoplankton biomass, and the water is clear, but in general, most water bodies exhibit high phytoplankton biomass and scarce macrophyte development, and are typically turbid (Allende et al., 2009). A third type of lake that can be encountered in this region corresponds to shallow lakes in which turbidity is mostly due to inorganic material, and in which both phytoplankton and macrophyte development is low (Allende et al., 2009). Nowadays, there is a gradual shift from clear to turbid-water conditions, which along with decreases in macrophyte abundance, has been shown to affect trophic interactions (Quirós, 1998; Quirós et al., 2002; Coops et al., 2003; González Sagrario et al., 2009; Sosnovsky et al., 2010). The prevailing low visibility during the turbid water condition suggests that macroinvertebrate prey species like P. argentinus probably rely almost completely on chemical senses to detect predators. Although P. argentinus is likely to play a key role in trophic interactions of these shallow lakes, chemosensory recognition of predation risk by adults of this shrimp has not yet been reported. We performed a short-term laboratory experiment to examine whether adults of P. argentinus can detect and react to chemical cues indicative of predation threat. We examined the ability of male shrimp to modify locomotor activities (swimming and walking) in response to chemical cues from starved individuals of a predatory fish (kairomones) and from crushed conspecific shrimp (alarm cues). We predicted that adults of P. argentinus will decrease their activity level when exposed to alarm cues, a reliable indicator of predation threat. Reduced movement to the presence of predators is a common response in prey taxa, including shrimps (e.g., Heck & Thoman, 1981). We exposed shrimp to chemical stimuli from the known predator (A. facetus) to verify that the response of shrimp to stimuli from crushed conspecifics represents antipredator behaviour. MATERIALS AND METHODS Sampling In March 2014, January and December 2015, mature individuals of P. argentinus and A. facetus were collected from La Brava Lake (37°52′52″S, 57°58′38″W), Buenos Aires province, Argentina. Both species co-occur in shallow lakes in the Pamapas, so the tested population of shrimp had previous experience with the experimental predator (Ituarte et al., 2014). Specimens were obtained from the littoral zone using a hand net (45 cm width, 30 cm deep; 1 mm mesh). In the laboratory, each group of animals was held in separate 50 l aerated aquaria (22 °C, 10:14 h light dark cycle) filled with dechlorinated tap water for at least five days before being included in experiments. During acclimation, shrimp and fish were fed daily on TetraMin Pro® (lipids 12%; proteins 46%) (Tetra GmbH, Melle, Germany). In order to avoid the possibility of sex differences in behavioural responses to predation risk during the breeding season, only males of P. argentinus were used for experimentation (Gancedo, 2015). As in many caridean shrimps, P. argentinus shows a ‘pure searching’ mating tactic, in which males are continually on the prowl for a receptive female (Bauer, 2004). In this type of mating, often referred to as promiscuous, males do not defend territories, are highly mobile, smaller than females, cryptic, and less obvious to visually oriented predators (Bauer, 2004). Male shrimp 4–6 mm carapace length were used in the experiments. Individuals were checked for the presence of metacercarial cysts of microphallid parasites (Trematoda, Microphallidae; Merlo et al., 2016), and only non-parasitized shrimp were used. Experimental procedure We tested the responses of male shrimp to chemical cues from three starved individuals of the fish A. facetus (collections made in March 2014, and January and December 2015; fork length = 14.1; 13.2 and 10.5 cm, respectively), and from crushed conspecific shrimp. Different male shrimp were used for each trial. Chemical stimuli from fish individuals were used as predator odour as suggested by Gelowitz et al. (1993), Wisenden et al. (1997), and Wudkevich et al. (1997) following the procedure described by Wisenden et al. (1997). During acclimation, approximately 12 h after the final feeding, each fish individual was placed in an aquarium (volume 3.5 l; 22 °C, 14:10 h light dark cycle) filled with dechlorinated tap water and was held there without food for three days. Specimens were then removed and the stimulus water was immediately used. The collection aquaria were well-aerated but contained no filtration system to avoid filtering active compounds. Chemical cues from conspecifics were prepared by crushing one adult shrimp using a mortar and pestle in 10 ml of distilled water; the stimulus preparation was immediately used. We tested the responses of male shrimp in an acrylic aquarium (10 × 10 × 10 cm) filled with 800 ml dechlorinated tap water. A video camera was installed on the side of the experimental aquaria to record shrimp behaviour. Each shrimp was left to acclimatise for 30 min before the beginning of each trial. Different male shrimp were used for each trial (N = 34 per trial). Shrimp behaviour (pre-stimulus activity) was recorded for 5 min before 3 ml of treatment water (Wisenden et al., 1997) were carefully introduced with a syringe into a corner of the aquarium. Twenty seconds after injection, behaviour was recorded for another 5 min (post-stimulus activity). Aquaria were thoroughly rinsed and cleaned between test trials to remove any trace of chemical stimuli from previous trials. All the recordings were randomly assigned to a video code and were blindly analysed by the same experimenter (BJG). From the recordings, we obtained the time in which each shrimp swam and walked in each of the two 5 min periods before and after adding a chemical stimulus to the water. Statistical analyses Shrimp response to a particular stimulus was defined as the difference between post- and pre-stimulus activity. All values were expressed as arithmetic mean ± standard error (SE). The effects of fish odour on changes in the swimming and walking time of shrimp were tested with mixed-model nested ANOVA with fish nested within control using InfoStat 2017 (Di Rienzo et al., 2017). Water treatment condition (distilled water and predator odour) was a fixed factor and fish identity was a random factor in the model. We compared behavioural changes in 34 male shrimp (8, 12, and 14 shrimp for each respective fish individual). The effects of the three treatment conditions (distilled water, predator odour, and crushed conspecifics) on the changes in time performing each activity were analysed by one-way ANOVA using SigmaStat v 4.0. Shrimp reactions to all three fish individuals tested were pooled as the predator odour treatment. We tested 102 male shrimp, 34 in each of the three treatment conditions. All ANOVAs were performed after checks for normal distribution and equality of variance (Shapiro-Wilk and Brown-Forsythe tests, respectively). When ANOVA indicated significant differences between treatments, they were tested with a post hoc Tukey test. RESULTS Basal behaviours of P. argentinus during the pre-stimulus period (before adding any water treatment) involved moving and stationary activities. Shrimp spent most of their time either swimming in the water column, motionless, or walking on the bottom of the aquarium. We focused our data analysis on the most frequently observed activities involving movement: swimming and walking. The two types of swim behaviour included slow forward motion by swimming through the water column with pereopods extended downward, and swimming up-side-down just below the surface of the water. To facilitate data recording, both types of swimming behaviour were grouped into a single activity category (“swimming”). Chemical cues from different fish individuals did not affect changes in swimming time of male shrimp relative to distilled water control (nested mixed-model ANOVA: F(1; 62) = 0.62; P = 0.48), whereas their walking time was affected (F(1; 62) = 25.44; P = 0.007). Shrimp increased their walking time in response to fish stimuli (P < 0.05). Data for all three fish were pooled as predator odour although variance for fish individuals differed from zero (swimming time: F(4; 62) = 34.4; P < 0.0001 and walking time: F(4; 62) = 2.52; P = 0.049). Changes in swimming time of male shrimp was affected by water treatment conditions (ANOVA: F(2; 101) = 46; P < 0.001). Male shrimp reduced their swimming time in response to chemical stimuli from predator odour (pooled data) and crushed conspecifics relative to distilled water, and the strongest reduction occurred in response to chemical stimuli from crushed conspecifics (Fig. 1A). Moreover, the amount of time that shrimp spent walking increased in response to both predator odour (pooled data) and conspecific stimuli relative to distilled water (ANOVA: F(2; 101) = 24; P < 0.001). Such increase was stronger in response to the predator odour treatment (Fig. 1B). Figure 1. View largeDownload slide Mean (± SE) change in time devoted to swimming (A), and walking (B) by males of Palaemon argentinus following exposure to a control of distilled water (DW), predator odour (PO, chemical stimuli from starved individuals of the predatory fish Australoheros facetus, or crushed conspecific shrimp (CC). For each behaviour, bars with different letters indicate significant differences (post-hoc Tukey test, α = 0.05); N = 34 in each treatment. Figure 1. View largeDownload slide Mean (± SE) change in time devoted to swimming (A), and walking (B) by males of Palaemon argentinus following exposure to a control of distilled water (DW), predator odour (PO, chemical stimuli from starved individuals of the predatory fish Australoheros facetus, or crushed conspecific shrimp (CC). For each behaviour, bars with different letters indicate significant differences (post-hoc Tukey test, α = 0.05); N = 34 in each treatment. DISCUSSION The ability to recognise and respond to a potential predator is an essential component of antipredator behaviour because failure to do so increases the probability of the predator capturing or injuring the prey (Lima & Dill, 1990). The importance of chemical cues in aquatic predator-prey systems is well known and chemical cues recognition has already been demonstrated in some caridean shrimps (e.g., Dunlop-Hayden & Rehage, 2011; Huang et al., 2011; Ocasio-Torres et al., 2014; Brooker & Dixson, 2016, 2017). Shrimps seem to have evolved a chemosensory ability that allows them to distinguish different organisms in their environment (Brooker & Dixson, 2016). Our experiment showed that the P. argentinus reacts to waterborne substances indicative of predation risk suggesting that chemical cues mediate behavioural antipredator responses in this species as well. Reduced swimming behaviour has been reported in palaemonids shrimps upon non-chemical detection of predatory fish (Heck & Thoman, 1981; Carson & Merchant, 2005; Kunz et al., 2006). By decreasing swimming activity, benthic prey such as P. argentinus can possibly be less vulnerable to predation by reducing the rate of encounter with potential predators (e.g., Wisenden et al., 1997; Chivers & Smith, 1998; Ferrari et al., 2010). Non-significant changes in the swimming behaviour of P. argentinus along with the high variability in shrimp behaviour when exposed to waterborne substances from each fish individual may be due to the small sample size for each fish. When data for all three fish were pooled, however, there was a clear reduction in the swimming time of shrimp. In turbid water and/or physically complex environments, preys able to detect predator odours will certainly be better suited to deal with predators than preys which solely rely on visual detection (Kats & Dill, 1998). Since many fishes feeding in light-limited environments locate their prey following hydrodynamic stimuli in the wake (e.g., Pohlmann et al., 2004; Schwalbe et al., 2012), a decrease in swimming activity will presumably be a good antipredatory response. Benthic invertebrate preys generally decrease their activities in response to predatory vertebrates (review by Wooster & Sih, 1995); however, some reports have shown an opposite response. Williams (1986) found in laboratory trials that larvae of the stonefly Paragnetina media (Walker, 1852) increase their movement when exposed to trout (Oncorhynchus mykiis (Walbaum, 1792)) odour. Moreover, response to predator odour is known to depend upon the presence or absence of a refuge (Sih & Kats, 1991). We found that male shrimp increased their walking time in response to predator odour and the crushed-conspecific treatment, suggesting that such reaction depends on the context of habitat (e.g., seeking for refuge). The increased walking time and the reduced swimming behaviour could provide protection against fish predators, but further experimental studies are needed to understand whether these observed reactions in males of P. argentinus are adaptive. The chemical characterization of predator-specific cues is still scarce (von Elert, 2012; Weiss et al., 2012), although faeces are often the source of predator odour (Kats & Dill, 1998). The fish in our experiments were starved for three days, indicating that shrimp reactions could be triggered by other metabolites of A. facetus rather than by faeces and/or by predator-associated bacteria that release specific metabolites (probably present in the mucus cover of fish; see Ringelberg & Van Gool, 1998). Almost every invertebrate species tested has shown an increase in antipredator behaviour when odours of crushed conspecifics were presented (e.g., Wisenden & Millard, 2001; Hazlett, 2011; Schaum et al., 2013), but the chemical identity of alarm cues has been determined in only a few species of sea anemones (Howe & Sheikh (1975) and ostariophysan fishes (e.g., Smith, 1992). There is no indication of specialized crustacean cells that could produce alarm cues (such as the epidermal club cells in ostariophysan fishes), but peptides found in the hemolymph have been suggested as alarm cues (Acquistapace et al., 2005; Shabani et al., 2008; Hazlett, 2011). Since multiple cues can act in an additive or synergistic fashion to provide additional information for risk assessment by prey (e.g., Schoeppner & Relyea, 2009), the observed reduction in swimming time of male P. argentinus could translate into a stronger learned response to the predator when the predator odour is paired with alarm cues. Future studies should test this hypothesis. The ability in small benthic species to identify other animals within proximity without visual cues would be highly useful (Brooker & Dixson, 2016). Since most of the shallow lakes in the Pampas are permanently limited by light (Quirós et al., 2002, Torremorell et al., 2007; Allende et al., 2009), macroinvertebrate prey such as P. argentinus, probably rely almost completely on chemical senses to detect the risk of predation. The fact that P. argentinus can distinguish between chemical exuded by a predatory fish and from crushed conspecifics highlights the important role of chemical cues in the behavioural ecology of caridean shrimps, especially with regards to predator-prey interactions (see Brooker & Dixson, 2016, 2017). ACKNOWLEDGEMENTS This article is based on work done by BJG in partial fulfilment of the bachelor’s degree at Universidad Nacional de Mar del Plata, Argentina, with the support of a fellowship from the Comisión de Investigaciones Científicas (CIC). We are also grateful to J. Nuñez and M.G. Vázquez for assistance with experiments, to E. Spivak, two anonymous reviewers for providing suggestions to improve previous drafts of the manuscript, and A. Cosulich for revising the English language. This research was supported by a grant from Consejo Nacional de Investigaciones Científicas y Técnicas, Argentina (PIP 112-201101-00830). REFERENCES Åbjörnsson, K., Wagner, B.M.A., Axelsson, A., Bjerselius, R. & Olsén, K.H. 1997. Responses of Acilius sulcatus (Coleoptera: Dytiscidae) to chemical cues from perch (Perca fluviatilis). Oecologia , 111: 166– 171. Google Scholar CrossRef Search ADS PubMed  Acquistapace, P., Calamai, L., Hazlett, B.A. & Gherardi, F. 2005. Source of alarm substances in crayfish and their preliminary chemical characterization. Canadian Journal of Zoology , 83: 1624– 1630. Google Scholar CrossRef Search ADS   Allende, L., Tell, G., Zagarese, H., Torremorell, A., Pérez, G., Bustingorry, J., Esaray, R. & Izaguirre, I. 2009. Phytoplankton and primary production in clear-vegetated, inorganic-turbid, and algal-turbid shallow lakes from the pampa plain (Argentina). Hydrobiologia , 624: 45– 60. Google Scholar CrossRef Search ADS   Bauer, R. 2004. Remarkable shrimps: adaptations and natural history of the carideans , Edn. 1. University of Oklahoma Press, Norman, OK, USA. Bauer, R. 2011. Chemical communication in decapod shrimps: the influence of mating and social systems on the relative importance of olfactory and contact pheromones. In: Chemical communication in crustaceans  ( T. Breithaupt & M. Thiel, eds.), pp. 277– 296. Springer, New York, USA. Google Scholar CrossRef Search ADS   Brönmark, C. & Hansson, L.-A. 2012. Chemical ecology in aquatic systems . Oxford, University Press, New York, USA. Google Scholar CrossRef Search ADS   Brooker, R.M. & Dixson, D.L. 2016. Comparable cross-taxa risk perception via chemical cues in marine and freshwater crustaceans. Marine and Freshwater Research , 68: 788– 792. Google Scholar CrossRef Search ADS   Brooker, R.M. & Dixson, D.L. 2017. Intertidal crustaceans use seaweed-derived chemical cues to mitigate predation risk. Behavioral Ecology and Sociobiology , 71: 47– 54. Google Scholar CrossRef Search ADS   Carson, M.L. & Merchant, H. 2005. A laboratory study of the behavior of two species of grass shrimp (Palaemonetes pugio Holthuis and Palaemonetes vulgaris Holthuis) and the killifish (Fundulus heteroclitus Linneaus). Journal of Experimental Marine Biology and Ecology , 314: 187– 201. Google Scholar CrossRef Search ADS   Chivers, D.P. & Smith, R.J.F. 1998. Chemical alarm signalling in aquatic predator-prey systems: a review and prospectus. Ecoscience , 5: 338– 352. Google Scholar CrossRef Search ADS   Coops, H., Beklioglu, M. & Crisman, T.L. 2003. The role of water-level fluctuations in shallow lake ecosystems – workshop conclusions. Hydrobiologia , 506: 23– 27. Google Scholar CrossRef Search ADS   DeGrave, S. & Ashelby, C.W. 2013. A re-appraisal of the systematic status of selected genera in Palaemoninae (Crustacea: Decapoda: Palaemonidae). Zootaxa , 3734: 331– 334. Google Scholar CrossRef Search ADS PubMed  Derby, C.D. & Zimmer, R.K. 2012. Neuroecology of predator-prey interactions. In: Chemical ecology in aquatic systems  ( C. Brönmark & L.-A. Hansson, eds.), pp. 158– 171. Oxford University Press, Oxford, UK. Di Rienzo, J.A., Casanoves, F., Balzarini, M.G., Gonzalez, L., Tablada, M. & Robledo, C.W. 2017. InfoStat versión . Grupo InfoStat, FCA, Universidad Nacional de Córdoba, Córdoba, Argentina. Dodson, S.I., Crowl, T.A., Peckarsky, B.L., Kats, L.B., Covich, A.P. & Culp, J.M. 1994. Non-visual communication in freshwater benthos: an overview. Journal of the North American Benthological Society , 13: 268– 282. Google Scholar CrossRef Search ADS   Dunlop-Hayden, K.L. & Rehage, J.S. 2011. Antipredator behavior and cue recognition by multiple Everglades prey to a novel cichlid predator. Behavior , 148: 795– 823. Google Scholar CrossRef Search ADS   Ferrari, M.C.O., Wisenden, B.D. & Chivers, D.P. 2010. Chemical ecology of predator-prey interactions in aquatic ecosystems: a review and prospectus. Canadian Journal of Zoology , 88: 698– 724. Google Scholar CrossRef Search ADS   Gancedo, B.J. 2015. Respuestas coportamentales inducidas por el riesgo de depredación en adultos del camarón Palaemontes argentinus . Undergraduate thesis, Universidad Nacional de Mar del Plata, Mar del Plata, Argentina. Gelowitz, C.M., Mathis, A. & Smith, R.J.F. 1993. Chemosensory recognition of northern pike (Esox lucius) by brook stickleback (Culaea inconstans): population differences and he influence predator diet. Behavior , 127: 105– 118. Google Scholar CrossRef Search ADS   González Sagrario, M.A., Balseiro, E., Ituarte, R.B. & Spivak, E.D. 2009. Macrophytes as refuge or risky area for zooplankton: a balance set by littoral predacious macroinvertebrates. Freshwater Biology , 54: 1042– 1053. Google Scholar CrossRef Search ADS   Hay, M.E. 2011. Crustaceans as powerful models in aquatic chemical ecology. In: Chemical communication in crustaceans  ( T. Breithaupt & M. Thiel, eds.), pp. 41– 63. Springer, New York, USA. Google Scholar CrossRef Search ADS   Hazlett, B.A. 2011. Chemical cues and reducing the risk of predation. In: Chemical communication in crustaceans  ( T. Breithaupt & M. Thiel, eds.), pp. 355– 370. Springer, New York, USA. Google Scholar CrossRef Search ADS   Heck, K.L., Jr. & Thoman, T.A. 1981. Experiments on predator-prey interactions in vegetated aquatic habitats. Journal of Experimental Marine Biology and Ecology , 53: 125– 134. Google Scholar CrossRef Search ADS   Holomuzki, J.R. & Short, T.M. 1988. Habitat use and fish avoidance behaviors by the stream-dwelling isopod Lirceus fontinalis. Oikos , 52: 79– 86. Google Scholar CrossRef Search ADS   Howe, N.R. & Sheikh, Y.M. 1975. Anthopleurine: a sea anemone alarm pheromone. Science , 189: 386– 388. Google Scholar CrossRef Search ADS PubMed  Huang, J., Wu, Z., Cai, F. & Liu, H. 2011. Responses of freshwater shrimp on alarm cues from injured-conspecific. In: International conference on remote sensing, environment and transportation engineering (RSETE), pp. 7078– 7082. Nanjing, China. Ituarte, R.B., Vázquez, M.G., González Sagrario, M.A. & Spivak, E.D. 2014. Carryover effects of predation risk on postembryonic life-history stages in a freshwater shrimp. Zoology , 117: 139– 145. Google Scholar CrossRef Search ADS PubMed  Kats, L.B. & Dill, L.M. 1998. The scent of death: chemosensory assessment of predation risk by prey animals. Ecoscience , 5: 361– 394. Google Scholar CrossRef Search ADS   Kunz, A.K., Ford, M. & Pung, O.J. 2006. Behavior of the grass shrimp Palaemonetes pugio and its response to the presence of the predatory fish Fundulus heteroclitus. American Naturalist , 155: 286– 294. Google Scholar CrossRef Search ADS   Lima, S.L. & Dill, L.M. 1990. Behavioral decisions made under the risk of predation: a review and prospectus. Canadian Journal of Zoology , 68: 619– 640. Google Scholar CrossRef Search ADS   Merlo, J.M., Parietti, M. & Ituarte, R.B. 2016. Influence of Microphallus szidatti Martorelli, 1986 (Trematoda) on the fecundity of the second intermediate host, Palaemonetes argentines Nobili, 1901 (Decapoda: Natantia). Journal of Crustacean Biology , 36: 94– 98. Google Scholar CrossRef Search ADS   Nobili, G. 1901. Decapodi raccolti dal Dr. Filipo Silvestri nell’America meridionale. Bolletino dei Musei di Zoologia ed Anatomia comparata della R. Università di Torino , 16: 1– 16. Ocasio-Torres, M., Crowl, T. & Sabat, A. 2014. Long rostrum in an amphidromous shrimp induced by chemical signals from a predatory fish. Freshwater Science , 33: 451– 458. Google Scholar CrossRef Search ADS   Paterson, R.A., Pritchard, D.W., Dick, J.T.A., Alexander, M.E., Hatcher, M.J. & Dunn, A.M. 2013. Predator cue studies reveal strong trait-mediated effects in communities despite variation in experimental designs. Animal Behavior , 86: 1301– 1313. Google Scholar CrossRef Search ADS   Pohlmann, K., Atema, J. & Breithaupt, T. 2004. The importance of the lateral line in nocturnal predation of piscivorous catfish. Journal of Experimental Biology , 207: 2971– 2978. Google Scholar CrossRef Search ADS PubMed  Quirós, R. 1998. Fish effects on trophic relationships in the pelagic zone of lakes. Hydrobiologia , 361: 101– 111. Google Scholar CrossRef Search ADS   Quirós, R., Rennella, A.M., Boveri, M.B., Rosso, J.J. & Sosnovsky, A. 2002. Factores que afectan la estructura y el funcionamiento de las lagunas pampeanas. Ecología Austral , 12: 175– 185. Ringelberg, J. & Van Gool, E. 1998. Do bacteria, not fish, produce ‘fish kairomone’? Journal of Plankton Research , 20: 1847– 1852. Google Scholar CrossRef Search ADS   Schaum, C.E., Batty, R. & Last, K.S. 2013. Smelling danger-alarm cue responses in the polychaete Nereis (Hediste) diversicolor (Müller, 1776) to potential fish predation. PlosOne , 8: e77431. Google Scholar CrossRef Search ADS   Schoeppner, N.M. & Relyea, R. 2009. Interpreting the smells of predation: how alarm cues and kairomones induce different prey defences. Functional Ecology, 23: 1114–1121. Schwalbe, M.A.B., Bassett, D.K. & Webb, J.F. 2012. Feeding in the dark: lateral line-mediated prey detection in the peacock cichlid Aulonocara stuartgranti. Journal of Experimental Biology , 215: 2060– 2071. Google Scholar CrossRef Search ADS PubMed  Shabani, S., Kamio, M. & Derby, D.D. 2008. Spiny lobsters detect conspecific blood-borne alarm cues exclusively through olfactory sensilla. Journal of Experimental Biology , 211: 2600– 2608. Google Scholar CrossRef Search ADS PubMed  Sih, A. & Kats, L.B. 1991. Effects of refuge availability on the response of salamander larvae to chemical cues from predatory green sunfish. Animal Behavior , 42: 330– 332. Google Scholar CrossRef Search ADS   Smith, R.J.F. 1992. Alarm signals in fishes. Reviews in Fish Biology and Fisheries , 2: 33– 63. Google Scholar CrossRef Search ADS   Sosnovsky, A., Rosso, J. J. & Quirós, R. 2010. Trophic interactions in shallow lakes of the Pampa Plain (Argentina) and their effects on water transparency during two cold seasons of contrasting fish abundance. Limnetica  29, 233– 246. Tollrian, R. & Harvell, C.D. 1999. The ecology and evolution of inducible defenses . Princeton University Press, Princeton, NJ, USA. Torremorell, A. Bustigorry, J. Escaray, R. & Zagarese, H.E. 2007. Seasonal dynamics of a large shallow lake, laguna Chascomús: the role of light limitation and other physical variables. Limnologica , 37: 100– 108. Google Scholar CrossRef Search ADS   von Elert, E. 2012. Information conveyed by chemical cues. In: Chemical ecology in aquatic systems  ( C. Brönmark & L.-A. Hansson, eds.), pp. 19– 38. Oxford University Press, Oxford, UK. Weiss, L., Laforsch, C. & Tollrian, R. 2012. The taste of predation and the defences of prey. In: Chemical ecology in aquatic systems  ( C. Brönmark & L.-A. Hansson, eds.), pp. 111– 126. Oxford University Press, Oxford, UK. Google Scholar CrossRef Search ADS   Williams, D.D. 1986. Factors influencing the microdistribution of two sympatric species of Plecoptera: an experiment al study. Canadian Journal of Fisheries and Aquatic Sciences , 43: 1005– 1009. Google Scholar CrossRef Search ADS   Wisenden, B.D. 2015. Chemical cues that indicate risk of predation. In: Fish pheromones and related cues  ( P.W. Sorensen & B.D. Wisenden, eds.), pp. 131– 148. John Wiley, Ames, IA, USA. Google Scholar CrossRef Search ADS   Wisenden, B.D., Chivers, D.P. & Smith, R.J.F. 1997. Learned recognition of predation risk by Enallagma damselfly larvae (Odonata, Zygoptera) on the basis of chemical cues. Journal of Chemical Ecology , 23: 137– 151. Google Scholar CrossRef Search ADS   Wisenden, B.D. & Millard, M.C. 2001. Aquatic flatworms use chemical cues from injured conspecifics to assess predation risk and to associate risk with novel cues. Animal Behavior , 62: 761– 766. Google Scholar CrossRef Search ADS   Wooster, D. & Sih, A. 1995. A review of the drift and activity responses of stream prey to predator presence. Oikos , 73: 3– 8. Google Scholar CrossRef Search ADS   Wudkevich, K. Wisenden, B.D., Chivers, D.P. & Smith, R.J.F. 1997. Reactions of Gammarus lacustris to chemical stimuli from natural predators and injured conspecifics. Journal of Chemical Ecology , 23: 1163– 1173. Google Scholar CrossRef Search ADS   Yafé, A., Loureiro, M., Scasso, F. & Quintans, F. 2002. Feeding of two cichlidae species (Perciformes) in an [sic] hypertrophic urban lake. Iheringia Serie Zoologica , 92: 73– 79. Google Scholar CrossRef Search ADS   © The Author(s) 2017. Published by Oxford University Press on behalf of The Crustacean Society. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com

Journal

The Journal of Crustacean BiologyOxford University Press

Published: Jan 1, 2018

There are no references for this article.

You’re reading a free preview. Subscribe to read the entire article.


DeepDyve is your
personal research library

It’s your single place to instantly
discover and read the research
that matters to you.

Enjoy affordable access to
over 12 million articles from more than
10,000 peer-reviewed journals.

All for just $49/month

Explore the DeepDyve Library

Unlimited reading

Read as many articles as you need. Full articles with original layout, charts and figures. Read online, from anywhere.

Stay up to date

Keep up with your field with Personalized Recommendations and Follow Journals to get automatic updates.

Organize your research

It’s easy to organize your research with our built-in tools.

Your journals are on DeepDyve

Read from thousands of the leading scholarly journals from SpringerNature, Elsevier, Wiley-Blackwell, Oxford University Press and more.

All the latest content is available, no embargo periods.

See the journals in your area

DeepDyve Freelancer

DeepDyve Pro

Price
FREE
$49/month

$360/year
Save searches from Google Scholar, PubMed
Create lists to organize your research
Export lists, citations
Access to DeepDyve database
Abstract access only
Unlimited access to over
18 million full-text articles
Print
20 pages/month
PDF Discount
20% off