Courtship and Spawning Behavior in sheephead...

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COURTSHIP AND SPAWNING BEHAVIOR IN THE CALIFORNIA SHEEPHEAD, Semicossyphus pulcher (Pisces: Labridae)

MIA S. ADREANI, BRAD E. ERISMAN AND ROBERT R. WARNER

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Environmental Biology of Fishes 71: 13–19, 2004. ! 2004 Kluwer Academic Publishers. Printed in the Netherlands.

Courtship and spawning behavior in the California sheephead, Semicossyphus pulcher (Pisces: Labridae) Mia S. Adreania,c, Brad E. Erismana,d & Robert R. Warnerb a Department of Biology, California State University, Northridge, CA 91330, U.S.A. b Department of Ecology, Evolution, and Marine Biology, University of California, Santa Barbara, CA 93106, U.S.A. c Current address: Department of Biological Science, Florida State University, Tallahassee, FL 32306, U.S.A. (e-mail: madreani@bio.fsu.edu) d Current address: Scripps Institution of Oceanography, University of California, San Diego, La Jolla, CA 92093, U.S.A. Received 24 November 2002

Accepted 11 December 2003

Key words: reproductive behavior, size advantage hypothesis, protogyny, kelp forest fishes, wrasses Synopsis We recorded the courtship and spawning behavior of a protogynous fish, the California sheephead, Semicossyphus pulcher, throughout their spawning season at Bird Rock, Santa Catalina Island, California.

We made additional observations at the Monterey Bay Aquarium and confirmed the details of behavior seen in the field. Large males held spawning territories in which females congregated approximately 1 h before sunset. Courtship commenced shortly before sunset and involved the male approaching each female, making lateral contact and leading her in a circular pattern. Smaller males attempted to court females within the territories, prompting large males to abort spawns and engage in chasing behavior with small males. Females visited several territorial males throughout the day, indicating that they are not part of a strict harem. Both field and aquarium observations confirm that the mating system can be successfully predicted from the size advantage model. Current regulations on the sheephead fishery, which allow for the removal of large, rare males, could have significant effects on the social structure, reproductive output, and mating processes of local populations. Moreover, understanding the mating system of the California sheephead illustrates the need for creating management strategies that better complement the unique life histories of marine fishes with alternative reproductive strategies.

Introduction The reproductive behavior of marine fishes has been studied extensively in the tropics, in part due to the clear, warm water, which makes observation of spawning relatively easy. Temperate reef fishes have not been studied in nearly the same detail and thus little is known about their mating systems and reproductive behavior. Temperate kelp forest communities are extremely productive and house a diverse assemblage of fishes, though only a few

studies in this habitat have focused on behavior (Feder et al. 1974, Hobson 1976, Coyer 1982, Helvey 1982). Information on the behavior surrounding spawning could prove crucial to management of some of these commercially important fishes.

The California sheephead, Semicossyphus pulcher, is commonly found in the temperate waters of the eastern Pacific, ranging between Monterey Bay, California, U.S.A. and Cabo San Lucas, Baja California, Mexico, including the northern Gulf of

14 California (Miller & Lea 1972). Their primary habitat is kelp and rocky reef between 5 and 50 m deep and they can reach sizes of up to 1 m. The distinct black, red and white coloration pattern of the males and their relatively docile and curious nature has made them a popular and easy target for spear fishermen and anglers.

Prior to the late 1980s, commercial fisherman did not target the California sheephead and average annual landings were about 10 000 pounds.

However, commercial interests have increased dramatically after a live fishery was developed in 1988 to supply Asian seafood markets. Consequently, commercial landings have also increased, with peak landings of 366 000 pounds recorded in 1997 (Stephens 2002). In contrast to the commercial fishing industry, the California sheephead has been an important component of the recreational fishery of California since the late 1940s, and recreational landings are believed to exceed commercial landings for most years (Stephens 2002).

Recent regulation changes have limited minimum catch size to 30 cm in an attempt to decrease the take of small fish for the live fish trade (Stephens 2002). Unfortunately, because males result from sex change of older and larger individuals, they are rare to begin with and thus traditional regulation strategies, such as minimum size limits, may not be effective for these protogynous fishes.

More specifically, the removal of large males could lead to sperm limitation in some populations, where not all eggs are fertilized (Warner et al.

1995). Selective extraction of males could also disrupt operational sex ratios, and consequently could affect mate selection, mate competition, and other important processes of mating (Vincent & Sadovy 1998).

S. pulcher is a monandric protogynous hermaphrodite and one of three wrasse species living off the coast of southern California. This sexually dimorphic and dichromatic species undergoes sex transformation through a series of documented gonadal development changes as well as color changes (Warner 1975a). Individuals from the Santa Catalina Island population mature as females at about 4 years and change sex at around 31 cm standard length. Both males and females increase in both size and age with latitude within their range (Cowen 1990). Females are likely to

spawn several times throughout their spawning season, which was predicted to be July through September by gonosomatic indices (Warner 1975a).

The California sheephead was the first sexchanging fish to be described from the temperate north Pacific Ocean. Population-level differences in the age of sex change correspond to differences in population size structure and these contrasts were used in one of the first tests of sex change theory (Warner 1975b). While it is now well established that sex change patterns can be predicted from mating systems (Warner et al. 1975, Warner 1984), the mating system of the California sheephead has never been described. Studies on the behavioral patterns of several tropical bodianine wrasses (e.g., Bodianus rufus, B. diplotaenia) are well documented, and have revealed a variety of social structures and mating systems to occur within the subfamily (e.g., Warner & Robertson 1978, Colin 1982, Hoffman 1985). The temperate distribution of the California sheephead warrants further investigation of behavioral patterns within this subfamily, including comparisons among temperate and tropical species. This species is currently gaining a great deal of attention among scientists as a target species for the formation and extension of marine reserves, thus making aspects of their natural history, including reproductive behavior and movement patterns, extremely important.

Methods Field observations We made primary observations at Bird Rock, Santa Catalina Island, California (33"29¢N, 118"27¢W), and additional observations at sites adjacent to Big Fisherman’s Cove, Santa Catalina Island, California, a marine reserve surrounding the University of Southern California’s Wrigley Marine Science Center (Figure 1). All study sites were rocky reefs covered with high relief macroalgae and bordered by dense kelp beds. Visibility ranged from 10 to 16 m and water temperatures ranged from 14 to 19"C. We recorded fish behavior while on SCUBA, using underwater slates and digital video at depths of 6–15 m. We analyzed

15

Figure 1. Map of Santa Catalina Island, California, with a close-up of the study sites surrounding Wrigley Marine Science Center.

Sites (indicated by dots) include the east and west ends of Bird Rock, Habitat Reef and Intake Pipe.

video recordings of six spawning events frame-byframe to determine the duration of courtship and spawning and to describe spawning behaviors in greater detail.

We chose specific study sites based on the occurrence of large males and many females present on survey dives done earlier in the day. Divers would enter the water about 30 min before sunset and remain until visibility was too low to describe behavior accurately. We observed males and females from distances of 2–6 m, and divers were able to swim within 2–3 m of the fish during courtship and spawning with no apparent disruption in their behavior. We made observations approximately once per week for an average of 34 min each dive, throughout the spawning season from late June through early September in 2001 and 2002. At the Bird Rock site, we observed two dominant males most frequently, because they were easily recognizable by their large size, the distinct markings on the black portions of the fish, and because they could be consistently relocated on any given dive.

These two males occupied territories that extended approximately 50 m along the length of the reef. We also observed smaller males at this site outside the spawning territories of these two dominant males.

Aquarium observations We made further details of mating behavior on 29 September 2000 at the Monterey Bay Aquarium.

The large kelp bed tank contained a large male and four females. Spawning commenced at 19:45 h and continued until 21:05 h, at which time all four females had spawned.

Results Field observations We first observed sheephead spawning on 29 June 2001 at Bird Rock, Santa Catalina Island, California, between 19:00 and 20:15 h. Initial spawning occurred in 7 m of water at the edge of a shallow shelf extending off the rock, which then dropped off to depths greater than 30 m just beyond the fish activity. The site is situated on the southeast corner of Bird Rock and is characterized by high flow in an eastward direction, making this a shallow, downcurrent area adjacent to an open ocean channel (Figure 1). Spawning sites for many fishes are often characterized by these features (Thresher 1984).

Rapid chases initiated by a large male sheephead (approximately 50 cm total length) toward smaller males were observed several times and were followed by the large male returning to the area where the chase originated. During chases, large males would use caudal fin bursts and swim rapidly towards smaller males, who would respond by flight behavior in the opposite direction of the larger male. There were three males in the vicinity

16 (within about 5 m diameter). The largest male appeared to concentrate his activity in an area surrounding a single, large kelp stipe where the interaction occurred. There were seven females swimming slowly around the kelp stipe at slightly different depths, averaging about 3 m off the substrate. This large male interacted with females that were in the immediate area by approaching and making physical contact (usually with the chin and pelvic fins). The females responded by moving in toward the kelp and higher in the water column along the kelp stipe.

Courting began shortly after when the male approached a female with pelvic fins down, circled above her and made contact with her laterally. He then positioned himself slightly above her and led her in a slow circular pattern with his pelvic fins down, maintaining constant pressure on the top of her head with his chin. After three to four downward circles and a series of head jerk motions, the female made a quick upward motion with her head and the two rushed to the surface, side by side. At 3–4 m below the surface, the pair tilted to touch vents while releasing gametes, swam apart and slowly spiraled back down toward the base of the kelp (Figure 2). The male immediately began courting another female upon

returning to the kelp stipe. Subsequently, a similar pattern resulted in matings with several females in the area.

On numerous occasions throughout the observation periods, another smaller male entered the area and approached one of the females, occasionally making physical contact. This was followed each time by an abrupt chase by the larger resident male for approximately 10 m in distance.

The same smaller males could occasionally be seen spawning with females a distance away from the dominant male territories but apparently were not as routinely able to gain access to females as were the larger territorial males.

Dominant males were observed to spawn up to eight times in an observation period, with an average spawning occurrence of 3.82 ± 0.83 (mean ± 1SE, n ¼ 10) spawns per observation period. During this time, it was not uncommon for a male to attempt courtship with a female who was unresponsive or with one who would be led around in the circular pattern, but then would break off before the final spawning rush. These aborted spawns occurred an average of 3.74 ± 0.45 (mean ± 1SE, n ¼ 10) times in the average 34 min observation period, creating a nearly 1:1 ratio of successful to unsuccessful

Figure 2. Spawning sequence of Semicossyphus pulcher showing the male approaching a female in the water column, extending pelvic fins upon approach. The male then circles above the female and upon aligning himself with her position, applies pressure to the top of her head with his chin. She then moves to his side and slightly below him and he leads her in a series of circular or zigzag patterns, maintaining contact until she makes an upward motion with her head, cueing the upward rush and release of gametes near the surface of the water.

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Figure 3. A typical agonistic behavior display between two large terminal phase males at the border of their territories at Bird Rock, Santa Catalina Island.

spawns per large male. The male would then immediately approach another female to begin courting. Females were not observed participating in multiple spawns on a single day, but individual females were not as easily recognizable and multiple spawning cannot be completely ruled out.

Typically, females would return to the substrate and disperse away from the site after spawning, whereas the other waiting females remained swimming slowly higher up in the water column.

This courtship and spawning pattern was consistent throughout the observations with minor variations, such as exact positioning of the female and the approach by the male. The number of females in the territory, however, was highly variable, with an average of 7.4 ± 2.1 (mean ± 1SE, n ¼ 10) and as many as 25 within a 5 m2 area of the large male. Females were scattered about the Bird Rock site during the day and began congregating in the male territories approximately 1 h before sunset. Once in the immediate area of the male (within 5 m), they swam around slowly near the substrate. This was a noticeable change in behavior, since they typically feed continuously on the substrate during the day.

Throughout the spawning season, the length of time spent interacting with and defending local females appeared to decrease and dominance among the males became more clearly established.

The two males recognizable by their distinct

markings were observed most frequently throughout the season. These males had established spawning territories, each spanning a 20 m distance along the rocky shelf, and would frequently face each other, opening their mouths wide, gaping and occasionally making contact, or even locking jaws (Figure 3). These encounters occurred at the border between the male territories an average of 2.3 ± 0.4 (mean ± 1SE, n ¼ 10) times per observation period. The entrance of a smaller male in either of these territories initiated an immediate response by the large males, usually consisting of fin flaring or chasing, and on rare occasion, gaping or jaw-locking. Throughout the day, the large males would remain in the same general area to feed and would occasionally display the agonistic behavior described above (e.g., gaping, fin flaring).

Females also would occasionally interact with one another but this was observed less frequently than male-male interactions and was typically less intense.

Spawning occurred during every observation period from late June through August and did not appear to be correlated with tides or lunar cycles.

Courtship commenced in the early evening (approximately 1 h before sunset) but all spawning witnessed occurred at or after sunset. The time spent by males courting averaged 11.8 ± 2.8 s per female, averaged across each of the observed males throughout the season. Observations were made

18 until the light levels were too low to allow observation. Spawning was not likely to continue after dark because sheephead are diurnal and will hide in rocks or kelp throughout the night (Feder et al. 1974, personal observations).

Aquarium observations We made observations of spawning at the Monterey Bay Aquarium and confirmed the details of courtship and spawning behavior seen in the field. All four females in the tank were gravid and eventually spawned, suggesting that females are capable of multiple spawns over the course of the mating season. Similar to what we saw in the field, spawning rises commenced between 1 and 2 m from the bottom, and finished near the surface. Females may have been more reticent to spawn in the captive situation, because the male engaged in 3.25 aborted spawning rises for every successful spawning. In each aborted attempt, it was the female that broke off the spawning by abruptly initiating a downward-directed movement. As in the field, the male would often turn his attention to another female after an aborted attempt.

Discussion Semicossyphus pulcher appears to follow the reproductive behavior typically associated with a strictly protogynous sex-changer (Warner 1975b).

Large male sheephead hold spawning territories and consistently are able to monopolize the matings of a group of females with whom they pair spawn. Sex-change theory predicts that mate monopolization is associated with protogyny because large individuals can fertilize many more eggs than they could produce themselves. In addition, S. pulcher lacks small males (Warner 1975b); in other labrid species, such small males can interfere with pair matings and decrease the overall success of large males (van den Berghe et al. 1989). Protogynous species with mating systems characterized by large male mate monopolization are prevalent on coral reefs, perhaps due to clear water, low mobility and absence of paternal care (Warner 1984). This holds true for the Santa Catalina Island sheephead populations

as well, and may be indicative of a behavioral trait conserved from the tropical environments from which labrids radiated.

The spawning behaviors of California sheephead differ from that of the other southern California wrasses; rock wrasse, Halichoeres semicinctus, which has a protogynous, dualistic mating system (M.S. Adreani & A. Allen unpublished observations) and senorita, Oxyjulis californica, which has a gonochoristic, group spawning mating system (personal observations), but they do have similarities with other studied Bodianines. Bodianus rufus, B. diplotaenia (Hoffman 1985) and Lachnolaimus maximus (Colin 1982) all appear to have a female defense territory as defined by Emlen & Oring (1977) and mating behavior involves guarding of females by a dominant male in specified spawning territories. Specific signals of female readiness and male display differ, but the basic mating system and behaviors associated with competition for females coincides with that observed in S. pulcher.

Species with mating systems in which a single male monopolizes mating could be highly vulnerable to overexploitation because large males are often rare in the first place. At this point, we do not know the extent to which other males might replace those that are removed. At the sheephead study sites, there were other males present in the area during observations, but it is unknown whether social control can produce more males if they are removed from the population, as has been shown in some tropical labrids, such as Labroides dimidiatus (Robertson 1972).

Females appear to congregate at spawning sites in the evenings but are more widely dispersed while feeding throughout the day, indicating that they are not part of a strict harem and may spawn with multiple males. Large males, however, appear faithful to specific sites throughout the day during the spawning season. Their site fidelity may make them vulnerable to fishing pressure and the removal of disproportionately high numbers of large males could adversely affect sheephead populations, even if male replacement occurs through sex change. When a larger female changes to male, her egg production is lost to the population and the age at which females change to males affects the size, sex structure, and production potential of the population.

19 Acknowledgements We thank K. Doctor, E. Bing-Saywer and M. Galima for their assistance in the field and the staff at Wrigley Marine Science Center for field station support. Many thanks to L. Allen for providing the illustrations and to R. Carpenter and L. Allen for insightful comments on early drafts of the manuscript. We also thank D. Noakes and two anonymous reviewers for their comments on the manuscript. This paper is contribution #225 from the Wrigley Marine Science Center, Santa Catalina Island, publication #134 from the Partnership for the Interdisciplinary Study of Coastal Oceans and publication #117 from the California State University, Northridge Marine Biology Program.

References Colin, P.L. 1982. Spawning and larval development of the hogfish, Lachnolaimus maximus. Fish. Bull. 80: 853– 862.

Cowen, R.K. 1990. Sex change and life history patterns of the labrid, Semicossyphus pulcher, across an environmental gradient. Copeia 3: 787–795.

Emlen, S.T. & L.W. Oring. 1977. Ecology, sexual selection, and the evolution of mating systems. Science 197: 215–223.

Feder, H.M., C.H. Turner & C. Limbaugh. 1974. Observations on fishes associated with kelp beds in southern California.

Fish. Bull. 160.

Helvey, M. 1982. First observations of courtship behavior in rockfish, genus Sebastes. Copeia 4: 763–770.

Hobson, E.S. 1976. The rock wrasse, Halichoeres semicinctus, as a cleaner fish. Calif. Dept. Fish Game 62: 73–78.

Hoffman, S.G. 1985. Effects of size and sex on the social organization of reef-associated hogfishes, Bodianus spp.

Environ. Biol. Fish. 14: 185–198.

Miller, D.J. & R.N. Lea. 1972. Guide to the coastal marine fishes of California. Calif. Dept. Fish Game, Fish Bull. 157: 235.

Robertson, D.R. 1972. Social control of sex reversal in a coral reef fish. Science 177: 1007–1009.

Stephens, J.S., Jr. 2002. California Sheephead. pp. 155–156. In: California’s Marine Living Resources: A Status Report, California Department of Fish and Game, Sacramento.

Thresher, R.E. 1984. Reproduction in Reef Fishes, T.F.H. Publications, Neptune City, New Jersey. 399 pp. van den Berghe, E.P., F. Wernerus & R.R. Warner. 1989. Female choice and the mating cost of peripheral males. Anim.

Behav. 38: 875–884.

Vincent, A.C.J. & Y. Sadovy 1998. Reproductive ecology in the conservation and management of fishes. pp 209–245. In: T. Caro (ed.) Behavioral Ecology and Conservation Biology, Oxford University Press, Oxford.

Warner, R.R. 1975a. The reproductive biology of the protogynous hermaphrodite, Pimelometopon pulchrum (Pisces: Labridae). Fish. Bull. 73: 262–283.

Warner, R.R. 1975b. The adaptive significance of sequential hermaphroditism in animals. Am. Nat. 109: 61–82.

Warner, R.R. 1984. Mating behavior and hermaphroditism in coral reef fishes. Am. Sci. 72: 128–136.

Warner, R.R. & D.R. Robertson, 1978. Sexual patterns in the labroid fishes of the Western Caribbean, I. The wrasses (Labridae). Smithsonian Contrib. Zool. 254: 1–24.

Warner, R.R., D.Y. Shapiro, A. Marconato & C.W. Petersen.

1995. Sexual conflict: males with highest mating success convey the lowest fertilization benefits to females. Proc. R. Soc. London, Ser. B, Biol. Sci. 262: 135–139.

Warner, R.R., D.R. Robertson & E.G. Leigh, Jr. 1975.

Sex change and sexual selection. Science 190: 633–638.