Abstract
Chemical alarm cues alert aquatic prey to the presence of an actively foraging predator. There is a large literature based upon responses to alarm cues derived from skin extract because it is anticipated that prey skin is damaged when prey are attacked by a predator. However, many predators feed by suction feeding whereby prey are quickly drawn into the buccal cavity and swallowed whole with little, if any, direct contact between the teeth of the predator and the skin of the prey. Here, we test if predation by suction feeding releases chemical information in sufficient quantity to elicit an antipredator response in conspecific prey. In tests of individual zebrafish Danio rerio, we found that odor of crushed zebrafish produced a clear antipredator behavioral response, but water collected immediately adjacent to staged predation events between a largemouth bass Micropterus salmoides (122–145 mm TL) and adult zebrafish (39 mm TL) did not elicit alarm behavior and did not differ from behavioral responses to blank water or bass odor (on a diet of earthworms). In a second experiment, zebrafish were swallowed by largemouth bass and then retrieved seconds later through gastric lavage, which produced zebrafish that were alive and completely intact with minimal epidermal damage. Published relationships between bass length, gape size, and the geometry of suction feeding suggest that in a hypothetical population of largemouth bass feeding on adult zebrafish or fathead minnows, the majority of predation events by piscivorous fish probably would not release detectable levels of prey alarm cue. Accounting for the role of feeding mechanics by fish predators requires a recalibration of the literature on risk assessment by small prey fishes. Chemically mediated antipredator behaviors against suction-feeding predators may occur primarily via post-ingestion dietary cues or disturbance cues released near the moment of attack.
Significance statement
Skin extract is commonly used to simulate predation and experimentally manipulate the perception of predation risk because it is generally assumed that epidermal tissue is damaged during predation. The resulting chemicals released by damaged skin induce nearby prey to engage in antipredator behavior. This study attempted to demonstrate behavioral responses to alarm cue released during staged predation events but was unable to do so, likely because of the mode of ingestion by the predator—suction feeding. Prey retrieved by gastric lavage from the gut of predators immediately after ingestion confirmed that the epidermis is largely intact when prey are swallowed by suction feeding. Because most fish predators employ suction feeding, this study calls for a recalibration of how chemical cues mediate predator–prey interactions in aquatic ecosystems. Release of alarm cues by fish predation cannot be assumed to occur in most cases. Chemical labeling by dietary cues or disturbance cues likely plays a larger role than previously appreciated for acquired predator recognition.
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taken from Fernando et al. (2018) and data sources reported therein (Lawrence 1958; Shireman 1978; Johnson and Post 1996; Timmerman et al. 2000; Hill et al. 2004), data for individual models shown in grey lines. The bold black line is the average of these models, defined by gape (mm) = 0.0001 TL2 + 0.0868 TL – 0.1083, R2 = 0.9998. Ingested volume of water (IVW) for suction feeding was calculated from the equation reported by Kane and Higham (2014): height = 0.670 + (0.018 × ram speed) + (1.311 × gape), using a ram speed of 0. Because the dimensions of the envelope of ingested water are greater than the gape, we used gape size to calculate minimize length of bass capable of swallowing whole prey such as zebrafish and fathead minnows
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Data availability
Data are available at https://doi.org/10.5061/dryad.51c59zw8z.
Abbreviations
- AC:
-
Alarm cue derived from crushed zebrafish
- BAC:
-
Alarm cue collected from water surrounding a bass that had eaten a zebrafish
- BEW:
-
Tank water from bass fed a diet of earthworms
- DH2O:
-
Distilled water
- Pre VD:
-
Pres-stimulus vertical distribution
- Post VD:
-
Post-stimulus vertical distribution
- Change in VD:
-
Post-pre vertical distribution
- Pre activity:
-
Pre-stimulus number of lines crossed
- Post activity:
-
Post-stimulus number of lines crossed
- Change in activity:
-
Post-pre activity
- Pre SH:
-
Pre-stimulus time in shelter
- Post SH:
-
Post-stimulus time in shelter
- Change in SH:
-
Post-pre shelter use
- Bass TL:
-
Total length (mm) of largemouth bass, mouth gape-at-length data from regression equations from the various sources shown as column headings and cited in full in the manuscript (Each individual data set was plotted, and we also averaged these together to produce an overall gape-length relationship plotted in Fig. 2 as a bold line and the height of the ingested volume of water (IVW Ht))
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We are grateful to two anonymous reviewers for constructive suggestions for improving the manuscript.
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Funding for this study was provided by a grant from the Judy Strong Undergraduate Research fund awarded to A.A.T. and J.D.U.
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Experimental protocols used in this study were reviewed and approved by the Minnesota State University Moorhead Institutional Animal Care and Use Committee under protocol number 19-R/T-BIO-018-N-Y-C. The use of animals adheres to the guidelines set forth by the Animal Behavior Society/Association for the Study of Animal Behaviour.
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Wisenden, B.D., Taylor, A.A., Undem, J.D. et al. Moby-bass: suction feeding by predators limits direct release of alarm cues in fishes. Behav Ecol Sociobiol 76, 33 (2022). https://doi.org/10.1007/s00265-022-03146-0
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DOI: https://doi.org/10.1007/s00265-022-03146-0