Collective defense by spiny lobster (Panulirus argus) against triggerfish (Balistes capriscus):...

15Lavalli & Herrnkind—Collective defense by spiny lobsterNew Zealand Journal of Marine and Freshwater Research, 2009, Vol. 43: 15–280028–8330/09/4301–0015 © The Royal Society of New Zealand 2009

M07088; Online publication date 24 February 2009 Received 30 November 2007; accepted 17 October 2008

Collective defense by spiny lobster (Panulirus argus) against triggerfish (Balistes capriscus): effects of number of attackers and defenders

KaRi L. LavaLLiDivision of Natural ScienceCollege of General StudiesBoston University871 Commonwealth avenueBoston, Ma 02115, United States

WiLLiaM F. HeRRNKiNDDepartment of Biological ScienceFlorida State UniversityTallahassee, FL 32306, United States

Abstract Migrating queues of Caribbean spiny lobsters, Panulirus argus, suffer attacks during daylight by variable numbers of triggerfish they encounter on patch reefs. When threatened, lobsters assemble into outward facing, rosette-like groups, remain coherent in their spacing, and defend themselves by parrying with their spinous antennae. In 90-min field tethering trials involving predatory grey triggerfish (Balistes capriscus), solitary lobsters were subdued 44% of the time whereas grouped lobsters suffered only minor bites; triggerfish present numbered from 1 to 23. Victims of fish attack were significantly smaller than survivors in the field trials. although attack/defense ratios did not differ between solitary and grouped lobsters, fish behaviours towards such different groups did differ with more bite attempts/bites being directed towards solitary lobsters. in a series of experiments in large seawater enclosures, we pitted 1, 3, 5, 10, or 20 free-moving lobsters against 2 or 5 grey triggerfish, all of which had previously killed lobsters. We hypothesised that larger fish numbers would be more effective in subduing the prey independent of lobster group size, but that lobsters in larger groups would benefit by a higher per capita survival rate, as compared with

smaller groups. We found that per capita mortality declined with lobster group size, but remained the same statistically whether there were two or five triggerfish. Triggerfish interference may have played a role in reducing the effect of greater numbers of attackers.

Keywords group behaviour; selfish herd; dilution effect

IntroductIon

One of the foremost inquiries of behavioural ecology is to ascertain the function (i.e., fitness value) and evolutionary origin of cooperative social group behaviours (e.g., Krebs & Davies 1993). Highly coordinated group formations and actions are well known in a variety of invertebrate and vertebrate taxa (e.g., Allee 1931; Shaw 1970; Götmark et al. 1986; Watt et al. 1997; Foster et al. 2001; ebensperger & Wallem 2002). However, the task of assigning fitness benefit and inferring evolutionary origin of these actions is complicated by the number of contexts in which group behaviours operate: e.g., feeding, reproduction, dominance, vigilance, movement, or defense against predators. a variety of spatial arrays are described for mammalian groups when resting, foraging, or moving across open land (e.g., Hamilton 1971; Wilson 1975). among ungulates and baboons, apparently cooperative individuals create specialised formations when on the move and when threatened (van Schaik 1983; Bowyer 1987; Heard 1992; Gueron & Levin 1993). Musk oxen and american bison form phalanxes in response to approaching wolves (Tener 1954; Heard 1992) and adult baboons assemble to confront actual or potential predators (model leopard, DeVore 1972; Boesch 1991). Likewise, similar arrays are seen in non-mammalian taxa—flocking birds, schooling fish, tadpole aggregations, fiddler crab herds, and aquatic insect congregation (e.g., Foster & Treherne 1981; Smith & Warburton 1992; Creswell 1994; Uetz et al. 2002; viscido & Wethey 2002). The

16 New Zealand Journal of Marine and Freshwater Research, 2009, vol. 43

lengthy associations among grouped individuals in some of these taxa potentially allow cooperation to evolve by any of the hypothesised mechanisms—mutualism, reciprocity, kin selection, sanctioning, or by-product mutualism (Mesterton-Gibbons & Dugatkin 1992; Dugatkin 1997; Stevens et al. 2005). However, it is difficult to ascertain the consequences of such phenomena by observation alone and without knowledge of the relatedness of interacting individuals. Where individuals aggregate to avoid or reduce predation mortality, observation of predatory events is often rare, difficult to witness and thus replicate, and difficult to experimentally manipulate for ethical reasons. For example, support for predation as an evolutionary driving force leading to sociality in primates results from the rejection of alternative hypotheses, or from comparative studies of groups in high and low predation situations (van Schaik 1983; van Schaik & Horstermann 1994; Janson 1998). Because it is often impractical to rigorously examine benefits to cooperatively defending individuals, a plethora of theoretical models have emerged to assess the potential benefits for gregarious individuals (e.g., Deneubourg et al. 2002; Parrish et al. 2002; Reluga & viscido 2005; Lee et al. 2006). Gregarious spiny lobsters, which form large, com-plexly coordinated groups (e.g., queues, phalanxes, and rosettes) when moving across shelterless substrate (Herrnkind 1969, 1985; Herrnkind et al. 2001), provide a useful system to determine the fitness value of group defense through experimental manipulation under field and captive conditions. Among numerous gregarious species in the Palinuridae, Caribbean spiny lobster, Panulirus argus (Latreille, 1804), mass migrate by the thousands in single-file queues of up to 65 individuals (Herrnkind 1969; Herrnkind et al. 1973). The queue members spiral into tightly packed rosette formations (outward-facing pods described in Kanciruk 1980 and Herrnkind et al. 2001) to rest in the open; they also form such formations when attacked by unspecialised durophagous triggerfish (Balistidae) that are known to break open hard-shelled echinoderms, gastropods, and decapods (Vose & Nelson 1994; Kurtz 1995; Turingan et al. 1995; Wainright & Friel 2000). a lobster pod remains coherent as numerous individuals retaliate against an attacker with their long, spine-covered antennae; few individuals tail flip away from the group (Herrnkind et al. 2001; Parsons 2005; Briones-Fourzan et al. 2006). Triggerfish typically subdue lobsters by attacking individuals at the periphery and driving them from the group. This attack behaviour of the fish conforms

to models that suggest that capture of a peripheral individual should be the preferred and most effective attack strategy compared to selecting the nearest individual or selecting an individual separated from the group (Nishimura 2002). The fish then attempt to “disarm” the lobster by biting at the antennae and attempting to remove eyestalks (K.L. Lavalli pers. obs.; Barshaw et al. 2003). Once the lobster is disarmed, the triggerfish ram their hard mouths into the carapace or abdomen, puncture it, and eat the flesh and internal organs (K.L. Lavalli,pers. obs.; Barshaw et al. 2003). The context of these events, their complexity and coordination, and evidence from preliminary experiments (Herrnkind et al. 2001), suggests cooperative defense evolves when individuals in the group benefit (survive, reduce injury) more by fighting together than by being solitary or by defecting from the group. in addition, the lengthy oceanic larval dispersal stage of spiny lobsters (estimated 6-month planktonic period, Yeung & Lee 2002) assures the absence of close kinship among benthic phase individuals. This lack of kinship is further augmented by their individually transient nature during benthic life (solitary feeding, no long-term bonding or social organisation; Herrnkind 1980; Childress & Jury 2006). Therefore, in this taxon, attention can focus on cooperation driven by mutualism or “pseudo-reciprocity” (Connor 1986) as the main underlying process in the evolution of anti-predatory group defense. That is, actions by group members can be attributed solely to anti-predation benefits accruing to individuals that may help other group members only incidentally. We evaluated and compared survival benefits to individuals ranging from solitary through a range of natural group sizes. We also assessed how collective defense might operate to reduce the probability of mortality above the simple effect of the per capita decrease as group numbers increase (dilution; Hamilton 1971). It is impossible, a priori, to distinguish between dilution, group defense, and combined effects without testing each effect through a manipulation of the grouped lobsters’ ability to defend themselves. empirical data are necessary to answer questions of both function (benefit) and mechanism (retaliation per se, dilution effect, confusion of targets, intimidation by group size; Table 1). To evaluate such predator-prey dynamics between P. argus and its common predator grey triggerfish Balistes capriscus (Gmelin, 1788), we pitted tethered solitary and grouped lobsters against triggerfish

17Lavalli & Herrnkind—Collective defense by spiny lobster

in the field. also, because free-moving lobsters spontaneously assemble when attacked by triggerfish, we used large shelterless enclosures to manipulate essential parameters of lobster and triggerfish group sizes while controlling predator and prey size and predator hunger-state and experience. We specifically asked: (1) to what extent does increasing lobster group size reduce an individual’s per capita risk of injury or death; (2) does increasing the numbers of attackers increase predatory success; and (3) how do the anti-predator benefits to members of a lobster group change when the number of attackers increases?

MAtErIALS And MEtHodS

Field studiesWe found it impractical to conduct field trials with free-moving lobsters because of their ability to rapidly attain refuge in natural and man-made structures (rocks, large sponges, sunken timbers) at sites that grey triggerfish (B. capriscus) and another durophagous predator sheepshead (Archosargus probatocephalus Walbaum, 1792) frequented. instead, we performed field-tethering trials of solitary (n = 10) and grouped lobsters (n = 4, 5 per group) during June 1999 at four different rocky reefs 11–14 m deep, in the northeastern Gulf of Mexico, United States (site 1 = 29°48.893′N, 84°26.523′W; site 2 = 29°48.879′N, 84°26.431′W; site 3 = 29°48.527′N, 84°26.766′W; site 4 = 29°45.824′N, 84°27.903′W), which held varying numbers (1–

23) of grey triggerfish ranging from 25 to 40 cm total length (number and size data based on post-experiment hook and line capture). each site was isolated amidst extensive sandy substrate, at least 1 km from the next reef. although there probably was some change of individual fish between trial days, daily counts of triggerfish at a site were typically consistent over a trial period (3 days), suggesting a quasi-stable population of residents. We conducted two to three trials per day alternating between solitary and grouped lobsters at a site. None of the field sites had spiny lobster naturally present. Spiny lobster are uncommon in the northeastern Gulf of Mexico, occurring in small numbers of typically large individuals (>100 mm carapace length (CL); W.F. Herrnkind pers. obs.). Therefore, we used lobsters that we captured (diving/hand nets) or purchased (from trappers) from various locations in the Florida Keys. We held them in a continuous flow, open seawater system at The Florida State University (FSU) Coastal and Marine Laboratory, Florida, at ambient temperature (23–25°C) and salinity (30–32 ppt) similar to their area of capture. Juvenile and adult lobsters of typical Florida and Bahamas migratory size, c. 50 to 90 mm CL, were daily fed chopped squid to satiation. all lobsters used in experiments were in intermoult (hard-shelled) stage, had both antennae intact, and exhibited strong tail-flip and stridulating responses when handled. Our lobster tethers were modified from Barshaw et al. (2003). A plastic “cable-tie” with a heavy-duty brass fishing snap-swivel was secured firmly

table 1 Hypothetical predictions for probabilities of per capita spiny lobster (Panulirus argus) mortality and grey triggerfish (Balistes capriscus) attack success at different respective group sizes.

Hypotheses

Prey defense (n predators) 1. Dilution: per capita probability of mortality decreases fractionally as group size increases; is directly related to number of lobsters in group 2. Cooperative defense: fish attack effectiveness and per capita mortality greatly decreases (beyond that owing to dilution) with increasing group size of lobsters 3. Combined dilution and defense: lobsters in groups benefit by both decreased probability of attack and effective defense to decrease probability of mortality as lobster group size increases Predator attack success (n prey) 1. equal per capita predation success: rate of subduing lobsters is same whether multiple or solitary triggerfish participate in attack 2. Collaborative attack: attack success improves with increasing numbers of triggerfish engaged in attack behaviours or acting collaboratively 3. Interference: attack success declines with increasing numbers of triggerfish engaged in attack behaviours as a result of competition and/or display of dominance in social hierarchies


around the carapace between the 3rd and 4th walking legs with the swivel ventrally located. On site, the lobster was attached to a chain of two snap-swivels connected by cable-tie to a 2 kg diver’s weight belt lead. This arrangement allowed the lobster a 10 cm radius of movement so that it could freely pirouette and lunge during defense. Tail flipping also was unencumbered, but the anchor prevented movement beyond the scope of the swivel chain. Both treatments (solitary and grouped) were equally barred from tail flipping beyond the swivel chain; thus, the act of tethering itself did not influence one treatment more than another (see Peterson & Black 1994 and Aronson & Heck 1995 for a discussion of tethering artifacts that require control). The short swivel chain positioned ventrally did not entangle the legs. To test groups of five lobsters, we placed each tethered lobster, on its anchor, in a circle spaced so only the antennae of neighbours overlapped. This approach produced formations similar to those witnessed in nature during mass migrations (Herrnkind et al. 2001). Trials took place between 1000 h and 1600 h, the active period for the highly diurnal grey triggerfish (Vose & Nelson 1994). Our trial protocol used two divers, one to set up the site and to take coded data and written notes on a prepared waterproof form, while the other operated the underwater videocamera (SONY DCR-VX2000 camera in Amphibico VHXV2000 UW housing or SONY DCR-TRV9 camera in Quest housing). We typically alternated solitary and group trials at a site, although we ran an initial series of primarily solitary trials thereby resulting in an unequal numbers of solitary versus group trials. visibility varied daily from c. 2 to 6 m. Grey triggerfish approached the divers within minutes of their arrival, usually closely inspecting, nudging, or biting any small discrete object (camera switch, wetsuit logo, finger, ear, hair), as well as a lobster as it was removed from the net transport bag and placed on the substrate. The fish showed no retreat or startle response to the presence and actions of the observers, who remained still c. 2 m away from the tether point. Trials lasted 90 min after which a second diver pair initiated the next trial. after all trials were completed at a site, we used squid-baited, barbless hook and line to capture and measure c. 5–9 of the triggerfish present.

Mesocosm studiesWe conducted experiments in 2000 and 2001 in a large seawater enclosure using different sized aggregations of P. argus pitted against several group sizes of triggerfish, based on the range of group sizes

of each species observed in the field. We assessed the efficacy of different lobster group sizes by pitting 1, 5 and 10 lobsters against 2 and 5 triggerfish, as well as pitting groups of 3 and 20 lobsters against 5 triggerfish. In all instances we assessed outcomes (lobster mortality, injuries, fish repulsions) and the dynamics of behavioural interactions. Trials were performed at Keys Marine Laboratory, Florida in fenced sections of a 300 m long, concrete-lined, continuously flowing waterway with sloped sides. We used 2 cm mesh plastic screen to create a 6.5 m × 7 m × 1 m deep arena to observe the interactions between free-moving lobsters and predators. This arena was featureless, providing only light algal cover on a concrete lining and no shelters were present for the lobsters. Spiny lobster were captured by prod and hand net near Long Key, held in 2.5 m diameter shaded tanks with flowing sea water, fed chopped squid, and used within 1–3 days. after the completion of a trial, a hole was punched into their uropod and they were released; thus assuring we could identify previously used individuals in subsequent collections and avoid using them again in trials. Grey triggerfish were collected in the Gulf of Mexico near Big Pine Key, Florida (24.1– 42.5 cm total length (TL), mean = 32.4 ± 3.3 SE) and offshore from the FSU Coastal and Marine Laboratory at St. Teresa, Florida (25.4–41.9 cm TL, mean = 34.1 ± 2.9 Se) using squid-baited, barbless hook and line; a hypodermic needle was used to reduce swim-bladder gas pressure. Because grey triggerfish are highly social (Cleveland 2002), we held them together in a large fenced section of the seawater runway. in some instances, we held especially aggressive individuals solitarily in adjacent 2 m × 2 m screen enclosures allowing proximity and sensory contact with cohorts, but preventing injury to the lowest ranking members. We found that the fish initially interacted aggressively to establish a dominance hierarchy when we mixed individuals from different sites. By allowing them to thereafter sustain contact for several days, they quickly began hunting when placed in the trial arena, rather than reordering their social hierarchy. We noted in preliminary observations that individual triggerfish varied greatly in their initial tendency to attack a lobster and their individual persistence to eventually subdue it. Most were unable to effectively attack and subdue a lobster upon first contact, especially those from the northern Gulf of Mexico where spiny lobster are uncommon. Well-fed fish inspected a lobster, but immediately


left it to wander about the arena and did not attack again during the 3 h observation period. Even fish withheld food for the previous 24–36 h usually only approached or attempted several brief attacks, and few persisted or successfully subdued the prey. in contrast, all lobsters defended similarly by pointing, whipping, or lunging (Table 2). To raise the predatory skill level and motivation of all the fish used in the trials to a minimal standard, newly captured fish were only provided lobster as a food source until each fish was able to subdue and consume it; generally, it took 3 days for fish to effectively attack and subdue their first lobster.

Thereafter, all fish were fed chopped squid daily except during the 24–36 h period preceding a trial, assuring a predatory attack. a shaded 3 m high platform at the edge of the arena was used to observe interactions and videotape trials with a digital videocamera (SONY DCR-VX2000 or DCR-TRV9 with polarising filters). Before trials, each lobster was sexed and measured (CL, to the nearest mm), and any existing injuries were recorded. in the 2000 trials, we introduced lobsters in randomised groups of 1, 3, 5, 10, or 20 to the arena and allowed them to acclimate for at least 1 h. in the 2001 trials, we introduced

table 2 Description of behavioural actions by spiny lobster (Panulirus argus) and grey triggerfish (Balistes capriscus) during predator-prey encounters, based on videotaped interactions.

Performed by Behaviour Description

Triggerfish Approach Fish swims towards lobster within 2 antenna-lengths, yet just out of reach of either antenna attack Fish moves directly towards lobster within 1 antenna length, but does not attempt to bite the lobster Bite attempt Fish tries (jaw snaps) but fails to bite a part of the lobster Bite Fish bites the lobsters; injury may or may not be apparent Circle Fish swims a full circle one or more times around a lobster, but no more than 2 antenna-lengths away from the lobsterLobster Point One or more antennae are pointed directly at a fish, but no physical contact is made Parry Tip or side of antenna makes contact with some part of the fish; can include swiping the fish or holding one or both antenna against the fish to keep it at a distance Pirouette The lobster rapidly spins around to continually face the attacker, usually while pointing or parrying; frequently used when multiple fish are involved in an approach or attack Rear back The lobster has its abdomen tucked under its carapace and lifts up its front walking legs while simultaneously pointing and parrying towards a fish that is directly behind it Walk an individual lobster walks to another location; it may move forwards or backwards Queue Two or more lobsters walk in a single-file; the follower keeps contact with the lobster ahead by touching its extended telson with the antennules and/or anterior walking legs Whip One or both antennae are used to strike the fish; when two antennae are used, they are swept together rapidly from an outspread position to slap against the fish’s body Lunge aggressive move where antenna are swept together rapidly from an outspread position in front of the lobster and the body is rapidly (<1 s) flung forward (c. half a body length) owing to a rapid extension of the abdomen; antenna may or may not make contact with the fish; is frequently accompanied by stridulation Rosette Multiple lobsters take positions as spokes of a wheel with antennae facing outward and abdomens touching in the centre of the wheel Phalanx Multiple lobsters take positions side by side, all facing a triggerfish Tail flip Rapid flexion of the extended abdomen that lifts the lobster off the substrate and propels it backward; repetitive tail flips result in swimming in the water column


lobsters in randomised groups of 1, 5, or 10 with an acclimatisation period of 1 h. Triggerfish were held within the arena in a 1 m3 screened cage, which was removed at the start of a trial. We found in preliminary trials that triggerfish do not usually initiate attack until c. 1 h after dawn. We ran a trial in the early morning and another, with different lobsters and a second group of triggerfish, in the early afternoon. For mesocosm studies in 2000, triggerfish predators were used multiple times as there were only two groups of 5 fish available; hence, whenever possible, one fish group was used in the morning trial whereas the other was used in the afternoon trial and the order of the groups was then reversed for the next day. However, initially only one group of 5 fish was available until the end of June when another fish group was captured. In 2001, there were two main groups of paired fish, and these were also alternated in morning/afternoon trials. All triggerfish faced each group size of lobsters a minimum of 24 times in 2000 (maximum of 44) and a minimum of 4 times in 2001 (maximum of 7 times). Trials per group size of lobster numbered 13–14 in 2000; in 2001, 12–13 trials were run per group size. We took visual scan samples every 5 min for 3 h to determine how group size structure changed over time and which groups were attacked by triggerfish. Data from trials with the same group numbers (lobster and triggerfish) were pooled across years.

data analysisFor field studies, size of survivors was compared with size of victims via Mann-Whitney tests (Zar 1999). Mean size of lobsters used for group and solitary trials was also compared with Mann-Whitney tests. To determine if lobster behaviour influenced the outcome of surviving fish assaults, we compared the frequency of points, pirouettes, rear backs, whips, lunges, tail flips, and walking used by lobsters in the different group types (solitary survivors, solitary victims, and grouped) via one-way aNOva with group type as the factor after arcsine transformation of the data and plotting of the variances to assure equality among group types (Zar 1999). To determine if the per capita frequency of lobster behaviours differed among group types (solitary survivors, solitary victims, and grouped), we divided the total number of behaviours shown in each group by the number of lobsters in the group (1 or 5), performed an arcsine transformation of the frequency data, and retested via one-way aNOva with group type as the factor. We also examined the

same lobster behavioural reactions in response to the different types of fish behaviour via one-way ANOVA with fish behaviour as the factor. When differences existed, we further examined those by Tukey post-hoc test (Zar 1999). Finally, we examined the attack/defense ratios for each type of lobster grouping (1, 5) by totalling all fish threatening behaviours (swim over, approach, attack, bite) within an individual replicate and dividing that number by the total number of lobster defensive behaviours (point, pirouette, rear back, whip, lunge, tail flip) within the same replicate. The mean and standard error of these ratios were then determined for each group type (solitary survivor, solitary victim, grouped) and the ratios were compared among groups by one-way aNOva. Lobster reactions to wild fish (untrained) behaviours were recorded in behavioural transition matrices for the field trials and were separated for solitary versus grouped lobsters and survivors versus victims. The transitional probabilities were tested via χ2 contingency analysis to determine if lobster behaviours were independent of specific fish behaviours (Zar 1999). Fish behaviours were examined to determine if they differed among lobster groups by χ2 contingency analysis with a Yates correction after combining individual trials (Zar 1999). Fish behaviours displayed against the different groups of lobsters were examined with one-way aNOva and then by post-hoc Tukey tests to determine which groups differed. For 2000 and 2001 mesocosm data, size of lobster in each group size was examined for differences by one-way aNOva. Because of the nested design of the experiment, where survival status possibly differed among different group sizes of lobsters present, surviving, injured, and killed lobsters were divided into 6 size classes (10 mm CL intervals from 40 to >90 mm CL) for each group size in 2000 and into 3 size classes (10 mm CL intervals from 40 to >70 mm CL) for each group size in 2001. We then used contingency tables to test if size class of surviving, injured, or killed lobster was independent of group size of lobster (Zar 1999). Data for lobster groups of 1, 5, and 10 from 2000 and 2001 trials were then compared with paired t tests to determine differences in per capita death rates and latency to a kill for different group sizes of fish attackers (Zar 1999). Per capita death rate as predicted by the dilution effect was determined by calculating a probability of death per individual based on the total number of individuals within a group. For all statistical tests, the a level was set at 0.05.


rESuLtS

Attack and defensive behavioursDuring a typical predaceous encounter between a triggerfish and a solitary lobster, the fish initially moved close but stayed out of antennae range. The fish usually hovered above or beside the lobster or repeatedly approached it (see Table 2 for behavioural descriptions) and then began circling. Over time, the intensity and frequency of these actions escalated. a walking or stationary lobster typically responded initially by pointing or pirouetting its body to face the fish. Antennal pointing was usually maintained during a pirouette. approaches often escalated into a series of attacks, which were manoeuvres within the distance of one antenna length. The fish made darting movements, rapidly changing direction or position in the water column, often swimming on its side or upside down. Doing so sometimes provided an opening for a bite or bite attempt. The lobster generally became stationary and countered by whipping and often lunging at the fish, which typically deflected an attack. Highly aggressive attacks often included grabbing antennae, biting the antennal tips, and attempting to pull the lobster away from the group; these antennal directed attacks did not result in autotomy of the antennae. Occasionally, one or more fish dived forcefully into a rosette to separate the lobsters and then targeted fleeing individuals. The fish-lobster interactions only occasionally involved a long series of nonstop, rapid actions; usually interactions were a series of multiple bouts with brief pauses (several min duration each). During pauses, the fish usually retreated or hovered about 1–2 m away. eventually, persistent attacks resulted in successful bites. eyes, antenna tips, legs, and the posterior abdomen and telson received the most bites. Once a triggerfish landed a hard bite, a lobster sometimes began walking and occasionally tail flipping. The fish quickly chased the lobster and resumed an attack. Removal of an eye, all walking legs on a side, or a gaping puncture of the cephalothorax or abdomen usually led to rapid death. Lobster groups occasionally assembled into a phalanx and more often a rosette, where all individuals were in contact and facing outward; the structure typically remained coherent while under attack. The lobsters within the group each exhibited the same actions as solitary individuals, although several (not all) lobsters usually engaged a triggerfish simultaneously or, in large rosettes, separated clusters of lobsters within the rosette each

engaged a different triggerfish. Occasionally, part or all of a large lobster group (10–20) that was not being attacked queued up and circled the perimeter of the enclosure, reforming the rosette if threatened. especially rapid formation of a rosette occurred within minutes of severe injury to a nearby lobster. Multiple triggerfish did not initially attack together but several together made approaches, immediately attending to any lobster that was isolated or that left the rosette. Sometimes, a socially dominant fish chased and otherwise interfered with cohorts attempting to approach or attack. in this instance, several fish swam around the enclosure while the dominant fish circled, approached, or attacked. However, all fish present gathered and engaged in simultaneous or successive attacks once a lobster’s carapace was punctured which led to dismemberment of the victim (<1 min).

Field tethering trialsFourteen tethering trials (10 solitary and 4 groups of five lobsters) were conducted at the 4 different field sites over 7 days. Of the 10 solitary lobsters tested, 6 survived (57.5–69.6 mm CL) for 90 min with little or no injury, whereas 4 were killed (57.2–61.6 mm CL) in an average time of 53 min (4–85 min). Among the rosettes of 5 tethered lobsters (50.2–76.2 mm CL), all survived the 90-min field trials. The size of solitary (mean ± 1 SE: 62.5 ± 1.5 mm CL, n = 10) and grouped (64.9 ± 1.0 mm CL, n = 4) lobsters used in trials was statistically equivalent (Mann-Whitney test, U = 131.5, P > 0.05). However, the size of survivors (65.1 ± 1.1 mm CL, n = 26) was significantly larger than that of victims (59.4 ± 0.9 mm CL, n = 4) (Mann-Whitney test, U = 17.5, P < 0.05). The successful attackers were among the larger triggerfish present at a site, but not always the largest one. attack attempts were made by at least one triggerfish in all trials. The triggerfish present numbered from 1 to 10 for surviving lobsters (3.5 ± 0.4 SE, n = 26), 2 to 23 for victims (6.2 ± 0.6 SE, n = 4), and 1 to 20 for grouped lobsters (3.8 ± 0.5 Se, n = 4). There was no difference in the frequency of behaviours (point, pirouette, rear back, whip, lunge, tail flip, walk) among the various groups of lobsters (solitary survivors, solitary victims, and grouped lobsters). But differences did exist in the types of behaviours that were displayed in response to fish approaches, attacks, or bites. Pointing by all lobsters in all groups was more commonly used against fish approaches (one-way ANOVA, F = 49.3, d.f. = 8, P < 0.001) than either attacks (Tukey post-hoc, P =


0.001) or bites (P < 0.001). Likewise, whipping was more commonly used against attacks (one-way aNOva, F = 59.2, d.f. = 8, P < 0.001) than against approaches (Tukey post-hoc, P < 0.01), but bites resulted in more whips than either approaches (P < 0.001) or attacks (P = 0.01). Lunges were more commonly used against attacks (one-way ANOVA, F = 11.1, d.f. = 8, P = 0.05) than approaches (Tukey post-hoc, P < 0.05), and more commonly used against attacks than bites (P = 0.01). Because the ANOVA analysis from the field trials demonstrated no difference among lobster group type in behaviours displayed, transitional probabilities of lobster reactions to fish behaviour were pooled. Both individual and pooled chi-square analysis of the transitional probabilities of lobster behaviours to wild fish behaviours showed that for all groups of lobsters (solitary survivors, solitary victims, and grouped survivors), lobster behaviours were contingent upon the type of behaviour displayed by the fish (χ2 = 196.17 pooled, d.f. = 12, P < 0.001). Transitional probabilities of behaviours for each of the group types (solitary lobster survivor, solitary lobster victim, grouped lobster survivors) revealed that lobsters pointed most frequently in response to fish approaches, followed by whipping, pirouetting, and lunging. Whipping was used most frequently in response to attacks and then to bites. Lunging, although less frequent overall than whipping, was the next most common response to fish attacks. Pointing was not a common response to attacks. Lobsters rarely tail flipped in response to fish approaches, attacks, or bites (Table 3). attack/defense ratios calculated for the different types of defense behaviours displayed by lobsters showed no significant differences among the groups of lobsters, except in pointing (one-way ANOVA, F = 13.4, d.f. = 17, P < 0.001), which was more commonly used by grouped lobsters than either solitary survivors (Tukey post-hoc, P < 0.01) or solitary victims (P < 0.001) (Fig. 1).

Fish behaviours differed among lobster groups (one-way ANOVA, F = 22.6, d.f. = 2, P < 0.001). Fish made significantly more bite attempts and bites on solitary victims than on solitary survivors (Tukey post-hoc, P < 0.001) or grouped lobsters (P < 0.001; Fig. 2). However, fish made no more swim overs, approaches, or attacks on any one group than another.

Mesocosm trialsThere was a difference in size among groups of lobsters in 2000 (1, 3, 5, 10, or 20 lobsters) (one-way aNOva, F = 3.09, d.f. = 4, P < 0.02), with solitary lobsters being significantly larger (72.8 ± 3.2 SE mm CL, n = 13) than lobsters in groups of 3 (62.5 ± 1.5 SE mm CL, n = 42), in groups of 5 (61.6 ± 1.2 Se mm CL, n = 65), in groups of 10 (62.7 ± 0.9 Se mm CL, n = 130), and in groups of 20 (63.9 ± 0.7 Se mm CL, n = 260). all other groups did not statistically differ from each other. There was no difference in size among groups in 2001 (1, 5, or 10 lobsters) (one-way ANOVA, F = 0.8, d.f. = 2, P = 0.005). in 2001, mean size for solitary lobsters was 52.5 ± 2.1 SE mm CL (n = 13), whereas that for lobsters in groups of 5 was 55.3 ± 1.5 SE mm CL (n = 65) and that for groups of 10 was 56.4 ± 1 SE mm CL (n = 120). Within the 5 group sizes of lobsters tested in 2000, there was no difference in size of victims (χ2 = 19.74, d.f. = 20, P > 0.05) or in size of injured lobsters (χ2 = 29.35, d.f. = 20, P > 0.05; Fig. 3A). Likewise, in 2001, with 3 tested group sizes of lobsters (1, 5, 10), there was no difference in size of victims (χ2 = 3.64, d.f. = 6, P > 0.05) or of injured lobsters (χ2 = 6.5, d.f. = 6, P > 0.05; Fig. 3B). On a per capita risk basis, as lobster group numbers increased, individual lobsters experienced reduced probability of mortality against both triggerfish pairs and quintets (one-way aNOva, F = 10.9, d.f. = 4, P < 0.0001; Fig. 4) with solitary lobsters suffering more mortality by 5 fish than either 3, 5, 10, or 20 lobsters (Tukey post-

table 3 Behavioural transition matrix showing effect of fish behaviour on lobster response. All numbers reported are frequencies and represent pooled data from the three different group types of lobsters (solitary survivor, solitary victim, and grouped) after testing for differences and finding none as differences among groups were non-significant (ANOVA, P > 0.05).

Lobster behaviourFish behaviour Point Pirouette Rear back Whip Lunge Tail flip Walk

approach 62.65 8.61 0.86 17.56 5.68 1.20 3.44attack 6.17 1.47 3.72 62.19 22.33 1.57 2.55Bite 0.00 0.00 0.00 92.86 3.57 3.57 0.00


hoc, P < 0.001). However, there was no difference in per capita mortality among the other groups of lobsters (3, 5, 10, or 20). Likewise in 2001, solitary lobsters suffered more mortality by 2 fish than either 5 or 10 lobsters (one-way ANOVA, F = 20.7, d.f. = 2, P < 0.001; Tukey post-hoc, P < 0.001), but no differences in per capita mortality existed between 5 and 10 lobsters. Number of fish did not affect the per capita risk rate for solitary lobsters (paired t test, t = 0.433, d.f. = 12, P > 0.05); however, for lobsters in groups of 5 or groups of 10, there was a trend, though not significant, for a reduction in the per capita death risk when facing 2 fish instead of 5 (P = 0.05 for both 5 and 10 lobsters). Per capita death rates differed from those predicted by the dilution effect. in comparison with per capita risk rates predicted by the dilution hypothesis, solitary lobsters fared better than predicted when facing 5 fish compared with groups of 5 lobsters (one-way aNOva, F = 11.0, d.f. = 2, P < 0.001; Tukey post-hoc, P < 0.01) or 10 lobsters (P < 0.001). Likewise, for trials using 2 fish, solitary lobsters fared better than predicted for either groups of 5 lobsters (one-way aNOva, F = 20.7, d.f. = 2, P < 0.001; Tukey post-hoc, P < 0.001) or groups of 10 lobsters (P < 0.001), but for all other groups per capita death rates fell within predicted values (Fig. 4). The latency or time needed to subdue a lobster was statistically equivalent for all lobster group

Fig. 1 Mean (+ SE) attack/defense ratios of solitary sur-vivors, solitary victims, and grouped (5) lobsters tethered in field trials. Ratios were calculated by totalling all fish threatening behaviours (swim over, approach, attack, bite) within an individual replicate and dividing that number by the total number of lobster defensive behaviours (point, pirouette, rear back, whip, lunge, tail flip) within the same replicate. Asterisk indicates significant difference (ANOVA, P < 0.001) between attack/defence ratios of grouped lobsters and solitary survivors (Tukey test, P < 0.001).

Fig. 2 Mean number (+ SE) of fish behaviours directed at lobster groups (solitary survivors, solitary victims, and grouped) in field tethering trials. Asterisk indicates signifi-cantly more bite attempts/bites on solitary victims than on solitary survivors (ANOVA and Tukey test, P < 0.001).

Fig. 3 Mean size, carapace length (CL + SE) of free-ranging lobsters in different group sizes for mesocosm trials in A, 2000 and B, 2001. Asterisk indicates significant difference among all types of solitary lobsters (intact, injured, killed) and lobsters in group sizes of 3, 5, 10, or 20 (ANOVA and Tukey test, P < 0.02).


numbers when fish group size numbered 5 (one-way aNOva, F = 0.47, d.f. = 4, P > 0.05) or 2 (one-way ANOVA, F = 0.61, d.f. = 2, P > 0.05; Fig. 5). That is, triggerfish that subdued a lobster when large numbers of lobsters were present (10, 20) did so as quickly (on average) as when there were relatively few lobsters (1, 3, 5), although the range in timing was large (5 to 180 min). Time-to-kill varied according to the number of fish participating in the attacks—5 fish took longer to subdue and kill a solitary lobster than 2 fish (Mann Whitney U test,

U = 10.0, P = 0.05); there was no difference in the time to subdue a lobster out of a group of 5 (U = 19.0, P > 0.05) or 10 (U = 35.5, P > 0.05) whether 5 or 2 fish were present. Successful triggerfish subdued a lobster similarly across all lobster group sizes. For all group sizes of lobster, triggerfish mainly targeted their attacks on the eyestalks so that the antennae could no longer be directed at the fish. Other areas typically attacked included the abdomen, breaking through the carapace to remove the vital organs, removal of the tail fan, and combinations of removal of appendages (antenna or legs) and attacks on the abdomen.

dIScuSSIon

Different models have been proposed to explain the potential anti-predatory benefits of group formation. individuals in groups may have a lower per capita risk of predation by dilution (Foster & Trehern 1981), by a selfish herd response (Hamilton 1971), by increased predator detection/vigilance (Pulliam 1973), or by cooperative defense once attacked (Hamilton 1971). It seems likely that individuals in groups potentially benefit from more than one of these mechanisms, although few studies have experimentally examined such multiple benefits (see Dehn 1990). Observations of different species in the field reveal defensive formations, such as the rosette (or phalanx) formations seen also in spiny lobsters (Herrnkind et al. 2001); however, the extent to which such formations benefit the individual participants has not been determined. in the present study, we have attempted to separate benefits to individuals that may distinguish among dilution, group defense, and combined effects. When lobster group size was tested in the field with wild fish of limited experience with spiny lobster, grouping conferred 100% survival compared with 40% mortality for solitary lobsters. although tethered pods of five lobsters were approached and attacked as frequently as solitary lobsters, only the latter suffered mortal bites. individual size conferred an advantage to solitary lobsters such that larger animals suffered fewer damaging bites (such as eye removal); otherwise, solitary survivors did not differ from solitary victims in their defensive reactions to fish attacks. In contrast, grouped lobsters pointed more frequently than solitary animals and this “fence” of multiple antennae may have thwarted fish from approaching close enough to land a damaging bite. individuals within the group had a lower defense/attack ratio than solitary individuals because

Fig. 4 Mean (+ SE) per capita death rate for different group sizes of lobsters attacked by triggerfish in mesocosm trials. asterisk indicates difference between solitary lob-sters attacked by 2 or 5 fish and all other groups of lobsters (3, 5, 10, 20) at P < 0.001 (ANOVA and post-hoc Tukey tests); double asterisk indicates significant difference between rate predicted by dilution and that determined for solitary lobsters attacked by 2 or 5 fish at P < 0.001 (ANOVA).

Fig. 5 Mean (+ SE) time used by triggerfish to kill lob-sters in different group sizes. Asterisk indicates significant difference in time to kill a solitary lobster by 5 versus 2 triggerfish (Mann Whitney U test, P = 0.01).


other group members repelled approaching fish. Furthermore, each member of a rosette expended less effort (fewer defensive actions) compared with solitary individuals. in the limited number of field trials we were able to conduct, no lobsters from within a group were killed. This result supports the hypothesis that observed coherent group actions provide a defense mechanism conferring a greater short-term survival advantage to grouped individuals than that accruing from dilution. This result is also supported by a reduced defense-attack ratio for individuals in a group. Such cooperative defense could arise from the selfish actions of individual lobsters attempting to fend off attacks from predators and benefiting nearest neighbours in so doing; i.e., by-product mutualism or pseudo-reciprocity (Connor 1986). The critical element of lobster group defensive behaviour is to remain in contact and alignment with cohorts while in the open, lobsters wedged into a co-occupied den (Kanciruk 1980). Defensive actions, pointing, whipping, lunging were all similarly performed by solitary lobsters. As in the field trials, solitary individuals in the mesocosm were considerably more likely to suffer mortality than grouped individuals, but their survival was better than predicted by dilution alone—most likely this lower mortality was the result of their effective self defense and varying motivation of the attacking fish. However, as opposed to field outcomes, mesocosm lobsters within groups suffered mortalities close to those predicted by dilution effects alone, rather than benefiting from dilution plus cooperative defense, regardless of the number of fish that could potentially attack. Numerically, lobsters in groups of 5 or 10 did better than predicted by dilution when pitted against 2 fish rather than 5 fish, but this trend was not statistically significant. Three main differences between field trials and mesocosm trials may have led to differences in results between field and mesocosm: (1) the effect of forcing a type of group cohesion by tethering grouped lobsters in the field versus allowing the lobsters to separate or defect in the mesocosm; (2) differences in the social hierarchy of the fish in the field versus in the mesocosm; and (3) the high predatory skill and heightened hunger state of triggerfish in the mesocosm. In the field, lobsters were forced to remain a cohesive unit during fish attacks because they were tethered in a rosette formation. Thus, no individual could defect from the group, which, in the mesocosm, caused the fish to shift their attack from the remaining group to

the now solitary defector. if cooperative defense effects are relevant and improve survival of group members above the fraction predicted by dilution, the continued coherence of the group could maintain cooperative defense. However, the ability to defect—a presumably selfish action by an individual to escape attacks directed at the whole group—could reduce the benefit to individuals remaining within the group and, thus, lessen the effect of cooperative defense. Cooperative defense was decreased in the mesocosm—100% of the lobsters that were killed in group trials were those that the fish either dragged out by the antennae, that were forced out from the periphery of the group, or that left the group while other individuals within the group were being attacked. These defecting individuals did not necessarily benefit from defection—they usually drew increased attention from the fish, which then shifted their attacks to the moving, now solitary individual. in some instances it is predicted that predators would benefit more by targeting peripheral individuals in a prey group than by rushing the group or targeting an individual that has separated from the group (Nishimura 2002); however, defecting lobsters were frequently targeted in our study. in contrast, remaining group members tightened the rosette formation as predicted by the selfish-herd hypothesis (Hamilton 1971). Occasionally, defectors attempted to re-enter a group. Once after a forced defection where the fish dragged a lobster from the periphery and punctured its carapace, we noted that the entire rosette moved away from it as it was attempting to rejoin the group while under attack. it is therefore likely that individuals within a group can sense when an injured lobster is nearby and may act as a “selfish group” to prevent an injured individual from putting the group in possible harm’s way. Odours of injured P. argus cause individual juvenile lobsters to exit their shelter (Bouwma 2006) or result in shelter avoidance by conspecifics (Briones-Fourzan et al. 2006), and the same odours could result in a defensive pod moving away from an injured individual. as a result of these competing modes of selfishness (from defecting individuals and from remaining group members), and the high degree of fusion-fission that could occur in freely moving lobsters in the mesocosm, it is likely that cooperative defense benefits decreased as a whole, such that mesocosm group members benefited mainly from dilution alone. Differing interactions among fish also could influence the success or failure of attacks. In the mesocosm trials of 2000, we were careful to keep groups together that we caught off a particular reef


to sustain whatever dominance relationships existed amongst them. Grey triggerfish typically form a linear hierarchy in which the largest individual is the alpha and displays its dominance by both coloration patterns and body postures (Cleveland 2002). We wanted to ensure during trials that fish would be more motivated by potential prey (lobster) instead of re-establishing dominance. However, the triggerfish hierarchy in a group of 5 fish often resulted in the lower ranked individuals forming coalitions to pursue an attack on a lobster. In response, the alpha fish then disrupted these coalitions and the predatory attacks. Thus, fish interfered with each other to the lobsters’ benefit. During 2-fish trials, there was less interference and more cooperation, but predatory attacks were initiated primarily by the dominant fish and, if that fish was not particularly motivated, attacks were less likely to occur. Nonetheless, the increased cooperation and decreased interference between pairs of fish resulted in solitary lobsters being subdued more quickly by 2 fish than by 5, with a tendency for the same trend when attempting to subdue a lobster from a rosette of 5. This result is in opposition to the expectation that a larger predatory group might be more efficient in its attacks. in contrast, in the field, disruption of attacks tended to occur less frequently between conspecifics than it did between different species of fish on the reef (i.e., triggerfish disrupted sheepshead attacks, but not necessarily other triggerfish’s attacks; W.F. Herrnkind and K.L. Lavalli pers. obs.). Triggerfish almost always targeted lobster eyestalks and, as a result, most victims (>80%) in the mesocosm lost both eyes. Fish frequently grabbed and pulled on antennae, frequently reducing them in length, which then allowed them to get closer to the lobster and to its eyes. Removal of the eyes renders the antennae useless because the lobster no longer can accurately point, whip or lunge. Damage to the antennae per se can increase the probability that a lobster might suffer additional injuries, but antenna damage alone does not always determine the fate of the lobster, as single-antennaed lobsters can fight nearly as well as two-antennaed lobsters against triggerfish under some circumstances (Parsons 2005). it was expected that no lobster autotomised an antenna even when dragged a distance from the group by the antenna. This result contrasts with the rapid autotomy when octopus attack lobsters (Joll 1977; Bouwma 2006). Experience of predators could play a significant role in the outcomes witnessed in these experiments.

although the behaviours and outcomes of field tethering and mesocosm experiments provide evidence for antipredation by grouping and coincident defense by cohesive individuals, both test situations differed from natural conditions. Based on the present study, it seems likely that lobster survival is enhanced if the area traversed has triggerfish relatively inexperienced in killing lobsters. in addition, it is likely that the rather lengthy time needed to subdue a lobster (5–180 min in our trials) is sufficiently long that, in nature, the fish may abort the attack to search for easier prey. Other caveats to interpretation include the absence of structured habitat. That is, mass migrants move across both open and complex terrain. Pods and queues not under immediate attack rapidly move past patch reefs and out of attack range of the resident triggerfish and they use available objects to shield the posterior or antenna-less side (even if they cannot withdraw under them; Parsons 2005) which reduces risk. Nevertheless, both wild queen (Balistes vetula) and ocean triggerfish (Canthidermis sufflamen) have been seen dragging lobsters out of shelter or structured habitat by their antennae (Weiss et al. 2006) which suggests that, when motivated, these fish can present a significant risk to spiny lobsters. Finally, evidence from research on mass movements suggests that the degree of inter-lobster cohesion is especially strong during migration (Herrnkind 1985). although the non-migrating lobsters we used here spontaneously queued and defended in groups, they probably varied in cohesiveness. We suggest that larger, more cohesive lobsters facing less experienced triggerfish, in areas with some structure, fare better than those in the mesocosm. Nonetheless, actions by grouped individuals can enhance per capita survival over dilution and solitary defense in certain natural situations similar to that witnessed during mass migration. Other studies show that aggregations of denned lobsters are effective at repelling attacks by both piscine (Eggleston & Lipcius 1992; Mintz et al. 1994; Butler et al. 1999; Bouwma 2006) and octopus predators (Lear 2004; Lear & Butler 2004). However, the degree to which spiny lobster group defense can be deemed cooperative, rather than the by-product of selfish actions, and its likely evolutionary origin remains for further study.

AcKnoWLEdGMEntS

We thank our dive team members of Mark Butler, Sara Kelly, Jason Schratweiser, Greg Farley, and Jim Cooper for help during field trials and Captain Steve Wilson for


his handling of the R/v Seminole and for locating good sites for the trials. We also thank Michael Childress, David Cleveland, Pete Bouwma, and andy evans for help in scoring mesocosm interactions at the Keys Marine Laboratory. Scott andree and Melissa Classon gave many hours of their time in scoring videotapes and their work is greatly appreciated. amy Parsons provided useful data on the similarities and differences in defensive behaviour of free-moving versus tethered lobsters. Partial funding for this project was provided by a Research enhancement Grant to K.L. Lavalli from Southwest Texas State University, San Marcos, Texas and a faculty grant to W. F. Herrnkind by Florida State University, Tallahassee, Florida. Fish were held according to Protocol No. 0105, approved by the Florida State University animal Care and Use Committee and both fish and lobsters were captured under FFWCC Permit No. 03SR-053.

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