Environmental Biology of Fishes 38: 393-397,1993. 0 1993 Kluwer Academic Publishers. Printed in the Netherlands. A new heterospecific foraging association between the puddingwife wrasse, Halichoeres radiatus, and the bar jack, Caranx ruber: evaluation of the foraging consequences Troy A. Baird Department of Biology, University of Central Oklahoma, Edmond, OK 73034, U.S.A. Received 24.6.1992 Accepted 12.3.1993 Key words: Feeding, Interspecific association, Social behavior, Labridae, Carangidae, Reef Fish Synopsis The bar jack, Caranx ruber, was commonly observed to follow individual puddingwife wrasses,Halichoeres radiatus, that were foraging on the substrate. Individuals of both speciesactively pursued the other to main- tain these heterospecific foraging ‘teams’, were sometimes attracted to feeding acts initiated by team partners, and the foraging rates of teamed jacks and wrasseswere positively correlated. Pilfering of food items was rare, suggestinglittle, if any, competition cost of this foraging association. The ratio of bites to search in teamed jacks was over three times that when solitary, and jacks were sometimes aggressiveto conspecifics attempting to join their team, suggestingthat the association is beneficial to the jacks. Both bite and search rates were higher in puddingwifes when teamed with a jack, indicating that the association also benefits the wrasses. Benefits to puddingwifes may be derived directly from attendants becausewrasses were sometimes attracted to jack foraging acts. However, increased foraging in wrassesmay also be a consequenceof heightened moti- vation to feed owing to heterospecific social facilitation. Introduction swimming closely to and above or beside a single individual of the ‘nuclear’ species(Moynihan 1962, Foraging in social groups is well known among ver- Strand 1988,Sikkel & Hardison 1992). tebrates (Pulliam & Millikan 1982,Pulliam & Cara- Although it is widely held that heterospecific as- co 1984,Clark & Mange11986) and feeding togeth- sociations in fishes increase feeding opportunities er with conspecifics has been shown to enhancethe for attendants (Strand 1988), apparently only three foraging effectiveness of individual birds (Krebs et studies have involved collection of the quantitative al. 1972, Gotmark et al. 1986,Benkman 1988) and data necessary to evaluate this hypothesis. Both fishes (Pitcher et al. 1982, Baird et al. 1991). Al- yellow-headed wrasses, Halichoeres garnoti, and though social foraging generally involves individu- yellowtail snapper, Ocyurus chrysurus, exhibit als of the same species, heterospecific foraging as- higher feeding rates when attending groups of goat- sociations have also been reported in mammals fishes (Aronson & Sanderson1987, Sikkel & Hardi- (Devore & Hall 1965) birds (Moynihan 1962,Cody son 1992) while grouper, Cephalopholis spp., in- 1971)and fishes (reviewed by Strand 1988).In fish- creased feeding rates by following octopus (Dia- es, these associations are usually characterized by mant & Shpigel 1985). The influence of being at- one or more individuals of an ‘attendant’ species tended by a heterospecific on the foraging 394 performance of nuclear individuals has not been by a jack (teamed, n = 24). During this set of obser- quantified. In many cases,foraging associationsin- vations, I recorded only the foraging acts of the volve specieswith little dietary overlap, hence,com- wrasses.Five minute focal observations were re- petition from attendants is unlikely (Strand 1988). corded on jacks when attending a puddingwife Other associationsinvolve two speciesthat some- (teamed, n = 18) and when foraging independently times eat the sameprey. Attendant pilfering of food from a wrasseor conspecifics(solitary, n = 18).Dur- items uncovered by nuclear individuals sometimes ing 5 min focal observations on teams, I recorded occurs (Dubin 1982,Strand 1988) suggestinga po- the foraging acts of both species.For both data sets, tential foraging cost to nuclear individuals. the order of observations on solitary and teamed Here I report on a previously undescribed forag- subjects was randomized. The number of foraging ing association involving the puddingwife wrasse, acts (defined below) per observation sessionwas di- Halichoeres radiatus, and the bar jack, Caranx rub- vided by the total minutes of observation to yield er. Puddingwife wrassesfeed exclusively on benthic per minute rates of foraging actswhich were usedin invertebrates (Randall 1967). Although bar jacks all analyses. feed largely on fish, remains of benthic-dwelling Feeding rates may vary as a function of body size mollusks and crustaceans,and sand in the guts of or time of day. To control for such variation, sub- jacks indicates that this speciessometimes eats the jects were categorized according to estimated fork same invertebrate prey as the wrasses (Randall length (small < 20 cm, medium 20-30 cm, large > 30 1967).Bar jacks are the faster, more mobile of these cm), and solitary and teamed observations were two species,and following wrassesthat are search- conducted on different individuals of the samesize ing the substrate is a striking departure from the class,within 15 min of one another. Becauseteamed usual tendency of jacks to swim higher in the water and solitary observations were conducted close to- column. Therefore, I expected that jacks might at- gether in time and on individuals of the same size tend wrassesin order to exploit benthic prey items class,I used a paired design for statistical analyses uncovered by puddingwifes, perhaps reducing the (Snedecor& Cochran 1980,p. 89). The sizeclass dis- foraging effectivenessof wrassesthrough increased tribution of 24 wrasse subject pairs was: small = 5, interspecific competition. To assessthe influence of medium = 9, large = 10,and for 18jack subject pairs this association on the foraging performance of was; small = 4, medium = 9, large = 5. both species,I recorded rates of feeding activities Although it is possible that subjects could have when individual fish were foraging solitarily, and been observedmore than once, the potential for re- when teamed together with one heterospecific. peated observationswas low becausestudy sessions were spread over a 500 m2area where both species were abundant. An inability to capture fish prohib- Methods ited correlation of food intake with the rate of fo- raging acts. Rather, I assumedthat rates of bite and Observations were conducted from 13July to 8 Au- search are correlates of food intake. Samples of gust 1991at Glover’s Reef, Belize, Central America, benthic invertebrates taken previously on this study in the channel between Long and Northeast Cays area show that prey are distributed randomly (described in Baird & Baird 1992). Fish were ob- (Baird & Liley 1989). Also, becausemany benthic served between 1300 and 1700h while snorkeling, invertebrates are mobile and secretive, it is prob- and data were recorded on slates.When not attend- able that detection of prey is correlated positively ed by a jack, puddingwife wrassesswam independ- with rate of foraging. ently from conspecificsor other species.Jacks often A foraging search was defined as the fish stop- swam with conspecifics, but solitary foraging was ping its forward swimming motion and angling its not unusual. I conducted separate 10 min focal ob- snout and visual field downward to scanthe bottom. servations on puddingwife wrassesforaging solita- Each of these species swam continuously except rily (n = 24 sessions)and when they were attended when foraging. Therefore, search acts were obvi- 395 swam beneath a coral formation whereupon the jack rapidly circled the coral, appearing to ‘wait’ for the wrasseto emerge. Of the nine separationsiniti- ated by wrasses,the team was maintained because jacks followed in eight instances(88.9%) and in the other casethe wrassereturned to the jack. Examination of the stomach contents of two specimensof each species,together with direct ob- servationson feeding, confirmed that both bar jacks Fig. 1. Bar jack (top) shown in typical position when attending a and puddingwife wrasseseat benthic invertebrates. puddingwife wrasse (bottom) in a heterospecific team. The wrasseswere not observed to pilfer food items from jacks. Jacksattempted to pilfer food items un- ous. A foraging bite was recorded eachtime the fish covered by wrassesduring only 3 of 70 bites taken in search posture contacted the substrate with its mouth. a I alsorecorded the frequency with which either of the two teamed fish temporarily swam more than three body lengths away from the other fish (sep- arations), and whether either fish swam back to re- I join the other within 15 sec.When teams separated for longer than 15 set prior to completion of a focal session, observations were terminated and these data were not used in analyses. Food pilfering events and interactions between the two teamed fish or with other conspecificswere also recorded. Results P J Bar jacks attended puddingwife wrassesby swim- ming parallel with, and above or to the side of the wrasse,usually with less than one body length sep- -I 1.6 arating the two fish (Fig. 1). Whether foraging sol- .- itarily or in a team, the wrassesswam continuously E' 1.2 along the bottom pausing only to search and take ti bites. Formation of jack-wrasseforaging teams was I: common, with many lasting longer than the dura- i! 0.8 tion of focal observations. Jacksinitiated 91.4% (96 E of 105) of the temporary separations between m 0.4 teamed fish, compared with only 8.6% that resulted from wrassesleaving