Courtship Behavior in the Dwarf Seahorse, Hippocampuszosterae

Home , Copulation (zoology), Courtship display, Dwarf seahorse, Mating system, Seahorse

Copeia, 1996(3), pp. 634-640

HEATHER D. MASONJONESAND SARA M. LEWIS

The seahorse genus Hippocampus (Syngnathidae) exhibits extreme morphological specialization for paternal care, with males incubating eggs within a highly vascularized brood pouch. Dwarf seahorses, H. zosterae, form monogamous 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 "copulatory 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, fish were also quivering, rapid side-to-side body vibrations ex- generally positioned side by side facing in the hibited alternately by males and females. The same direction except during phase 4 when fish remaining phases all occurred sequentially on faced one another in preparation for rising. the day of copulation, each distinguished by the Courtship took place in discrete bouts, which appearance of novel courtship behaviors. Phase were defined as beginning with the first display 2 on the day of copulation was marked by fe- of any courtship behavior (quivering, pointing, male pointing, in which females raised their or rising) by either fish and ending when one heads to form an oblique angle with the main or both individuals stopped courting and moved body axis. In phase 3, males began to point in out of the side-by-side position. Pumping by response to pointing by females. During the fi- males that occurred following phases 1 and 2 nal phase of courtship, seahorse pairs repeat- was not included as courtship interaction be- edly rose upward together in the water column, cause males and females were not in the side- ending in midwater copulation and the transfer by-side position and females were no longer of eggs from females directly into the male brood bright. Courtship activity levels (representing pouch. These four courtship phases are de- the percentage of time spent in courtship) were scribed below. calculated separately for each courtship phase by dividing the total time that pairs spent court- Phase 1: initial courtship (reciprocal quivering).- ing (summed across all bouts) by either the total Initial courtship took place in all seahorse pairs observation time each day (for phase 1) or the about 30 min after dawn on each courtship day total time spent in that phase (phases 2-4). until the day of copulation. During the night, Nineteen seahorse pairs were observed each fish remained immobile on separate holdfasts, day from the day of introduction until copula- but after dawn, males and females assumed ad- tion took place, and 15 of these trials resulted jacent side-by-side positions, brightened, and in successful copulations. Courtship duration engaged in 2-38 min of courtship. Courtship and number of bouts, as well as initiators of each in this phase was characterized by repeated oc- approach, brightening, and courtship behavior currences of reciprocal quivering, in which one within each bout were recorded for all 15 pairs. fish quivered and the other responded by quiv- The frequency and duration of specific court- ering within 5 sec. During reciprocal quivering, ship behaviors were recorded for seven of these tails of the two seahorses were positioned within pairs. Pairs that failed to mate within seven days 1 cm on the same holdfast, and their bodies = were analyzed separately (n 4 pairs). were angled outward slightly from the point of To examine which sex was more likely to in- attachment. As a male quivered, he rotated his itate courtship interactions, we conducted exact body toward the female, who generally rotated binomial tests against a null hypothesis of equal her body away before responding. Females pe- probability of either sex being the initiator. riodically shifted their tail attachment site, which Changes in courtship duration and activity level led to some pairs circling around their common across phases were examined using nonpara- holdfast. metric procedures, because within-phase vari- On the first courtship day, males approached ances were unequal. To examine changes in females to initiate courtship significantly more courtship duration and time from dawn to the often than expected by chance (Table 1: exact beginning of courtship within pairs between the binomial, P = 0.011). During this initial ap- first and second courtship days, we used Wil- proach, males also brightened before females coxon paired-sample tests. Changes in courtship (P = 0.029). After a male approached and level over activity time within pairs were ex- brightened, females responded by brightening. amined the using Kruskal-Wallis test proce- Once both fish had brightened, males generally dure. showed the first courtship behavior by quivering, although the prevalence over females quiv- RESULTS ering first was not significant (P = 0.212). During the first bout on the first day of court- Hippocampus zosterae exhibited four distinct ship, females always responded to males' quiv- of phases courtship marked by prominent be- ering by quivering. This reciprocal quivering havioral as well as changes, by differences in the behavior was repeated 36 (? 8.2) times during intensity of courtship. An initial courtship phase, the first courtship bout. The first bout was ter- designated as phase 1, took place early each minated when either fish, often the female, for the one morning or two days preceding cop- moved away (P = 0.133). Following the first ulation. The primary courtship behavior char- courtship bout, males in four out of 15 pairs this acterizing courtship phase was reciprocal (27%) displayed pumping behavior. In eight of MASONJONES AND LEWIS-SEAHORSE COURTSHIP BEHAVIOR 637

15 pairs, 2-3 additional courtship bouts ensued TABLE 1. Hippocampus zosterae COURTSHIPPHASES 1-23 min later in the morning on the first day. WITH THE NUMBER OF PAIRS IN WHICH APPROACH, Identical behaviors occurred during all subse- BRIGHTENING, COURTSHIP, AND COURTSHIP TERMINA- quent bouts, except for one pair in which the TION WERE INITIATED BY EACH SEX AND THE MOST female did not respond to the male's approach, FREQUENT COURTSHIP BEHAVIORSDISPLAYED BY EACH SEX. Seahorse = were observed brightening, and quivering. pairs (n 15) from the of introduction the of Courtship occurred in the morning for either day through day copulation in which both fish exhibited behaviors simul- one day (seven pairs) or two days (eight pairs) (pairs are excluded). preceding the day of copulation. Courtship du- taneously ration was on the first significantly longer day Phase (15.2 ? 4.2 than on of Courtship min) subsequent days Phase 1 Phase 2 Phase 3 Phase 4 courtship (5.3 ? 0.8 min; Wilcoxon T = 3, n = 8 pairs, P = 0.05). Males continued to initiate Approach Initiated By: courtship interactions on each day before cop- Male 11 12 6 9 ulation, with males approaching females, Female 2 2 6 4 before females, and ex- brightening generally Brightening Initiated By: behavior first. hibiting quivering Male 11 9 2 2 Female 3 1 1 1 Phase 2: day of copulation (pointing-pumping).- First Behavior On the day of copulation, H. zosterae pairs ex- Courtship By: hibited a series of dramatic changes in behavior Male 9 3 6 7 during the prolonged and active courtship that Female 5 12 8 8 began shortly after dawn and lasted until cop- Courtship Terminated By: ulation had occurred, an average of 3.9 (? 0.4) Male 4 5 9 h after dawn. This second courtship phase was Female 9 7 3 distinguished by females exhibiting the point- Courtship Behaviors Exhibited: ing posture. As a female pointed, she leaned Male Quiver Quiver Point her body toward the male, who simultaneously Point/Rise Female Quiver Point Point leaned away. Males generally responded to fe- Point/Rise male pointing by leaning back toward the female and quivering. Females leaned away as the male quivered, but in contrast to reciprocal quivering, females maintained their position on (? 6.8) min on the first day of courtship (Wil- the common holdfast. Pumping behavior was coxon T = 20, n = 15 pairs, P < 0.05). The displayed by males in all seahorse pairs follow- second phase of courtship lasted 54.3 (? 12.6) ing the first courtship bout in this phase. min, with a total courtship duration of 10.9 (+ During phase 2 of courtship, males continued 1.9) min during one to six bouts. Phase 2 was to initiate approach significantly more often than followed by a latency period lasting 23-220 min did females (Table 1: P = 0.006), and males (median = 111 min), during which no courtship brightened before females did (P = 0.011). behaviors were observed and females were not However, in contrast to previous courtship in- bright. During this latency period, males in ev- teractions, females rather than males almost al- ery seahorse pair displayed pumping behavior, ways (P = 0.018) displayed the first courtship with frequencies varying from 8-30 pumps/h. behavior, pointing, which occurred an average of 28 times during this courtship phase. In re- Phase 3: day of copulation (pointing-pointing).- sponse to female pointing, males most often The third phase of courtship occurred on the quivered (55 ? 6.1% of female points respond- day of copulation and was distinguished by males ed to by male quivering), although males did assuming the pointing posture in response to fe- not respond to 45% (? 6%) of female points. male pointing. During this phase, males and fe- Pointing remained the predominant female be- males initiated courtship by approaching equally havior throughout this phase of courtship, but often (Table 1), and they tended to brighten females also quivered in six of the 15 pairs. simultaneously (79% of pairs). Males and females Courtship bouts were equally likely to be ter- also exhibited the first courtship behavior, which minated by either sex (P = 0.387). was pointing in both sexes, equally often (P = Courtship began earlier on the day of copu- 0.395). During the first courtship bout, males lation than on previous days: time from dawn generally responded to female points by pointing to first courtship behavior on the day of copu- (38 ? 8.8% of female points responded to by lation was 15.7 (? 3.3) min, compared with 31.9 male point), by quivering (34 ? 11.2%), or rare- 638 COPEIA, 1996, NO. 3

60 - creased in this courtship phase to 92%. Inter- spersed with these courtship behaviors, pairs 50- engaged in 5-44 rises/h during this phase. During this phase, females became increas- 3: 40- ingly active in courtship. The first rise, consisting of a male and female moving upward in the 30- water column together, was initiated by females significantly more often than by males (P = ? 20- 0.018). During the final copulatory rise, the female inserted her and transferred 0 - ovipositor o 10- eggs through the opening into the male's brood pouch. The copulatory rise was also initiated by the female (P = 0.018), and copulations lasted 13.3 (? 0.8) sec. This phase ended after copulation, and the male and female generally swam down to separate plants to feed. For a few min- utes after copulation, males remained bright and swayed back and forth. The total duration of this phase was 41.5 (? 3.9) min, which in- Courtship Phase cluded 20.4 (? 3.1) min of courtship. Fig. 1. Courtshipactivity levels (representingthe Courtship activity (time pairs spent courting percentageof time spent in courtship)observed across as a percentage of the total time spent in that different courtship phases in Hippocampuszosterae (x phase) changed significantly across courtship + 1 SE). phases (Fig. 1; Kruskal-Wallis H = 36.5, 4 df, P < 0.0001). Courtship increased from relatively low levels on the first and second days of courtship to increasingly active courtship during the ly, by pumping (8 ? 3.9%). Males did not re- three consecutive courtship phases on the day spond at all to 20 (? 6)% of the female's points. of copulation. During the final courtship bout of phase 3, males showed an increased tendency to respond to fe- Courtshipinteractions in pairs thatfailed to mate.- male points by pointing (57 ? 21.6%), rather Four of 19 seahorse pairs failed to court or mate than by quivering or pumping. Phase 3 typically within seven days. In successfully mating pairs, ended with the male departing (P = 0.073). This males generally initiated courtship by ap- courtship phase had a total duration of 48.0 (? proaching the female and brightening first. Af- 13.8) min with courtship lasting 9.1 (? 1.8) min ter females brightened, the male quivered, and during one to six bouts. A single seahorse pair females then responded by quivering within 3- did not show phase 3 but, rather, proceeded di- 5 sec. In two pairs that failed to mate, the initial rectly from phase 2 to phase 4. approach and brightening was made by the male, but both females failed to brighten in response. Phase 4: day of copulation(rising and copulation).- In both pairs, males then proceeded to quiver, The final courtship phase on the day of copu- but again neither female responded. In the re- lation included a series of 5-8 courtship bouts. maining two pairs that failed to mate, females Each bout began with the male and female on made the initial approach and brightened first, the same plant about 3 cm apart, usually facing and the male responded by brightening and then one another. Bouts during this phase were dis- quivering. However, neither female responded tinguished by rising, in which both fish rose further by quivering after this initial contact, upward together 2-13 cm in the water column. even though the males remained bright and At the start of this phase, pairs were usually continued to quiver. These unsuccessful at- already close, and both fish retained their tempts at courtship were usually repeated in the brightened color from the previous phase. Males morning on the first 2-3 days that the pairs and females were equally likely to display the were together, but the fish were rarely close for first courtship behavior (Table 1; P = 0.500), the remaining 4-5 days. which as in phase 3 was predominantly pointing. Males to a female's either responded point by DISCUSSION pointing (79 ? 10.6%), pumping (12 ? 3.5%), or more rarely quivering (1 ? 1.4 %). The over- This study provides the first quantitative de- all rate of male response to female points in- scription of courtship behavior in the dwarf sea- MASONJONES AND LEWIS-SEAHORSE COURTSHIP BEHAVIOR 639 horse, H. zosterae,and reveals several major be- final stage of oocyte maturation during which havioral changes occurring among four distinct eggs are hydrated prior to ovulation (Wallace phases of seahorse courtship. Reciprocal quiv- and Selman, 1981; Vincent, 1990; Selman et ering characterizes the first phase of courtship al., 1991). Toward the end of this latency pe- that occurs in early morning for one or two days riod, distinctive orange coloration of the eggs preceding copulation. On the day of copulation, becomes visible through the abdominal wall of there are three distinct phases of courtship. the female. Ovulation seems to represent an Phase 2 is marked by the novel appearance of irreversible commitment by the female to trans- female pointing and male pumping. During ferring eggs, because, if pairs are separated af- phase 3 on the day of copulation, males exhibit ter this point, the female will eventually release an increasing tendency to point, rather than to the unfertilized clutch into the water (HDM, quiver, in response to female points. In the final pers. obs.; Vincent, 1990). The increasingly ac- phase of courthip, seahorse pairs repeatedly rise tive role played by females in initiating pointing together in the water column, ending in mid- and rising in the final two courtship phases fol- water copulation during which eggs are depos- lowing ovulation may reflect the exigency for a ited by females directly into the male brood female to find a male to fertilize and incubate pouch. her eggs. In addition to the large material in- Initial courtship behavior during phase 1 in vestment in eggs, loss of a clutch is also costly H. zosterae is similar to the elaborate sunrise because these females generally do not mate greeting rituals that have been described for again until after the normal gestation period field populations of the pipefish Corythoichthys would have elapsed (HDM, per. obs.; Vincent, intestinalis (Gronell, 1984) and Hippocampuswhi- 1990, 1994b). tei (Vincent, 1990), both of which exhibit mo- In spite of their extreme male care, seahorses nogamous pair-bonding throughout a repro- do not appear to show a reversal of traditional ductive season. It has been suggested that daily courtship roles as has been predicted by sexual repetition of this elaborate courtship display selection theory. The present study indicates an serves to facilitate reproductive synchroniza- active role by H. zosterae males in initiating tion of males and females (Gronell, 1984; Vin- courtship interactions up until the day of cop- cent 1995). Laboratory experiments on H. fus- ulation. This finding is consistent with previous cus indicate that this daily greeting plays a role studies on H. fuscus (Vincent, 1994a), in which in the establishment and maintenance of pair males were found to compete more intensely bonds (Vincent, 1995), since females were found than females for access to mates. These results to mate preferentially with their greeting part- contradict some influential summaries (Wil- ner rather than with their previous mate. liams, 1975; Trivers, 1985) that have suggested There are distinct changes across the differ- that seahorses are courtship-role reversed. In ent phases of seahorse courtship in whether the seahorse species studied to date, the pres- males or females are more likely to initiate ence of traditional courtship roles in terms of courtship interactions. Males initiate courtship males being more active in courtship and males interactions on each day before copulation, with competing for access to females has demon- males approaching females, males exhibiting strated that courtship roles are not necessarily brightened coloration before females, and males reversed in species with a high degree of pa- generally displaying the first courtship behav- ternal care. ior. During phase 2 on the day of copulation, males continue to approach and brighten first, but females exhibit the first courtship behavior ACKNOWLEDGMENTS by pointing. Later on the of copulation, day We thank A. Vincent for useful discussion females become increasingly active in the ini- and and I. and R. Cohen tiation and continuation of courtship bouts, ini- encouragement Dodge for technical assistance. Financial was tiating courtship approaches as often as males, support in a from the Howard and females consistently initiate the rises that provided part by grant lead to The four H. zos- Hughes Medical Institute. The manuscript was eventually copulation. the comments of terae pairs that never courted or mated also greatly improved by insightful sup- three reviewers. port a more active courtship role for males, since anonymous courtship apparently fails to progress when females do not to respond repeated brightening LITERATURE CITED and quivering by males. The latency period following phase 2 on the BERGLUND, A., G. ROSENQVIST, AND I. SVENSSON. day of copulation appears to coincide with the 1989. Reproductive success of females limited by 640 COPEIA, 1996, NO. 3

males in two pipefish species. Am. Nat. 133:506- STRAWN,K. 1958. Life history of the pigmy seahorse, 516. Hippocampus zosteraeJordan and Gilbert, at Cedar BOHLKE,J. E., AND C. C. G. CHAPLIN. 1966. Fishes Key, Florida. Copeia 1958:16-22. of the Bahamas and adjacent tropical waters. Liv- THORNHILL,R., AND D. GWYNNE. 1986. The evo- ingston Publishing Co., Wynnewood, PA. lution of sexual differences in insects. Amer. Sci. BOISSEAu,J.P. 1967. Les regulations hormonales de 74:382-389. l'incubation chez un vertebre male: recherches sur TRIVERS,R. L. 1972. Parental investment and sexual la reproduction de l'Hippocampe. Unpubl. Ph.D. selection, p. 136-179. In: Sexual selection and the diss., Univ. of Bordeaux, Bordeaux, France. descent of man. B. Campbell (ed.). Aldine Publish- BREDER,C. M., AND D.E. ROSEN. 1966. Modes of ing Company, Chicago. reproduction in fishes. T.F.H. Publishing, Garden . 1985. Social evolution. Benjamin Cummings City, NY. Publishers, Menlo Park, CA. CLUTTON-BROCK,T. H. 1991. The evolution of pa- VINCENT, A. C. J. 1990. Reproductive ecology of rental care. Princeton Univ. Press, Princeton, NJ. seahorses, Unpubl. Ph.D. diss., Univ. of Cam- FIEDLER,K. 1954. Vergleichende Verhaltenstudien bridge, Cambridge. an Seenadeln, Schlangennadeln und Seepferdchen . 1994a. Seahorses exhibit conventional sex (Syngnathidae). Z. Tierpsychol. 11:358-416. roles in mating competition, despite male pregnan- GILL, T. 1905. The life history of the sea-horses cy. Behaviour 128:135-151. (Hippocampids). Proc. US Nat. Mus. 28:805-814. . 1994b. Operational sex ratios in seahorses. GINSBURG,I. 1937. Review of the seahorses (Hippo- Behaviour 128:153-167. campus) found on the coasts of the American con- . 1995. A role for daily greetings in maintain- tinents and of Europe. Ibid. 83:497-595. ing seahorse pair bonds. Anim. Behav. 49:258-260. GRONELL,A. M. 1984. Courtship, spawning and so- , AND L. SADLER. 1995. Faithful pair bonds in cial organization of the pipefish, Corythoichthysin- wild seahorses, Hippocampus whitei. Ibid. 50:1557- testinalis (Pisces: Syngnathidae) with notes on two 1569. congeneric species. Z. Tierpsychol. 65:1-24. , I. AHNESJ6, A. BERGLUND,AND G. ROSENQVIST. GWYNNE,D. T. 1991. Sexual competition among fe- 1992. Pipefishes and seahorses: are they all sex role males: what causes courtship-role reversal? Trends reversed? Trends in Ecol. Evol. 7:237-241. in Ecol. Evol. 6:118-121. WALLACE,R. A., ANDK. SELMAN.1981. Cellular and HERALD, E. S. 1959. From pipefish to seahorse-a dynamic aspects of oocyte growth in teleosts. Amer. study of phylogenetic relationships. Proc. Calif. Zool. 21:325-343. Acad. Sci. 29:465-473. WILLIAMS,G. C. 1975. Sex and evolution. Princeton LINTON,J. R., AND B.L. SOLOFF. 1964. The physi- Univ. Press, Princeton, NJ. ology of the brood pouch of the male seahorse Hip- pocampus erectus. Bull. Mar. Sci. 14:45-61. RIDLEY,M. 1978. Paternal care. Anim. Behav. 26: DEPARTMENT OF BIOLOGY, TUFTS UNIVERSITY, 904-932. MEDFORD, MASSACHUSETTS02155. Send re- ROSENQVIST,G. 1990. Male mate choice and female- print to SML. Submitted: 18 female for mates in the Ner- requests July competition pipefish 1995. 1996. Section editor: Ibid. 39:1110-1115. Accepted: 30Jan. ophis ophidion. S. T. Ross. SELMAN,K., R.A. WALLACE,AND D. PLAYER. 1991. Ovary of the seahorse, Hippocampus erectus.J. Mor- phol. 209:285-304.