Behavioral Ecology and Sociobiology

Behav Ecol Sociobiol (1988) 22: 335-340

9 Springer-Verlag 1988

Diversionary displays of paternal stickleback Defenses against cannibalistic groups Susan A. Foster Department of Ecology and Evolution, State University of New York at Stony Brook, Stony Brook, NY 11794, USA Received July 23, 1987 / Accepted November 26, 1987

Summary. In Crystal Lake, British Columbia, male threespine stickleback (Gasterosteus aeuleatus) perform a diversionary display that deters cannibalistic conspecifics from entering their territories and destroying their nests or consuming offspring. In this population, the display consists of males swimming directly out of their territories and rooting aggressively in the substratum, mimicking stickleback feeding on nests of others, or digging for nesting materials. The display is elicited solely by conspecifics, and usually by benthic foraging groups of 2-300 individuals. It usually is elicited when groups are approaching the territory directly. Otherwise the male typically joins the group or remains still in his territory until the group leaves. This observation suggests that males are capable of discriminating conditions under which the display is most likely to be successful. The display is absent in a population in Garden Bay Lake, British Columbia, in which benthic foraging groups are absent. In Crystal Lake the males themselves do not risk predation by the groups, and the tendency of males to perform the display does not change with reproductive condition. Comparison with diversionary displays performed in two additional allopatric populations suggests that diversionary displays in this species incorporate elements of other behavioral sequences "displaced" to the display, and that variation in the structure of the display exists among populations.

Introduction Diversionary displays, or types of behavior that "have the effect of deflecting the attention or attack of a potential predator or other potentially dangerous intruder from the nest, eggs or young

to the adult" (Armstrong 1949a, p. 89) have long intrigued ornithologists (Armstrong 1949a, b; Skutch 1955; Simmons 1955). Though such displays are employed in defense of offspring by many avian species, they are rarely observed in other taxa (Armstrong 1949 b). In many avian species, parents are less likely to perform diversionary displays when a predator is detected at a distance from the nest than when it is detected nearby (Skutch 1955). Parental birds move inconspicuously away from the nest when a predator is detected at a distance, possibly because the predator is unlikely to discover the nest by chance if the parent (a cue to nest location) is absent. A display performed under these conditions could be disadvantageous either because it would attract the predator to offspring it is otherwise unlikely to find or because, if dangerous to perform, the parent would increase risk to itself unnecessarily. Apparently, these parental birds are able to assess the effectiveness of alternative behavioral defenses under different circumstances. In birds, diversionary displays typically involve a parent mimicking an injured and hence vulnerable bird, or a relatively vulnerable small mammal or chick (Armstrong 1949a; Simmons 1955; Skutch 1955) thus drawing the predator to themselves as alternative prey. Such behavior could place the parent at risk. Theory predicts that adults should balance the risk taken in defense of offspring against their reproductive value, such that greater risks are taken when the return expected from the defensive behavior is greatest (Williams 1966; Pressley 1981; Carlisle 1982). That performance of diversionary displays does place parental birds at risk is suggested by the observation that many birds perform these displays more often when the reproductive value of their offspring is highest (Armstrong 1949 b; Simmons 1955; Skutch

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1955), though the timing is also determined by the relative vulnerability of chicks at equivalent ages (e.g. Pederson and Steen 1985). Thus, birds that draw the attentions of predators to which they also are vulnerable tend to perform diversionary displays most often around the time of hatching and after (Armstrong 1949b; Simmons 1955; Skutch 1955; Pederson and Steen 1985) even though the risk to the parent may be small (Greig-Smith 1980). Vulnerability of nests might also influence the value of diversionary displays, and hence the probability of their evolution. Armstrong (1949a) and Skutch (1955) have argued that birds that nest well above the ground or in burrows or tree cavities tend not to perform such displays, while those nesting in more exposed sites near the ground do. Skutch (1955) also noted that pigeons with white eggs sit on their eggs tenaciously, suggesting that conspicuousness of offspring can influence the effectiveness of diversionary displays. A final relevant observation on avian diversionary displays is that they often incorporate elements of other behavior patterns (Armstrong 1949a, b; Skutch 1955). Extensive variation in the form of the displays of closely related species (Skutch 1955) and regional variation in that of the oystercatcher (Williamson 1952) suggest that diversionary displays can be added to, or lost fairly readily in response to differences in selection pressures. Here I provide a description of a display performed by members of one population of the threespine stickleback fish (Gasterosteus aculeatus), and use a detailed analysis of factors affecting the probability of the expression of this display to infer a diversionary function. Characteristics of the display are contrasted with those of birds, and variation in expression of this behavior pattern is explored by comparison with those in two other allopatric populations, including one previously described by Whorisky and FitzGerald (1985).

fry were free swimming and left the territory 12-16 days after spawning. This care included defense of offspring against potential predators and fanning to provide oxygen to the embryos (Wootton 1976). The nests were cryptic during courtship, often being identified by observers the first time by the activities of the males. They subsequently became less cryptic because sticks and rushes were placed around them as they were opened to form a pit when fry neared hatching.

Study sites Both populations described here are lacustrine forms from British Columbia, Canada. Because the Crystal Lake population is on Vancouver Island, and the Garden Bay population is on the Sechelt Peninsula across the Strait of Georgia, they probably have independent origins from an anadramous population (Bell 1984). The substratum in Crystal Lake consists of thick organic detritus upon which males nest at water depths of up to 3 m. Predators on adults include cutthroat trout (Salmo elarki clarki) and nymphs of a hemipteran insect. The major predators on embryos guarded by males were conspecifics (see below), though the leech, Haemopis marmorata, might also consume a portion of the embryos in some nests. Adult stickleback in this lake cannibalize eggs and fry up to a size of 15 mm SL. At the time male care of fry ended, 1-5 days after fry rose from the nest and were free swimming, they were still less than 10 mm SL (Foster et al. 1988). The threespine stickleback in this lake are of the relatively deep-bodied benthic form (sensu McPhail 1984). Adults fed primarily on benthic invertebrates and often foraged in groups of up to 300 fish. The population is essentially annual, with most adults breeding the summer after hatching and then dying. A small proportion might defer reproduction until the second year. Like Crystal Lake, Garden Bay Lake remains sufficiently clear for observations to be made throughout the breeding season. Much of the lake periphery consists of large granitic boulders and gravel, but breeding grounds are like those in Crystal Lake. The major predators on adults were cutthroat trout and prickly sculpin (Cottus asper). Predators on fry were prickly sculpin. In more than 400 hr of observation, conspecifics were never seen feeding on embryos or fry, though males cared for offspring for the same period of time as in Crystal Lake (in prep.). Stickleback in Garden Bay Lake are of the limnetic form (McPhail 1984). Adults have shallower bodies than the benthic form in Crystal Lake and feed primarily on plankton. This population is also essentially an annual population, though again a few males might defer reproduction until their second year.

Methods

Observations and procedures

The study species

Three and four 4 m x 4 m grids were demarcated on the breeding grounds of stickleback in Crystal and Garden Bay Lakes, respectively. At least one 10-min observation was made daily on all males that acquired territories in these grids dm'ing the reproductive season (103 and 83 males, respectively). All territories were mapped, and most males were tagged by injection of acrylic paints below lateral plates (modified scales) so that individuals could be recognized. Through sequential observations, the stage of the reproductive cycle could be ascertained for focal males. Males typically renested in the same territories, and on the rare occasions they left, they renested within 10 m (unpublished data). Nest loss and condition of the nest following loss were recorded, whether it occurred during observations

The threespine stickleback is a small fusiform fish that in the two study populations described here, Crystal Lake and Garden Bay Lake, reached maximum standard lengths (SL; the distance from the tip of the snout to the end of the fleshy lobe of the caudal peduncle) of 65 mm and 58 mm, respectively. The reproductive cycle in these populations is typical of the species (see Wootton 1976 for details). Males developed red nuptial coloration at the time they moved onto shallow littoral breeding grounds where they built nests and courted and spawned with up to 15 females before initiating parental care (see Wootton 1976 for details). Males provided all care for offspring until

337 or between them. Because nest depredations by foraging groups (Crystal Lake) or by sculpin (Garden Bay Lake) usually left large holes (not always in the case of conspecific foraging groups), loss to these predators was often evident even if not observed directly. Behavior observations were made while snorkelling or from a chair on the shore to minimize disturbance of the males. Timed behavior records were constructed using underwater time budget recorders and notes on clipboards (Foster 1985). Time records were read directly into a desk top computer, and were subsequently edited using field notes. Time records indicated the position and activity of the male (nest-directed activities, courtship, out of territory, etc.) when conspecifics were observed. Notes documented the position of the conspecifics when first detected, their movements at time of detection, and group size. All interactions with conspecifics and all other species were recorded in detail. Research was conducted in Crystal Lake between 15 May and 15 July 1985 and in Garden Bay Lake between 15 May and 1 July 1986.

Results

Crystal Lake In Crystal Lake male threespine stickleback perform a diversionary display when defending their breeding territories, nests, and offspring. The display is only performed by male stickleback with breeding territories, and is only elicited by the approach of conspecifics. In more than 700 h of observation in Crystal Lake, this display was never observed to be performed in any other context. This display involves mimicking an adult stickleback feeding on offspring in the nest of a conspecific, feeding on other resources, or rooting for nesting materials. Males swim erratically out of their territories, sometimes tilted somewhat to one side, displaying nuptial coloration, and dig vigorously in the substratum with movements like those of stickleback feeding in the nest of a conspecific. On three occasions males picked up a bright object, such as a cigarette butt or the body of a dead stickleback and swam vigourously, with lateral darting motions, out of their territories. If the display was successful (36 of 47 occasions) the male was joined or followed by approaching conspecifics which were thus deterred from entering his territory. When the display culminated in digging in the substratum, the group members joined the male in similar digging. On two occasions a male found a piece of suitable nesting material and attempted to return to his nest with it, stopping and turning around when the others followed. This was repeated several times until the others left or the male dropped the material. From nest building onward, males defended their territories against intruders capable of damaging the nest or consuming offspring. Males

Table 1. Frequencies of five responses (defined in text) by territorial male stickleback to solitary individuals and groups Response

Watch Escort Join Diversionary display Chase Total

Solitary conspecifics Male

Female Other

0 10 1 3 167 181

88 9 0 0 304 401

9 4 0 0 87 100

Group

31 28 66 44 16 185

chased newts (Taricha granulosa) by biting them and carried leeches (Haemopis marmorata) from their territories, but the majority of interactions involved conspecifics (unpublished data). The relative frequencies with which different responses were elicited by groups and by solitary individuals differed. RxC analysis (Sokal and Rohlf 1981) demonstrated significant heterogeneity among the columns in Table 1 (G= 585.15, d f = 12, P<0.001). Females and "others" (immatures and large individuals that could not be sexed) fell into one homogenous subgroup (P>0.05, unplanned G-test between all pairs of columns; Sokal and Rohlf 1981). Responses of males to this subgroup and to males and groups all differed ( P < 0.05, unplanned G-test between all pairs of columns). Solitary conspecifics were usually (82% of 682 encounters, Table 1) chased from the territory, though they were occasionally escorted (the male swims laterally adjacent to them) at the territory periphery or, in the case of gravid females, were watched as they swam through. Chases were effective; in all 558 recorded cases (Table 1) solitary intruders left the territory when chased. In contrast, groups of conspecifics larger than 10 were rarely chased, and when they were, the chase was rarely effective. Nine of the 16 chases at groups recorded in Table 1 were at fewer than five individuals. In the remaining seven cases, chases were directed at peripheral members of groups leaving the territory, and in no case was there any perceptible effect of the attacks on the movement of the group as a whole. In 8 cases in which attacks by groups on nests were observed, chases failed to end the attack until the nest was destroyed and all offspring were consumed. In only 2 cases did the attack end before all of the young were eaten. Conspecific groups consumed the embryos in at least 13 of the 38 focal nests in which spawning occurred in the 1985 breeding season at Crystal Lake (based on direct observation or on the presence of pits where nests had been pre-

338 Table 2. Frequencies of four responses of territorial male stickleback to groups (two or more individuals) in relation to the position and movement of the group at the time it was first detected by the male

Response

Outside territory

Approaching In territory territory

Watch/Escort Join Diversionary display Chase

33 58 3 3

3 3 34 6

23 5 7 7

Stage in the male reproductive cycle, even when stages prior to spawning were included, had no effect on the tendency to perform diversionary displays (Table 3). RxC analysis of Table 3 did not detect significant heterogeneity among columns (G=2.05, d f = 3 , P>0.50). Garden Bay Lake

Table 3. Frequencies of diversionary displays and of all other

responses combined (see Table 1 for list) in relation to male reproductive condition Response

No nest

Nest only

Embryos or wrigglers

Fry

Diversionary display Other

7 22

24 93

12 25

2 7

Diversionary displays were never observed in over 400 h of observation in this lake, even when groups feeding on plankton were present above territories. Males either joined the groups and fed, or they attempted to solicit females for spawning (unpublished data). Discussion

viously). The majority of an additional 13 losses were also probably due to predation by conspecific groups, though desertion by males, predation on males by trout, and predation on embryos by leeches and newts might have been responsible for some failures. No such causes of nest failure were ever observed directly, however. Though the diversionary display of the threespine stickleback in Crystal Lake is usually performed only in interactions with groups of conspecifics, there is considerable variation in the responses that are elicited by groups. A four-way contingency table analysis using log-linear models (SAS 1985) demonstrated no significant interactions between group size and stage of the male in the reproductive cycle, or between these factors and response of the male or position of the group when first detected by the male (P > 0.725, all interactions). Only the position of the group when it was first detected had an effect on male response (Table 2). RxC analysis of Table 2 demonstrated significant heterogeneity among columns (G= 122.62, 6 df, P<0.001), each of which differed from the others (P<0.05, unplanned G-test between all pairs of columns). When groups were first detected outside the territory males typically watched (oriented toward the group while remaining motionless in the territory), or joined them until the group left the vicinity. When the group was first detected in the territory males often ceased activity and remained still until the group left (23 of 40 cases, Table 1). Only when groups were approaching the territory were diversionary displays performed frequently (Table 2).

The diversionary display was a prominent component of offspring defense against groups of conspecifics in Crystal Lake where cannibalistic foraging groups were common, but was never observed in Garden Bay Lake, where such groups do not form. The diversionary display of males in Crystal Lake was frequently successful in diverting approaching groups from entering the territory of the male. Thus, the primary function of the diversionary display in Crystal Lake is apparently to divert conspecifics from feeding on guarded offspring or destroying the nest. Male stickleback are unable to defend nests from foraging groups by attacking individual members, probably because these attacks are spread among all group members (Barlow 1974; Robertson etal. 1976; Foster !985). Foraging groups of the threespine stickleback in this and other populations (Kynard 1978; Whorisky and FitzGerald 1985) might form solely to gain access to embryos defended effectively against solitary individuals, as they do in one species of Pacific wrasse (Foster 1987). This hypothesis remains to be tested. In any case, these groups, ranging in size from 2-300, consumed the embryos in up to 26 of the 38 focal nests in which spawning occurred in the 1985 breeding season, and were thus the primary cause of nest failure in Crystal Lake. As is the case in many species of birds, diversionary displays in the threespine stickleback are probably disadvantageous when groups are unlikely to enter the territory, because they can attract the attention of the group. Support for this hypothesis is found in the relatively high frequencies with which males watch or join groups that are not approaching their territories. Similarly, displays could be risky when the group is already

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in the territory, because movement near the nest can alert the group to its presence. Both courtship activities and nesting activities of paternal stickleback often attract the attention of conspecifics (in prep.). Thus, parental birds and threespine stickleback appear able to assess differences in the effectiveness of alternative behavioral defenses under different circumstances and to perform them appropriately. A contrast between the stickleback and other species of fishes that guard resources that are subject to the depredations of foraging groups suggests the importance of a cryptic nest or resource for the evolution of diversionary displays. Foraging groups can feed within five cm of threespine stickleback nests in any stage and fail to attack (pers. obs.), demonstrating that even once sticks and rushes have been placed around the nest it is not readily detectable to conspecifics. In contrast, the defended resources of other species of fish which have not evolved diversionary displays are either highly visible algal mats (e.g. Barlow 1974; Robertson et al. 1976; Foster 1985) or exposed, large, bright purple egg masses (Foster 1987). This comparison corroborates the suggestion made by Armstrong (1949a) and Skutch (1955) in a comparison of avian diversionary displays, that these displays are unlikely to be effective when young are obvious and easily detected by predators. Unlike many species of birds (Armstrong 1949 b; Skutch 1955; Simmons 1955; Greig-Smith 1980; Pederson and Steen 1985), stickleback in Crystal Lake show no tendency to perform diversionary displays more often when the reproductive value of their offspring is highest (Table 3). This probably reflects the difference in risk to the parent performing the display. Although the risk to some parental birds in performing diversionary displays appears to be low (Greig-Smith 1980), the reasonable inference that avian parents performing such displays are attracting predators to themselves as alternative prey suggests that they are increasing risk to themselves by doing so. In contrast, stickleback incur no similar risk in performing the diversionary display because as adults they are not vulnerable to predation by adult conspecifics. Thus, the tendency of Crystal Lake stickleback to perform this display is influenced only by the probability of success. It is possible that in a third lake, Hotel Lake on the Sechelt Peninsula of British Columbia, males will be more risk-sensitive because both prickly sculpin (which do prey on adult stickleback) and benthic foraging groups are present. Performance of diversionary displays could make

males more vulnerable to the sculpin even though the display is elicited by conspecific groups. An intriguing, though infrequent, modification of the diversionary display observed in Crystal Lake involves males picking up bright objects (cigarette butts and dead stickleback) and swimming rapidly away from their territories. These displays are particularly effective, usually attracting groups of several hundred, including most of the nearby paternal males. The male with the object will swim long distances (up to 5 m) with the groups following him, until another grabs the object (in which case the male then follows the group) or the male drops it and returns to his territory. This interesting display bears some resemblance to tool use by other animals, though this may be an extreme interpretation of the behavior. That males occasionally find nesting materials during diversionary displays and attempt to return to their nests with them despite the presence of conspecifics, suggests strongly that this display has its origins in nestmaterial acquisition or feeding behavior patterns. This hypothesis is further supported by the similarity of the digging behavior in the display to the behavior of stickleback feeding on nests of conspecifics, and by the frequency with which groups join the male and appear also to perform this behavior. As in the case of avian diversionary displays, the displays of stickleback vary. As in the case of oyster catchers (Williamson 1955) they are absent in some populations, and vary in form among the stickleback populations in which they are found. A form of the display different from that performed by Crystal Lake stickleback is exhibited by males in a salt marsh population in Quebec, Canada (Whorisky and FitzGerald 1985), which prominently incorporates components of the courtship ritual. These authors described males as assuming the show position (in which the male turns on his side with his snout in the nest opening, apparently indicating the location of the nest entrance to a potential mate; Wootton 1976) and swimming rapidly out of their territories where they tap the substrate rapidly with their snouts, attracting the groups if the display is successful. Whorisky and FitzGerald suggested that these males were attracting females in the group with "sex" apparently in the form of a possible spawning opportunity. A third form of this display is observed in stickleback in Hotel Lake. In this population, males turn on their sides, as in the display observed by Whorisky and FitzGerald (1985), but swim with their tails twisted upward, and then root frantically in the substratum, as at Crystal Lake. The swim-

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ming pattern is extremely erratic. This, combined with the way the tail is held, causes the fish to appear injured. The contrast in the form of the diversionary display in these populations suggests that in the stickleback, differences in selective regimes to which allopatric populations are exposed might have favored the addition of different types of behavior to the diversionary display, or that such differences have evolved by chance. Similar variation in the components of behavior patterns incorporated into the diversionary displays of birds have also been documented within and between species (Armstrong 1949a; Williamson 1952; Skutch 1955). Variation in the forms of diversionary displays among stickleback populations might result from parallel evolution or local modification of a pre-existing display. Both explanations have been advanced to explain the enormous morphological variation among populations of the threespine stickleback and other taxa (Bell 1984, 1987). Current research suggests that stickleback behavior will prove as variable among populations as morphology, and that the differences in the diversionary displays described here only represent a small part of this variation. Acknowledgements. This manuscript benefited from comments by J.A. Baker, M.A. Bell, G.C. Williams, two anonymous reviewers and from discussions with J.D. McPhail and G.J. FitzGerald. D.C. Houle helped with statistical analyses, and M.Y. Town and V.G. Garcia provided field assistance. J.D. McPhail provided invaluable advice. This research was made possible by the Ministry of Environment, Province of British Columbia, Canada. W.R. Pollard of MacMillan Bloedel graciously arranged access to Crystal Lake. The research was supported by a National Research Service Award (1 F32 MH09244) from NIMH. This paper is contribution No. 646 in Ecology and Evolution at the State University of New York at Stony Brook.

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Bell MA (1984) Evolutionary phenetics and genetics: the threespine stickleback, Gasterosteus aculeatus and related species. In: Turner BJ (ed) Evolutionary genetics of fishes. Plenum, New York, pp 829-835 Bell MA (1987) Interacting evolutionary constraints in pelvic reduction of threespine sticklebacks, Gasterosteus aculeatus (Pisces: Gasterosteidae). Biol J Linn Soc 31:347-382 Carlisle TR (1982) Brood success in variable environments: implications for parental care allocation. Anita Behav 30:824-836 Foster SF (1985) Group foraging by a coral reef fish: a mechanism for gaining access to defended resources. Anim Behav 33: 782-792 Foster SF (1987) Aquisition of a defended resource: a benefit of group foraging for the neotropical wrasse, Thalassoma lucasanum. Envtl Biol Fish 19:215-222 Foster SF, Garcia VB, Town MY (1988) Cannibalism as a cause of ontogenetic shifts in resource use by fry of the threespine stickleback (Gasterosteus aculeatus). Oecologia (Berlin) 74: 577-585 Greig-Smith PW (1980) Parental investment in nest defence by stonechats (Saxicola torquata). Anim Behav 28:604-619 Kynard BE (1978) Breeding behavior of a lacustrine population of three-spine sticklebacks (Gasterosteus aculeatus L.). Behaviour 67 : 178-207 McPhail JD (1984) Ecology and evolution of sympatric sticklebacks Gasterosteus: morphological and genetic evidence for a species pair in Enos Lake, British Columbia. Can J Zool 62:1402-1408 Pederson HC, Steen JB (1985) Parental care and chick production in a fluctuating population of willow ptarmigan. Ornis Scand 16 :270-276 Pressley PH (1981) Parental effort and the evolution of nestguarding tactics in the threespine stickleback (Gasterosteus aculeatus). Evolution 35: 282-295 Robertson DR, Sweatman HPA, Fletcher EA, Cleland MG (1976) Schooling as a mechanism for circumventing the territoriality of competitors. Ecology 57:1208-1220 SAS Institute (1985) SAS user's guide: statistics, version 5 edition. SAS Institute, Cary, NC Simmons KEL (1955) The nature of the predator reactions of waders towards humans, with special reference to the role of aggressive-, escape- and brooding-drives. Behaviour 8:130-173 Skutch AF (1955) The parental strategems of birds. Ibis 97: lJ 8-142 Sokal RR, Rohlf FJ (1981) Biometry. Freeman, San Francisco Whorisky FG, FitzGerald GJ (1985) Sex, cannibalism and sticklebacks. Behav Ecol Sociobiol 18 : 15-~8 Williams GC (1966) Adaptation and natural selection. Princeton University Press, Princeton Williamson K (1952) Regional variation in the distraction displays of the oystercatcher. Ibis 94:85-96 Wootton RJ (1976) The biology of sticklebacks. Academic Press, New York