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Courtship Behavior in the Dwarf Seahorse, Hippocampuszosterae

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Courtship Behavior in the Dwarf Seahorse, Hippocampuszosterae Copeia, 1996(3), pp. 634-640 Courtship Behavior in the Dwarf Seahorse, Hippocampuszosterae HEATHER D. MASONJONESAND SARA M. LEWIS The seahorse genus Hippocampus (Syngnathidae) exhibits extreme morpho- logical specialization for paternal care, with males incubating eggs within a highly vascularized brood pouch. Dwarf seahorses, H. zosterae, form monoga- mous pairs that court early each morning until copulation takes place. Daily behavioral observations of seahorse pairs (n = 15) were made from the day of introduction through the day of copulation. Four distinct phases of seahorse courtship are marked by prominent behavioral changes, as well as by differences in the intensity of courtship. The first courtship phase occurs for one or two mornings preceding the day of copulation and is characterized by reciprocal quivering, consisting of rapid side-to-side body vibrations displayed alternately by males and females. The remaining courtship phases are restricted to the day of copulation, with the second courtship phase distinguished by females pointing, during which the head is raised upward. In the third courtship phase, males begin to point in response to female pointing. During the final phase of courtship, seahorse pairs repeatedly rise together in the water column, eventually leading to females transferring their eggs directly into the male brood pouch during a brief midwater copulation. Courtship activity level (representing the percentage of time spent in courtship) increased from relatively low levels during the first courtship phase to highly active courtship on the day of copulation. Males more actively initiated courtship on the days preceding copulation, indicating that these seahorses are not courtship-role reversed, as has previously been assumed. SEXUAL selection theory predicts that the the ventral surface of the male (Berglund et al., relative investment made by males and fe- 1989; Rosenqvist, 1990). Seahorses (genus Hip- males in their offspring is a primary determi- pocampus) possess the greatest specialization for nant of sexual selection intensity and patterns paternal care, with females depositing their eggs of courtship behavior within species (Trivers, directly into an abdominal brood pouch on the 1972; Williams, 1975; Thornhill and Gwynne, male where fertilization takes place (Fiedler, 1986). Across the animal kingdom, female in- 1954). In Hippocampus, the male brood pouch vestment in offspring typically exceeds that of epithelium is highly vascularized and provides males (reviewed by Clutton-Brock, 1991), and gas exchange and osmoregulation for devel- traditional sex roles during courtship involve oping embryos throughout gestation (Boisseau, males playing a more active role in initiating 1967; Linton and Soloff, 1964). courtship, males competing for access to fe- Due to their high degree of morphological males, and females being selective about mates specialization for paternal care, seahorses are (Trivers, 1972; Williams, 1975; Gwynne, 1991). an important group for testing the prediction In numerous groups, however, males provide that relative parental investment determines sex considerable paternal care (Ridley, 1978), which roles during courtship. However, previous de- may take the form of egg incubation or aera- scriptions of seahorse mating behavior have been tion, protection, or provisioning ofjuveniles. In largely anecdotal (Gill, 1905; Fiedler, 1954; species where male investment exceeds that of Breder and Rosen, 1966). Recent laboratory females, sexual selection theory predicts that studies on Hippocampusfuscus (Vincent, 1994a, these traditional courtship patterns should be 1994b, 1995) and field studies on H. whitei (Vin- reversed. cent and Sadler, 1995) have revealed both of Fishes in the family Syngnathidae (pipefishes these species to be monogamous, with a single and seahorses) show wide variation in the de- male and female mating repeatedly and exclu- gree of male anatomical and physiological spe- sively over the course of the reproductive sea- cialization for paternal care (Herald, 1959; Vin- son. Studies on H. fuscus have shown that males cent et al., 1992). In some pipefishes such as compete more intensely for access to mates than Nerophis ophidion, females attach their eggs onto do females (Vincent, 1994a), indicating that ex- ? 1996 by the American Society of Ichthyologists and Herpetologists MASONJONES AND LEWIS-SEAHORSE COURTSHIP BEHAVIOR 635 treme male care is not associated with court- We began daily behavioral observations for ship-role reversal, as has previously been as- each pair starting on the day of introduction sumed (Trivers, 1985). into tanks and continuing until copulation oc- Here we present a quantitative analysis of curred. Observations were made continuously courtship and copulatory behavior in the dwarf during the first 3 h after tank lights came on seahorse, Hippocampus zosteraeJordan and Gil- (defined as dawn) on each day before copula- bert, a species exhibiting an extreme degree of tion, and from dawn until copulation occurred paternal care. This study is based on daily ob- on the last day. Previous observations have in- servations of paired seahorses maintained un- dicated that all seahorse courtship occurs in the der standardized conditions in the laboratory morning, except on the day of copulation (Vin- from the day of introduction until copulation cent, 1994a; pers. obs.). Our analyses were based occurred. Hippocampus zosteraecourtship is par- on a total of approximately 320 h of observa- titioned into four discrete phases, distinguished tion. by marked behavioral changes as well as by dif- Beginning at dawn each day, the location of ferences in courtship intensity. both fish and their proximity was recorded. Proximity was classified as either far apart (dis- MATERIALS AND METHODS tance > 4 cm), close (' 4 cm), or touching (in direct physical contact). When transitions be- Study organism.-Hippocampus zosteraeoccurs in tween these states occurred, the individual ap- shallow seagrass beds from the Gulf of Mexico proaching or departing was identified. Behavior east through the Bahamas and to Bermuda was recorded continuously using the following (Ginsburg, 1937; B6hlke and Chaplin, 1966), definitions of behavior patterns (modified from and adult size ranges from 16-38 mm (mea- Fiedler, 1954; Vincent 1990, 1994a): "bright- sured as the linear distance from the top of ening" refers to a rapid change in coloration coronet to end of tail; Strawn, 1958). The mo- from normal body color (varying from black to nogamous mating system exhibited by H. fuscus white) to lighter body color over most of the and H. whitei (Vincent, 1995) is also observed body, excluding portions of the head as well as in laboratory studies of H. zosterae, with a male the dorsal midline that remain dark. Bright- and female remaining together and mating re- ening characterizes social interaction in sea- peatedly over the course of the breeding season horses and is not restricted to courtship (HDM, (HDM, unpubl. data). Females transfer one en- pers. obs.). In "quivering," fish assume an erect tire clutch of eggs to a single male [x (+ 1 SE) posture, with pectoral fins expanded, and rap- = 12.4 (+ 2.2) eggs, n = 9]. Three to 16 fully idly vibrate their body from side to side at a independent young are born after approxi- rate of approximately 12 cycles per sec. In mately 10 days of gestation within the male "pointing," a fish raises its head upward toward brood pouch, and pairs remate within 4-20 h the water surface to form an oblique angle with of the male's releasing young. main body axis and then lowers it again to a Hippocampus zosteraewere collected near Key horizontal position. "Pumping" is shown exclu- Largo, FL, and maintained in same-sex groups sively by males in H. zosteraeand consists of males for 1-8 weeks before trials in an attempt to opening their brood pouch and repeatedly flex- standardize reproductive states. Tanks were ing the tail in a motion similar to that displayed maintained at 25.5 C on a 13L:11D photope- during the release of young. A single pumping riod, and two plastic seagrass plants were sup- motion lasts from 1-32 sec, with a mode of 8 plied for attachment sites. Fish were fed re- sec. During "rising," males and females release cently hatched Artemia supplemented with cal- their respective holdfasts and rise up into the cium (Kalkwasser, Thiel Aquatech) daily. water column facing one another. In a "copu- latory rise," the female genital papilla is placed Courtship behavior trials.-On the morning be- inside the male brood pouch opening, followed fore each trial began, wet mass of adult male by egg transfer. Additional behaviors not in- and female seahorses were measured by blot- volved in courtship, including feeding and ting fish dry and weighing them to the nearest swimming, were also recorded during each ob- 10 mg in seawater in a plastic cuvette. Experi- servation period. mental fish ranged from 90-280 mg wet mass, We defined courtship interactions as occur- and pairs were selected for similarity of body ring when a male and female were within 4 cm size, with a mean difference between paired in- of one another and both fish exhibited bright- dividuals of 27 (? 4) mg. Pairs were placed sin- ened coloration. During courtship interactions, gly in 57 liter aquaria, and each seahorse was both sexes exhibited a characteristic posture used in only one courtship trial. consisting of an erect body with head inclined 636 COPEIA, 1996, NO. 3 downward. During courtship,
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