Ethology 84, 281-294 (1990) 0 1990 Paul Parey Scientific Publishers, Berlin and Hamburg ISSN 0179-1613

Department of Ecology and Evolution, State Uniziersity of N e w York, Stony Brook, N e w York

Determinants of Variation in Antipredator Behavior of Territorial Male Threespine Stickleback in the Wild

SUSAN FOSTER & STEPHEN PLOCH

FOSTIR, S. & P [ ~ ( : H , S. 1990: Determinants of variation in antipredator behavior of territorial male threespine stickleback in the wild. Ethology 84, 281-294.

Abstract

Although antipredator behavior of threespine stickleback has been extensively studied in the laboratory, interactions between stickleback and their predators in nature have never been described. This paper describes interactions between territorial male stickleback and four predators on males o r on the young the); guard. T w o of the predators, cutthroat t rout and a hemipteran nymph (Belo- stomatidae), prey on males but not on young. Another, the roughskin newt, is a potential predator of young but does not pose a threat to males. Prickly sculpin prey both on the males and on offspring that males guard. Differences in behavior toward the four predators indicate that males are capable of rapid discrimination among predators and the threats they pose. Males also discriminate among size classes of sculpin that present different predation risks, but not among size classes of trout large enough to pose a threat. The difference in response to these predators probably reflects the difference in risk to offspring and the amount of time each predator typically stays in the territory of a male. Trout pass through rapidly, whereas sculpin, which are ambush predators, can remain within a territory for a long period of time if not chased out . The presence of young in the nest had no apparent effect on the response of males to these predators. This could, however, be due to a masking effect o f uncontrolled variation in natural encounters. Responses to newts were similar to those directed toward sculpin too small to attack the male. They involved rapid chases and bites, often directed at the heid, a part of the body that was typically avoided in encounters with larger sculpin. Males watch and avoid the belostomatid nymphs, but d o not attack them.

Corresponding author: Susan A . FOSTER, Department of Ecology and Evolution, State University of N e w York, Stony Brook, N.Y. 11794, U.S.A.

Introduction

The ability to avoid predators is of fundamental importance in determining the fitness of an individual. The ubiquity and diversity of morphological and behavioral defenses against predators provide ample testimony to the role of predation as an agent of natural selection (e.g. CURIO 1976; ZAKFT 1980; ENDLLR

U S Cop\ r igh t Ckar.inie ( e n t c r CoJe hatcrnent 01 79-1613/90/8404-0281$02.50/0

282 SUSAN FOSTEK & STFPIEN PI ocii

1986). Prey are often capable of modifying their responses to predators with respect to context and to the identity of the predator. By doing so, prey can enhance their survival probabilities in encounters with predators because, for example, different kinds of avoidance behavior can be effective against different kinds of predators (WALTHEK 1969; T U K N ~ R 1973, WEBB 1982; ENIILI~K 1986), against different sizes of the same predator (WALTHEK 1969), o r against the same predator under different conditions (COATES 1980; WIJB 1982; ENI)LI.K 1986; HELI;MAN 1986). Furthermore, allopatric populations of prey can differ in their responses to predators, often in an adaptive manner (e.g. SEGHEKS 1974; HUN- TINGI:ORI) 1976b, 1982; OWINGS & Coss 1977; OWINGS & OWINGS 1979; GILF,S 1984; GILES & HUNTINGIWW 1984; BKEIIEN et a]. 1987; TULLEY & HUNTINGI.ORI> 1987; LOUGHKY 1988).

Variation in antipredator behavior is particularly well documented in the threespine stickleback, Gusterosteus uculeutus. This fish is well known for its morphological defense structures, including elongate dorsal and pelvic spines and bony lateral plates that are effective deterrents to many vertebrate predators (e.g. HOCKLAND 1951; HWGLAND et al. 1957). In freshwater stickleback these struc- tures tend to be best developed in populations sympatric with fish predators (HAGI:N & GII-BERTSON 1973 a, b ; BELL 1984). Similarly, antipredator behavior is best developed in populations subject to intense predation by fish and birds (HUNTINGFORI) 1976 b, 1982; GILFS 1984; GILES & HUNTINGFOKD 1984; Tu I I ’ r & H U N T I N G r O K I ) 1 9 8 7).

Within populations, female stickleback tend to have better developed fright responses than males (GILES 1984; GILES & HUNTINGIURI) 1984), possibly because males provide all care for offspring in the nest and cannot flee during the breeding season without increasing risk to guarded young (HUNTINGI-OKI) 1976 a ; GILM 1984). Males accept more risk in defending nests against prickly sculpin (Cottus uspeu), a predator on males and young, when nests contain young than when empty, and when offspring number in the nests is relatively high (PRESSLEY 1981). Even when a predator poses no direct threat to offspring, males guarding young tend to be “bolder” in their responses to the predator than d o males without nests, o r males with nests but n o young (HUNTINGFOKL) 1976a, b; KVNAKD 1978).

Although interactions between stickleback and their predators have been investigated in remarkable detail, only two studies were conducted in situ (PmssLtY 1981 ; KVNAKL) 1978). Even in these studies, antipredator responses were elicited using a preserved prickly sculpin (PKLSSLIY 1981) or a tethered, live trout as predators. Such research is valuable because more variables are controlled than in observations of natural interactions between predators and prey, permitting more detailed evaluation of causative factors. Nevertheless, completely natural in situ observations are essential if the results of laboratory and seminatural observa- tions are to be interpreted in an evolutionary context.

Here we present the first detailed descriptions of interactions between stickleback and their predators under completely natural conditions. We observed interactions between territorial male stickleback and predators that pose threats 1) to the male only, 2) to the guarded young only and 3) to both. For the two most abundant predators, sample sizes allowed us to evaluate the roles of

Antipredator Behavior of Threespine Stickleback 283

male reproductive stage and predator size in determining male response to predators. These were the cutthroat trout, Oncorhynchus cfarki (formerly Safmo clurki), that preys on adult stickleback (MOODIE 1972), and the prickly sculpin, Cottus asper, that preys on embryos and fry guarded by parental males as well as on adult stickleback (MOODIE 1972; PRESSLLY 1981). We also describe interactions between territorial male stickleback and the roughskin newt, Taricha granufosa, a potential predator on guarded young, and between males and a belostomatid nymph that attacks adult stickleback.

Methods

Most observations reported here were made in Garden Bay Lake o n the Sechelt Peninsula, British Columbia, Canada between 20 May and 7 July 1986. Although vegetation was abundant on the littoral breeding grounds of stickleback, males were never observed to nest in vegetation or under rocks and logs, also abundant in the littoral zone. Thus, the behavior of males could be readily observed. Less extensive observations were made in Crystal Lake on the east side of Vancouver Island, British Columbia, between 15 May and 15 July 1985. The breeding grounds in this lake were similar to those in Garden Bay Lake and again, because fewer than 5 % of males nested in cover, observations on the behavior of most males were possible.

Predators differed in the two lakes. Cutthroat trout and prickly sculpin are common in Garden Bay Lake. Neither is native to Crystal Lake, although cutthroat trout have been maintained by stocking during the last 20 years (records of the Ministry of Environment, Province of British Columbia). T rou t were rarely observed in Crystal Lake during the 1985 field season, apparently because unusually high temperatures forced them to remain in deep water. The roughskin newt, 7urrrha grrntrrlosa, was abundant in Crystal Lake, but rare in Garden Bay Lake. Adult newts primarily consume small invertebrates but also feed regularly o n eggs of conspecifics and other amphibians (NUSSBAUM et al. 1983). This newt probably would consume stickleback embryos. although this has never been documented directly. In Crystal Lake, interactions were also observed between male stickleback and nymphs of a large hernipteran (Belostomatidae). The latter capture and kill adult stickleback late in the breeding season. Although several insects prey on juvenile stickleback in these lake5 (I'05TFR et a]. 1988). none was ever observed to attack adults.

All interactions between predators and stickleback were recorded during extensive observations on individually tagged male stickleback that held reproductive territories. Tagging was accomplished by injection of acrylic paint beneath the lateral plates. Comparison of behavior profiles constructed for tagged and untagged males indicated that tagging had no effect on the behavior of males, o r on the responses of conspecitics or predators to the males (FOSTER, in prep.). All observations were made while snorkelling. Males only occasionally responded to the approach of observers, and even these resumed normal activities within 30 s. Movements were minimized throughout. Ten-min time budgets were constructed daily for all tagged males so that the reproductive behavior of each could he followed through the breeding season (FOSTER 1988). As a result, we knew the reproductive stages of the males observed interacting with predators.

Approximately 400 h of observations were made in Garden Bay Lake (83 males), and 700 h in Crystal Lake (103 males), as part of a field investigation of stickleback reproductive behavior. During this study, details o f the reactions of focal males to the approach of predators were recorded whenever possible. Behdvioral records of predator-prey interactions a w e sometimcs incomplete. Approxi- mately half of the interactions with cutthroat trout, prickly sculpin and newts were discarded for this reason. Additionally, characteristics of the predator (e.g. size) or its position were erratically recorded, resulting in differences in sample sizes for different statistical tests. Interactions with the belostomatid nymph were rare, and the details of all six observations were recorded.

Trout size was visually estimated as small, medium or large. Comparison with angler's catches indicated that these estimates corresponded roughly to < 200 mni, 200-300 mm and > 300 mm standard length (SL, the distance from the tip of the snout to the end of the hypural plate at the end of the vertebral column). Stickleback the size of Garden Bay Lake adults have been found in the

20::.

284 SUSAN FO~TER & STEPI{I.N PI OCH

stomachs of cutthroat trout as small as 170 mm SL although they are not abundant in stomach contents until the trout reach about 200 mm SL (MOODII: 1972). To calibrate size estimates of prickly sculpin, we visually classified individuals in situ and then captured them with a lift net, measured and released them. Size classes were < 80 mm (small), 80-120 mm (medium), and > 120 mm SL (large). Sculpin of 100 mm SL are capable of preying on adult stickleback ( P R E S S L ~ Y 1981).

We compared the responses of male stickleback in Garden Bay Lake, where sculpin are native, to the responses of those in Crystal Lake, where they are absent, using a large (132 mm SL) preserved sculpin (PRI:SSL.I:Y 1981). As in PRESS1 I:Y’s study, the sculpin was lowered onto a nest, and feeding behavior was simulated by moving strings attached to the sculpin. All male responses to the sculpin were recorded.

Results

Cutthroat Trout

In Garden Bay Lake, cutthroat trout were often observed on stickleback breeding grounds. When small trout (< 200 mm) entered territories, males approached to within 5 cm and watched (1 time), chased (3 times), o r failed to respond to them ( 3 times). Only once, when a trout just under 200 mm SL passed rapidly within 0.5 m, was an avoidance response elicited (binocular orientation followed by slow sinking to the bottom). Neither close approaches without a chase (described below), nor chases, were directed at trout > 200 mm SL.

Males rarely responded to trout passing at a distance of more than 1.5 m but they usually (63 of 72 encounters) responded when trout > 200 mm SL swam rapidly on a trajectory bringing them within 1.5 m of the male. In the other 9 encounters, the trout evoked no reaction, possibly because the male did not detect it. In three cases the male was already motionless and oriented to watch the trout swim through, so n o behavior modification would have been necessary for binocular orientation. Because these alternatives could not be distinguished, these observations were not included in analyses.

Males responded to the approach of trout > 200 mm SL in 8 ways (Table I) . Dorsal spines were typically raised during the first four behavior patterns listed. Rapid movement during the last four precluded determining spine position. The

Table I: Responses of territorial male stickleback with (n = 23) and without (n = 40) offspring in their nests, to the approach of a rapidly moving cutthroat trout more than 200 mm SL. The behavior patterns recorded here are those that followed the first overt response to the approach of the trout. In parentheses: randomly chosen subset of the data in which only one observation per male is included

Behavior Empty nest Young in nest

Binocular orientation, hold position Binocular orientation, sink to bottom Slow swim away from trout Slow swim away, then sink to bottom Rapid swim to bottom Rapid swim to weeds Dive to bottom Dive into weeds

Antipredator Behavior of Threespine Stickleback 285

most frequent response (52 %) involved binocular orientation toward the trout and holding of position until the trout departed. An alternative response involved slowly sinking to the bottom, sometimes preceded by a slow, smooth swim. Rapid swims to vegetation or the bottom involved normal, but faster than usual, swimming. Diving, a rapid body flex and stroke of the caudal fin, caused the fish to move rapidly to cover o r to the bottom. Once cover was reached, the male remained motionless until the trout left. After the trout departed, the male resumed normal activities.

Typically, trout swam through rapidly and disappeared. Strikes were observed twice. Once, a male working on his nest jumped sideways as the trout struck, and then dived into the sediment. In the second case, the male was glueing his nest when the trout approached. H e stopped, oriented, and held position facing the trout. The trout struck and the stickleback iumped sideways. The trout struck again and the stickleback dived to the bottom where it lay motionless. Although these two attacks were not successful, on three occasions trout were observed with stickleback in their mouths, and reproductive males were found in the guts of trout caught by anglers at both lakes.

We evaluated the effects of trout size (medium o r large) and male reproduc- tive state (empty nest o r nest with young) on the reactions of male stickleback to trout, using two-way contingency-table analysis (R x C analysis, SOKAL & ROHLI: 1981) on a randomly selected subset of the data that included only single observations on each male (Table 1). To ensure that cell values were large enough for the analysis, responses were divided into only two categories: low fright reactions consisted of the first two responses in Table 1 and high fright reactions, the remaining six. Low fright reactions d o not require the male to leave the vicinity of the nest whereas high fright reactions do. The analyses did not reveal significant associations between reproductive condition and response (n = 27, GH = 0.008, df = 1, p > 0.9) or trout size and response (n = 27, df = 1, GH = 0.305, p > 0.5). A three-way analysis (log-linear model analysis, SOKAL & ROHLF 1981) of the larger data set that included replicate observations of individual males failed to reveal a significant three-way interaction (GH = 0.086, df = 1, p > O S ) , nor were there significant interactions between any pairs of factors (p > 0.5, all interactions). Together, these analyses indicate that there is no effect of trout size o r male reproductive condition on male responses to trout.

Prickly Sculpin

Prickly sculpin frequently entered or approached the territories of male stickleback in Garden Bay Lake. Table2 describes the range of responses to sculpin of all sizes, although only those directed at medium and large sculpin are tabulated. Small sculpin are not a threat to the male, so that an effect of male reproductive condition is expected only in response to sculpin in the larger size classes.

Responses to sculpin (Table 2) can be divided into low, medium and high- risk responses. In low-risk responses, males moved no closer than 20 cm in their initial approach to the sculpin. They then watched the sculpin (binocular orienta-

286 SUSAN FOSTER & STEPHEN PLOCH

Tuble 2: Responses of territorial male stickleback with (n = 42) and without (n = 101) offspring in their nests, to the movement of a prickly sculpin toward o r into their territories. The behavior patterns recorded here are those that followed the first overt response to the sculpin. In parentheses: randomly

chosen subset of the data in which only one observation per male is included

Behavior Empty nest Young in nest

Low Risk: Approach no closer than 20 cm watch only 17 (7) 6 (4)

watch and chase sculpin as it moves 9 ( 3 ) 2 (1)

Medium Risk: Approach to < 20 cm from behind

watch and chase sculpin as it moves 4 (1) 0 (0) bite and chase 8 (4) 6 (2)

watch and chase sculpin as it moves 4 (1) 2 (0) bite and chase 5 (0) 3 (1)

Slow head-on approach to < 20 cm bite and chase 3 (2) 4 (0) Bite and chase following rapid approach 51 (14) 19 (5)

Approach to < 20 cm from the side

High Risk:

tion) until it left, sometimes chasing it as it left. Medium-risk responses involved approaching more closely from the side or behind. These approaches often required males to swim around the head at a distance, only moving closer once the head region had been skirted. Sometimes, males approached to within 3 cm of the side or tail of a sculpin and assumed a head-down posture, staring at the back of the sculpin. They then drifted back and forth along the spine, from the tail to just behind the head. This typically persisted until the sculpin began to move, at which point the male chased the sculpin, sometimes biting its tail. Three times, males confronted by large sculpin repeatedly approached and retreated without attacking. Usually, however, the male bit the tail of the sculpin quickly, causing it to flee. All of these approaches were relatively slow. High-risk responses involved either a slow direct approach to the head region, followed by a bite and chase sequence, or a rapid direct swim and bite at the sculpin. In the latter cases, approaches were made to all parts of the sculpin’s body. A slow approach to the head of a large sculpin was observed only once, the remainder being directed at smaller sculpin. Even when approaches were from the front, the head was never bitten.

The effects of male reproductive state and sculpin size on male response were evaluated in the same way as responses to trout using a randomly selected subset of the full data set including single observations for each male (Table 2). Sculpin were divided into three size categories, small (< 80 mm SL, no risk to male), medium (80-120 mm SL, intermediate risk) and large (> 120 mm SL, high risk). Male responses were collapsed into low, medium and high-risk responses (Table 2) to ensure adequate cell sizes for analysis. Two-way R x C analysis revealed no significant association between male reproductive condition and

Antipredator Behavior ot Three9pine Stickleback 287

Fig. I : Responses of territorial male Stickleback to the approach of pricklv sculpin of different sizes. Unshaded bars = low-risk re- sponses, hatched bars = intermedi- ate-risk responses, dark bars = high-risk responses (see Table 2 and

text for Jefinitions'i

< 80 80-120 >120

S c u l p i n S i z e (mm S L )

response (df = 2, G H = 0.347, p > 0.5), but there was a significant effect of sculpin size on male response (d i = 4, Gt, = 41.502, p < 0.001). Similarly, three- way analysis of the full data set (143 observations) revealed no significant three- way interaction and only sculpin size was significantly associated with male response (GH = 101.766, df = 6, p < 0.001).

R x C contingency table analysis using the STP procedure to test for differences in responses of males to sculpin of different sizes (SOKAL & ROHM 1981) demonstrated heterogeneity in the two-way table for the data subset (GH = 41.502, df = 4, p < 0.001) and for the full data set (GH = 93.174, df = 4, p < 0.001) as well as significant differences in responses directed at each of the three size classes of sculpin using the data subset (GI, > 8.155 each size pair, df = 2, p < 0.05) and the full data set (GH > 9.488 each size pair, df = 2 , p < 0.05). Males directed higher-risk responses at small sculpin, lower-risk responses at large sculpin and an intermediate mixture of responses at medium sculpin (Fig. 1).

Usually, following an interaction with a sculpin that had been chased from the territory, the male immediately resumed normal nest-directed activities. However, unlike trout, sculpin did not always leave the territory after an interaction with a male. In five cases sculpin entered a hole beneath a log in o r near the territory of the male. The stickleback then repeatedly approached the hole and peered into it, remaining more than 20 cm distant. On four occasions, males performed normal nesting activities between approaches to the hole. In the fifth case a male with embryos fanned his nest from 10 cm rather than at the usual 2 cm o r less. The male alternated peering at the hole with fanning for 23 min, slowly decreasing fanning distance.

Direct attacks on territorial male stickleback by sculpin were observed four times. Each time, the male was at his nest and the sculpin had moved within 0.5 m of the stickleback, apparently without being detected. In each case, the sculpin

288 SUSAN FOSTER & STEPHEN PLOCH

made a rapid dash at the stickleback, in one instance, successfully. In the three unsuccessful attacks, the stickleback jumped rapidly to the side, turned and swam around the sculpin to the tail, and bit and chased the sculpin.

To determine whether stickleback in Crystal Lake, where sculpin do not occur, would respond to a preserved sculpin in the same risk-sensitive manner documented by PRESSLEY (1981) in Garden Bay Lake where sculpin are abundant, we lowered a preserved sculpin onto the nests of 10 Crystal Lake males in different locations. The sculpin immediately attracted numerous stickleback, including foraging adults and territorial males, that nipped at it before it could be placed on the nest. Thus, this method could not be used to assay male responses to sculpin because it would have resulted in lowering conspecifics onto the nest with the sculpin.

Lowering the same sculpin onto nests of males in Garden Bay Lake never had this effect. Instead, the sculpin could be lowered onto nests without attracting nearby stickleback, and the responses of the territory-holder were the same as those reported by PRESSLEY (1981). Males initially fled, but returned within 5 s to attack the sculpin. Five males attacked the tail only. One attacked both head and tail repeatedly. The preserved sculpin did not elicit the more complex behavior patterns observed in natural encounters with living sculpin.

Roughskin Newt

Roughskin newts frequently swam or walked through the territories of males in the 1985 breeding season at Crystal Lake. When they swam through the territory (7 occasions) they were watched (binocular orientation) but not attacked. When they stopped in the territory they were usually immediately bitten by the male (17 occasions). In three cases however, the newts stopped moving well before the male reached them. O n these occasions, the male approached to within 5 cm, peered at the newt for 5 to 10 s, and then left before the newt moved. When these newts moved after the male had left, the male returned to chase them (twice) or watched from a distance (once).

When stickleback bit newts, the newts usually moved immediately, although twice repeated bites occurred before the newt swam out of the territory. Bites usually involved a lateral twisting motion by the stickleback once the skin had been grabbed. Similar twisting motions were never observed when sculpin were bitten in Garden Bay Lake. During attacks on newts, 17 males showed no tendency to avoid the head region. A chi-square test against equal expected frequencies of first attacks (SOKAL& ROHLF 1981) at the head region (nose, cheek, and back of head; n = 6), mid-region (armpit and leg/foot; n = 4) and tail (n = 7) demonstrated no significant departure from expectation (x’ = 0.824, df = 2, p = 0.663).

Belostomatid Nymph

Interactions with belostomatid nymphs were observed on only six occa- sions. All were at Crystal Lake late in the breeding season, between 27 June and 7 July 1985. In three cases the males approached nymphs that swam into the territory and settled on the substratum. They watched the nymphs from < 5 cm

Antipredator Behavior of Threespine Stickleback 289

for 5-10 s, and then moved away to resume nesting activities. One of these males turned to watch the nymph when it swam out of his territory subsequently. O n the fourth occasion, following the stickleback’s approach to within 5 cm of the nymph, the nymph jumped toward the stickleback, which jumped rapidly to the side. The nymph then entered a hole beneath a log. The male approached the hole to within 10 cm, peered inside, and then resumed normal nesting activities. In two interactions, the male approached a nymph which then jumped on his tail, grasping the tail with its front legs. The stickleback immediately began twisting erratically and rubbing against vegetation and the substratum. The nymph was brushed off and swam away. These maneuvers are not always successful because stickleback were occasionally observed late in the breeding season swimming weakly with nymphs feeding on them.

Discussion

The differences in the responses of stickleback to trout and prickly sculpin reflect differences in the risks posed by each kind of predator. Presumably because trout often chase prey after the first attack (WEBB 1982) and because they pose no risk to young in the nest, most escape responses involve a dive for the substratum or for weeds. Weeds have been shown to reduce the hunting efficiency of many chasing piscine predators (GLASS 1971; CROWDER & COOPER 1982; SAVINO & STEIK 1982; COOK & STREAMS 1984; FOSTER et al. 1988). In contrast, males often attack prickly sculpin directly, apparently because prickly sculpin are ambush predators that rely on surprise (PRESSLEY 1981) and because they pose a continued threat if they remain near the nest.

Differences in the sizes of trout greater than 200 mm SL did not affect the responses of male stickleback. In contrast, stickleback discriminated rapidly among size classes of sculpin. As sculpin size increased, so did the proportion of low-risk responses and the tendency to avoid the head. Avoidance of the head region has also been documented in the responses of mosquitofish, Gambusiu patraelis, to chain pickerel, Esox niger (GEORGE 1960), and in responses of bluegill sunfish, Lepomis rnacrochirus, to snapping turtles, Chelydra serpentina serpentina (DOMINEY 1983), both ambush predators.

The data presented here offer no evidence of an effect of male reproductive state on the responses of stickleback to trout or sculpin. These results differ from those of PRESSLEY (1 981) and KYNARD (1 978) who addressed the same issue using a large, preserved sculpin and a tethered, live trout, respectively. PRESSLEY found that in Garden Bay Lake, males with young in their nests took greater risks in defending the nest when the sculpin was lowered onto the nest than did males without young. Similarly, KYNARD demonstrated that males in Wapato Lake with young in their nests fled from the trout for shorter periods than did those without young. PRESSLEY’S and KYNAKD’S methods provided greater, more uniform threats than were present in our observations on natural encounters in which the speed of approach and trajectory varied. Thus, differences in methods could acount for the difference in results if reproductive condition has a relatively weak effect on male responses to predators.

290 SUSAN FOSTER & STEPHEN PLOCH

PRESSLEY (1981) also found that males with older progeny or more progeny in their nests accepted greater risk during encounters with sculpin than did those with younger or fewer. H e interpreted this as indicating that the level of effort expended by a male in defending his nest or young from sculpin reflected both risk to the parent and the reproductive value of offspring (if any) in the nest. A plausible alternative explanation, however, is that the aggressiveness of territorial male stickleback toward conspecific male intruders is correlated with the boldness (a composite score based on several behavior patterns) of their responses toward live and model pike (€sox lucius) both within and between populations (HUNTING- FORD 1976 b; TULLEY & HUNTINGFORD 1988). Because both aggressiveness and boldness scores are lowest for males without nests, highest for males with newly- hatched young and intermediate for males with nests but no offspring, HUNTING- FORD (1976 a) has postulated shared internal causal factors. If aggressiveness toward conspecifics and boldness toward predators are genetically correlated, the differences in male responses to predators that PRESSLEY (1981) found to be associated with male reproductive stage could have evolved as a correlated response to selection favoring increased aggressiveness toward conspecifics. This hypothesis cannot explain positive associations between the risk of responses toward sculpin and the number of embryos in the nest. However, none of PRESSLEY’S correlations were significant in Garden Bay Lake when only nests containing embryos were included in the analysis, and a correlation was signifi- cant (p < 0.025) for only one of three risk measures in a second lake (PRESSLEY 1981), so it is not clear that such a relationship exists.

In Crystal Lake, where there are no prickly sculpin, stickleback exhibited none of the risk-sensitivity to a large, preserved sculpin that was apparent in the behavior of Garden Bay males. In a third lake, Trout Lake, that also does not contain sculpin, males responded in a manner indistinguishable from that of Garden Bay males (PRESSLEY 1981), indicating that even though they do not encounter sculpin, they recognize them as a threat. Thus, there is variation among British Columbia stickleback populations in individual responses to sculpin, just as there is variation among Scottish populations in individual responses to live and model pike and to models of avian predators (HUNTINGFORD 1976b; GILES & HUNTINGFORD 1984; HUNT~NGFORD & GILES 1987). The ability to recognize the threat posed by sculpin is probably an ancestral trait, because sculpin are abundant in shallow marine habitats in British Columbia (HART 1973), and the marine stickleback population is thought to have given rise to the vast majority of freshwater stickleback populations in coastal British Columbia since the last glacial advance (e.g. MCPHAIL & LINDSEY 1986).

The responses of stickleback to roughskin newts were like their responses to sculpin except that they did not avoid the head region and would bite and twist the skin of the newts more aggressively. These differences presumably reflect the lack of risk in attacking newts. In contrast, males never bit belostomatid nymphs, presumably because of the high risk of such a close approach. On the two occasions that a nymph grasped a male, the males rubbed frantically against vegetation and the substratum until the nymph had been brushed off. Males also rubbed against vegetation or the substratum on other occasions without apparent

Antipredator Behavior of Threeapine Stickleback 291

cause, indicating that this is a generalized response to an irritant on the skin as suggested by BAERENDS & BAERENDS-VAN ROON (1950). The behavior was much more pronounced when a nymph had grasped the male than on other occasions.

A behavior pattern recently termed “predator inspection behavior” (e.g. PITCHER 1986) is common to the responses of males to prickly sculpin, roughskin newts and belostomatid nymphs. The males approached the predator to within 20 cm and watched it (binocular orientation). Similar inspection behavior has been documented in the responses of a variety of fishes to predators that include chain pickerel (GEORGE 1960), pike (e.g. MAGURRAN 1986; MAGURRAN & GIRLING 1986; MAGURRAN & PITCHER 1987), several predatory coral-reef fishes (MOITA 1983) and a snapping turtle (DOMINEY 1983). All of these prey fishes inspected potential predators while in groups or in close proximity to other individuals. This differs from our observations of inspection behavior by solitary, territorial male stickleback.

The function of predator-inspection behavior may vary with context, as has been suggested for other kinds of antipredator behavior (e.g. CARO 1986a, b; FANSHAWE 1989). GEORGE (1960) and DOMINEY (1983) suggested that predator- inspection behavior could inhibit pursuit by signalling to the predator that it has been detected and that attacks are therefore unlikely to be successful. This is a plausible benefit to inspection of sculpin by stickleback because attacks never occurred after inspection. However, because inspection was often followed by biting, and biting always caused sculpin to move, inspection could also intimidate the sculpin into leaving the territory to avoid being bitten, thereby enabling the stickleback to avoid the risk of approaching more closely. Neither explanation seems likely when newts are inspected because they pose no risk to the male and biting always caused them to flee. These explanations are also unlikely for inspection of the belostomatid nymph because nymphs were never bitten and males could avoid attacks simply by remaining more than 10 cm from the nymphs .

Alternatively, MAGURRAN & GIRLING (1986) argued that predator inspection allows inspectors to confirm the identities of predators. This is an unlikely explanation for inspection of sculpin because the risk sensitivity evidenced in the complex of responses to sculpin of different sizes indicates that sculpin are identified as soon as they are detected. It is also an unlikely explanation for inspection of roughskin newts. If newts resting near nests had been recognized and ignored as harmless, they should not have been chased when they moved subsequently, but were. Attacking a newt incurs no risk, so it seems most likely that males can only identify moving newts. Stickleback may however, identify belostomatid nymphs by inspection.

O u r observations demonstrate that male stickleback perform a diverse array of antipredator behavior patterns, and that they discriminate rapidly and effec- tively among predators. Many of these behavior patterns have been elicited in the laboratory in response to pike (e.g. BENZIE. 1965; HUNTINGFORD 1982; HUNTING- FORD & GILES 1984, 1987). Other behavior patterns observed here are probably not elicited by the predators that have been studied in the laboratory. Further- more, performance of particular behavior patterns is apparently affected by past

292 SUSAN FOSTER & STEPHEN PLocti

history of the population as well as by immediate context. Through judicious combination of laboratory and field research it should be possible to untangle the complex of factors that mold the antipredator behavior of the threespine stick- leback.

Acknowledgements

Comments by J . A. BAKER, C. KURTZ, D. H . OWINGS and an anonymous reviewer improved the manuscript. V. B. GARCIA, M. SADAGURSKY, M. Y. TOWN and C. VESTUTO provided assistance in the field. J. MCOUAT provided friendship, enthusiasm and the roof over our heads. The research was supported by a National Research Service Award from N I M H to the senior author. This is contribution No. 747 in Ecology and Evolution at the State University of New York at Stony Brook.

Literature Cited

BAERENDS, G. P. & BAERENDS-VAN ROON, J . M. 1950: An introduction to the study of the ethology of cichlid fishes. Behaviour Suppl. 1.

BELL, M. A. 1984: Evolutionary phenetics and genetics. The threespine stickleback, Gasterosreus aculeatus, and related species. In: Evolutionary Genetics of Fishes. (TURNER, B. J., ed.) Plenum Publ., New York, pp. 431-528.

BENZIE, U. L. 1965: Some aspects of the anti-predator responses of two species of stickleback. D. Phil. Thesis, Univ. of Oxford, Oxford.

BREDEN, F., S C O ~ , M. & MICHEL, E. 1987: Genetic differentiation for anti-predator behavior in the Trinidad guppy, Poeczlia retzculara. Anim. Behav. 35, 61 8-620.

CARO, T. M. 1986a: The functions of stotting: a review of the hypotheses. Anim. Behav. 34,

_ - 1986b: The functions of stotting in Thomson’s gazelles: some tests of the predictions. Anim. Behav. 34, 663-684.

COATES, D. 1980: The discrimination of and reactions towards predatory and non-predatory species of fish by humbug damselfish, Dascylfus uruunus (Pisces, Pomacentridae). 2. Tierpsychol. 52, 347-354.

COOK, W. L. & STREAMS, F. A. 1984: Fish predation on Notonecta (Hemiptera): relationship between prey risk and habitat utilization. Oecologia 64, 177-183.

CROWDER, L. B. & COOPER, W. E. 1982: Habitat structural complexity and the interaction between bluegills and their prey. Ecology 63, 1802-1813.

CURIO, E. 1976: The Ethology of Predation. Springer-Verlag, Berlin. DOMINEY, W. J. 1983: Mobbing in colonially nesting fishes, especially the blue-gill, Lepomzs

ENDLER, J. A. 1986: Defense against predators. In: Predator-prey relationships. (FEDER, M. E. &

FANSHAWE, J. H. 1989: Serengeti’s painted wolves. Nat. Hist. 3/89, 56-67. FOSTER, S. A. 1988: Diversionary displays of paternal stickleback: defenses against cannibalistic

groups. Behav. Ecol. Sociobiol. 22, 335-340. _ _ , GARCIA, V. B. & TOWN, M. Y. 1988: Cannibalism as the cause of an ontogenetic shift in

habitat use by fry of the threespine stickleback. Oecologia 74, 577-585. GEORGE, C. J. W. 1960: Behavioral interaction of the pickerel and the mosquitofish. D. Phil. Thesis

Harvard Univ., Cambridge. GILES, N . 1984: Implications of parental care of offspring for the anti-predator behaviour of adult

male and female three-spined sticklebacks, Gasterosreus aculeatus L. In: Fish Reproduction. (Pons, G. W. & WOOTTON, R. J., eds.) Acad. Press, London, pp. 275-289.

_ _ & HUNTINGFORD, F. A. 1984: Predation risk and interpopulation variation in anti-predator behaviour in the three-spined stickleback, Gasterosreus uculeutus L. Anim. Behav. 32, 264-275.

64 1-648.

marrochirus. Copeia 1983, 1 0 8 6 1 0 8 8 .

LAUDER, G. V., eds.) Univ. of Chicago, Chicago, pp. 109-134.

Antipredator Behavior of Threespine Stickleback 293

G I ASS, N . R. 1971: Computer analysis of predation energetics in the largemouth bass. In : Systems Analysis and Simulation in Ecology. (PATEN, B. C., ed.) Acad. Press, New York, pp. 32h-363.

HAGI,.N, L). W. & GILBI:KTSON, L. G. 1973a: The genetics of plate morphs in freshwater threespine sticklebacks. Heredity 31, 75-84,

_ _ & <;II.HEKTSOI\;, L. G. 1973 b: Selective predation and the intensity of selection acting upon the latcral plates of threespine sticklebacks. Heredity 30, 273-287.

HART, J . 1.. 1973: Pacific fishes of Canada. Fish. Res. Bd. Canada Bull. 180, 1-740. H I Lf MAN, G. S. 1986: Behavioral responses of prey fishes during predator-prey interactions. In:

Predator-Prey Relationships. ( F E D ~ R , M. E. & LAUIIER, G. V. eds.) Univ. of Chicago, Chicago, pp. 135-156.

HOWI.AN[I , R. D. 1951: On the fixing-mechanism in the spines of Gasterosteus aculeatus. Ned. Akad. Wet. Ser. C 54, 171-180.

_ _ , MORRIS, I). & TINBFRGEN, N . 1957: The spines of sticklebacks (Gasterosteus and Py'gosteits) as means of defense against predators (Perm and Esox). Behaviour 10, 205-236.

H U N T I N G I OKI), I:. A . 1976a: A comparison of the reaction of sticklebacks in different reproductive conditions towards conspecifics and predators. Anim. Behav. 24, 694-697.

_ _ 1976 b: The relationship between anti-predator behaviour and aggression among conspecifics in three-spined stickleback, Gasterosteus aculcatus. Anirn. Behav. 24, 245-260.

_ _ 1982: Do inter- and intra-specific aggression vary in relation to predation in sticklebacks? Anim. Behav. 30, 9C6-916.

_ _ & G I I IS, N. 1987: Individual variation in anti-predator responses in the three-spined stick- leback (Gasterosteus aculeatus L.). Ethology 74, 205-210.

KI N A R D , H. E. 1978: Breeding behavior of 3 lacustrine population of three-spine stickleback (Gasterosteus aculeatus L.). Behaviour 67, 178-207.

LOUGIIRY, W. J. 1988: Population differences in how black-tailed prairie dogs deal with snakes. Behav. Ecol. Sociobiol. 22, 61-67.

M A G U R K A ~ , A. E. 1986: Predator inspection behaviour in minnow shoals: differences between populations and individuals. Behav. Ecol. Sociobiol. 19, 267-273.

.- - & G I K I I N G , S. L. 1986: Predator model recognition and response habituation in shoaling minnows. Anim. Behav. 34, 510-518.

_ _ 8r ~'lTClll.K, T. J . 1987: Provenance, shoal size and the sociobiology of predator-evasion behaviour in minnow shoals. Proc. R. Soc. Lond. B. 229, 439-465.

MC,PIIAII , J . D. 8r LINIISFY, C. C. 1986: Zoogeography of the freshwater fishes of Cascadia (the Columbia system and rivers north of the Stikine). In: The Zoogeography of North American Freshwater Fishes. (HOCUTT, C. H. & W I L I . ~ , E. W., eds.) Wiley and Sons, New York, pp. 6 15-63 7.

M O ~ ~ I I E , G. E. E. 1972: Predation, natural selection and adaptation in an unusual threespine stickleback. Hereditv 28, 155-167.

MOTTA, P. J . 1983: Response by potential prey to coral reef fish predators. Anim. Behav. 31, 125 7- 1 259.

NUSBAUM, R. A,, BRODIE, E. D. J. & STORM, R. M. 1983: Amphibians and Reptiles of the Pacific

C)U,INGS, D. H. & COSS, R. G. 1977: Snake mobbing by California ground squirrels: adaptive

__ - & OWINGS, S. C. 1979: Snake directed behaviour by blacktailed prairie dogs (Cynornys

PIT( : I I I ,K, T. J . 1986: The functions of shoaling in teleosts. In : The Behaviour of Teleost Fishes.

PRI-\SI I ~ Y , P. H. 1981: Parental effort and the evolution of nestguarding tactics in the threespine

SAVINO, J . F. & STEIN, R. A. 1982: Predator-prey interaction between largemouth bass and bluegills

Sl~(;Ht~KS, B. H. 1974: Schooling behavior in the guppy (Poecilia reticdata): an evolutionary response

S O i i A l , R. R. & Rot{w, I:. J . 1981: Biometry. Freeman, New York.

Northwest. Idaho Univ., Moscow.

variation and ontogeny. Behaviour 62, 50-69.

lutloz.manus). Z. Tierpsychol. 49, 35-54.

(PITCIII:R, T. J., ed.) Croom Helm, London, pp. 294-337.

stickleback, Gasterosteus aculeatus L. Evolution 35, 282-295.

as influenced by simulated, submersed vegetation. Trans. Am. I4sh Soc. 111, 255-266.

to predation. Evolution 28, 4 8 6 4 8 9 .

294 SUSAN FOSTER & STEPHEN PLOCH, Antipredator Behavior of Threespine Stickleback

TULI.EY, J. J. & HUNTINGFORD, F. A. 1987: Age, experience and the development of adaptive variation in anti-predator responses in three-spined sticklebacks (Gasterosteus aculeatus).

_ - &- - 1988: Additional information on the relationship between intra-specific aggression and anti-predator behaviour in the three-spined stickleback, Gasterosteus aculeatus. Ethology 78, 219-222.

TURNER, L. W. 1973: Vocal and escape responses of Spermophilus beldingi to predators. J. Mammal.

WALTHER, F. R. 1969: Flight behavior and avoidance of predators in Thompson’s gazelle. Behaviour

WEBB, P. W. 1982: Avoidance responses of fathead minnow to strikes by four teleost predators.

ZARET, T. M. 1980: Predation and Freshwater Communities. Yale Univ., New Haven.

Received: May 16, 1989

Accepted: Januavy 30, 1990 (G. Barlow)

Ethology 75, 285-290.

34, 184-221.

34, 184-221.

Comp. Phyiol. 147, 371-378.