Assessment of predation risk through conspecific alarm odors by spiny lobsters

Abstract

Strong “alarm odors” emanating from lethally injured conspecifics may indicate an imminent risk of predation to spiny lobsters. In laboratory trials,¹ strong conspecific alarm odors elicited avoidance in Panulirus argus, a highly gregarious species that displays collective defense behavior, but not in Panulirus guttatus, a species that tends to aggregate when reproductive activity is high (spring) but not when it is low (late summer) and does not display collective defensive behavior. To reduce predation risk, however, lobsters may automize limbs, thus sustaining non-lethal injuries. I tested the response of these lobsters to scents emanating from intact, lethally-injured, and non-lethally injured conspecifics. In P. argus, these scents elicited, respectively, attraction, avoidance, and a random response, suggesting that, in P. argus, avoidance of conspecific alarm odors depends on their strength. In contrast, P. guttatus lobsters responded at random to scents of lethally injured conspecifics and showed a similar response to scents of intact and non-lethally injured conspecifics in the spring (attraction) and in the summer (random), reflecting the more cryptic defensive behavior of this species. Therefore, both species use conspecific alarm odors for risk-assessment, but each responds to these cues in the most effective way to reduce its risk of predation.

Marine animals that forage at night strongly rely on their chemical senses for assessing predation risk.2 In particular, chemical cues emanating from injured conspecifics (“alarm odors”) can indicate a more imminent risk of predation, especially to animals that live in groups.3,4 Spiny lobsters (Crustacea: Palinuridae) tend to aggregate in diurnal shelters, a social behavior that is mediated by conspecific chemical attraction.5–8 However, different species vary in their degree of gregariousness.9 For example, Caribbean spiny lobsters (Panulirus argus) have a strong tendency to aggregate and use collective defensive behavior to reduce predation risk.10–12 These lobsters, which are highly mobile and forage away from their shelters,10,13 use conspecific chemical cues to find shelter faster14 and to assess the quality (potential for gregariousness) of shelters.15 Given the strong adaptive value of gregariousness for P. argus,16 these lobsters tend to aggregate irrespective of season or size.5,11,17 In contrast, spotted spiny lobsters (Panulirus guttatus) are sedentary, obligate reef-dwellers that forage close to their shelters.17–19 We recently found that these lobsters tend to aggregate when reproductive activity in the population is high (spring), but not when reproductive activity is low (late summer).11,20 Also importantly, P. guttatus lobsters do not display collective defense behavior and, to reduce predation risk, they hide as deeply as possible in any available crevice and remain still.11,12,18

In a recent study,1 we tested the effect of conspecific alarm odors on the shelter choice by individuals of P. argus and P. guttatus. Each test lobster was free to choose between two identical shelters, one in each arm of a Y-maze. One shelter received plain seawater flowing through a separate head tank while the other shelter received seawater flowing through another head tank that held a lethally injured lobster (one half of a freshly killed conspecific), not visible to the test lobster. P. argus lobsters significantly avoided shelters emanating conspecific alarm odors, whereas the shelter choice by P. guttatus lobsters did not differ significantly from random, suggesting that, in spiny lobsters, decision making upon predation risk-assessment via conspecific alarm odors is related to gregarious behavior.

Although injured lobsters release all kinds of bodily fluids, it was recently shown that, in P. argus, chemicals that act as alarm odors are blood-borne and that even highly diluted blood elicits avoidance behavior in conspecifics.21 This finding is relevant because spiny lobsters, like many decapods, can escape imminent death from predators by shedding limbs (autotomy), a process that causes non-lethal injuries.22 Loss of blood through autotomy is limited but might benefit nearby conspecifics if they can detect it.21 Interestingly, Parsons and Eggleston,23 also using Y-mazes, found that P. argus lobsters significantly chose shelters with scents of intact conspecifics but responded at random to shelters emanating scents from lobsters that had been subjected to the breakage of three limbs before the trials.

Given these findings, I reanalyzed results from our trials1,20 (including some not previously reported) because some of our experimental lobsters lost limbs as a result of handling just before the trials or during acclimatization. Thus, for each species, I separated all trials into three groups depending on whether the stimulus lobster was intact (stimulus A), non-lethally injured (i.e., had lost one or more limbs, stimulus B), or lethally injured (stimulus C). I separated the P. argus trials in this way irrespective of season, but further separated the P. guttatus trials into trials conducted in the spring or in late summer (but trials with stimuli C were conducted only in the spring). Then, for each stimulus, I subjected the results to a 1-tail binomial test (α = 0.05) where the null probability of choosing the shelter receiving the stimulus was equal to 0.5. For each species, I pooled trials with stimuli B irrespective of whether the loss of limbs occurred just before the trial of during acclimatization because, although the blood of spiny lobsters clots very fast, its clotting time tends to increase with stress, particularly in captive lobsters.24–26 Also, the frequencies of stimuli B that had lost 1, 2 or ≥3 limbs did not differ significantly (χ²₄ = 5.246, p = 0.263) between the three groups of trials with these stimuli (one for P. argus, two for P. guttatus). On average, 59% of all lobsters used as stimuli B (n = 109) lost only one limb, 23% lost two, and 18% three to five limbs.

Panulirus argus lobsters significantly chose shelters with stimulus A, showed a random response to shelters with stimulus B, and significantly avoided shelters with stimulus C (Fig. 1). The shelter choice by lobsters subjected to stimuli A and B was consistent with Parson and Eggleston's23 results despite the variable number of limbs lost by our stimuli B. These results suggest that P. argus lobsters are able to assess the strength of conspecific alarm odors and to make a decision as to whether or not to avoid the source of these alarm odors accordingly. These results are consistent with previous findings that this species is highly chemosensitive21,27 and with the notion that avoiding conspecific alarm odors is a particularly effective antipredator strategy for highly gregarious species.1,3,4

In contrast, the shelter choice by P. guttatus lobsters subjected to stimuli A or B was similar in the spring (attraction) and also in late summer (random), whereas the shelter choice of those subjected to stimuli C in the spring did not differ from random (Fig. 2). Thus, for these lobsters, the presence of weak conspecific alarm odors would not appear to affect the seasonal tendency to aggregate. In the season of high reproductive activity, some individuals would appear to avoid shelters with strong conspecific alarm odors (stimulus C), but the overall random response to this stimulus is consistent with the more cryptic antipredator behavior of this species. Therefore, although all species of spiny lobster likely use conspecific alarm odors for risk-assessment, the behavioral response of lobsters of each species to these cues would be that which reduces the risk of encountering active predators most.

Figures and Tables

Figure 1 Results of Y-maze experiments investigating the effects of scents emanating from intact (A), non-lethally injured (B) or lethally-injured (C) conspecifics on shelter choice by individuals of Panulirus argus. p-values were based on one-tail binomial tests to test for attraction, where null probability of choosing a shelter receiving scents emanating from the stimulus = 0.5.

Figure 2 Results of Y-maze experiments investigating the effects of scents emanating from intact (A), non-lethally injured (B), or lethally-injured (C) conspecifics on shelter choice by individuals of Panulirus guttatus. The spring trials correspond to the season of high reproductive activity, and the late-summer trials correspond to the season of low reproductive activity. p-values were based on one-tail binomial tests to test for attraction, where null probability of choosing a shelter receiving scents emanating from the stimulus = 0.5.

Acknowledgements

I thank C. Barradas-Ortiz and F. Negrete-Soto for their invaluable technical support in both field and laboratory activities, and E. Ramírez-Zaldívar, A. Osorio-Arciniegas, R. Domínguez-Gallegos, M. Pérez-Ortiz, J. Valladárez-Cob, K. Baeza-Martínez and D. Placencia-Sánchez for additional assistance. Funding was provided by Consejo Nacional de Ciencia y Tecnología, México (Project 40159-Q). Permits to capture experimental lobsters were issued by Comisión Nacional de Acuacultura y Pesca, México.

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