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Visual and Chemical Prey Cues as Complementary Predator Attractants in a Tropical Stream Fish Assemblage

Visual and Chemical Prey Cues as Complementary Predator Attractants in a Tropical Stream Fish... Hindawi Publishing Corporation International Journal of Zoology Volume 2012, Article ID 510920, 7 pages doi:10.1155/2012/510920 Research Article Visual and Chemical Prey Cues as Complementary Predator Attractants in a Tropical Stream Fish Assemblage Chris K. Elvidge and Grant E. Brown Department of Biology, Concordia University, 7141 Sherbrooke St. West, Montreal, QC, Canada H4B 1R6 Correspondence should be addressed to Chris K. Elvidge, chris.k.elvidge@gmail.com Received 27 March 2012; Revised 25 April 2012; Accepted 30 April 2012 Academic Editor: Marie Herberstein Copyright © 2012 C. K. Elvidge and G. E. Brown. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. To date, little attention has been devoted to possible complementary effects of multiple forms of public information similar information on the foraging behaviour of predators. In order to examine how predators may incorporate multiple information sources, we conducted a series of predator attraction trials in the Lower Aripo River, Trinidad. Four combinations of visual (present or absent) and chemical cues (present or absent) from each of two prey species were presented. The occurrences of three locally abundant predatory species present within a 1 m radius of cue introduction sites were recorded. The relative attractiveness of cue type to each predator was directly related to their primary foraging modes, with visual ambush predators demonstrating an attraction to visual cues, benthivores to chemical cues, and active social foragers demonstrating complementary responses to paired cues. Predator species-pair counts were greatest in response to cues from the more abundant prey species, indicating that individuals may adopt riskier foraging strategies when presented with more familiar prey cues. These differences in predator attraction patterns demonstrate complementary effects of multiple sensory cues on the short-term habitat use and foraging behaviour of predators under fully natural conditions. 1. Introduction limited under conditions of relatively high background noise, as in lotic systems. The behavioural strategies adopted by participants in pre- Many groups of freshwater fishes produce chemical cues dator-prey interactions are often mediated by publicly avail- in the epidermis which are released into the water following able cues [1] conveying information with some degree of mechanical damage, as would occur during a predation immediate contextual relevance to the receiver. Public, or event [8]. Upon detection by conspecific receivers, these cues non-species-specific, cues may convey qualitatively different have been shown to elicit a suite of antipredator or alarm information to and elicit quantitatively different behavioural responses [9]incentrarchid [10], salmonid [11], cyprinid responses from different receivers [2]. Therelativeimpor- [12], cyprinodontiform [2], esocid [13], and poeciliid [14] tance of different types of public cues in predator-prey inter- species. Due to their manner of release, these chemical cues actions may be mediated by interactions between receiver cannot be manipulated by a predator and likely serve as taxon and environmental constraints; for example, visual reliable indicators of increased risk to receivers subject to cues are typically limited by photoperiod [3]. In aquatic similar predation pressures [15], which is not always the environments, visual and chemical cues have been identified case with potentially misleading visual cues [3]. Damage- as the primary sources of information eliciting short-term released chemical cues have been shown to elicit different behavioural processes for both vertebrate (e.g., fishes, [4]) responses from conspecific receivers differing in ontogenetic and invertebrate (e.g., crustaceans, [5, 6]) species. Although stage from the cue sender [16], with similarly sized receivers acoustic cues have been demonstrated to elicit behavioural demonstrating alarm or antipredator responses and larger responses in freshwater fish receivers under laboratory receivers demonstrating behaviours consistent with foraging conditions [7], the reliability of acoustic information may be responses under laboratory conditions. Similar effects have 2 International Journal of Zoology been observed in heterospecific receivers belonging to the length of P. reticulata (R. hartii maximum standard length, same prey guild and subject to similar predation risks as L , 100 mm, P. reticulata common L 28 mm; [26]) and P. S S chemical cue senders [17, 18]. Conversely, heterospecific reticulata can account for up to 10% of the diet of large R. receivers of larger size than the sender have demonstrated hartii, in the presence of piscivores similarly sized P. reticulata foraging responses following exposure to damage-released and R. hartii are likely subject to similar predation pressures chemical cues under both laboratory [18] and field [19] [17]. conditions. Of the three predatory species examined, the pike cichlid Due to the potentially ultimate costs incurred by failing Crenicichla alta is a solitary, visually foraging ambush pre- to respond to ambient cues indicating elevated predation dator and obligate piscivore which is considered the main risk, the responses of prey to public cues have thus far predator of P. reticulata in Trinidad whenever they co-occur received considerably more attention from researchers than [25]. The blue acara cichlid Aequidens pulcher is a solitary have responses by predators [20]. In freshwater fishes, labo- forager which typically feeds on invertebrates and benthos, ratory experiments have documented attraction responses to displaying only opportunistic piscivory [27]. The two-spot chemical cues from heterospecific prey [21], while predators sardine Astyanax bimaculatus, by contrast, is a highly social under natural conditions have demonstrated preferences and active forager [23, 26], whose predominantly algae- for areas labelled with damage-released chemical cues over and insect-based diet undergoes an ontogenetic switch to longer time scales (hours, [19]). Recently, Lonnstedt et include opportunistic piscivory when individuals exceed al. [22]demonstratedanattractionresponseinapreda- ∼50 mm total length [28]. These three species likely account tory coral reef fish, the dottyback Pseudochromis fuscus to for the majority of predation pressure on P. reticulata and heterospecific damage-released chemical cues under fully any incidental R. hartii within the study area [29]. Based natural conditions over short (minutes) timescales. In on these differences in social behaviour and foraging mode, addition, under both natural and laboratory conditions, P. we predict that A. bimaculatus incorporates information fuscus demonstrated a strong preference for chemical cues received through both visual and chemical cues into their extracted from heterospecific donors belonging to the ideal foraging decisions, while A. pulcher responds more strongly prey size class [22] for gape-limited predators [17]. Similarly, to chemical than to visual cues and C. alta responds primarily Elvidge et al. [2] demonstrated significant positive linear to visual cues. relationships between foraging behaviours and receiver size in an opportunistic predator, Hart’s rivulus Rivulus hartii,in response to chemical cues from Trinidadian guppies Poecilia 2.2. Prey Cues. Damage-released chemical cues were extract- reticulata. Together, these results indicate that damage- ed from female P. reticulata (L 27.6 ± 2.7mm (mean ± released chemical cues provide predators with information SD), N = 18) and R. hartii (L 42 ± 7.9 mm (mean ± SD), about the availability and quality of potential prey. N = 8) donors collected from the Naranja River tributary ◦  ◦ In order to examine the effects of different combinations (10 41 N; 61 14 W) approximately 6 km upstream from the of visual and chemical cues indicating the availability of prey observation sites in the Lower Aripo River using a beach seine on the behaviour of predators in fresh water, the present net (length 2.5 m, height 1 m, mesh size 3 mm). Donors were study focused on short-term changes in local abundances of collected from the Naranja River because intensive sampling three predatory species differing in foraging modes to the via seine net did not find any R. hartii present at the study cues of two cooccurring prey species. In general, we predict sites in the Lower Aripo during the course of the present that multiple complementary cues indicating the presence of experiment. Chemical cues from P. reticulata donors from familiar prey species will result in greater local abundances of the Naranja River have previously been demonstrated to predators, with the relative contribution of each type of cue elicit qualitatively similar responses to those of Lower Aripo (visual or chemical) mediated by the typical foraging mode donors [23] in conspecific receivers from either population. of the predator. Chemical cue donors were euthanized via cervical dis- location, measured (L ), immediately decapitated behind the opercula, and had their tails removed at the caudal peduncle. Visceral tissues were manually extruded, and 2. Materials and Methods the remaining carcasses were mechanically homogenized in 2.1. Study Species and Area. Predator attraction trials were dechlorinated tap water, diluted to a final concentration of 2 −1 conducted at N = 16 sites in a series of eight pools (two sites 0.1 cm skin mL , and filtered through polyester floss. This per pool) along a 1 km stretch of the Lower Aripo River in concentration of skin extract has previously been shown to the Caroni drainage, Northern Range Mountains, Trinidad elicit both antipredator and foraging behavioural responses ◦  ◦ and Tobago, W. I. (10 39 N, 61 13 W) 04–12 May 2009. in tropical stream fish under laboratory [30] and field [23] These pools have been described in an earlier study involving conditions. The chemical cues from each prey species, as well free-swimming Trinidadian guppies P. reticulata [23]. The as a stream water control treatment, were packaged in 60 mL Lower Aripo is a species-rich, high-predation environment aliquots and frozen at −20 C until use. [24] with abundant P. reticulata and incidental R. hartii Several female P. reticulata (L 27.9 ± 2.9mm (mean ± populations. These two prey species are nearly ubiquitous in SD), N = 8) and juvenile R. hartii (L 25.4 ± 4.8mm streams in northern Trinidad but do not always cooccur [25]. (mean ± SD), N = 8) were retained from the pools of Although R. hartii may grow to as much as three times the wild-caught chemical cue donors to serve as visual prey International Journal of Zoology 3 Table 1: Effects of different combinations of cues from two prey species indicating potential foraging opportunities on the local abundance of three predatory species in a nested ANOVA with observation site nested within prey species . Treatment effects Nested effects Variance components Predator Prey cue F df P Nested factor FP Prey cue Prey species Site Visual 19.41 2,92 <0.0001 Prey species 1.02 0.3145 C. alta 73.1% 5.2% 21.7% Chemical 0.09 2,92 0.91 Site 0.05 0.8234 Visual 2.12 2,92 0.126 Prey species 0.92 0.3394 A. pulcher 65.4% 17.4% 17.2% Chemical 6.36 2,92 0.0026 Site 23.58 <0.0001 Visual 6.08 2,92 0.0033 Prey species 0.45 0.5036 A. bimaculatus 52.7% 47.3% 0% Chemical 19.21 2,92 <0.0001 Site 6.71 0.0108 The interactions between prey cue types were nonsignificant in all tests so the analyses were limited to main and nested effects only. cues. Subjects were transported to the observation site and model components on the variance in response using the placed singly into clear plastic bottles (250 mL) that had varcomp command in the ape library [33]. Secondarily, the been perforated to allow water exchange. The bottles were dataset was split into two parts by prey species and analyzed attached to 1 m lengths of wooden dowelling (1 cm diameter) as univariate two-way ANOVAs to enable direct comparisons by transparent fishing wire and held stationary in the water of the attractiveness of visual and chemical prey cues to column approximately 5 cm off the substrate. The bottles each predator species. Additionally, in order to examine the were also presented empty to serve as a control treatment possibility that the presence of the top predator, C. alta,at to the visual prey cues and provide estimates of ambient an observation site may have inhibited the attraction of the predator abundance in the presence of observers. Each site other predatory species to the area, predator species-pair (N = 16) was presented with the four combinations of counts were square-root transformed and compared using cues for each prey species (N = 8 trialsper site)for atotal Pearson’s correlation analyses. of N = 128 observations. 3. Results 2.3. Experimental Protocol and Analysis. Chemical stimuli consisting of 60 mL of either P. reticulata or R. hartii chemical 3.1. Predator Attraction. In no predator versus prey species cues (CC) or a stream water control (SW) were delivered by combination was there a significant interaction between syringe through 2 m lengths of airline tubing anchored by a chemical and visual prey cues on predator species counts rock (5 cm diameter) placed at the site of an observation. The (P> 0.05), so further analyses examined main effects of bottles containing the visual stimuli or visual control were prey cue types only. Results of two-way nested ANOVAs on introduced into the water column directly above the stimulus the attraction of each predatory species to the combinations injection sites. The apparatus was left in place for 1-minute of prey cues with observation site as a factor nested within prior to an observation to allow nearby fish to acclimate to prey species are presented in Table 1. Despite the likelihood its presence. Subsequent observations were conducted in an of a high degree of spatial heterogeneity in the distribution upstream direction to minimize the likelihood of attracting of predatory species in the Lower Aripo, observation site as additional predators from the downstream dispersion of the anestedfactoraccounted for ≤21.7% of the variability in chemical prey cues. mean predator counts (Table 1). The least spatial variability Following the 1 minute acclimation period, a stopwatch in predator counts was demonstrated by the highly active was activated to begin a 5-minute observation, throughout A. bimaculatus, with the less motile and solitary A. pulcher which the chemical stimuli or chemical controls were and C. alta demonstrating greater heterogeneity in their −1 delivered through the airline tubing at a rate of 10 mL min distributions throughout the study sites. and the numbers of individuals of the three predatory species The response patterns of each predator to the chemical within a 1 m radius of the cue presentation site were recorded and visual cue combinations appear to be similar for both P. every 15 seconds. These predator counts were then averaged reticulata and R. hartii cues (Figure 1). Prey species accounts by species over the 5-minute observation periods. A similar for 5–47% of the variance in mean predator counts within protocol has previously been used to examine the predator study areas with C. alta demonstrating the least difference in inspection behaviour of free-swimming P. reticulata under response between prey species and A. bimaculatus demon- field conditions [23]. The mean counts for each predatory strating the greatest difference (Table 1). Overall, there species were subsequently examined as univariate responses appears to be a nonstatistically significant preference for the in two-way nested ANOVAs with the chemical and visual P. reticulata cues as suggested by the greater mean counts prey cues as main effects, and replicated observation site of predators within an observation radius relative to the R. nested within prey species. All analyses were conducted as hartii cues (Figure 1). Prey cue treatments (main effects) linear mixed-effects lme models using the nlme statistical accounted for 52.7% of the variability in mean counts of A. package [31] for R (version 2.12.1; [32]). The models were bimaculatus and 73.1% of the variability in C. alta counts. As then decomposed to determine the relative influence of with the effect of prey species, the portions of variance in A. 4 International Journal of Zoology P. reticulata R. hartii 0.3 0.3 0.2 0.2 0.1 0.1 Control Guppy Control Rivulus Visual cue Visual cue (a) (b) 0.6 0.6 0.5 0.5 0.4 0.4 0.3 0.3 0.2 0.2 0.1 0.1 Control Guppy Control Rivulus Visual cue Visual cue (c) (d) 3 3 2.5 2.5 1.5 1.5 0.5 0.5 Control Guppy Control Rivulus Visual cue Visual cue CC SW (e) (f) Figure 1: Mean (±SE) number of predators present within a 1.5 m radius of prey cue presentation sites in the Lower Aripo over 5 minutes. Crenicichla alta attraction to (a) guppy Poecilia reticulata and (b) rivulus Rivulus hartii cues. Aequidens pulcher attraction to (c) guppy and (d) rivulus cues. Astyanax bimaculatus attraction to (e) guppy and (f) rivulus cues. Visual cues (horizontal axes) were paired with either conspecific chemical cues (shaded bars) or a stream water control (open bars). N = 16 for each cue combination. pulcher responses (65.4%) were intermediate relative to the is nonsignificant. Crenicichla alta did not demonstrate any other two predators. attraction to chemical cues from either prey species (P> As predicted by its primary foraging strategy, Crenicichla 0.05). This is in keeping with its foraging strategy of ambush alta, a visual ambush predator, was observed in greater hunting, as diffusive chemical cues may not reliably indicate numbers when presented with visual cues indicating foraging the location of potential prey to visual predators. opportunities of either P. reticulata (F = 24.3, P< Aequidens pulcher responded to both P. reticulata (F = 1,46 1,46 0.0001; Figure 1(a))or R. hartii (F = 8.78, P = 0.0057; 6.52, P = 0.014; Figure 1(c))and R. hartii (F = 6.25, P = 1,46 1,46 Figure 1(b)); although its response to P. reticulata visual cues 0.016; Figure 1(d)) chemical cues but not to the visual cues appears to be greater than to those of R. hartii, the difference of either prey species (P> 0.05). A significant response to A. bimaculatus A. pulcher C. alta A. bimaculatus A. pulcher C. alta International Journal of Zoology 5 r = 0.414 2 r = 0.298 2.5 1.5 1.5 0.5 0.5 0 0 0 0.2 0.4 0.6 0.8 0 0.2 0.4 0.6 0.8 C. alta C. alta (a) (b) Figure 2: Pearson’s correlation analyses of square-root transformed mean counts of Astyanax bimaculatus (a) and Aequidens pulcher (b) observed within 1 m radii of the prey cue introduction sites in the presence of the top predator, Crenicichla alta. Poecilia reticulata cues, closed points; Rivulus hartii cues, open points. Significant linear relationships (P< 0.05) are indicated by solid lines; nonsignificant relationships are indicated by dashed lines for illustrative purposes. the chemical but not the visual cues of both prey species more locally abundant prey species, P. reticulata, particularly is in keeping with the prediction that the importance of in the case of the top predator C. alta. chemical cues is greater than visual cues for a bottom-feeding The importance of foraging mode in determining the detritivore. relevance of prey cue type on predator behaviour in the Astyanax bimaculatus demonstrated a response to P. present study may provide an explanation for earlier find- reticulata visual cues (F = 11.7, P = 0.0013; Figure 1(e)) 1,46 ings that damage-released chemical cues did not function but not to R. hartii visual cues (P> 0.05) and responded as predator attractants. Specifically, Cashner [34]found to the chemical cues of both prey species (P. reticulata: that juvenile spotted bass Micropterus punctulatus did not F = 21.3, P< 0.0001; R. hartii: F = 16.9, P = 0.0002; 1,46 1,46 demonstrate an attraction to the chemical cues of a suite Figure 1(f)). Additionally, the response by A. bimaculatus of sympatric prey species. However, M. punctulatus may to complementary chemical and visual cues of both prey rely more on visual cues than chemical ones, as this species species appears to be approximately additive (Figures 1(e) tends to be actively foraging, solitary predators. Although and 1(f)). This social foraging species was alone in this study Chivers et al. [35] demonstrated attraction of the visually in demonstrating complementary responses to both types of foraging, ambush predator northern pike Esox lucius to sensory cues indicating the presence of potential prey. the chemical cues of fathead minnows Pimephales promelas; their experiment involved releasing chemical cues over a 30- 3.2. Predator Interactions. During trials involving P. retic- minute period. Similar experiments have been conducted ulata cues, the mean counts of C. alta were positively over even longer timescales (hours, [19]). The present study correlated with the counts of both A. bimaculatus (P = involves five-minute observations, which may be a more 0.0007; Figure 2(a))and A. pulcher (P = 0.017; Figure 2(b)). ecologically relevant timeframe due to the mechanism of Conversely, there were no relationships between the species- release and intransigence of damage-released chemical cues. pair counts in trials involving the cues of the less locally Interspecific trophic differences may also be insufficient to abundant R. hartii (Figure 2). predict responses to heterospecific chemical cues. In addition to intraspecific differences in predator behaviour and prey size preference [36], recent findings [2] have established a 4. Discussion relative size threshold between antipredator and foraging These results demonstrate the importance of foraging mode responses to damage-released chemical cues (predator L > in determining the relative influence of different types of prey 150% prey L ;[17]) as well as the ability of predators cues on predator behaviour and habitat use. Introducing to determine prey quality and condition from information conveyed by these cues. Earlier studies (e.g., [34]) may chemical and visual prey cues resulted in increased local abundances of predators, with the demonstrated responses have failed to include predators above such a relative size of each species to the cue combinations varying with the threshold or chemical cue donors of ideal size or condition and consequently were not able to elicit foraging responses primary foraging mode of a predator. Predators involved in this study appear to respond more strongly to cues of the in heterospecific receivers. A. bimaculatus A. pulcher 6 International Journal of Zoology As the top fish predator in this section of the Aripo sur la Nature et les Technologies (FQRNT) to C. K. Elvidge River [25], C. alta preys upon smaller individuals of both and the Natural Sciences and Engineering Research Council of the other predatory species involved in this study and of Canada (NSERC) to G. E. Brown. All work reported is likely to compete for forage opportunities with larger herein was conducted in accordance with the guidelines heterospecific size classes. Likely as a result of these predatory of the Canadian Council on Animal Care and the laws of and trophic interactions, A. bimaculatus and A. pulcher are Canada and was approved by the Concordia University rarely observed in close proximity to C. alta (personal obser- Animal Research Ethics Committee (Protocol no. AREC- vations), whose presence may indicate relatively high levels of 2008-BROW). risk. The presence of significant linear relationships between predator species-pair counts in response to P. reticulata cues References and insignificant relationships in response to R. hartii cues is consistent with the notion that predators generally display [1] E. Danchin, L. A. Giraldeau, T. J. Valone, and R. H. Wagner, greater attraction responses to the cues of more abundant “Public information: from nosy neighbors to cultural evolu- tion,” Science, vol. 305, no. 5683, pp. 487–491, 2004. or familiar prey species. This observation may imply that A. [2] C. K. Elvidge, I. W. Ramnarine, J. G. J. Godin, and G. E. Brown, bimaculatus and A. pulcher adopt riskier foraging strategies “Size-mediated response to public cues of predation risk in a and enter potentially more dangerous areas when presented tropical stream fish,” Journal of Fish Biology,vol. 77, no.7,pp. with more familiar foraging opportunities, increasing the 1632–1644, 2010. likelihood of encountering C. alta and potentially incurring [3] T. W. Cronin, “The visual ecology of predator-prey interac- the risks of interspecific competition and/or predation. An tions,” in Behavioural Ecology of Teleost Fishes, J. G. J. Godin, adaptationist hypothesis for the evolution of this damage- Ed., pp. 105–138, Oxford University Press, Oxford, UK, 1997. released chemical signalling system is that, in addition to [4] J.W.Kim,G.E.Brown,I.J.Dolinsek,N.N.Brodeur,A.O.H. the survival benefits accrued to conspecific chemical cue C. Leduc, and J. W. A. Grant, “Combined effects of chemical receivers through antipredator behavioural responses, chem- and visual information in eliciting antipredator behaviour in ical signalling may be advantageous to the sender by attract- juvenile Atlantic salmon Salmo salar,” Journal of Fish Biology, ing secondary predators [15]. The differences in localized vol. 74, no. 6, pp. 1280–1290, 2009. [5] B.A.Hazlett andC.McLay,“Responsestopredation risk:al- species-pair abundances in response to less familiar prey cues ternative strategies in the crab Heterozius rotundifrons,” Animal described above lend some support to this predator attrac- Behaviour, vol. 69, no. 4, pp. 967–972, 2005. tion/interference hypothesis, in that predators of lower [6] J. M. Hemmi, “Predator avoidance in fiddler crabs: 2. The trophic levels appear to avoid predators or competitors of visual cues,” Animal Behaviour, vol. 69, no. 3, pp. 615–625, higher trophic levels, sacrificing foraging opportunities in the process. [7] B. D. Wisenden, J. Pogatshnik, D. Gibson, L. Bonacci, A. Schu- Prey fishes may experience increased mortality under macher, and A. Willett, “Sound the alarm: learned association conditions which eliminate sources of information on the of predation risk with novel auditory stimuli by fathead level of predation risk (e.g., damage-released chemical cues minnows (Pimephales promelas)and glowlighttetras(Hemi- lose functionality at pH < 6.6; [37]). The attraction of grammus erythrozonus) after single simultaneous pairings with predators to heterospecific chemical cues demonstrated in conspecific chemical alarm cues,” Environmental Biology of Fishes, vol. 81, no. 2, pp. 141–147, 2008. the current study suggests that predators may be similarly [8] M. C. O. Ferrari, B. D. Wisenden, and D. P. Chivers, “Chemical deprived of information on the presence and quality of for- ecology of predator-prey interactions in aquatic ecosystems: a aging opportunities under certain environmental conditions. review and prospectus,” Canadian Journal of Zoology, vol. 88, Predators similarly deprived of sensory information may no. 7, pp. 698–724, 2010. consequently experience negative fitness consequences. The [9] R. J. F. Smith, “Avoiding and deterring predators,” in Behav- differences in response in predator species and species-pairs ioural Ecology of Teleost Fishes, J. G. J. Godin, Ed., pp. 163–190, to cues from different prey suggest directions for further Oxford University Press, Oxford, UK, 1997. research into both the fitness benefits accrued from the use [10] J. L. Golub, V. Vermette, and G. E. Brown, “Response to con- of information on prey availability as well as the interactions specific and heterospecific alarm cues by pumpkinseeds in between predator species in the context of predator interfer- simple and complex habitats: field verification of an ontoge- ence. netic shift,” Journal of Fish Biology, vol. 66, no. 4, pp. 1073– 1081, 2005. [11] G. E. Brown and R. J. F. Smith, “Conspecific skin extracts elicit Acknowledgments antipredator responses in juvenile rainbow trout (Oncorhyn- chus mykiss),” Canadian Journal of Zoology, vol. 75, no. 11, pp. The authors wish to thank the Director of Fisheries in 1916–1922, 1997. the Trinidadian Ministry of Agriculture, Land and Marine [12] G. E. Brown, D. P. Chivers, and R. J. Smith, “Localized def- Resources for permission to collect fish for use in this study. ecation by pike: a response to labelling by cyprinid alarm They also thank J.-G. J. Godin and I. W. Ramnarine for pheromone?” Behavioral Ecology and Sociobiology, vol. 36, no. discussions on experimental design and potential locations 2, pp. 105–110, 1995. forthe presentstudy andC.J.Macnaughton,P.H.Malka, [13] B. D. Wisenden, J. Karst, J. Miller, S. Miller, and L. Fuselier, and two anonymous reviewers for comments on an earlier “Anti-predator behaviour in response to conspecific chemical version of this paper. Financial support was provided by alarm cues in an esociform fish, Umbra limi (Kirtland 1840),” Concordia University, le Fonds queb ´ ec ´ ois de la Recherche´ Environmental Biology of Fishes, vol. 82, no. 1, pp. 85–92, 2008. International Journal of Zoology 7 [14] G. E. Brown and J. G. J. Godin, “Chemical alarm signals in wild [32] R Development Core Team, R: A Language and Environment Trinidadian guppies (Poecilia reticulata),” Canadian Journal of for Statistical Computing, R Foundation for Statistical Com- Zoology, vol. 77, no. 4, pp. 562–570, 1999. puting, Vienna, Austria, 2010. [15] R. J. F. Smith, “Alarm signals in fishes,” Reviews in Fish Biology [33] E. Paradis,J.Claude, andK.Strimmer, “APE:analysesof and Fisheries, vol. 2, no. 1, pp. 33–63, 1992. phylogenetics and evolution in R language,” Bioinformatics, vol. 20, no. 2, pp. 289–290, 2004. [16] M. C. Harvey and G. E. Brown, “Dine or dash?: ontogenetic shift in the response of yellow perch to conspecific alarm cues,” [34] M. F. Cashner, “Are spotted bass (Micropterus punctulatus) Environmental Biology of Fishes, vol. 70, no. 4, pp. 345–352, attracted to Schreckstoff? A test of the predator attraction hy- 2004. pothesis,” Copeia, no. 3, pp. 592–598, 2004. [17] O. A. Popova, “The role of predaceous fish in ecosystems,” in [35] D. P. Chivers, G. E. Brown, and R. J. F. Smith, “The evolution Ecology of Freshwater Fish Production,S.D.Gerking,Ed.,pp. of chemical alarm signals: attracting predators benefits alarm 215–249, Blackwell Scientific, Oxford, UK, 1978. signal senders,” American Naturalist, vol. 148, no. 4, pp. 649– 659, 1996. [18] G. E. Brown, V. J. Leblanc, and L. E. Porter, “Ontogenetic changes in the response of largemouth bass (Micropterus sal- [36] P. A. Nilsson and C. Bronmark, “Prey vulnerability to a gape- moides, Centrarchidae, Perciformes) to heterospecific alarm size limited predator: behavioural and morphological impacts pheromones,” Ethology, vol. 107, no. 5, pp. 401–414, 2001. on Northern pike piscivory,” Oikos, vol. 88, no. 3, pp. 539–546, [19] B. D. Wisenden and T. A. Thiel, “Field verification of predator attraction to minnow alarm substance,” Journal of Chemical [37] A. O. H. C. Leduc, J. M. Kelly, andG.E.Brown,“Detection Ecology, vol. 28, no. 2, pp. 433–438, 2002. of conspecific alarm cues by juvenile salmonids under neutral and weakly acidic conditions: laboratory and field tests,” Oe- [20] S. L. Lima and L. M. Dill, “Behavioral decisions made under cologia, vol. 139, no. 2, pp. 318–324, 2004. the risk of predation: a review and prospectus,” Canadian Jour- nal of Zoology, vol. 68, no. 4, pp. 619–640, 1990. [21] A. Mathis, D. P. Chivers, and R. J. Smith, “Chemicl alarm signals: predator deterrents or predator attractants?” American Naturalist, vol. 145, no. 6, pp. 994–1005, 1995. [22] O. M. Lonnstedt, M. I. McCormick, and D. P. Chivers, “Well- informed foraging: damage-released chemical cues of injured prey signal quality and size to predators,” Oecologia, vol. 168, no. 3, pp. 651–658, 2012. [23] G. E. Brown, C. K. Elvidge, C. J. Macnaughton, I. Ramnarine, and J. G. J. Godin, “Cross-population responses to conspecific chemical alarm cues in wild Trinidadian guppies, Poecilia reticulata: evidence for local conservation of cue production,” Canadian Journal of Zoology, vol. 88, no. 2, pp. 139–147, 2010. [24] D. P. Croft, L. J. Morrell, A. S. Wade et al., “Predation risk as a driving force for sexual segregation: a cross-population comparison,” American Naturalist, vol. 167, no. 6, pp. 867– 878, 2006. [25] A. E. Magurran, Evolutionary Ecology: The Trinidadian Guppy, Oxford University Press, Oxford, UK, 2005. [26] R. Froese and D. Pauly, “FishBase. 2011,” World Wide Web electronic publication, (01/2010)http://www.fishbase.org/. [27] J. Krause and J. G. J. Godin, “Predator preferences for attacking particular prey group sizes: consequences for predator hunting success and prey predation risk,” Animal Behaviour, vol. 50, no. 2, pp. 465–473, 1995. [28] K. E. Esteves, “Feeding ecology of three Astyanax species (Characidae, Tetragonopterinae) from a floodplain lake of Mogi-Guacu River, Parana River Basin, Brazil,” Environmental Biology of Fishes, vol. 46, no. 1, pp. 83–101, 1996. [29] B. H. Seghers, An analysis of geographic variation in the anti- predator adaptations of the guppy, Poecilia reticulata [Ph.D. the- sis], Department of Zoology, University of British Columbia, Vancouver BC, Canada, 1973. [30] G. E. Brown, C. J. MacNaughton, C. K. Elvidge, I. Ramnarine, and J. G. J. Godin, “Provenance and threat-sensitive predator avoidance patterns in wild-caught Trinidadian guppies,” Be- havioral Ecology and Sociobiology, vol. 63, no. 5, pp. 699–706, [31] J. Pinheiro, D. Bates, S. DebRoy, D. Sarkar, and R Development Core Team, “nlme: Linear and Nonlinear Mixed Effects Models,” R package version 3.1-97, 2010. 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Visual and Chemical Prey Cues as Complementary Predator Attractants in a Tropical Stream Fish Assemblage

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Copyright © 2012 Chris K. Elvidge and Grant E. Brown. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
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10.1155/2012/510920
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Hindawi Publishing Corporation International Journal of Zoology Volume 2012, Article ID 510920, 7 pages doi:10.1155/2012/510920 Research Article Visual and Chemical Prey Cues as Complementary Predator Attractants in a Tropical Stream Fish Assemblage Chris K. Elvidge and Grant E. Brown Department of Biology, Concordia University, 7141 Sherbrooke St. West, Montreal, QC, Canada H4B 1R6 Correspondence should be addressed to Chris K. Elvidge, chris.k.elvidge@gmail.com Received 27 March 2012; Revised 25 April 2012; Accepted 30 April 2012 Academic Editor: Marie Herberstein Copyright © 2012 C. K. Elvidge and G. E. Brown. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. To date, little attention has been devoted to possible complementary effects of multiple forms of public information similar information on the foraging behaviour of predators. In order to examine how predators may incorporate multiple information sources, we conducted a series of predator attraction trials in the Lower Aripo River, Trinidad. Four combinations of visual (present or absent) and chemical cues (present or absent) from each of two prey species were presented. The occurrences of three locally abundant predatory species present within a 1 m radius of cue introduction sites were recorded. The relative attractiveness of cue type to each predator was directly related to their primary foraging modes, with visual ambush predators demonstrating an attraction to visual cues, benthivores to chemical cues, and active social foragers demonstrating complementary responses to paired cues. Predator species-pair counts were greatest in response to cues from the more abundant prey species, indicating that individuals may adopt riskier foraging strategies when presented with more familiar prey cues. These differences in predator attraction patterns demonstrate complementary effects of multiple sensory cues on the short-term habitat use and foraging behaviour of predators under fully natural conditions. 1. Introduction limited under conditions of relatively high background noise, as in lotic systems. The behavioural strategies adopted by participants in pre- Many groups of freshwater fishes produce chemical cues dator-prey interactions are often mediated by publicly avail- in the epidermis which are released into the water following able cues [1] conveying information with some degree of mechanical damage, as would occur during a predation immediate contextual relevance to the receiver. Public, or event [8]. Upon detection by conspecific receivers, these cues non-species-specific, cues may convey qualitatively different have been shown to elicit a suite of antipredator or alarm information to and elicit quantitatively different behavioural responses [9]incentrarchid [10], salmonid [11], cyprinid responses from different receivers [2]. Therelativeimpor- [12], cyprinodontiform [2], esocid [13], and poeciliid [14] tance of different types of public cues in predator-prey inter- species. Due to their manner of release, these chemical cues actions may be mediated by interactions between receiver cannot be manipulated by a predator and likely serve as taxon and environmental constraints; for example, visual reliable indicators of increased risk to receivers subject to cues are typically limited by photoperiod [3]. In aquatic similar predation pressures [15], which is not always the environments, visual and chemical cues have been identified case with potentially misleading visual cues [3]. Damage- as the primary sources of information eliciting short-term released chemical cues have been shown to elicit different behavioural processes for both vertebrate (e.g., fishes, [4]) responses from conspecific receivers differing in ontogenetic and invertebrate (e.g., crustaceans, [5, 6]) species. Although stage from the cue sender [16], with similarly sized receivers acoustic cues have been demonstrated to elicit behavioural demonstrating alarm or antipredator responses and larger responses in freshwater fish receivers under laboratory receivers demonstrating behaviours consistent with foraging conditions [7], the reliability of acoustic information may be responses under laboratory conditions. Similar effects have 2 International Journal of Zoology been observed in heterospecific receivers belonging to the length of P. reticulata (R. hartii maximum standard length, same prey guild and subject to similar predation risks as L , 100 mm, P. reticulata common L 28 mm; [26]) and P. S S chemical cue senders [17, 18]. Conversely, heterospecific reticulata can account for up to 10% of the diet of large R. receivers of larger size than the sender have demonstrated hartii, in the presence of piscivores similarly sized P. reticulata foraging responses following exposure to damage-released and R. hartii are likely subject to similar predation pressures chemical cues under both laboratory [18] and field [19] [17]. conditions. Of the three predatory species examined, the pike cichlid Due to the potentially ultimate costs incurred by failing Crenicichla alta is a solitary, visually foraging ambush pre- to respond to ambient cues indicating elevated predation dator and obligate piscivore which is considered the main risk, the responses of prey to public cues have thus far predator of P. reticulata in Trinidad whenever they co-occur received considerably more attention from researchers than [25]. The blue acara cichlid Aequidens pulcher is a solitary have responses by predators [20]. In freshwater fishes, labo- forager which typically feeds on invertebrates and benthos, ratory experiments have documented attraction responses to displaying only opportunistic piscivory [27]. The two-spot chemical cues from heterospecific prey [21], while predators sardine Astyanax bimaculatus, by contrast, is a highly social under natural conditions have demonstrated preferences and active forager [23, 26], whose predominantly algae- for areas labelled with damage-released chemical cues over and insect-based diet undergoes an ontogenetic switch to longer time scales (hours, [19]). Recently, Lonnstedt et include opportunistic piscivory when individuals exceed al. [22]demonstratedanattractionresponseinapreda- ∼50 mm total length [28]. These three species likely account tory coral reef fish, the dottyback Pseudochromis fuscus to for the majority of predation pressure on P. reticulata and heterospecific damage-released chemical cues under fully any incidental R. hartii within the study area [29]. Based natural conditions over short (minutes) timescales. In on these differences in social behaviour and foraging mode, addition, under both natural and laboratory conditions, P. we predict that A. bimaculatus incorporates information fuscus demonstrated a strong preference for chemical cues received through both visual and chemical cues into their extracted from heterospecific donors belonging to the ideal foraging decisions, while A. pulcher responds more strongly prey size class [22] for gape-limited predators [17]. Similarly, to chemical than to visual cues and C. alta responds primarily Elvidge et al. [2] demonstrated significant positive linear to visual cues. relationships between foraging behaviours and receiver size in an opportunistic predator, Hart’s rivulus Rivulus hartii,in response to chemical cues from Trinidadian guppies Poecilia 2.2. Prey Cues. Damage-released chemical cues were extract- reticulata. Together, these results indicate that damage- ed from female P. reticulata (L 27.6 ± 2.7mm (mean ± released chemical cues provide predators with information SD), N = 18) and R. hartii (L 42 ± 7.9 mm (mean ± SD), about the availability and quality of potential prey. N = 8) donors collected from the Naranja River tributary ◦  ◦ In order to examine the effects of different combinations (10 41 N; 61 14 W) approximately 6 km upstream from the of visual and chemical cues indicating the availability of prey observation sites in the Lower Aripo River using a beach seine on the behaviour of predators in fresh water, the present net (length 2.5 m, height 1 m, mesh size 3 mm). Donors were study focused on short-term changes in local abundances of collected from the Naranja River because intensive sampling three predatory species differing in foraging modes to the via seine net did not find any R. hartii present at the study cues of two cooccurring prey species. In general, we predict sites in the Lower Aripo during the course of the present that multiple complementary cues indicating the presence of experiment. Chemical cues from P. reticulata donors from familiar prey species will result in greater local abundances of the Naranja River have previously been demonstrated to predators, with the relative contribution of each type of cue elicit qualitatively similar responses to those of Lower Aripo (visual or chemical) mediated by the typical foraging mode donors [23] in conspecific receivers from either population. of the predator. Chemical cue donors were euthanized via cervical dis- location, measured (L ), immediately decapitated behind the opercula, and had their tails removed at the caudal peduncle. Visceral tissues were manually extruded, and 2. Materials and Methods the remaining carcasses were mechanically homogenized in 2.1. Study Species and Area. Predator attraction trials were dechlorinated tap water, diluted to a final concentration of 2 −1 conducted at N = 16 sites in a series of eight pools (two sites 0.1 cm skin mL , and filtered through polyester floss. This per pool) along a 1 km stretch of the Lower Aripo River in concentration of skin extract has previously been shown to the Caroni drainage, Northern Range Mountains, Trinidad elicit both antipredator and foraging behavioural responses ◦  ◦ and Tobago, W. I. (10 39 N, 61 13 W) 04–12 May 2009. in tropical stream fish under laboratory [30] and field [23] These pools have been described in an earlier study involving conditions. The chemical cues from each prey species, as well free-swimming Trinidadian guppies P. reticulata [23]. The as a stream water control treatment, were packaged in 60 mL Lower Aripo is a species-rich, high-predation environment aliquots and frozen at −20 C until use. [24] with abundant P. reticulata and incidental R. hartii Several female P. reticulata (L 27.9 ± 2.9mm (mean ± populations. These two prey species are nearly ubiquitous in SD), N = 8) and juvenile R. hartii (L 25.4 ± 4.8mm streams in northern Trinidad but do not always cooccur [25]. (mean ± SD), N = 8) were retained from the pools of Although R. hartii may grow to as much as three times the wild-caught chemical cue donors to serve as visual prey International Journal of Zoology 3 Table 1: Effects of different combinations of cues from two prey species indicating potential foraging opportunities on the local abundance of three predatory species in a nested ANOVA with observation site nested within prey species . Treatment effects Nested effects Variance components Predator Prey cue F df P Nested factor FP Prey cue Prey species Site Visual 19.41 2,92 <0.0001 Prey species 1.02 0.3145 C. alta 73.1% 5.2% 21.7% Chemical 0.09 2,92 0.91 Site 0.05 0.8234 Visual 2.12 2,92 0.126 Prey species 0.92 0.3394 A. pulcher 65.4% 17.4% 17.2% Chemical 6.36 2,92 0.0026 Site 23.58 <0.0001 Visual 6.08 2,92 0.0033 Prey species 0.45 0.5036 A. bimaculatus 52.7% 47.3% 0% Chemical 19.21 2,92 <0.0001 Site 6.71 0.0108 The interactions between prey cue types were nonsignificant in all tests so the analyses were limited to main and nested effects only. cues. Subjects were transported to the observation site and model components on the variance in response using the placed singly into clear plastic bottles (250 mL) that had varcomp command in the ape library [33]. Secondarily, the been perforated to allow water exchange. The bottles were dataset was split into two parts by prey species and analyzed attached to 1 m lengths of wooden dowelling (1 cm diameter) as univariate two-way ANOVAs to enable direct comparisons by transparent fishing wire and held stationary in the water of the attractiveness of visual and chemical prey cues to column approximately 5 cm off the substrate. The bottles each predator species. Additionally, in order to examine the were also presented empty to serve as a control treatment possibility that the presence of the top predator, C. alta,at to the visual prey cues and provide estimates of ambient an observation site may have inhibited the attraction of the predator abundance in the presence of observers. Each site other predatory species to the area, predator species-pair (N = 16) was presented with the four combinations of counts were square-root transformed and compared using cues for each prey species (N = 8 trialsper site)for atotal Pearson’s correlation analyses. of N = 128 observations. 3. Results 2.3. Experimental Protocol and Analysis. Chemical stimuli consisting of 60 mL of either P. reticulata or R. hartii chemical 3.1. Predator Attraction. In no predator versus prey species cues (CC) or a stream water control (SW) were delivered by combination was there a significant interaction between syringe through 2 m lengths of airline tubing anchored by a chemical and visual prey cues on predator species counts rock (5 cm diameter) placed at the site of an observation. The (P> 0.05), so further analyses examined main effects of bottles containing the visual stimuli or visual control were prey cue types only. Results of two-way nested ANOVAs on introduced into the water column directly above the stimulus the attraction of each predatory species to the combinations injection sites. The apparatus was left in place for 1-minute of prey cues with observation site as a factor nested within prior to an observation to allow nearby fish to acclimate to prey species are presented in Table 1. Despite the likelihood its presence. Subsequent observations were conducted in an of a high degree of spatial heterogeneity in the distribution upstream direction to minimize the likelihood of attracting of predatory species in the Lower Aripo, observation site as additional predators from the downstream dispersion of the anestedfactoraccounted for ≤21.7% of the variability in chemical prey cues. mean predator counts (Table 1). The least spatial variability Following the 1 minute acclimation period, a stopwatch in predator counts was demonstrated by the highly active was activated to begin a 5-minute observation, throughout A. bimaculatus, with the less motile and solitary A. pulcher which the chemical stimuli or chemical controls were and C. alta demonstrating greater heterogeneity in their −1 delivered through the airline tubing at a rate of 10 mL min distributions throughout the study sites. and the numbers of individuals of the three predatory species The response patterns of each predator to the chemical within a 1 m radius of the cue presentation site were recorded and visual cue combinations appear to be similar for both P. every 15 seconds. These predator counts were then averaged reticulata and R. hartii cues (Figure 1). Prey species accounts by species over the 5-minute observation periods. A similar for 5–47% of the variance in mean predator counts within protocol has previously been used to examine the predator study areas with C. alta demonstrating the least difference in inspection behaviour of free-swimming P. reticulata under response between prey species and A. bimaculatus demon- field conditions [23]. The mean counts for each predatory strating the greatest difference (Table 1). Overall, there species were subsequently examined as univariate responses appears to be a nonstatistically significant preference for the in two-way nested ANOVAs with the chemical and visual P. reticulata cues as suggested by the greater mean counts prey cues as main effects, and replicated observation site of predators within an observation radius relative to the R. nested within prey species. All analyses were conducted as hartii cues (Figure 1). Prey cue treatments (main effects) linear mixed-effects lme models using the nlme statistical accounted for 52.7% of the variability in mean counts of A. package [31] for R (version 2.12.1; [32]). The models were bimaculatus and 73.1% of the variability in C. alta counts. As then decomposed to determine the relative influence of with the effect of prey species, the portions of variance in A. 4 International Journal of Zoology P. reticulata R. hartii 0.3 0.3 0.2 0.2 0.1 0.1 Control Guppy Control Rivulus Visual cue Visual cue (a) (b) 0.6 0.6 0.5 0.5 0.4 0.4 0.3 0.3 0.2 0.2 0.1 0.1 Control Guppy Control Rivulus Visual cue Visual cue (c) (d) 3 3 2.5 2.5 1.5 1.5 0.5 0.5 Control Guppy Control Rivulus Visual cue Visual cue CC SW (e) (f) Figure 1: Mean (±SE) number of predators present within a 1.5 m radius of prey cue presentation sites in the Lower Aripo over 5 minutes. Crenicichla alta attraction to (a) guppy Poecilia reticulata and (b) rivulus Rivulus hartii cues. Aequidens pulcher attraction to (c) guppy and (d) rivulus cues. Astyanax bimaculatus attraction to (e) guppy and (f) rivulus cues. Visual cues (horizontal axes) were paired with either conspecific chemical cues (shaded bars) or a stream water control (open bars). N = 16 for each cue combination. pulcher responses (65.4%) were intermediate relative to the is nonsignificant. Crenicichla alta did not demonstrate any other two predators. attraction to chemical cues from either prey species (P> As predicted by its primary foraging strategy, Crenicichla 0.05). This is in keeping with its foraging strategy of ambush alta, a visual ambush predator, was observed in greater hunting, as diffusive chemical cues may not reliably indicate numbers when presented with visual cues indicating foraging the location of potential prey to visual predators. opportunities of either P. reticulata (F = 24.3, P< Aequidens pulcher responded to both P. reticulata (F = 1,46 1,46 0.0001; Figure 1(a))or R. hartii (F = 8.78, P = 0.0057; 6.52, P = 0.014; Figure 1(c))and R. hartii (F = 6.25, P = 1,46 1,46 Figure 1(b)); although its response to P. reticulata visual cues 0.016; Figure 1(d)) chemical cues but not to the visual cues appears to be greater than to those of R. hartii, the difference of either prey species (P> 0.05). A significant response to A. bimaculatus A. pulcher C. alta A. bimaculatus A. pulcher C. alta International Journal of Zoology 5 r = 0.414 2 r = 0.298 2.5 1.5 1.5 0.5 0.5 0 0 0 0.2 0.4 0.6 0.8 0 0.2 0.4 0.6 0.8 C. alta C. alta (a) (b) Figure 2: Pearson’s correlation analyses of square-root transformed mean counts of Astyanax bimaculatus (a) and Aequidens pulcher (b) observed within 1 m radii of the prey cue introduction sites in the presence of the top predator, Crenicichla alta. Poecilia reticulata cues, closed points; Rivulus hartii cues, open points. Significant linear relationships (P< 0.05) are indicated by solid lines; nonsignificant relationships are indicated by dashed lines for illustrative purposes. the chemical but not the visual cues of both prey species more locally abundant prey species, P. reticulata, particularly is in keeping with the prediction that the importance of in the case of the top predator C. alta. chemical cues is greater than visual cues for a bottom-feeding The importance of foraging mode in determining the detritivore. relevance of prey cue type on predator behaviour in the Astyanax bimaculatus demonstrated a response to P. present study may provide an explanation for earlier find- reticulata visual cues (F = 11.7, P = 0.0013; Figure 1(e)) 1,46 ings that damage-released chemical cues did not function but not to R. hartii visual cues (P> 0.05) and responded as predator attractants. Specifically, Cashner [34]found to the chemical cues of both prey species (P. reticulata: that juvenile spotted bass Micropterus punctulatus did not F = 21.3, P< 0.0001; R. hartii: F = 16.9, P = 0.0002; 1,46 1,46 demonstrate an attraction to the chemical cues of a suite Figure 1(f)). Additionally, the response by A. bimaculatus of sympatric prey species. However, M. punctulatus may to complementary chemical and visual cues of both prey rely more on visual cues than chemical ones, as this species species appears to be approximately additive (Figures 1(e) tends to be actively foraging, solitary predators. Although and 1(f)). This social foraging species was alone in this study Chivers et al. [35] demonstrated attraction of the visually in demonstrating complementary responses to both types of foraging, ambush predator northern pike Esox lucius to sensory cues indicating the presence of potential prey. the chemical cues of fathead minnows Pimephales promelas; their experiment involved releasing chemical cues over a 30- 3.2. Predator Interactions. During trials involving P. retic- minute period. Similar experiments have been conducted ulata cues, the mean counts of C. alta were positively over even longer timescales (hours, [19]). The present study correlated with the counts of both A. bimaculatus (P = involves five-minute observations, which may be a more 0.0007; Figure 2(a))and A. pulcher (P = 0.017; Figure 2(b)). ecologically relevant timeframe due to the mechanism of Conversely, there were no relationships between the species- release and intransigence of damage-released chemical cues. pair counts in trials involving the cues of the less locally Interspecific trophic differences may also be insufficient to abundant R. hartii (Figure 2). predict responses to heterospecific chemical cues. In addition to intraspecific differences in predator behaviour and prey size preference [36], recent findings [2] have established a 4. Discussion relative size threshold between antipredator and foraging These results demonstrate the importance of foraging mode responses to damage-released chemical cues (predator L > in determining the relative influence of different types of prey 150% prey L ;[17]) as well as the ability of predators cues on predator behaviour and habitat use. Introducing to determine prey quality and condition from information conveyed by these cues. Earlier studies (e.g., [34]) may chemical and visual prey cues resulted in increased local abundances of predators, with the demonstrated responses have failed to include predators above such a relative size of each species to the cue combinations varying with the threshold or chemical cue donors of ideal size or condition and consequently were not able to elicit foraging responses primary foraging mode of a predator. Predators involved in this study appear to respond more strongly to cues of the in heterospecific receivers. A. bimaculatus A. pulcher 6 International Journal of Zoology As the top fish predator in this section of the Aripo sur la Nature et les Technologies (FQRNT) to C. K. Elvidge River [25], C. alta preys upon smaller individuals of both and the Natural Sciences and Engineering Research Council of the other predatory species involved in this study and of Canada (NSERC) to G. E. Brown. All work reported is likely to compete for forage opportunities with larger herein was conducted in accordance with the guidelines heterospecific size classes. Likely as a result of these predatory of the Canadian Council on Animal Care and the laws of and trophic interactions, A. bimaculatus and A. pulcher are Canada and was approved by the Concordia University rarely observed in close proximity to C. alta (personal obser- Animal Research Ethics Committee (Protocol no. AREC- vations), whose presence may indicate relatively high levels of 2008-BROW). risk. The presence of significant linear relationships between predator species-pair counts in response to P. reticulata cues References and insignificant relationships in response to R. hartii cues is consistent with the notion that predators generally display [1] E. Danchin, L. A. Giraldeau, T. J. Valone, and R. H. Wagner, greater attraction responses to the cues of more abundant “Public information: from nosy neighbors to cultural evolu- tion,” Science, vol. 305, no. 5683, pp. 487–491, 2004. or familiar prey species. This observation may imply that A. [2] C. K. Elvidge, I. W. Ramnarine, J. G. J. Godin, and G. E. Brown, bimaculatus and A. pulcher adopt riskier foraging strategies “Size-mediated response to public cues of predation risk in a and enter potentially more dangerous areas when presented tropical stream fish,” Journal of Fish Biology,vol. 77, no.7,pp. with more familiar foraging opportunities, increasing the 1632–1644, 2010. likelihood of encountering C. alta and potentially incurring [3] T. W. Cronin, “The visual ecology of predator-prey interac- the risks of interspecific competition and/or predation. An tions,” in Behavioural Ecology of Teleost Fishes, J. G. J. Godin, adaptationist hypothesis for the evolution of this damage- Ed., pp. 105–138, Oxford University Press, Oxford, UK, 1997. released chemical signalling system is that, in addition to [4] J.W.Kim,G.E.Brown,I.J.Dolinsek,N.N.Brodeur,A.O.H. the survival benefits accrued to conspecific chemical cue C. Leduc, and J. W. A. Grant, “Combined effects of chemical receivers through antipredator behavioural responses, chem- and visual information in eliciting antipredator behaviour in ical signalling may be advantageous to the sender by attract- juvenile Atlantic salmon Salmo salar,” Journal of Fish Biology, ing secondary predators [15]. The differences in localized vol. 74, no. 6, pp. 1280–1290, 2009. [5] B.A.Hazlett andC.McLay,“Responsestopredation risk:al- species-pair abundances in response to less familiar prey cues ternative strategies in the crab Heterozius rotundifrons,” Animal described above lend some support to this predator attrac- Behaviour, vol. 69, no. 4, pp. 967–972, 2005. tion/interference hypothesis, in that predators of lower [6] J. M. Hemmi, “Predator avoidance in fiddler crabs: 2. The trophic levels appear to avoid predators or competitors of visual cues,” Animal Behaviour, vol. 69, no. 3, pp. 615–625, higher trophic levels, sacrificing foraging opportunities in the process. [7] B. D. Wisenden, J. Pogatshnik, D. Gibson, L. Bonacci, A. Schu- Prey fishes may experience increased mortality under macher, and A. Willett, “Sound the alarm: learned association conditions which eliminate sources of information on the of predation risk with novel auditory stimuli by fathead level of predation risk (e.g., damage-released chemical cues minnows (Pimephales promelas)and glowlighttetras(Hemi- lose functionality at pH < 6.6; [37]). The attraction of grammus erythrozonus) after single simultaneous pairings with predators to heterospecific chemical cues demonstrated in conspecific chemical alarm cues,” Environmental Biology of Fishes, vol. 81, no. 2, pp. 141–147, 2008. the current study suggests that predators may be similarly [8] M. C. O. Ferrari, B. D. Wisenden, and D. P. Chivers, “Chemical deprived of information on the presence and quality of for- ecology of predator-prey interactions in aquatic ecosystems: a aging opportunities under certain environmental conditions. review and prospectus,” Canadian Journal of Zoology, vol. 88, Predators similarly deprived of sensory information may no. 7, pp. 698–724, 2010. consequently experience negative fitness consequences. The [9] R. J. F. Smith, “Avoiding and deterring predators,” in Behav- differences in response in predator species and species-pairs ioural Ecology of Teleost Fishes, J. G. J. Godin, Ed., pp. 163–190, to cues from different prey suggest directions for further Oxford University Press, Oxford, UK, 1997. research into both the fitness benefits accrued from the use [10] J. L. Golub, V. Vermette, and G. E. Brown, “Response to con- of information on prey availability as well as the interactions specific and heterospecific alarm cues by pumpkinseeds in between predator species in the context of predator interfer- simple and complex habitats: field verification of an ontoge- ence. netic shift,” Journal of Fish Biology, vol. 66, no. 4, pp. 1073– 1081, 2005. [11] G. E. Brown and R. J. F. Smith, “Conspecific skin extracts elicit Acknowledgments antipredator responses in juvenile rainbow trout (Oncorhyn- chus mykiss),” Canadian Journal of Zoology, vol. 75, no. 11, pp. The authors wish to thank the Director of Fisheries in 1916–1922, 1997. the Trinidadian Ministry of Agriculture, Land and Marine [12] G. E. Brown, D. P. Chivers, and R. J. Smith, “Localized def- Resources for permission to collect fish for use in this study. ecation by pike: a response to labelling by cyprinid alarm They also thank J.-G. J. Godin and I. W. Ramnarine for pheromone?” Behavioral Ecology and Sociobiology, vol. 36, no. discussions on experimental design and potential locations 2, pp. 105–110, 1995. forthe presentstudy andC.J.Macnaughton,P.H.Malka, [13] B. D. Wisenden, J. Karst, J. Miller, S. Miller, and L. Fuselier, and two anonymous reviewers for comments on an earlier “Anti-predator behaviour in response to conspecific chemical version of this paper. Financial support was provided by alarm cues in an esociform fish, Umbra limi (Kirtland 1840),” Concordia University, le Fonds queb ´ ec ´ ois de la Recherche´ Environmental Biology of Fishes, vol. 82, no. 1, pp. 85–92, 2008. International Journal of Zoology 7 [14] G. E. Brown and J. G. J. Godin, “Chemical alarm signals in wild [32] R Development Core Team, R: A Language and Environment Trinidadian guppies (Poecilia reticulata),” Canadian Journal of for Statistical Computing, R Foundation for Statistical Com- Zoology, vol. 77, no. 4, pp. 562–570, 1999. puting, Vienna, Austria, 2010. [15] R. J. F. Smith, “Alarm signals in fishes,” Reviews in Fish Biology [33] E. Paradis,J.Claude, andK.Strimmer, “APE:analysesof and Fisheries, vol. 2, no. 1, pp. 33–63, 1992. phylogenetics and evolution in R language,” Bioinformatics, vol. 20, no. 2, pp. 289–290, 2004. [16] M. C. Harvey and G. E. Brown, “Dine or dash?: ontogenetic shift in the response of yellow perch to conspecific alarm cues,” [34] M. F. Cashner, “Are spotted bass (Micropterus punctulatus) Environmental Biology of Fishes, vol. 70, no. 4, pp. 345–352, attracted to Schreckstoff? A test of the predator attraction hy- 2004. pothesis,” Copeia, no. 3, pp. 592–598, 2004. [17] O. A. Popova, “The role of predaceous fish in ecosystems,” in [35] D. P. Chivers, G. E. Brown, and R. J. F. Smith, “The evolution Ecology of Freshwater Fish Production,S.D.Gerking,Ed.,pp. of chemical alarm signals: attracting predators benefits alarm 215–249, Blackwell Scientific, Oxford, UK, 1978. signal senders,” American Naturalist, vol. 148, no. 4, pp. 649– 659, 1996. [18] G. E. Brown, V. J. Leblanc, and L. E. Porter, “Ontogenetic changes in the response of largemouth bass (Micropterus sal- [36] P. A. Nilsson and C. Bronmark, “Prey vulnerability to a gape- moides, Centrarchidae, Perciformes) to heterospecific alarm size limited predator: behavioural and morphological impacts pheromones,” Ethology, vol. 107, no. 5, pp. 401–414, 2001. on Northern pike piscivory,” Oikos, vol. 88, no. 3, pp. 539–546, [19] B. D. Wisenden and T. A. Thiel, “Field verification of predator attraction to minnow alarm substance,” Journal of Chemical [37] A. O. H. C. Leduc, J. M. Kelly, andG.E.Brown,“Detection Ecology, vol. 28, no. 2, pp. 433–438, 2002. of conspecific alarm cues by juvenile salmonids under neutral and weakly acidic conditions: laboratory and field tests,” Oe- [20] S. L. Lima and L. M. Dill, “Behavioral decisions made under cologia, vol. 139, no. 2, pp. 318–324, 2004. the risk of predation: a review and prospectus,” Canadian Jour- nal of Zoology, vol. 68, no. 4, pp. 619–640, 1990. [21] A. Mathis, D. P. Chivers, and R. J. Smith, “Chemicl alarm signals: predator deterrents or predator attractants?” American Naturalist, vol. 145, no. 6, pp. 994–1005, 1995. [22] O. M. Lonnstedt, M. I. McCormick, and D. P. Chivers, “Well- informed foraging: damage-released chemical cues of injured prey signal quality and size to predators,” Oecologia, vol. 168, no. 3, pp. 651–658, 2012. [23] G. E. Brown, C. K. Elvidge, C. J. Macnaughton, I. Ramnarine, and J. G. J. Godin, “Cross-population responses to conspecific chemical alarm cues in wild Trinidadian guppies, Poecilia reticulata: evidence for local conservation of cue production,” Canadian Journal of Zoology, vol. 88, no. 2, pp. 139–147, 2010. [24] D. P. Croft, L. J. Morrell, A. S. Wade et al., “Predation risk as a driving force for sexual segregation: a cross-population comparison,” American Naturalist, vol. 167, no. 6, pp. 867– 878, 2006. [25] A. E. Magurran, Evolutionary Ecology: The Trinidadian Guppy, Oxford University Press, Oxford, UK, 2005. [26] R. Froese and D. Pauly, “FishBase. 2011,” World Wide Web electronic publication, (01/2010)http://www.fishbase.org/. [27] J. Krause and J. G. J. Godin, “Predator preferences for attacking particular prey group sizes: consequences for predator hunting success and prey predation risk,” Animal Behaviour, vol. 50, no. 2, pp. 465–473, 1995. [28] K. E. Esteves, “Feeding ecology of three Astyanax species (Characidae, Tetragonopterinae) from a floodplain lake of Mogi-Guacu River, Parana River Basin, Brazil,” Environmental Biology of Fishes, vol. 46, no. 1, pp. 83–101, 1996. [29] B. H. Seghers, An analysis of geographic variation in the anti- predator adaptations of the guppy, Poecilia reticulata [Ph.D. the- sis], Department of Zoology, University of British Columbia, Vancouver BC, Canada, 1973. [30] G. E. Brown, C. J. MacNaughton, C. K. Elvidge, I. Ramnarine, and J. G. J. Godin, “Provenance and threat-sensitive predator avoidance patterns in wild-caught Trinidadian guppies,” Be- havioral Ecology and Sociobiology, vol. 63, no. 5, pp. 699–706, [31] J. Pinheiro, D. Bates, S. DebRoy, D. Sarkar, and R Development Core Team, “nlme: Linear and Nonlinear Mixed Effects Models,” R package version 3.1-97, 2010. 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