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Predator odor recognition and antipredatory response in fish: does the prey know the predator diel rhythm?
acta oecologica 31 (2007) 1–7
available at www.sciencedirect.com
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Original article
Predator odor recognition and antipredatory response in fish: does the prey know the predator diel rhythm? Hannu Ylo¨nena,*, Raine Kortetb, Janne Mynttia, Anssi Vainikkac a
Department of Biological and Environmental Science, University of Jyva¨skyla¨, P.O. Box 35, FIN-40014 Jyva¨skyla¨, Finland Behaviour, Ecology and Evolution Team (Integrative Ecology Unit), Department of Biological and Environmental Sciences, University of Helsinki, P.O. Box 65, 00014 Helsinki, Finland c Institute of Coastal Research, Swedish Board of Fisheries, Box 109, 74071 O¨regrund, Sweden b
article info
abstract
Article history:
We studied in a laboratory experiment using stream tanks if two percid prey fish, the perch
Received 17 December 2004
(Perca fluviatilis) and the ruffe (Gymnocephalus cernuus), can recognize and respond to
Accepted 30 May 2005
increased predation risk using odors of two piscivores, the pike (Esox lucius) and the burbot
Published online 6 December 2006
(Lota lota). Burbot is night-active most of the year but pike hunts predominantly visually whenever there is enough light. Perch is a common day-active prey of pike and dark-active
Keywords:
ruffe that of burbot. We predicted that besides recognizing the predator odors, the prey
Predation risk
species would respond more strongly to odors of the predator which share the same activ-
Odors
ity pattern. Both perch and ruffe clearly responded to both predator fish odors. They de-
Recognition
creased movements and erected the spiny dorsal fins. Fin erection showed clearly the
Antipredatory behavior
black warning ornamentation in the fin and thus erected fin may function besides as
Perch
mechanical defense also as warning ornament for an approaching predator. No rapid
Ruffe
escape movements were generally observed. Both perch and ruffe responded more strongly to pike odor than to burbot. There were no clear differences in response between day and night. In conclusion, we were able to verify clear predator odor recognition by both prey fish. Both perch and ruffe responded to both predator odors and it seemed that pike forms a stronger threat for both prey species. Despite of diel activity differences both perch and ruffe used the same antipredatory strategies, but the day-active perch seemed to have a more flexible antipredatory behavior by responding more strongly to burbot threat during the night when burbot is active. ª 2006 Elsevier Masson SAS. All rights reserved.
1.
Introduction
Predation risk is shown to alter prey behavior, and antipredatory behavior should enhance prey survival (see Lima and Dill, 1990; Chivers and Smith, 1998; for reviews). Increased risk can affect immediate foraging decisions (Sih, 1980), and cause microhabitat shifts (Milinski and Heller, 1978; Werner et al., 1983)
and activity shifts (Abramsky et al., 1996). Predation risk and predator-induced behaviors may vary according to predator type, predator presence, time and environment. However, an ultimate prerequisite for any effective antipredatory behavior is a correct recognition of acute increase of risk due to an approaching predator. Recognition should be timed so that it provides the possibility to escape predation (Vermej, 1982).
* Corresponding author. Tel.: þ358 14260 2250; fax: þ358 14260 2291. E-mail address: [email protected] (H. Ylo¨nen). 1146-609X/$ – see front matter ª 2006 Elsevier Masson SAS. All rights reserved. doi:10.1016/j.actao.2005.05.007
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acta oecologica 31 (2007) 1–7
In many aquatic systems prey fish can detect presence or approach of a predatory fish visually and act accordingly, for instance by avoidance behaviors, schooling or seeking a refuge (Milinski and Heller, 1978; Magurran, 1990; Dowling and Godin, 2002). However, often low light, dense vegetation or hiding without acute predation risk, may hinder visual recognition of a predator timely enough to enable an antipredatory response by the prey. Water is an effective carrier of odor signals. Chemical alarm signals in aquatic predator–prey systems has been a field of active research for decades (Brown et al., 1997; Chivers and Smith, 1998, a review by Kats and Dill, 1998). Despite some controversy on active alarm signaling between conspecific or heterospecific fish (Magurran et al., 1996; Smith, 1997), it seems clear that prey fish are able to use predator fish odors as an indicator of increased predation risk (e.g. Magurran, 1989; Mathis and Smith, 1993; Jachner and Janecki, 1999; Kats and Dill, 1998; Brown et al., 2000; Jachner, 2001). Often in darkness and for hiding animals chemosensory cues might be the best source for information about predation risk and predator presence. That prey fish can detect detailed information through odor perception has been shown in studies where the prey has responded more strongly to predator fish odor if the predator had been feeding on that particular prey (Mathis and Smith, 1993; Hirvonen et al., 2000; Brown et al., 2001) or if the predator had been feeding recently (Jachner, 1997). Therefore accurate reading of available information on temporally or spatially changing predation risk should have evolved in aquatic predator–prey systems. The initial idea for this study arose from the prediction that fish should be able to specify information and recognize species specific predator odors and respond accordingly. Further, the response strength should vary according to the temporal variation of threat by different predators. Species specific responses on predator odors has been shown for mammals, e.g. the bank voles (Clethrionomys glareolus) (Jedrzejewski et al., 1993), for fishes, e.g. the Arctic charr (Salvelinus alpinus) (Hirvonen et al., 2000) and the crucian carp (Carassius carassius) (Pettersson et al., 2000), and for amphibians like the wood frog (Rana sylvatica) (Relyea, 2003). Bank voles responded most strongly to odors of the least weasel (Mustela nivalis), a vole specialist, causing the strongest mortality of all mammalian predators in boreal vole populations (Norrdahl and Korpima¨ki, 1995). Because chemoreception is well developed in fish and water is a good carrier of odor cues, we expected accurate responses to predatory fish in our experimental prey fish (see Pettersson et al., 2000). We conducted a laboratory study on the ability of prey fish to recognize and respond accordingly to odors of sympatric predator fish. Further, we focused on the effects of diel activity period of the predator, occurring simultaneously or not with the prey fish, on prey response. We used two common Percidae fishes as prey, the day-active perch (Perca fluviatilis) and the night-active ruffe (Gymnocephalus cernuus) (Jamet and Lair, 1991), and as predator odor sources the predominantly dayactive pike (Esox lucius) (Diana, 1980) and the mainly nocturnal burbot (Lota lota) (Mu¨ller, 1973; Carl, 1994; Pa¨a¨kko¨nen et al., 2000). All four species are common in Finland, perch being one of the main prey of pike (Wysujack et al., 2001) and ruffe one of the main prey of burbot (Koli, 1990). Pike is a visual hunter in daytime and we predicted prey fish could use pike
odor for increased vigilance timely enough to avoid an ambush. In the night any potential prey fish, but more pronouncedly the night-active ruffe, should use odor cues of predation risk to increase vigilance. We exposed perch and ruffe to both pike or burbot odors, unmanipulated lake water serving as control, in a stream aquarium tank during daytime and the night, and observed subsequent behavioral changes in the prey. We predicted that: 1. If prey fish use predator fish odors as a general cue for increased risk of being killed they respond similarly regardless of predator species. 2. If prey fish recognize specific odors of pike or burbot, they should show a stronger response to odor of the predator which shares the same activity pattern and causes a stronger threat. Perch should respond more strongly to pike odor and ruffe to burbot odor. 3. Supposing that the prediction 2 is true, we predicted that prey fish should show a stronger response during the experiments carried out during the time when the specific predator is active, than when it is inactive.
2.
Methods
2.1.
Experimental fish and holding conditions
We conducted the study at the Konnevesi Research Station of the University of Jyva¨skyla¨ under license from the Ethical Committee for Animal Research of the University of Jyva¨skyla¨ (LS-31/2000). All four fishes used in the experiments are common in Central Finland. They were caught either from Lake Konnevesi, just outside the research station, or from Lake Tuomioja¨rvi by Jyva¨skyla¨ using jigs or stake nets. Both lakes have relatively clear water allowing light penetration and hence clear differences in light between day and night. Further, both pike and burbot live in both lakes, so the prey fish have had the possibility to experience their presence before the experiment. In the laboratory each species was held in separate tanks at a temperature of 11 C in a long-day light regime 16L: 8 D, lights being off between 22:00 and 06:00 h. Around 120 perch and 150 ruffe individuals were held in separate tanks of 2 2 0.6 m tank with water content of 2000 l each. Six pike and 11 burbot were held in round 1500 l tanks. Pike weighed in average around 1.2 kg (range 0.6–2.0 kg), and were in average larger than burbot. There was one large, ca. 2 kg burbot and several small between 100 and 500 g in the tank. Because pike were larger than burbot the number and size of them in the tanks were adjusted to the water volume of the tank (ca. 1 kg fish/100 l water), since we used the predator tank water as the odor source in the subsequent experiments. Predator fish were fed in the afternoon with both prey species, perch and ruffe, in similar proportions. Both pike and burbot consumed the fed fish rapidly. After ca. 10 min from the feeding the predator fish tanks were checked and all fed fish were eaten by that time. This verified that both our predator species consumed both prey species in about the same proportions, and that possible specialized diet of pike or burbot did not
acta oecologica 31 (2007) 1–7
affect their chemical cues differently (Mathis and Smith, 1993; Jachner, 1997; Hirvonen et al., 2000; Brown et al., 2001). Perch and ruffe individuals used in the experiment were of different size, but of similar size within species (average perch length 13 cm, range 11–15 cm, range of ruffe length 7–8 cm).
2.2.
Experimental tank
The experimental tank was a one meter long section of a long stream tank of 730 cm length and 47 cm width. The water level during the experiments was kept at 65 cm. The section was divided at both ends by walls made of wire mesh of 10 10 mm mesh size. The bottom of the experimental tank was covered by sand and five stones with a diameter of ca. 10 cm, that were provided evenly distributed along the length of the tank as a refuge for the fish. We used two experimental tanks, which allowed us to conduct four trials in a 24 h period: two during daytime and two during early night-time. Tanks were kept in a long-day light rhythm, 16L:8D, and covered with a plastic tarpaulin, with only a small hole of 5 cm diameter for observation of fish behavior. During the day as light were on in the research hall light could penetrate the experimental tank underneath and from both ends of the tarpaulin. Night trials were started 30 min–1 h after the lights were turned off. For observation of fish behavior there was a Table lamp with 25 W bulb under the tarpaulin, providing indirect dim light for behavioral observations but kept the tank otherwise in darkness. In the pilot trials we tried to use red light, but behavior of fish was not visible then. During the summer the nights are light in Finland. Thus, in their natural lake habitat the fish like perch and ruffe do not experience total darkness in the night. Water for the stream tank came aerated but otherwise untreated from Lake Konnevesi. Temperature of the stream tank varied slightly during our experiments, between 11 and 13 C, according to the normal variation in the lake. Velocity of water was kept low, app. 2 m/min, and constant during the experiments. Four meters up-stream from our experimental tank we built a funnel apparatus 30 cm in diameter and a hose 1.5 m in length, attached to the end wall of the stream tank, to pour our stimulus and control water to the stream tank. To measure the time which our stimulus water needed to reach the experimental section of the tank we used water stained with beetroot. We added the water so that the stimulus was distributed over the whole water body of the tank before reaching the experimental section. We kept the stream velocity so that a researcher could pour the stimulus water into the funnel, move silently to the experimental tank and start observation before the stimulus reached the focal fish. This way we were always able to observe immediate changes in behavior, should they occur.
2.3.
Experimental procedure and observed behaviors
One focal prey fish, perch or ruffe, was removed from the large tank to the experimental tank ca. 12 h before daytime trials (i.e. after each night trial) and 10 h before night trials (after each day-trial) for acclimation without any disturbance in the experimental tank. All 20 trials of each experimental combination had a pre-treatment observation period of 3 min, to
3
document that the fish was undisturbed and did not exhibit any abnormal behavior. Treatment observation period was ca. 5 min, consisting of 25–30 behavioral recordings every 10 s In the analysis we used the first 25 recordings for all trials. Observation period started immediately after the stimulus water was poured into the funnel. As the predator odor stimulus, we used 2 l of water from the holding tanks of either pike or burbot. A clean water bucket was filled from the bottom valve of the holding tank, so the odor sample was always the same quality bottom water. As the control we used the same volume of untreated lake water. After each trial the funnel and hose were cleaned by flushing them with lake water. During the treatment period behavior and position of the fish was documented. Both were recorded using a Palm III hand-held computer. The data were analyzed using ‘‘FitSystem’’ program package (Held 2000). We recorded the following data every 10 s: (a) distance fish moved (in cm) from the last location. Movements were classified to 0–5, 5–10, 10–20 and > 20 cm; (b) orientation of the fish (head towards up-stream, downstream, to the side); (c) erecting the dorsal spiny fin; (d) freezing, i.e. stopping any movement and staying still in the new position; (e) fleeing, a panic-like rapid swim to the other end of tank; (f) gliding slowly to the bottom, or; (g) no change in behavior. Each individual was used in six trials; Control, Pike and Burbot as odors and Day and Night as time of the experiment. The order of each trial for each fish was random. The total data consists of 120 trials for both species, 240 trials in total. Daytime experiments were conducted between 12:00 and 15:00 h, and the night experiments between 23:00 and 02:00 h. After all six experiments focal prey fish were released into Lake Konnevesi to prevent their use for a second time.
2.4.
Statistical analysis
We present results and statistics for movements and those behavioral variables that occurred commonly enough for reasonable analysis. The following movement variables were analyzed: no movement (¼ staying in the same position as during previous observation), clear movements 5 cm (including groups 5–10 and 10–20 cm), and long movements (> 20 cm). Freezings were uncommon (observed only in 16 cases out of 220). We did not analyze rapid movements (¼ fleeing) or gliding to the bottom, since they were observed only in four (fleeing) and 14 (gliding to the bottom) experiments out of 220. In addition, directional change of the fish was left unanalyzed due to zero or very low frequencies during the trials. As the observations of behavioral responses were collected every 10 s for 25 times, their frequencies represent proportion of time used for a specific behavior. Thus all the frequencies were first divided by 25 and then square root arcsine transformed (Zar, 1999) to facilitate parametric analysis. Same fish were used for control, pike and burbot odors both during
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day and night. Thus, saturated model repeated measures ANOVA (RM-ANOVA) with two within-subject factors (1. predator: control, pike and burbot and 2. time: day or night) was used to analyze the data. Within-subject effects, with Greenhouse–Geisser correction for degrees of freedom when sphericity assumption was violated, are reported. This was only the case for the variable movements > 20 cm (see Table 1A). Species (perch or ruffe) was used as a between-subject factor to compare responses of these species. All statistical analyses were performed using SPSS 11.0.1 (SPPS Inc., USA). Pre-trial data were not used as it was collected just to confirm there were no behavioral abnormalities before the experiments.
3.
Results
3.1.
Reaction to predator fish odors
the only clear change in behavior and it was combined with predominant inactivity (Fig. 1). Ruffe was in general more active and changed position more often (Fig. 1 and Table 1A,B). Perch and ruffe did not differ in > 20 cm movements, erection of dorsal fin or in freezing behavior (Table 1A,B).
3.2. Responses during the day and the night towards pike and burbot The differences between the day and the night in behavioral responses in perch and in ruffe were negligible: the only statistically significant difference was in freezing (Table 1A,B), being more common during the day in both species (Fig. 2).
4.
Both perch and ruffe clearly distinguished the odors of pike and burbot from the control (Table 1A,B). This was mostly reflected in both species as decreased movements and especially erecting fin (Figs. 1 and 2 and Table 1A.). The reaction in fin erecting was apparent immediately as the odor stimulus reached the focal fish and the fish kept the fin erected throughout the trial. When the fin was erected, black dots or triangles below every spine were clearly visible. Any rapid escape movements were very rare or absent. It seemed that both perch and ruffe recognized and responded to both odors from either pike or burbot, but both prey species responded more strongly to pike odor with the clearest response of erecting fin (Figs. 1 and 2). This was especially clear for the day experiments, which simulated the active hunting period of pikes. In perch erecting the fin was in most cases
Discussion
We were clearly able to verify the first prediction of our study. Both perch and ruffe were able to detect the increased risk level by using odors of predator fish as cues for the threat. This general phenomenon has been shown before, for instance by Magurran (1989), Chivers and Smith (1995) for two minnow species, by Huuskonen and Karjalainen (1997) for perch, by Jachner (1997) for bleak (Alburnus alburnus) and Hirvonen et al. (2000) for Arctic charr. Secondly, both prey species were able to distinguish between the two predator odors, and showed a stronger response in erecting the fin to pike odor. However, against our prediction there was no stronger response of prey fish to that piscivore species sharing mainly the common diel activity pattern, which we hypothesized would cause a stronger threat for the prey fish. Because pike can hunt also in relative low-light conditions (A. Vainikka, pers. observation) and burbot changes its activity pattern to
Table 1 – ANOVA Table of the effects of time when the experiment was conducted (Day/Night), the predator (Pike/Burbot/ Control) and their interactions on movements and behavior of perch and ruffe A. Movements Source of variation
Time Time species Predator Predator species Time predator Time predator species Species
0 cm
5–20 cm
> 20 cm
F
df
P
F
df
P
F
df
P
0.11 0.46 3.38 3.80 3.08 1.92 32.07
1.31 1.31 2.62 2.62 2.62 2.62 1.31
0.746 0.501 0.041 0.028 0.053 0.156 < 0.001
0.15 0.84 4.61 0.11 1.16 1.96 6.24
1.31 1.31 2.62 2.62 2.62 2.62 1.31
0.705 0.368 0.014 0.898 0.320 0.149 0.018
3.00 1.84 3.62 1.67 0.22 3.20 1.00
1.31 1.31 1.75,54.33 1.75,54.33 1.68,51.98 1.68,51.98 1.31
0.093 0.185 0.039 0.0201 0.745 0.057 0.325
B. Behavior Source of variation
Time Time species Predator Predator species Time predator Time predator species Species
No change
Erected fin
Freezing
F
df
P
F
df
P
F
df
P
0.00 0.34 2.43 54.16 0.83 1.58 42.50
1.31 1.31 2.62 2.62 2.62 2.62 1.31
0.994 0.566 0.096 < 0.001 0.441 0.214 < 0.001
0.39 0.01 55.80 1.48 2.29 1.35 3.02
1.31 1.31 2.62 2.62 2.62 2.62 1.31
0.539 0.946 < 0.001 0.236 0.109 0.266 0.092
4.87 1.32 1.51 2.95 3.08 3.15 0.10
1.31 1.31 2.62 2.62 2.62 2.62 1.31
0.035 0.260 0.228 0.060 0.053 0.050 0.759
acta oecologica 31 (2007) 1–7
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Fig. 1 – Movements of perch a) and ruffe b) under control, pike odor and burbot odor treatment of the experiments. The frequency of position change occurring between the subsequent behavioral observations every 10 s (out of 25 units in total) are shown. Error bars show S.E. of mean.
day-active during autumn and early winter (Mu¨ller, 1973), it might be that prey do not predict predator activity but respond to all threats. Pike odor seemed to form a greater threat for both prey species. Pike hunt differently compared to burbot. Pike are ambush hunters with a high-speed attack, so timely recognition of the presence of pike using odor cues should be an important antipredatory behavior in any potential prey fish species. Burbot seek prey more slowly in the darkness of the lake bottom where ruffe is more common than perch. Against our prediction ruffe did not respond differently to increased risk depending on the predator species. We predicted that, in the darkness, an odor might be the best cue for vigilance against a slowly approaching predator, like burbot. Especially, this should be true if burbot had been feeding before on ruffe, which was the case in our experiment. It has been shown in previous studies that if piscivores have been preying and feeding on a certain prey species, their odors provide a more accurate cue for an acute threat (Mathis and Smith, 1993; Hirvonen et al., 2000; Brown et al., 2001). Rapid escape movements were very rare, especially in perch. Perch did not change position or did not cause any potential movement cue for a predator, when receiving the odor
signal. Ruffe showed a stronger general alertness, reflected in frequent changes of position and erecting fins, but also avoided rapid movements. Previous studies reported decreased activity as a response to increased predation risk (e.g. Magurran, 1990; Eklo¨v and Persson, 1995; Vainikka et al., 2005). This has been shown for instance in fathead minnows (Pimephales promelas) by Mathis and Smith (1993). However, a rapid escape might be a good strategy, especially towards a more slowly moving burbot. Against our expectation we did not observe behaviors like slow gliding to the bottom of the tank or hiding. Huuskonen and Karjalainen (1997) defined perch as a hider compared to escaping coregonids like the vendace (Coregonus albula). They used respiratory response as a measure of alertness in three fishes, vendace, perch and roach (Rutilus rutilus). Perch responded to pike presence by decreasing oxygen consumption, immobility or hiding. We did not observe hiding at all in our study. The clearest single behavioral response which we observed was the lifting of the dorsal fin. Avoiding any movement initially and then lifting the spiny dorsal fin if the predator attacks, might be the most effective antipredatory response for percid fish. Besides acting as a mechanical defense against attack, when the dorsal fin is erected the black triangles in the
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acta oecologica 31 (2007) 1–7
Fig. 2 – Behavior of a) perch and b) ruffe during the control or after the odor signal of pike or burbot. Frequency of behaviors (no change, erecting fin, freezing) are shown for each 10-s unit out of 25 units in total. Error bars show S.E. of mean.
fin become clearly visible. This might function as a visual warning ornament for an approaching predator during the day. Swallowing a perch or a ruffe with an erected fin might be difficult especially for a small or medium size predator fish. Huuskonen and Karjalainen (1997), Vainikka et al. (2005) also observed lifting the fin in perch as a response to the visual cue of pike. Both perch and ruffe erected the fin more strongly under pike predation risk. Perch also responded slightly stronger to burbot odor during the night when the risk by burbot is increased. We conclude that pike seems to be an overwhelming predator for both small percids and an effective adaptation to avoid it is chemoreception. Against slowly approaching bottom predator, like the burbot, other tactile senses like the lateral line could be important as well.
Acknowledgements We thank J. Koskinen, R. Latvanen and J. Raatikainen at the Konnevesi Research Station for providing excellent facilities for the study and keeping our study fish. We thank Tony Arthur, Christina Lynch, Heikki Hirvonen, Juha Karjalainen and Ines Klemme for valuable comments on the manuscript. The study was supported by the Academy of Finland and the Centre of Excellence research programme.
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Magurran, A.E., Irving, P.W., Henderson, P.A., 1996. Is there a fish alarm pheromone? A wild study and critique. Proc. R. Soc. Lond, B 263, 1551–1556. Mathis, A., Smith, R.J.F., 1993. Fathead minnow, Pimephales promelas, learn to recognize northern pike, Esox lucius, as predators on the basis of chemical stimuli from minnows in the pike’s diet. Anim. Behav. 46, 645–656. Milinski, M., Heller, R., 1978. Influence of a predator on the optimal foraging behaviour of sticklebacks. Nature 275, 642–644. Mu¨ller, K., 1973. Seasonal phase shift and the duration of activity time in the burbot, Lota lota (L.) (Pisces, Gadidae). J. Comp. Physiol. 84, 357–359. Norrdahl, K., Korpima¨ki, E., 1995. Mortality factors in a cyclic vole population. Proc. R. Soc. Lond, B 261, 49–53. Pettersson, L.B., Nilsson, P.A., Bro¨nmark, C., 2000. Predator recognition and defence strategies in crucial carp, Carassius carassius. Oikos 88, 200–212. Pa¨a¨kko¨nen, J.J., Laitinen, M., Marjoma¨ki, T., 2000. Total activity of burbot Lota lota (L.) measured with bioelectric monitoring system: seasonal differences in activity length. In: Paragamian, V.L., Willis, D.W. (Eds.), Burbot: Biology, Ecology and Management. Amer. Fisher. Soc. Fisher. Manage, pp. 38–47. Relyea, R.A., 2003. How prey respond to combined predators: a review and an empirical test. Ecology 84, 1827–1839. Sih, A., 1980. Optimal behaviour: can foragers balance two conflicting demands? Science 210, 1041–1043. Smith, R.J.F., 1997. Does one result trump all others? A response to Magurran, Irving and Henderson. Proc. R. Soc. Lond, B 264, 445–450. Vainikka, A., Jokelainen, T., Kortet, R., Ylo¨nen, H., 2005. Predation risk allocation or direct vigilance response in the predation interaction between perch (Perca fluviatilis L.) and pike (Esox lucius L.). Ecol. Fresw. Fish. 14, 225–232. Vermej, G.J., 1982. Unsuccessful predation and evolution. Am. Nat. 120, 701–720. Werner, E.E., Gilliam, J.F., Hall, D.L., Mittelbach, G.G., 1983. An test f the effects of predation risk on habitat use in fish. Ecology 64, 1540–1548. Wysujack, K., Laude, U., Anwand, K., Mehner, T., 2001. Stocking, population development and food composition of pike Esox lucius in the biomanipulated Feldberger Haussee (Germany) implications for fisheries management. Limnologica 31, 45–51. Zar, J.H., 1999. Biostatistical Analysis. Prentice-Hall, New Jersey.
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Original article
Predator odor recognition and antipredatory response in fish: does the prey know the predator diel rhythm? Hannu Ylo¨nena,*, Raine Kortetb, Janne Mynttia, Anssi Vainikkac a
Department of Biological and Environmental Science, University of Jyva¨skyla¨, P.O. Box 35, FIN-40014 Jyva¨skyla¨, Finland Behaviour, Ecology and Evolution Team (Integrative Ecology Unit), Department of Biological and Environmental Sciences, University of Helsinki, P.O. Box 65, 00014 Helsinki, Finland c Institute of Coastal Research, Swedish Board of Fisheries, Box 109, 74071 O¨regrund, Sweden b
article info
abstract
Article history:
We studied in a laboratory experiment using stream tanks if two percid prey fish, the perch
Received 17 December 2004
(Perca fluviatilis) and the ruffe (Gymnocephalus cernuus), can recognize and respond to
Accepted 30 May 2005
increased predation risk using odors of two piscivores, the pike (Esox lucius) and the burbot
Published online 6 December 2006
(Lota lota). Burbot is night-active most of the year but pike hunts predominantly visually whenever there is enough light. Perch is a common day-active prey of pike and dark-active
Keywords:
ruffe that of burbot. We predicted that besides recognizing the predator odors, the prey
Predation risk
species would respond more strongly to odors of the predator which share the same activ-
Odors
ity pattern. Both perch and ruffe clearly responded to both predator fish odors. They de-
Recognition
creased movements and erected the spiny dorsal fins. Fin erection showed clearly the
Antipredatory behavior
black warning ornamentation in the fin and thus erected fin may function besides as
Perch
mechanical defense also as warning ornament for an approaching predator. No rapid
Ruffe
escape movements were generally observed. Both perch and ruffe responded more strongly to pike odor than to burbot. There were no clear differences in response between day and night. In conclusion, we were able to verify clear predator odor recognition by both prey fish. Both perch and ruffe responded to both predator odors and it seemed that pike forms a stronger threat for both prey species. Despite of diel activity differences both perch and ruffe used the same antipredatory strategies, but the day-active perch seemed to have a more flexible antipredatory behavior by responding more strongly to burbot threat during the night when burbot is active. ª 2006 Elsevier Masson SAS. All rights reserved.
1.
Introduction
Predation risk is shown to alter prey behavior, and antipredatory behavior should enhance prey survival (see Lima and Dill, 1990; Chivers and Smith, 1998; for reviews). Increased risk can affect immediate foraging decisions (Sih, 1980), and cause microhabitat shifts (Milinski and Heller, 1978; Werner et al., 1983)
and activity shifts (Abramsky et al., 1996). Predation risk and predator-induced behaviors may vary according to predator type, predator presence, time and environment. However, an ultimate prerequisite for any effective antipredatory behavior is a correct recognition of acute increase of risk due to an approaching predator. Recognition should be timed so that it provides the possibility to escape predation (Vermej, 1982).
* Corresponding author. Tel.: þ358 14260 2250; fax: þ358 14260 2291. E-mail address: [email protected] (H. Ylo¨nen). 1146-609X/$ – see front matter ª 2006 Elsevier Masson SAS. All rights reserved. doi:10.1016/j.actao.2005.05.007
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acta oecologica 31 (2007) 1–7
In many aquatic systems prey fish can detect presence or approach of a predatory fish visually and act accordingly, for instance by avoidance behaviors, schooling or seeking a refuge (Milinski and Heller, 1978; Magurran, 1990; Dowling and Godin, 2002). However, often low light, dense vegetation or hiding without acute predation risk, may hinder visual recognition of a predator timely enough to enable an antipredatory response by the prey. Water is an effective carrier of odor signals. Chemical alarm signals in aquatic predator–prey systems has been a field of active research for decades (Brown et al., 1997; Chivers and Smith, 1998, a review by Kats and Dill, 1998). Despite some controversy on active alarm signaling between conspecific or heterospecific fish (Magurran et al., 1996; Smith, 1997), it seems clear that prey fish are able to use predator fish odors as an indicator of increased predation risk (e.g. Magurran, 1989; Mathis and Smith, 1993; Jachner and Janecki, 1999; Kats and Dill, 1998; Brown et al., 2000; Jachner, 2001). Often in darkness and for hiding animals chemosensory cues might be the best source for information about predation risk and predator presence. That prey fish can detect detailed information through odor perception has been shown in studies where the prey has responded more strongly to predator fish odor if the predator had been feeding on that particular prey (Mathis and Smith, 1993; Hirvonen et al., 2000; Brown et al., 2001) or if the predator had been feeding recently (Jachner, 1997). Therefore accurate reading of available information on temporally or spatially changing predation risk should have evolved in aquatic predator–prey systems. The initial idea for this study arose from the prediction that fish should be able to specify information and recognize species specific predator odors and respond accordingly. Further, the response strength should vary according to the temporal variation of threat by different predators. Species specific responses on predator odors has been shown for mammals, e.g. the bank voles (Clethrionomys glareolus) (Jedrzejewski et al., 1993), for fishes, e.g. the Arctic charr (Salvelinus alpinus) (Hirvonen et al., 2000) and the crucian carp (Carassius carassius) (Pettersson et al., 2000), and for amphibians like the wood frog (Rana sylvatica) (Relyea, 2003). Bank voles responded most strongly to odors of the least weasel (Mustela nivalis), a vole specialist, causing the strongest mortality of all mammalian predators in boreal vole populations (Norrdahl and Korpima¨ki, 1995). Because chemoreception is well developed in fish and water is a good carrier of odor cues, we expected accurate responses to predatory fish in our experimental prey fish (see Pettersson et al., 2000). We conducted a laboratory study on the ability of prey fish to recognize and respond accordingly to odors of sympatric predator fish. Further, we focused on the effects of diel activity period of the predator, occurring simultaneously or not with the prey fish, on prey response. We used two common Percidae fishes as prey, the day-active perch (Perca fluviatilis) and the night-active ruffe (Gymnocephalus cernuus) (Jamet and Lair, 1991), and as predator odor sources the predominantly dayactive pike (Esox lucius) (Diana, 1980) and the mainly nocturnal burbot (Lota lota) (Mu¨ller, 1973; Carl, 1994; Pa¨a¨kko¨nen et al., 2000). All four species are common in Finland, perch being one of the main prey of pike (Wysujack et al., 2001) and ruffe one of the main prey of burbot (Koli, 1990). Pike is a visual hunter in daytime and we predicted prey fish could use pike
odor for increased vigilance timely enough to avoid an ambush. In the night any potential prey fish, but more pronouncedly the night-active ruffe, should use odor cues of predation risk to increase vigilance. We exposed perch and ruffe to both pike or burbot odors, unmanipulated lake water serving as control, in a stream aquarium tank during daytime and the night, and observed subsequent behavioral changes in the prey. We predicted that: 1. If prey fish use predator fish odors as a general cue for increased risk of being killed they respond similarly regardless of predator species. 2. If prey fish recognize specific odors of pike or burbot, they should show a stronger response to odor of the predator which shares the same activity pattern and causes a stronger threat. Perch should respond more strongly to pike odor and ruffe to burbot odor. 3. Supposing that the prediction 2 is true, we predicted that prey fish should show a stronger response during the experiments carried out during the time when the specific predator is active, than when it is inactive.
2.
Methods
2.1.
Experimental fish and holding conditions
We conducted the study at the Konnevesi Research Station of the University of Jyva¨skyla¨ under license from the Ethical Committee for Animal Research of the University of Jyva¨skyla¨ (LS-31/2000). All four fishes used in the experiments are common in Central Finland. They were caught either from Lake Konnevesi, just outside the research station, or from Lake Tuomioja¨rvi by Jyva¨skyla¨ using jigs or stake nets. Both lakes have relatively clear water allowing light penetration and hence clear differences in light between day and night. Further, both pike and burbot live in both lakes, so the prey fish have had the possibility to experience their presence before the experiment. In the laboratory each species was held in separate tanks at a temperature of 11 C in a long-day light regime 16L: 8 D, lights being off between 22:00 and 06:00 h. Around 120 perch and 150 ruffe individuals were held in separate tanks of 2 2 0.6 m tank with water content of 2000 l each. Six pike and 11 burbot were held in round 1500 l tanks. Pike weighed in average around 1.2 kg (range 0.6–2.0 kg), and were in average larger than burbot. There was one large, ca. 2 kg burbot and several small between 100 and 500 g in the tank. Because pike were larger than burbot the number and size of them in the tanks were adjusted to the water volume of the tank (ca. 1 kg fish/100 l water), since we used the predator tank water as the odor source in the subsequent experiments. Predator fish were fed in the afternoon with both prey species, perch and ruffe, in similar proportions. Both pike and burbot consumed the fed fish rapidly. After ca. 10 min from the feeding the predator fish tanks were checked and all fed fish were eaten by that time. This verified that both our predator species consumed both prey species in about the same proportions, and that possible specialized diet of pike or burbot did not
acta oecologica 31 (2007) 1–7
affect their chemical cues differently (Mathis and Smith, 1993; Jachner, 1997; Hirvonen et al., 2000; Brown et al., 2001). Perch and ruffe individuals used in the experiment were of different size, but of similar size within species (average perch length 13 cm, range 11–15 cm, range of ruffe length 7–8 cm).
2.2.
Experimental tank
The experimental tank was a one meter long section of a long stream tank of 730 cm length and 47 cm width. The water level during the experiments was kept at 65 cm. The section was divided at both ends by walls made of wire mesh of 10 10 mm mesh size. The bottom of the experimental tank was covered by sand and five stones with a diameter of ca. 10 cm, that were provided evenly distributed along the length of the tank as a refuge for the fish. We used two experimental tanks, which allowed us to conduct four trials in a 24 h period: two during daytime and two during early night-time. Tanks were kept in a long-day light rhythm, 16L:8D, and covered with a plastic tarpaulin, with only a small hole of 5 cm diameter for observation of fish behavior. During the day as light were on in the research hall light could penetrate the experimental tank underneath and from both ends of the tarpaulin. Night trials were started 30 min–1 h after the lights were turned off. For observation of fish behavior there was a Table lamp with 25 W bulb under the tarpaulin, providing indirect dim light for behavioral observations but kept the tank otherwise in darkness. In the pilot trials we tried to use red light, but behavior of fish was not visible then. During the summer the nights are light in Finland. Thus, in their natural lake habitat the fish like perch and ruffe do not experience total darkness in the night. Water for the stream tank came aerated but otherwise untreated from Lake Konnevesi. Temperature of the stream tank varied slightly during our experiments, between 11 and 13 C, according to the normal variation in the lake. Velocity of water was kept low, app. 2 m/min, and constant during the experiments. Four meters up-stream from our experimental tank we built a funnel apparatus 30 cm in diameter and a hose 1.5 m in length, attached to the end wall of the stream tank, to pour our stimulus and control water to the stream tank. To measure the time which our stimulus water needed to reach the experimental section of the tank we used water stained with beetroot. We added the water so that the stimulus was distributed over the whole water body of the tank before reaching the experimental section. We kept the stream velocity so that a researcher could pour the stimulus water into the funnel, move silently to the experimental tank and start observation before the stimulus reached the focal fish. This way we were always able to observe immediate changes in behavior, should they occur.
2.3.
Experimental procedure and observed behaviors
One focal prey fish, perch or ruffe, was removed from the large tank to the experimental tank ca. 12 h before daytime trials (i.e. after each night trial) and 10 h before night trials (after each day-trial) for acclimation without any disturbance in the experimental tank. All 20 trials of each experimental combination had a pre-treatment observation period of 3 min, to
3
document that the fish was undisturbed and did not exhibit any abnormal behavior. Treatment observation period was ca. 5 min, consisting of 25–30 behavioral recordings every 10 s In the analysis we used the first 25 recordings for all trials. Observation period started immediately after the stimulus water was poured into the funnel. As the predator odor stimulus, we used 2 l of water from the holding tanks of either pike or burbot. A clean water bucket was filled from the bottom valve of the holding tank, so the odor sample was always the same quality bottom water. As the control we used the same volume of untreated lake water. After each trial the funnel and hose were cleaned by flushing them with lake water. During the treatment period behavior and position of the fish was documented. Both were recorded using a Palm III hand-held computer. The data were analyzed using ‘‘FitSystem’’ program package (Held 2000). We recorded the following data every 10 s: (a) distance fish moved (in cm) from the last location. Movements were classified to 0–5, 5–10, 10–20 and > 20 cm; (b) orientation of the fish (head towards up-stream, downstream, to the side); (c) erecting the dorsal spiny fin; (d) freezing, i.e. stopping any movement and staying still in the new position; (e) fleeing, a panic-like rapid swim to the other end of tank; (f) gliding slowly to the bottom, or; (g) no change in behavior. Each individual was used in six trials; Control, Pike and Burbot as odors and Day and Night as time of the experiment. The order of each trial for each fish was random. The total data consists of 120 trials for both species, 240 trials in total. Daytime experiments were conducted between 12:00 and 15:00 h, and the night experiments between 23:00 and 02:00 h. After all six experiments focal prey fish were released into Lake Konnevesi to prevent their use for a second time.
2.4.
Statistical analysis
We present results and statistics for movements and those behavioral variables that occurred commonly enough for reasonable analysis. The following movement variables were analyzed: no movement (¼ staying in the same position as during previous observation), clear movements 5 cm (including groups 5–10 and 10–20 cm), and long movements (> 20 cm). Freezings were uncommon (observed only in 16 cases out of 220). We did not analyze rapid movements (¼ fleeing) or gliding to the bottom, since they were observed only in four (fleeing) and 14 (gliding to the bottom) experiments out of 220. In addition, directional change of the fish was left unanalyzed due to zero or very low frequencies during the trials. As the observations of behavioral responses were collected every 10 s for 25 times, their frequencies represent proportion of time used for a specific behavior. Thus all the frequencies were first divided by 25 and then square root arcsine transformed (Zar, 1999) to facilitate parametric analysis. Same fish were used for control, pike and burbot odors both during
4
acta oecologica 31 (2007) 1–7
day and night. Thus, saturated model repeated measures ANOVA (RM-ANOVA) with two within-subject factors (1. predator: control, pike and burbot and 2. time: day or night) was used to analyze the data. Within-subject effects, with Greenhouse–Geisser correction for degrees of freedom when sphericity assumption was violated, are reported. This was only the case for the variable movements > 20 cm (see Table 1A). Species (perch or ruffe) was used as a between-subject factor to compare responses of these species. All statistical analyses were performed using SPSS 11.0.1 (SPPS Inc., USA). Pre-trial data were not used as it was collected just to confirm there were no behavioral abnormalities before the experiments.
3.
Results
3.1.
Reaction to predator fish odors
the only clear change in behavior and it was combined with predominant inactivity (Fig. 1). Ruffe was in general more active and changed position more often (Fig. 1 and Table 1A,B). Perch and ruffe did not differ in > 20 cm movements, erection of dorsal fin or in freezing behavior (Table 1A,B).
3.2. Responses during the day and the night towards pike and burbot The differences between the day and the night in behavioral responses in perch and in ruffe were negligible: the only statistically significant difference was in freezing (Table 1A,B), being more common during the day in both species (Fig. 2).
4.
Both perch and ruffe clearly distinguished the odors of pike and burbot from the control (Table 1A,B). This was mostly reflected in both species as decreased movements and especially erecting fin (Figs. 1 and 2 and Table 1A.). The reaction in fin erecting was apparent immediately as the odor stimulus reached the focal fish and the fish kept the fin erected throughout the trial. When the fin was erected, black dots or triangles below every spine were clearly visible. Any rapid escape movements were very rare or absent. It seemed that both perch and ruffe recognized and responded to both odors from either pike or burbot, but both prey species responded more strongly to pike odor with the clearest response of erecting fin (Figs. 1 and 2). This was especially clear for the day experiments, which simulated the active hunting period of pikes. In perch erecting the fin was in most cases
Discussion
We were clearly able to verify the first prediction of our study. Both perch and ruffe were able to detect the increased risk level by using odors of predator fish as cues for the threat. This general phenomenon has been shown before, for instance by Magurran (1989), Chivers and Smith (1995) for two minnow species, by Huuskonen and Karjalainen (1997) for perch, by Jachner (1997) for bleak (Alburnus alburnus) and Hirvonen et al. (2000) for Arctic charr. Secondly, both prey species were able to distinguish between the two predator odors, and showed a stronger response in erecting the fin to pike odor. However, against our prediction there was no stronger response of prey fish to that piscivore species sharing mainly the common diel activity pattern, which we hypothesized would cause a stronger threat for the prey fish. Because pike can hunt also in relative low-light conditions (A. Vainikka, pers. observation) and burbot changes its activity pattern to
Table 1 – ANOVA Table of the effects of time when the experiment was conducted (Day/Night), the predator (Pike/Burbot/ Control) and their interactions on movements and behavior of perch and ruffe A. Movements Source of variation
Time Time species Predator Predator species Time predator Time predator species Species
0 cm
5–20 cm
> 20 cm
F
df
P
F
df
P
F
df
P
0.11 0.46 3.38 3.80 3.08 1.92 32.07
1.31 1.31 2.62 2.62 2.62 2.62 1.31
0.746 0.501 0.041 0.028 0.053 0.156 < 0.001
0.15 0.84 4.61 0.11 1.16 1.96 6.24
1.31 1.31 2.62 2.62 2.62 2.62 1.31
0.705 0.368 0.014 0.898 0.320 0.149 0.018
3.00 1.84 3.62 1.67 0.22 3.20 1.00
1.31 1.31 1.75,54.33 1.75,54.33 1.68,51.98 1.68,51.98 1.31
0.093 0.185 0.039 0.0201 0.745 0.057 0.325
B. Behavior Source of variation
Time Time species Predator Predator species Time predator Time predator species Species
No change
Erected fin
Freezing
F
df
P
F
df
P
F
df
P
0.00 0.34 2.43 54.16 0.83 1.58 42.50
1.31 1.31 2.62 2.62 2.62 2.62 1.31
0.994 0.566 0.096 < 0.001 0.441 0.214 < 0.001
0.39 0.01 55.80 1.48 2.29 1.35 3.02
1.31 1.31 2.62 2.62 2.62 2.62 1.31
0.539 0.946 < 0.001 0.236 0.109 0.266 0.092
4.87 1.32 1.51 2.95 3.08 3.15 0.10
1.31 1.31 2.62 2.62 2.62 2.62 1.31
0.035 0.260 0.228 0.060 0.053 0.050 0.759
acta oecologica 31 (2007) 1–7
5
Fig. 1 – Movements of perch a) and ruffe b) under control, pike odor and burbot odor treatment of the experiments. The frequency of position change occurring between the subsequent behavioral observations every 10 s (out of 25 units in total) are shown. Error bars show S.E. of mean.
day-active during autumn and early winter (Mu¨ller, 1973), it might be that prey do not predict predator activity but respond to all threats. Pike odor seemed to form a greater threat for both prey species. Pike hunt differently compared to burbot. Pike are ambush hunters with a high-speed attack, so timely recognition of the presence of pike using odor cues should be an important antipredatory behavior in any potential prey fish species. Burbot seek prey more slowly in the darkness of the lake bottom where ruffe is more common than perch. Against our prediction ruffe did not respond differently to increased risk depending on the predator species. We predicted that, in the darkness, an odor might be the best cue for vigilance against a slowly approaching predator, like burbot. Especially, this should be true if burbot had been feeding before on ruffe, which was the case in our experiment. It has been shown in previous studies that if piscivores have been preying and feeding on a certain prey species, their odors provide a more accurate cue for an acute threat (Mathis and Smith, 1993; Hirvonen et al., 2000; Brown et al., 2001). Rapid escape movements were very rare, especially in perch. Perch did not change position or did not cause any potential movement cue for a predator, when receiving the odor
signal. Ruffe showed a stronger general alertness, reflected in frequent changes of position and erecting fins, but also avoided rapid movements. Previous studies reported decreased activity as a response to increased predation risk (e.g. Magurran, 1990; Eklo¨v and Persson, 1995; Vainikka et al., 2005). This has been shown for instance in fathead minnows (Pimephales promelas) by Mathis and Smith (1993). However, a rapid escape might be a good strategy, especially towards a more slowly moving burbot. Against our expectation we did not observe behaviors like slow gliding to the bottom of the tank or hiding. Huuskonen and Karjalainen (1997) defined perch as a hider compared to escaping coregonids like the vendace (Coregonus albula). They used respiratory response as a measure of alertness in three fishes, vendace, perch and roach (Rutilus rutilus). Perch responded to pike presence by decreasing oxygen consumption, immobility or hiding. We did not observe hiding at all in our study. The clearest single behavioral response which we observed was the lifting of the dorsal fin. Avoiding any movement initially and then lifting the spiny dorsal fin if the predator attacks, might be the most effective antipredatory response for percid fish. Besides acting as a mechanical defense against attack, when the dorsal fin is erected the black triangles in the
6
acta oecologica 31 (2007) 1–7
Fig. 2 – Behavior of a) perch and b) ruffe during the control or after the odor signal of pike or burbot. Frequency of behaviors (no change, erecting fin, freezing) are shown for each 10-s unit out of 25 units in total. Error bars show S.E. of mean.
fin become clearly visible. This might function as a visual warning ornament for an approaching predator during the day. Swallowing a perch or a ruffe with an erected fin might be difficult especially for a small or medium size predator fish. Huuskonen and Karjalainen (1997), Vainikka et al. (2005) also observed lifting the fin in perch as a response to the visual cue of pike. Both perch and ruffe erected the fin more strongly under pike predation risk. Perch also responded slightly stronger to burbot odor during the night when the risk by burbot is increased. We conclude that pike seems to be an overwhelming predator for both small percids and an effective adaptation to avoid it is chemoreception. Against slowly approaching bottom predator, like the burbot, other tactile senses like the lateral line could be important as well.
Acknowledgements We thank J. Koskinen, R. Latvanen and J. Raatikainen at the Konnevesi Research Station for providing excellent facilities for the study and keeping our study fish. We thank Tony Arthur, Christina Lynch, Heikki Hirvonen, Juha Karjalainen and Ines Klemme for valuable comments on the manuscript. The study was supported by the Academy of Finland and the Centre of Excellence research programme.
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