Assessment Strategies in Stoma Topods - IngentaConnect

BULLETIN OF MARINE SCIENCE, 41(2): 135-150,1987

ASSESSMENT STRATEGIES IN STOMA TOPODS Roy L. Caldwell ABSTRACT Every animal contest has a unique set of costs and benefits. Individuals better able to estimate these values and use this information to decide on whether or not to fight for a resource should achieve higher relative fitness. Two major classes of information can influence when and how an animal will fight. The value of the contested resource sets the benefits to be gained. The relative fighting ability of the contestants determines the potential costs. This paper discusses how stomatopod Crustacea assess and use these types of information. Not surprisingly, as the value of a resource such as a cavity increases, an individual is more likely to fight for it. More interesting are situations where stomatopods attempt to determine the fighting abilities and/or motivation of an opponent. Stomatopods use several tactics to assess an opponent's lighting ability including escalated contests, ritualized tests of strength, and estimates of size. They also can recognize individuals and use previous experience with an opponent to gauge future interactions. I also show that variations in an animal's own lighting ability enter into decisions on how and when to light. Such a sophisticated assessment repertoire most likely evolved in stomatopods in association with the development of powerful offensive weapons.

There are several requisites for the evolution of aggressive competitive strategies (Dingle, 1983). First, the resource must be defendable or quickly consumable once acquired. A resource that can be occupied (a burrow or nest), sequestered (stored food or a guarded mate) or that occurs within a limited and well-defined space may be worth fighting for, while more scattered resources may be too costly to gather and/or impossible to defend (Zahavi, 1971; Rubenstein, 1981). Similarly, it may be worth fighting for access to a resource that can be quickly consumed or used, but not worth the cost if possession invites continued attacks by competitors.

Second, the animal must be able to acquire and/or defend the resource by increasing its cost to competitors. By altering the cost/benefit balance to the point that competitors are unwilling to incur greater costs to obtain or maintain the resource, an aggressive animal can increase the probability that its opponent will defer. Parker (1974) calls this ability to increase costs through aggression "Resource Holding Power" (RHP). Although the term appears to focus on the defense of resources, RHP, as originally defined, is " ... a measure of the absolute fighting ability of a given individual." It includes both the defensive and offensive abilities required to fight for a given resource. RHP consists of some combination of morphological and physiological traits such as weapons, armor, greater energy reserves, strength and endurance, and the behavioral repertoire needed to effectively use them during a contest (Caldwell and Dingle, 1975; Geist, 1977). Finally, the contested resource must be worth more than the cost of engaging in aggressive actions (Brown, 1964; MacArthur, 1972). Unless, on average, the extra costs of aggression are more than repaid by the additional resources gained, we would not expect aggressive strategies to evolve or be learned. This has been particularly well-documented for species defending feeding territories, with value usually expressed as a function of quality or quantity of the required resource (Carpenter and MacMillen, 1976; Myers et aI., 1979; Davies and Houston, 1984). However, the principle should hold for any limiting resource whether it is food, 135

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mates, shelter, or others. If at least these conditions are satisfied, aggressive strategies of intra- and/or interspecific competition may evolve. Not every contest will carry the same potential costs and benefits. At times, it will pay to fight. At other times, it will not. Individuals that accurately assess payoffs and avoid unprofitable contests will have a selective advantage. Also, the effectiveness of various strategies and tactics may vary depending on the opponent and the context of the interaction. Again, the animal that can best assess when to alter its aggressive behavior will be favored (Parker, 1974; Maynard Smith and Parker, 1976; Maynard Smith, 1979; 1982; Parker and Rubenstein, 1981). There are two major classes of information that can influence when and how an animal will fight. One class, resource value, reflects the benefits to be gained and is largely independent of aggressive interactions with the opponent. (An individual, by non-aggressively removing a limiting resource, may decrease an opponent's relative fitness while increasing its own. The results of such competition will effectively increase resource value.) Value is determined by the specific needs of the animal for a resource, the resource's distribution and abundance, and the ease with which it can be accrued. A second class of information pertains to the costs of fighting for a resource. This includes the effects of interactions with an opponent. These costs largely will be determined by the relative RHP of the two contestants. However, other factors, such as the context of the interaction, the number of individuals competing, and the value of the resource to each of the protagonists must also be considered. We know surprisingly little about how assessments of either resource value or the potential costs of fighting are made and used. Most research on the assessment of resource value by animals has been in the context of optimal foraging decisions (Krebs and McCleery, 1984; Shettleworth, 1984; Kamil and Roitblat, 1985). An animal's ability to assess resource value has been considered less often in studies of aggression. Some notable exceptions that consider resource quality include the work of Rand and Rand (1976) studying contests by female iguanas for nesting pits, Dawkins and Brockman (1980) examining decisins made by digger wasps to fight for burrows, Sigurjonsdottir and Parker (1981) observing mate-guarding by male dung-flies, Austad (1983) investigating male bowl and doily spiders contesting access to females, and the extensive research by Riechert (1978; 1979; 1982; 1984) on resource assessment and web defense in the spider Agelenopsis aperta. Considerable attention has also been paid to the role of shell quality in fights by hermit crabs for shells (Hazlett, 1966; 1970; 1981; 1983; Reese, 1969; Fotheringham, 1976; Bertness, 1980; Dowds and Elwood, 1983; Elwood and Stewart, 1985). To assess the potential costs of a contest, an animal requires information on the other individual's fighting ability as well as its own. Relatively few studies have addressed the question of how an animal estimates its own current RHP. In some cases, this may occur through previous fighting experience. For example, the frequency of previous aggressive encounters and how the animal fared may influence its behavior in future contests (Waser and Wiley, 1979). In many species, individuals 'learn' to become winners or losers based on the outcome of previous contests, even though the same opponents are never encountered twice (Barnard and Burk, 1979, for what they call "confidence hierarchies"). In some instances, internal monitoring of physiological condition adjusts aggressive behavior in relation to changes in RHP. In lobsters, for example, the frequency and form of aggressive defense change as individuals undergo a molt, a time when RHP drops precipitously (Tamm and Cobb, 1978). A greater number of studies have considered the assessment of an opponent's

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fighting ability. Easily quantified variables such as size that directly influence RHP have received the most attention (for Crustacea see: Hazlett, 1968; Hazlett and Estabrook, 1974; Hyatt and Salmon, 1978; Caldwell and Dingle, 1979; Vannini et aI., 1983; Dowds and Elwood, 1983). Animals can obtain such information in several ways depending on the biology of the species involved, the context of the agonistic interaction, and the physical environment in which the contest occurs. Assessment methods can include: (I) actual escalated combat; (2) ritualized contests or tournaments where evaluation of physical components of fighting ability such as body size, agility, or size of weapons can occur; (3) the assessment of other correlates of fighting prowess indicating past successes (possible indicators of previous victories might include the size or quality of an occupied territory or the number of mates acquired); (4) previous experience with, and recognition of, an opponent. While it is important to be able to estimate an opponent's fighting capabilities, it is also critical to predict whether or not that individual will fight and, if so, how far it is willing to escalate the contest. Under most conditions, animals might be expected to attempt to conceal such information (Maynard Smith and Parker, 1976; Maynard Smith, 1979; but see van Rhijn and Vodegel, 1980; Moynihan, 1982). However, there are tactics that an animal may employ to acquire some indication of an opponent's intentions. One way is to determine the value of the contested resource to an opponent. (In trying to evict a bear from a cave, most of us would be much more cautious if we knew that she had cubs.) Another way is by reputation or personal experience. If the animal fought under similar circumstances in the past, it is likely to do so again. In this paper, I will explore the assessment strategies and tactics used by stomatopod Crustacea to determine when and how they fight for a resource. My goal is not to present an exhaustive survey of what is known about assessment in this group, but rather to select examples representing the diversity and complexity of information used by these animals to govern their aggressive actions. This should also provide insight into those factors that shape the evolution of assessment behaviors.

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BRIEF REVIEW OF STOMATOPOD BIOLOGY

Stomatopods are predatory marine crustaceans found primarily in shallow tropical and semi-tropical seas. Species range in size from a maximum length of 15 to 380 mm, although most reach only 30 to 90 mm total length. Sexes are separate and fertilization is internal. Mating systems are quite varied in stomatopods, ranging from life-long pairing in some lysiosqillids (Caldwell, in prep.) to promiscuous mating by females with coy males, as in Pseudosquilla ciliata (Hatziolos and Caldwell, 1983). Females brood their eggs, occasionally holding the unattached mass in their mouthparts. Larvae may remain with their mother in her cavity for up to a week, although in most burrowing species studied, they enter the plankton shortly after hatching. After considerable growth, post-larvae settle out of the plankton, molt to the juvenile form, and, depending on the species, begin excavating burrows or occupying cavities. Growth is indeterminate and molting occurs at least every few months with smaller individuals molting more frequently. Estimates oflifespan are lacking for most species, but I have evidence that individuals of some species live from 2 to 6 years, some species probably considerably longer (Reaka, 1976; Steger and Caldwell, in prep.). The biology of stomatopods is dominated by the evolution of the second thoracopods into greatly enlarged, powerful raptorial appendages used in prey capture

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and processing. The strike of a stomatopod takes less than 4 msec. Even small species must be treated with respect, since they can drive their sharp dactyl spines to the bone of a careless biologist's finger. Large species, such as the 20 cm Hemisquilla ensigera found off the southern California coast, can generate much greater power and have been known to break through thick glass aquarium walls. Functionally, stomatopods can be divided into two groups, spearers and smashers (Caldwell and Dingle, 1975). In spearers, the dactylus of the raptorial appendage is slender and is armed with multiple spines. During a strike, as the propodus snaps forward, the dactylus unfolds and impales the prey on its barbs. Spearers typically prey on soft-bodied animals such as shrimp and fish. In smashers, the second thoracopod is modified to deliver crushing blows. The merus is enlarged, containing a proportionally greater muscle mass to power the strike. The usually unarmed dactylus typically has an inflated, calcified heel that serves as a hammer. When attacking armored prey, smashers strike with the dactylus folded tightly against the propodus so that the point of impact is the armored heel. The protective coverings of even large snails and crabs are easily broken apart by repeated strikes. These appendages also serve as formidable offensive and defensive weapons used in intra- and interspecific aggressive contests. In response to the danger posed by a stomatopod strike, several morphological and behavioral adaptations appear to have evolved for use in combat. These include heavy body armor, sophisticated sensory and communication systems, and considerable learning ability. Often, such adaptations used in fighting are most developed in those groups, such as the smashing gonodactylids and odontodactylids, that possess the most dangerous weapons. For published reviews of stomatopod biology and behavior, see Caldwell and Dingle (1975; 1976), Caldwell (1985), Reaka (1979) and Reaka and Manning (1981). CONTESTED RESOURCES

Earlier in this paper, I made the point that for aggressive competitive strategies to evolve, the animal had to be able to aggressively increase the cost of a resource to its opponents, the resource had to be defendable, and the resource had to be worth the added cost of the aggressive actions. There is little question that stomatopods with their powerful weapons are capable of inflicting cost on an opponent. Even heavily armored stomatopods can be killed by a strategically placed blow. Injuries during combat are frequent (Berzins and Caldwell, 1983). While stomatopods occasionally may fight over food or mates, the resource that serves as the most common focus of aggressive competition is shelter. Nearly all species occupy some type of defended, multi-purpose burrow or cavity. Aside from affording protection from predation, these refuges offer places to mate, to brood offspring, to capture and process prey, and security when molting or wounded. Burrows and cavities are discrete, defendable resources that meet the second criteria for the evolution of aggressive competition. In both laboratory and field studies, we have found repeatedly that residents have an advantage defending their cavities and burrows against other stomatopods (Dingle and Caldwell, 1975; Caldwell, 1979; Berzins and Caldwell, 1983; Steger and Caldwell, 1983; Caldwell, 1986a). Most spearing species are found in association with soft substrates and excavate their own burrows. The initial stages of digging in these stomatopods are remarkably similar, whether by a 15-mm Nannosquilla decemspinosa or a 300-mm Lysioquilla maculata. The animal starts by opening a slit trench, using its pleopods to fan sediment backwards, and bulldozing material forward with its mouthparts.


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Once the trench is about the size of the animal, it pushes more material to the front, forming a nearly vertical wall. It then scoops up sediment from the base and carries it backward, occasionally using the pleopods to blow the material out of the trench. As a depression begins to form, the stomatopod dives into it headfirst, grabs a load of substrate in its thoracopods, backs out and deposits the material in the rear of the trench. Once the hole is about one half a body length deep, the animal no longer backs out, but turns around and emerges head-first, carrying or pushing the tailings from the developing burrow. Frequently, when the animal jack-knifes in the tube, it flexes its body, compacting the walls. Some lysiosquillids also appear to mix a mucus-like secretion with sand to help stabilize the walls and entrance. As the burrow becomes longer, the excavated sediment is carried up to several body-lengths from the entrance and is distributed evenly to avoid forming a mound. The length and shape of the burrow varies with the species, but most are slightly larger in diameter than the occupant. Typical squillid and pseudosquillid burrows are u-shaped with two entrances 5 to 15 body lengths apart (Dingle and Caldwell, 1975; 1978). Most small lysiosquillids dig simple vertical tubes, but larger species, such as Lysiosquilla tredecimdentata, can have enormous u-shaped burrows. We measured one burrow at Phuket, Thailand, that was 10.5 cm in diameter and nearly 10m long (Dingle et a1., 1977). The majority of smashing species defend cavities in rock, coral, or other hard materials. While the stomatopods may modify these cavities by chipping away or filling in entrances, they are usually not responsible for their initial formation. Most cavities originate through natural erosion or the work of a variety of boring organisms such as clams and sipunculids. There are exceptions. For example, Gonodactylus ternatensis from the Indo-Pacific is found living inside Pocillopora coral heads in chambers which it forms by chipping away the interior branches. In the Caribbean, G. bredini is commonly found in shallow back reef areas inhabiting hollow coralline algae nodules. These are formed when the stomatopods occupy a small piece of coral rubble and construct a chamber by filling in the interstices with pieces of coral and shell. Openings are continually repaired. Gradually, coralline algae establishes itself on the rubble, over-grows it, and cements the structure together (Caldwell, pers. obs.). For very large species, however, there are few natural cavities that can accommodate adults. For this reason, perhaps it is not surprising that two of the largest species of smashers, Odontodactylus scyllarus and Hemisquilla ensigera, excavate burrows in sand and mud respectively. Both, however use large pieces of shell and rubble to fortify their entrances (Caldwell, unpubl.). What evidence is there that burrows and cavities represent to stomatopods a resource worth the costs of aggression? Ideally, we would like to know the effects on an individual's fitness of not having a cavity or burrow and the costs associated with acquiring and maintaining one. Unfortunately, such data are not available. However, we can infer cost from several kinds of observation. One cost is the risk of being preyed upon while away from shelter. Most stomatopods are secretive and only briefly leave their burrows or shelters to feed or locate mates. Those species that cover large distances while foraging do so either when predators are absent or they are large enough to ward off predators. For example, on shallow reef flats where I have studied gonodactylids, it is rare to see stomatopods out of their cavities during high tide when large fish are present. Yet during low tide, in areas where water depth is less than 10-15 cm and the fish have been forced to leave, many gonodactylids actively forage in the open. As the tide turns, and predatory fish move back into the area, the stomatopods return to their cavities. Actual predation on stomatopods has rarely been observed, although they are

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frequently recorded from fish stomachs, Stomatopods caught in the open are also subject to other predators. For example, during several consecutive days of severe exposure on the reef flats around the Galeta Marine Laboratory in Panama, many gonodactylids were forced to vacate their cavities. Great egrets and little blue herons converged on the area and were observed to take up to 4 G. bredini per heron per min. For several months, many stomatopods collected from this area had beak marks and there was an unusually high incidence of missing appendages (Caldwell and Caldwell, in prep.). Perhaps the strongest circumstantial evidence for the costs of being without a cavity comes from size/sex ratio analysis. In most gonodactylids, a male and female co-habit a cavity for a few days prior to oviposition. Immediately after the female lays her eggs, the male leaves. If the female moved into the male's cavity, he must now find another. But even if he searched for the female and entered her cavity, the chances are that his is now occupied by another stomatopod. In a Panamanian population of G, bredini, most females lay their eggs during the full moon. During the following week, almost twice as many adult males colonize vacant artificial cavities as at any other time of the month. Presumably, these males recently bred and are now searching for new cavities. At the size of first reproduction (25-30 mm), the sex ratio in this population is 1:1. However, for animals that have bred for a year or more (>40 mm), only 30% are males. Males and females do not differ in maximum size or growth rate and both sexes leave their cavities to search for mates. The most plausible explanation for the loss of large males is that after each breeding episode, they are exposed to increased predation while searching for cavities (Caldwell, 1986b). Similar changes in sex ratio occur in most gonodactylid populations that I have studied. The value of burrows and cavities appears to influence the nature of aggressive contests for them. Generally, burrowing species are less aggressive in the defense oftheir homes than are cavity-living species (Caldwell and Dingle, 1975). Perhaps suitable cavities are often difficult to acquire, while burrows can be constructed quickly at relatively little cost. We might, therefore, expect species using cavities to engage in more frequent and costly contests for shelters. Data supporting the assumption that cavities may be limiting for at least some gonodactylids are beginning to appear (Steger, 1985; Reaka, 1985; Caldwell et a1., in press). However, since most burrowers have spearing raptorial appendages and most smashers live in cavities, it is impossible to separate the confounded effects of weapon type and nature of their shelter on the intensity of aggression. Studies on the aggressive behavior of the few smashers that burrow, and the spearers that occupy cavities would be useful, but we have very little information on these species. Preliminary observations on H. ensigera and O. scyllarus, both large, heavily armed smashers that construct burrows, suggest that, as expected, they are much less aggressive than most other cavity-living smashers that have been studied (Caldwell, unpubl.). Comparative studies of closely related species have revealed that the cost of burrow construction or scarcity of cavities are correlated with levels of aggression. For example, in the Bay of Panama, I studied two species of Meiosquilla that often occur in the same habitat. However, M. dawsoni usually digs its burrows in soft mud, while M. swetti prefers more rocky substrates. Although the size and shape of the burrows of the two species are similar, excavation of a burrow in the preferred substrate takes M. swetti 10 times longer than M. dawsoni. In staged intra-specific contests, M. swetti was more vigorous in its burrow defense. Also, when the two species were matched against one another, M. swetti usually won (Dingle, 1983). A somewhat similar situation is described by Dingle and Caldwell (1975) for two burrowing squillids from the Gulf of Siam. Again, the species that


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appears to invest the most in burrow construction is the most aggressive in its defense. ASSESSMENT OF RESOURCE VALUE

Given that stomatopods compete aggressively for burrows and cavities, I would now like to focus discussion on how various costs and benefits associated with fighting are assessed, and how this information is used. One important variable is the specific value of the shelter. This will be affected by many factors such as physical location, the availability of food, the competitors and predators in the area, and the cavity's defensibility. Data are available only with respect to a stomatopod's defense of cavities of different size and shape. Working with G. bredini, Steger (1985) found that residents were more successful defending cavities of a preferred size (10 times their volume) against same-sized intruders. It could be argued that such cavities were more easily defended or that intruders were less willing to fight for undesirable cavities. However, as cavities became larger than the preferred size, the residents were less likely to be first to escalate a contest. When the cavities were even larger, 40% of the residents deserted the cavity without a fight. This contrasts with the situation when the cavity was the preferred size and none of the residents fled without some sort of aggressive interaction. It appears that the residents weigh the value of the cavity against the potential costs of an escalated contest and are unwilling to fight when cavity value is too low. Cavity value also varies with an animal's need for protection. Montgomery and Caldwell (1984) found that G. bredini females were more likely to defend cavities against intruders when they were brooding eggs or larvae. Against slightly larger intruders, 96% of the females with eggs retained their cavities while only 64% of non-brooding females were successful. Brooding females were not more likely to escalate contests, but they were less likely to flee the cavity when struck by the opponent. This willingness to persist in a contest reflects the value of the eggs to the female and the need for a cavity to protect them. While females are capable of taking their eggs with them if evicted, it is unlikely that the brood would survive without a cavity. One interesting finding of this study was that even if a female's eggs had been taken from her 5 days earlier, she remained more likely to successfully defend her cavity. This suggests a general change of aggressive state in brooding females, and not a more proximate response to the presence of eggs. When stomatopods molt, they are unable to strike and their body armor is ineffective. Adults within 2 or 3 days of ecdysis cannot stop the process. If a cavity-dwelling stomatopod were to be evicted just prior to molting, the chances are poor that it could secure another cavity and avoid predators until its exoskeleton hardened several days later. This is another situation where the value of a cavity increases because of the greater need for protection. As expected, G. bredini are more likely to escalate the defense of their cavity a few days prior to the molt, incurring greater risk to increase the probability that they will be able to retain the cavity (Caldwell, 1986a). ASSESSMENT OF AN OPPONENT'S FIGHTING ABILITY

When making decisions about when and how to fight, information about an opponent's ability and inclination to contest a resource is crucial. Obviously, the most direct way to obtain such information is to engage the enemy. In stomatopods, this involves considerable risk, due to the strength of the raptorial appendages. But many fights do involve a full escalation with the two contestants attempting to strike and stab one another. Often, one individual gives up only after

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it has been injured. Still, most contests are settled before they escalate to this level, with one or both individuals withdrawing. The benefit to be gained is not worth the risk of combat. One way to estimate an opponent's strength is through ritualized combat or tournaments. While stomatopods do not appear to have evolved contests as ritualized as head butting in rams or roaring in red deer, gonodactylids do engage in somewhat similar behaviors. The power of an opponent's strike has an obvious bearing on the risk of a contest. Gonodactylids appear to use their heavily armored tel sons to determine the striking power of the opponent. During the initial stages of a contest for a cavity, the resident will often coil in the entrance, blocking the opening with its telson. Intruders, attempting to enter, strike the resident's telson. If the contestants are evenly matched, this usually has little effect. If the intruder is larger than the resident, often a single solid strike to the resident's telson will cause it to flee. A better indication of the use of the telson to assess an opponent's strength can be seen in the intruder's behavior. Because the resident is hidden inside the cavity, the intruder usually has little information about the resident's size or ability to fight. Frequently, the intruder will coil just outside the cavity, directing its telson toward the entrance. If it receives a solid strike, it may break off the interaction. However, if the resident fails to strike, the intruder will move closer, thrusting its tel son toward the opponent, sometimes even inserting its telson into the entrance, until it draws a response. If the resident is small, has recently molted, or has damaged or regenerating raptorial appendages and strikes weakly or not at all, the intruder will immediately dive head-first into the cavity and press the attack (Caldwell, 1979; 1986a; Berzins and Caldwell, 1983). Sometimes an opponent's fighting ability can be estimated without making physical contact. For example, size is usually correlated with fighting ability and is an important variable in determining the outcome of a contest. Stomatopods are no exception. Caldwell and Dingle (1979) showed that in open field contests between two G. viridis, a 10% difference in body length was sufficient to influence the outcome of a contest. In G. bredini. a difference as small as 5% total length can affect contests for cavities (Caldwell, in prep.). It appears that stomatopods can determine such size differences without actually contacting the opponent. For example, when newly molted G. bredini were established in cavities and matched against intruders their own size or 15% larger, 85/163 or 52% fled their cavities when the same-sized intruder appeared, but 128/163 or 79% left when they saw an intruder 15% larger (G-test, P < .001). This decision to withdraw was made when the intruder was still several body lengths away, before any contact between the contestants. Gonodactylids have acute vision (Manning et aI., 1984) which is probably the modality used in making this assessment. Size can also be assessed using chemical cues. In a series of tests using G.festae from Panama, I allowed intruders access to a test cavity that contained either the odor of another stomatopod their own size and sex or that of an animal 30% smaller. The test waters were drawn from the home container of the donor stomatopods 5 min prior to the test. I attempted to maintain a constant odor concentration by adjusting the volume of sea water in the donor aquaria (800 ml/g). The intruders were familiar with the test apparatus and had previously entered the cavity, but they had no experience with the donor animals or their odor. Each of 24 intruders was tested once against the odor of a large and small donor. The order of presentation was balanced and the tests were 1 day apart. (Caldwell, 1979, for a discussion of the apparatus and procedures used.) The intruders took significantly longer to enter the cavities containing the odor


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of large animals (median entry times, same sized donor = 25 s, smaller donor = 7 s; Wilcoxon matched-pairs signed-ranks test, N = 23, T = 63.5, P < .05). Intruders also entered the two kinds of cavities differently. Most dived into the cavities containing the odor of small individuals head-first, but were much more cautious and entered telson-first when encountering the odor of large individuals (McNemar Test for Significance of Change, x2 = 9.0, P < .OI). Apparently, the intruders could estimate the size of the possible resident and therefore the potential danger of entering a cavity. How they were able to distinguish between the odors of the large and small stomatopods is unknown. In another experiment of similar design, I presented each of 24 G. festae with the odor of a single size and sex-matched con-specific at two concentrations. In one trial, the odor was at a normal concentration and for the other it was diluted to 20%. The intruder had no previous experience with the odor of the donor. The presentations were made 24 h apart and the order balanced. The intruders entered the cavities containing the diluted odor more rapidly (median entry times, normal concentration = 35 s, dilute = 5 s; Wilcoxon, N = 21, T = 52.5, P < .05) suggesting that concentration can provide information about a potential opponent. There is usually a strong correlation between the size of a stomatopod and the size of the cavity that it occupies (Steger, 1985). This being the case, and if the amount of material released is related to the size of the stomatopod, we might expect there to be a "normal" range of concentrations for odors emitting from cavities. Intruders can determine the size of the entrance to a cavity and therefore have some basis on which to estimate the size of the cavity and the probable size of a resident. A concentration weaker than expected could mean either that the resident is a relatively small animal for the volume of the cavity or that the resident is away from the cavity and that the concentration of its odor is waning. In either case, the intruder might be expected to attempt to enter. However, in the previous experiment using different sized donors, I attempted to control for concentration by adjusting the volume of the water in their home aquaria. That intruders could still distinguish between large and small donors suggests that there is also a size or age specific cue imbedded in the odor. Previous experience with an individual can also provide information about an opponent's fighting ability, provided that it can be identified at a later date. Such abilities are common among vertebrates and frequently structure their social interactions (Halpin, 1980), but have rarely been reported for invertebrates (but see Barrows et al., 1975; Linsenmair, 1985). I have found that some stomatopods can identify previous opponents by odor and alter their aggressive behavior accordingly (Caldwell, 1979; 1985). Furthermore, this ability can even extend across species. G. zacae and G. bahiahondensis are two similar stomatopods that commonly compete for cavities in the Gulf of Chiriqui. To explore the possibility of interspecific individual recognition, the following experiment was run. A G. bahiahondensis was established in a cavity and repelled a somewhat smaller G. zacae that was attempting entry. After a 5-min contest, both animals were removed. One h later, the odor of the G. bahiahondensis that defeated the intruder or the odor ofa different animal of the same species, size and sex as the original resident was placed in the cavity. (The odors were drawn from the home containers of the donors prior to the cavity defense.) The intruder was then re-introduced and its behavior recorded. Intruders took much longer and were more cautious entering the cavity containing the odor of the G. bahiahondensis that had previously defeated them. Apparently, they recognized the odor of the individual that posed a serious threat and exercised more care when approaching a cavity labeled by its odor (Caldwell, 1982).

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As discussed earlier, not only is it useful to have information about the fighting ability of an opponent, but ideally, one would also like to know the probability that it will fight. Previous experience with an individual will give some indication not only of an opponent's fighting ability, but also of its willingness to use it. A good example of this can be found in the behavior of G. bredini prior to molting. As discussed above, a few days prior to a molt, most individuals become quite aggressive, increasing the speed and level to which they escalate a contest (Caldwell, 1986a). I established animals nearing a molt in cavities and matched them against the same intruder over several consecutive days. The aggressive residents defeated the intruders, who, upon subsequent introductions, either would not approach the entrance of the resident's cavity, or, after an initial approach and sampling of the water near the entrance, fled the area. Even after the residents molted and were no longer able to defend their cavities, the intruders were unwilling to challenge them. While it is difficult to separate fighting ability from willingness to fight, it seems unlikely that the intruders would have avoided the residents had they not initially waged such a vigorous defense. Another observation helps make this point. I have observed that when a resident G. festae successfully defends a cavity and the intruder is fleeing the area, the resident will frequently strike the substrate, producing an audible click. Animals are less likely to return and attempt to enter a cavity if the resident struck the substrate while the intruder was fleeing (Caldwell, 1979). I view this as a kind of "victory display" that punctuates the defeat of the opponent (Caldwell, 1986a). An alternative explanation might be that the striking of the substrate is redirected aggression that occurs only after a particularly vigorous or protracted defense. If that were the case, we might also expect the intruders to be less likely to return. However, examining all cases where the intruder fled, I could find no correlation between the strength or duration of the aggressive defense by residents and whether or not they struck the substrate. Assessing the value of a resource to an individual may also give some indication of how vigorously it is prepared to fight. In contests for cavities, this would be difficult to determine, because of asymmetries in the information available to the contestants and because of the correlation between cavity quality and defensibility. There are circumstances, however, where this might occur. For example, given the value of a cavity to a female with eggs or larvae, we might expect that if intruders could detect that a female was brooding, they would be less likely to try to take over the cavity. However, in the experiments discussed above, there was no indication that intruders were making such assessments (Montgomery and Caldwell, 1984). ASSESSMENT OF OWN FIGHTING ABILITY

When an animal makes a decision on whether to fight, one variable that is relevant is its own fighting ability. It might be possible to compare this information against some absolute standard or against an assessment of the opponent's fighting ability to determine the risk of fighting. How, for example, does a stomatopod know that it is larger or smaller than an opponent and how is this assessment recalibrated as the animal grows? Or why, when its raptorial appendages are damaged, does an animal no longer attack an opponent? In some cases, such information may be acquired only through experience. In other cases, physiological changes may trigger pre-programmed behavioral responses. We know very little about these mechanisms in any animal, but stomatopods do provide some indication that information about an animal's own fighting ability is important in its decisions on when and how to fight.


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Stomatopods are frequently injured in aggressive contests. One of the most common wounds is the loss of one or both raptorial appendages. Without its most potent weapons, there is little chance that a stomatopod can defeat an opponent in a physical contest. However, it still might retain its cavity by adopting alternative tactics. For example, many stomatopods searching for cavities are themselves wounded or have recently molted and are unwilling to fight. Residents that remain hidden in a cavity, even if detected, may escape being challenged. When we surgically removed both raptorial appendages from resident G. bredini and introduced intact size- and sex-matched opponents 1to 15 days later, the residents were much more likely to remain concealed in their cavities than were controls from which we removed the third pair of walking legs. This was true even though it was the first time after the operation that the residents had encountered opponents (Berzins and Caldwell, 1983). An even more dramatic shift in behavior occurs when a stoma topod molts. Without body armor and the ability to strike, the animal is essentially helpless for several days. Yet many new-molts are able to retain their cavities by adopting alternative defensive tactics. Like animals that have lost their raptorial appendages, many hide. Others immediately flee, avoiding the possibility of being trapped and eaten by the intruder. Still others give an aggressive threat display which involves the spreading and extension of the raptorial appendages. In non-molting G. bredini, this display correlates with a tendency to attack (Dingle, 1969; Dingle and Caldwell, 1969) and also is an effective display of an animal's size and weapons. Steger and Caldwell (1983) present evidence that the raptorial display of G. bredini is effective in repulsing intruders. Since new-molts use the raptorial display more frequently than do inter-molts, they argue that it serves as a bluff of both RHP and intent. The bluff remains resistant to probing because about 80% of the residents using the raptorial display are inter-molts, fully capable of striking. Of particular relevance here is the observation that G. bredini vary the use of this raptorial display not only as their molt status changes, but also in response to the size of their opponent (Caldwell, 1986a; Adams and Caldwell, in prep.). G. bredini were placed in cavities within 12 h after molting. A second, inter-molt animal, matched for size and sex, was placed in an identical cavity in another aquarium. Two potential intruders were then selected, one the same size and sex as the residents and a second 15%larger. The next morning, each resident defended against one of the intruders. Twelve h later, the other intruder was introduced. The study consisted of 164 replications. Figure 1 presents data on the use of the raptorial display by the new-molt and inter-molt residents. Note that non-molting residents are more likely to use the raptorial display against larger intruders while new-molts employ it more frequently against animals their own size. The residents respond both to changes in their own fighting ability as well as to their assessment of the RHP of the intruder. Against larger opponents, bluffing is of questionable value since it also shows the resident's size. With this information, the intruder might be more inclined to attack. On the other hand, the raptorial display should be more effective against similar-sized intruders. Intact residents hold a strong positional advantage, making it dangerous to probe their defenses. Many intruders, particularly if suffering some deficit in fighting ability, may be unwilling to challenge a potentially dangerous opponent. Why intact residents use the raptorial display more against larger intruders is less obvious. Perhaps by signalling a willingness to defend, they deter some large animals from testing them. Even if challenged, with their positional advantage,

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a NEW-MOLT INTER-MOLT STAGE IN MOLT CYCLE 1/ / / / /1 SAME SIZE 1\ \ \ \ \115~ LARGER Figure I. Use of raptorial displays by new-molt Gonodactylus bredini residents defending cavities against con-specific, sex-matched intruders. The intruders were either the same size or 15% larger than the residents. Cavity size was that preferred by the residents. New-molts use the raptorial display more against individuals their own size (McNemar Test, P < 0.01, N = 162). Inter-molts used the raptorial display more against intruders 15% larger (McNemar Test, P < 0.0 I, N = 163).

formidable weapons, and strong body armor, they still have an even chance of holding off a 15% larger intruder. Against opponents their own size, residents have such a strong advantage that the threat display may not be necessary. CONCLUSIONS

In this review of the assessment strategies used by stomatopods, I have presented a sampling of the diversity of information available to animals that might influence decisions about when and how to fight. Even from this limited survey, it becomes


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obvious that stomatopods adjust their aggressive interactions in response to a large number of variables. They appear to assess a variety of parameters related to resource value. They have several ways of determining the fighting ability and probable behavior of their opponents. And they alter their actions in response to changes in their own capabilities and experience. In some cases, such as the use of individual recognition, the assessment behaviors of stoma top ods rival in complexity those characteristic of vertebrates. What is it about stomatopods that has led to the development of such a sophisticated assessment repertoire? As with most aspects of the biology of stomatopods, the evolution of the second thoracopods into raptorial appendages has been the driving force leading to the appearance of such complex behaviors. Once these weapon systems developed to the point that they were effective not only for feeding, but also in intra- and interspecific aggressive interactions, the stage was set for the coevolution of morphological, physiological and behavioral adaptations for the acquisition and defense of resources (Caldwell and Dingle, 1975; Reaka and Manning, 1981). During a contest for a cavity, the resident usually has more information than the intruder about its value. And because the resident is hidden inside the cavity, it also is in a better position to assess the fighting ability of its opponent. A resident also enjoys a stronger defensive position. Because of the narrow cavity entrance, it is difficult for an intruder to attack without exposing itself to counter-attack. Finally, the longer the intruder remains in the open trying to enter its opponent's cavity, the greater the risk it takes of attracting predators. This asymmetry in the information available and in the potential cost of fighting favored the evolution of assessment mechanisms by intruders that did not require physical contact. I think this is why some stomatopods that possess particularly lethal weapons, and which occupy cavities, have developed such complex assessment behaviors, rarely encountered in other invertebrates. Finally, let me end with a brief caveat. There is a tendency when discussing fighting behavior and assessment strategies in animals to resort to descriptive shorthand that is anthropomorphic. While I have tried not to fall into this trap, it is almost inevitable that the use of terms such as assessment, decision, and intent will imply conscious behavior. When I use such terms, I mean nothing more than that some evolutionary process has selected mechanisms that generate appropriate response. ACKNOWLEDGMENTS I would like to thank H. Dingle for introducing a farm kid from Iowa to the mysteries of stomatopod behavior and for several years of collaborative research. I am also indebted to many former and current graduate students who contributed greatly to my stomatopod research. They include: M. Reaka, K. Evans, M. Hatziolos, R. Steger, I. Berzins, E. Adams, G. Roderick, and S. Shuster. Thanks also must go the Western Society of Naturalists for arranging this symposium, to Dr. M. Salmon for his outstanding stewardship as Chair, and to J. Christy and B. Hazlett for their critical reading of the manuscript. Supported by NSF Grants BNS 78-27363 and 80-23414. LITERATURE CITED Austad, S. N. 1983. A game theoretical interpretation of male combat in the bowl and doily spider (Frontinella pyramitela). Anim. Behav. 31: 59-73. Science 211: 1390-1396. Barnard, C. J. and T. Burk. 1979. Dominance hierarchies and the evolution of 'Individual Recognition.' J. Theor. BioI. 81: 65-73. Barrows, E. M., W. J. Bell and C. D. Michener. 1975. Individual odor differences and their social functions in insects. Proc. Natl. Acad. Sci. 72: 2824-2828.

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