Pacific Science (1978), vol. 32, no. 2 © 1978 by The University Press of Hawaii. All rights reserved

Diel, Lunar, and Seasonal Periodicity in the Reproductive Behavior of the Pomacanthid Fish, potteri, and Some Other Reef Fishes in Hawaii!

PHIL S. LoBEL2

ABSTRACT: The reproductive behavior of five Hawaiian reef fishes are described for the first time: an angelfish (), three butterflyfishes (Chaetodon fremblii, C. multicinctus, C. unimaculatus), and a goatfish (Paru­ peneus multifasciatus). The angelfish, , was examined in detail. It was determined that every month from December until May it spawns each evening during the week preceding a full moon. On extensive coral reefs C. potteri occurs mostly in pairs, whereas on patch reefs a single male may control access to several females. Thus, males on patch reefs seem to enjoy greater reproductive success than males on extensive reefs. The advantages potentially associated with spawning synchronized at dusk between the first quarter and full moon primarily involve reduced mortality of offspring. The annual reproductive period, which is shared by several other Hawaiian shore fishes, is correlated with a semiannual shift in ocean currents that may retain larvae in the vicinity of the Hawaiian reefs at that time.

REPRODUCTIVE BEHAVIOR OF MARINE FISHES pomacanthid, Centropyge potteri, which has been scarcely described for any but a few spawns at dusk. Also included are observa­ taxa (Breder and Rosen 1966), e.g., some tions of other that at the same pomacentrids (Clarke 1970, Helfrich 1958, time, notably three chaetodontids, one mul- Myrberg, Brahy, and Emery 1967, Sale 1971, lid, and three acanthurids. .. Stevenson 1963, Swerdloff 1970, Walters 1967) and some labrids and scarids (Potts 1974, Randall and Randall 1963, Reinboth 1973, Roede 1972, Youngbluth 1968). De­ METHODS spite numbers field studies, the reproductive Direct Observations activities of many reef fishes remain un- known. Most observations on the activity of Fishes were watched under water using reef fishes have been during midday and thus scuba equipment during approximately 300 have missed peaks of reproductive activity at hr at all times of day and night, including 30 dusk, where and when such peaks occur. hr immediately before sunset, from June A similar situation existed with predatory 1974 to June 1975. I soon.recognized t~lat the activities until observations were made during ree~ fishes were sJ?a:v~mg pr~dommantly the crepuscular periods (e.g., Hobson 1965, dunng dusk. To m~mmI~e.the mflu~n.ce of --)-968~)-972~19i4)4nisarticle reports --me--my-presen€e-<::m-t-hls-aettvlt-y.---:I-posttIoned- spawning behavior and periodicity of a myself on statIOn .at least 30 mm before the fish began courtshIp. The sudden appearance of a diver (or a large fish) caused many fishes to cease spawning activity. I remained on I Manuscript accepted 11 February 1978. station until convinced that all activity had 2 University of Hawaii, Department of , Honolulu, Hawaii 96822. Current address: Harvard ceased and that the fishes had retired for the University, Museum of Comparative Zoology, Cam­ night [for approximate timing of various bridge, Massachusetts 02138. species, see Hobson (1972)]. Spawning activ- 193 194 PACIFIC SCIENCE, Volume 32, April 1978

TABLE I SIZE AND RATIO OF THE SEXES OF Centropyge potteri ON PATCH REEF AREAS

NUMBER STANDARD DEPTH OF FISH NUMBER, RATIO, LENGTH, MEAN LOCATION (m) SAMPLED MALE: FEMALE MALE: FEMALE AND RANGE (mm) PATCH HABITAT

Outside 16 14 3: II 1:3.67 76.5 (61-87) Fish from two rubble areas 2 Kaneohe meters apart; total area Bay (Oahu) approximately 24 m2 Waikiki 8.3 4 1:3 1:3 76.5 (63-91) Solitary coral cluster (Oahu) approximately 3 meters from extensive reef; patch approximately I meter diameter 16-20 7 1:6 1:6 65 (45.5-83) Three rocks, 0.6 meter at greatest length; close together with scattered rubble 20 8 2:6 1:3 76 (61-94) Three rocks, I meter at greatest length; spaced I meter apart with rubble around 25-30 5 1:4 1:4 63 (54-68) Single coral cluster 1.4 m 2, 0.6 meter high 25-30 7 1:6 1:6 71 (59-89) Patch of large rock rubble approximately 16 m2 Totals 8.5-30 45 9: 36 1:4.28 ± 1.39 71 (45.5-94)

NOTE: The difference between sex ratios between patch and extensive reefs (Table 2) was significant (I statistic, two·tail level of significance; 0.01 < P < 0.02).

TABLE 2 SIZE AND RATIO OF THE SEXES OF Centropyge potteri ON EXTENSIVE REEF AND RUBBLE HABITATS

NUMBER STANDARD EXTENSIVE REEF AND DEPTH OF FISH NUMBER, RATIO, LENGTH, MEAN RUBBLE LOCATION (m) SAMPLED MALE:FEMALE MALE:FEMALE AND RANGE (mm) HABITAT

Mahukona 11-16 26 12: 14 1: 1.17 62 (47-81) Extensive reef with dense layers (Hawaii) of coral including Porites lobata, Porites compressa, Poci//opora meandrina Makaha 8.3-16 12 4:8 I: 2 57.5 (38-71) Vast area of large rubble on top (Oahu) and below a ledge Makua 8.3-10 10 6:4 1:0.67 66 (55-81) Large cave surrounded by rubble (Oahu) and coral; total area approximately 67,000 m2 Moanalua Bay 8.3-13 18 6: 12 1:2 75 (51-98) Scattered , mostly (Oahu) Poci//opora meandrina, and large rubble spaced less than _meter apart Waikiki 16-30 58 24:34 1: 1.42 73 (42-95) Large rubble covering vast areas; (Oahu) rubble in some patches, but less than 1 meter part; very little live coral Wreck buoy 8.3-10 50 20:30 I: 1.5 77.5 (49-101) Extensive region of large corals, mainly Porites lobaw and Pocillopora meandrina corals spaced less than I meter apart Totals 8.3-30 174 72:98 I: 1.46 ± 0.51 68.5 (38-101)

NOTE: See note for Table I.

.. f'(. , -~ Reproductive Behavior of Centropyge potteri-LoBEL 195

TABLE 3

DIRECT OBSERVATION OF Cenlropyge pOlleri SPAWNING, 1975

DATE OF DATE OF FULL MOON OBSERVATION REEF NUMBER OF FISH SEEN SPA WNING

27 January 25 January Extensive Six pairs 26 February 25 February Patch One male and six females, male spawned with 27 March 22-26 March Patch three or four of six females each evening 25 April 19 April Patch One male and three females 20-24 April Extensive Eight pairs spawned each evening 23 June 21 June Extensive One pair out of eight spawned

NOTE: All spawning occurred within 1 hr of sunset. Each female spawned once, although where more than one female was available, males spawned more than once. A total of7 harem and 31 pair spawnings were observed (a pair spawning refers to a single spawning by a male with one female; a harem spawning refers to one male spawning repeatedly with two or more females). ity was not observed during the several dives the notion of coral reefs, a vast expanse of at sunrise. coral and rubble. Terms such as abundant, common, oc­ casional, and rare are used as defined by Study Areas Chave and Eckert (1974). Study sites were located primarily on the reefs off Waikiki and the Waianae coast, Oahu Island, and the Kona coast, Hawaii Island. These reefs were typically composed HABITAT EFFECT ON SEX RAno of stony corals (Porites spp. and Pocillopora Adult Centroyge potteri inhabit reefs spp.) and rubble. Species composition of consisting oflarge corals and boulders within comparable regions has been reported by the 3- to 50-meter depth range. In such areas, Hobson (1974). this species is among the ten most frequently seen fishes (Hobson 1974). Weights and Measures The ratio of males to females differed between patch reefs and extensive reefs. There Specimens were collected by spear. All were approximately two to four more females weights were assessed on a Mettler electronic per male on a patch reef than on extensive balance. Fishes were generally examined reefs (Tables 1, 2). This differential avail­ while fresh or frozen. Percentage gonad ability of females was evident during repro­ weight was determined by dividing the blot­ duction. Males on patch reefs spawned with dry gonad weight by the blot-dry total body each female, one at a time consecutively per weight of a fish and multiplying by 100. A evening, whereas males on extensive reefs total of 315 specimens of Centropyge potteri did not spawn with more than one female were examined. per evening (Table 3). The basis for these differing sex ratios has Definitions not been thoroughly tested; however, there e-indications-rharirmay De relarecn--o-" Reefs inhabited by Centropyge potteri male defense of a spawning site. The most were classified as either extensive or patch important aspect of such territory appears to reefs. A patch of rock/coral with an area of be a towering rock or coral knoll over which less than 24 m 2 (the largest patch reef found), the fish spawn (see details below). I intro­ surrounded by sand, and at least 100 meters duced foreign males onto patch reefs on five distant from neighboring reefs is defined as occasions and each time the resident male a patch reef. Patches near other reefs are attacked and kept the intruder over the sand defined as satellite reefs. Extensive reefs are beside the patch reef. Presumably it is characteristic ofareas usually associated with dangerous for the fish to travel between reefs. 196 PACIFIC SCIENCE, Volume 32, April 1978

~~ PAIR SPAWNS ~ /::~

FISH RETURN TO ,~ , SHEl TER ::ll~ ""~ MALE "FLUTTERS" ~ ~ OJ AROUND FEMALE ~

CENTROPYGE POTTERI

FIGURE I. Generalized courtship and spawning sequence.

The attacks by the resident were most per­ has been entirely recorded on super-8 mm sistent during the time of reproduction. movie film. The general sequence of behavior Centropyge potteri is a herbivore and did not is presented diagramatically in Figure I. defend the territory against other species Courtship was initiated by the male, who with similar food habits. During 20 hr of ceased feeding and began courting about I hr observation at midday only four agonistic before sunset. The male swam toward a encounters occurred between C. potteri and female in a vertical undulating style distinct Ctenochaetus strigosus (Acanthuridae) and from normal swimming motion. He stopped Eupomacentrus fasciolatus (= Pomacentrus above her and erected all median fins while jenkinsi, Pomacentridae). In the extensive fluttering the pectoral fins. This display con­ coral reef habitat the availability ofspawning tinued as the male drifted slowly upward sites, by inspection,. was greater than on with his head diagonally up or with his side patch reefs, perhaps allowing more males to parallel to the substrate. If the female failed occupy spawning sites and giving females a to follow, the male halted immediately and broader choice of mates or merely reducing darted back to her. The male continued the ability of anyone male to exclude other courtship by swimming around the female males from the large reef (see description of in the undulating fashion. In this way, the spawning site below). Individuals limit their male approached the female as he swam movements to restricted, well-defined loca- forward while rising and dropping in a ----tlons (Hl)bs-01rt~74')-.------SW(')(')fliflg,fluHeFing-m()tiQn~Gourtship-con­ tinued until the female was enticed over to the prominent coral or rock tower and she rose above the tower with the male. This SPAWNING BEHAVIOR OF Centropyge potteri usually only required a few courting passes. The following generalized description of Spawning occurred only over the tallest coral Centropyge potteri spawning is based upon or rock in the immediate area. During court­ 31 observations of pair spawning and 7 ship and spawning the overall blue color of harem spawnings (Table 3). One sequence both fish paled as the red color intensified. Reproductive Behavior of Centropyge potteri-LoBEL 197

during the full moon period of May 1975 at Enewetak Atoll, Marshall Islands.

REPRODUCTIVE PERIODICITY The peak reproductive season for Cen­ tropyge potteri began in December and con­ tinued through May (Figure 3). Development of the gonad within this annual season was correlated with the full moon; the female's ovary attained its greatest weight before spawning commenced-about 1 week before the full moon (Figure 4). Centropyge potteri FIGURE 2. Centropyge potteri during the climax of was observed to spawn only during the week spawning. The male is the larger individual on the right. preceding the full moon from January to April 1975 (Table 3). No observation dives During the first few encounters, the female were performed during the full moon period rose up with the male and then darted back of May 1975. In June 1975, however, three to cover when the male attempted to move dives during the full moon week revealed to the spawning position. The male pursued only one spawning event, although nine her while continuing his courtship display. other pairs were in full view. Observation Spawning climaxed when the female re­ during other evenings of the lunar cycle and mained in midwater, about I meter above other times of the year gave no indications of the coral/rock tower. The male approached spawning having occurred. from underneath and appeared to press his The question whether spawning occurs snout against her abdomen (Figure 2). Such during the months of June to December may contact may signal or facilitate egg release. still be debated. However, it is evident that A single burst of eggs was broadcast. Be­ if spawning does occur at that time, the size cause of the low light level I could not see of spawn will be very much less than during sperm released in the field, but in aquaria the months of December through May. The spawnings of related it one male seen spawning in June did so only occurred simultaneously with egg release. once, although he pursued two neighboring Immediately after release of eggs and sperm, females that fled rather than respond to the pair darted to cover with the female courtship. If spawning does occur during the chasing the male, apparently nipping at his off-season, it is probably infrequent. caudal fin. Chasing by the female happened only after consummation of the spawnirig act and not during earlier episodes of court­ SPAWNING BEHAVIOR OF CHAETODONTIDS ship. Spawning was consummated befote sunset, but the absolute time varied. Sodn During the observations of Centropyge after sunset the fish retired into a cavity in potteri, spawning was observed coincidental­ --t-he-reeHor--the-night. ly in rnree species ofCliaetodontiClS:Lhaeto­ During courtship various sounds, like don fremblii, C. unimaculatus (three observa­ clicks and grunts, were produced by theSe tions of each), and C. multicinctus (six fish, although their precise role during repro­ observations). All spawned within the hour duction was not examined. preceding sunset during the week before the Similar reproduction behavior was noted full moon, February and March 1975. in aquarium spawnings of Centropyge bi­ The reproductive behavior of C. multi­ spinosus (Bauer and Klay 1974, Lobel 1975), cinctus appeared typical. Although more C. fisheri; C. flavissimus spawned likewise than two fish were present, only pairs 198 PACIFIC SCIENCE, Volume 32, April 1978

3,0 .... '"I ... r ~ 2. w ~ · >- 2.0 ·. c '. ··. 0 "" 1.5 .. '"w ·.. 0.. • c 1.0 <{ ...... Z .. 0 . (l,5 ." ... '"' K >< *- )(. ~ ~ •• S )( )( )( )( ~ ~ )( x .. ,,1" JA 0.1 .'" " ~ 0 J F M A M J J A s o N o J F 1974 CENTROPYGE POTTERI 1975

FIGURE 3. Annual reproductive season. Percentage gonad weight for Centropyge pOlleri from December 1973 through February 1975, indicating a peak reproductive season beginning in December and ending in June.

spawned. When spawning, C. unimaculatus eggs. Chaetodon multicinctus and C. unimacu­ and C. fremblii occurred solely as pairs. latus rose up approximately 0.5 meter above Aggregations of spawning C. multicinctus the substrate to spawn. Chaetodon fremblii consisted four times of four individuals and rose into the water between 1 and 2 meters two times of three individuals. One group of when it spawned. four C. multicinctus apparently included at At midday during the week before the full least one female and two males. I did not moon of May 1975 at· Enewetak Atoll, spear any fish so that my actions would not Marshall Islands, a pair of Megaprotodon disturb the behavior sequence. Female trifascialis were filmed in a brief encounter chaetodontids, obviously swollen with roe, that culminated with the assumption of the led the group or pair as they swam along the spawning position, but spawning did not reef. The sex of an individual was determined occur. M egaprotodon trifascialis are solitary by observation as it spawned. Courtship territorial fish with males and females residing among chaetodontids was less elaborate on neighboring Acropora sp. corals (Reese than among Centropyge potteri. As the 1973). chaetodontids swam along the reef, the Forcipiger j1.avissimus was also sighted in female tilted her head slightly downward the chaetodontid spawning position although as she continued in front of the male. The actual spawning was not seen. The position male swam from behind and up alongside differed slightly because of the long snout. the female. As the male reached the female The male nuzzled with his forehead and kept -----=a=-=n:-::ld"p1aced-liis snounoner alxlom-en;-b-oth-his-snoutunderneath-:-rhis-single-ebservat-ien fish quivered and eggs and sperm were was made during the hour before sunset, 23 released (Figure 5). In one case, a male March 1975 (4 days before the full moon). Chaetodon multicinctus approached a female in this fashion three times before spawning. SPAWNING BEHAVIOR OF A MULLID The chaetodontid spawning posture was strikingly similar to that described for The mullid Parupeneus multifasciatus was Centropyge potteri. Again, the nuzzling by sighted spawning four times at dusk on 25 the male may signal the female to release March 1975,2 days before the full moon. Reproductive Behavior of Centropyge potteri-LoBEL 199

An aggregation of approximately ten fish 3.0 hovered about I meter above a sandy area next to a reef at 10 meters depth. The largest member, most probably the male, was a 2.5 darker color than the others and darted conspicuously around and through the aggre­ ... " gation until another fish joined along its % 2,0 ~ side. The pair ascended, side by side, to the w slY"face, where they spawned while swimming ~ forward just beneath the surface. After > c 1.5 0 spawning, they separated and returned to the III reef, whereupon I lost sight of them. This a: ...w mullid was the most difficult of all fish to 1.0 30 c 24 approach. When I came within 5 meters they C Z ceased all spawning activity. In contrast, I 0 Cl was able to get within 1 meter of spawning * 0.5 Centropyge potteri and within 2 meters of the chaetodontids. 0.1 Randall and Randall (1963) also reported upward movement leading to spawning and NR NR NR N NR NR NR NR I 2 3 4 123 4 large aggregations for the Caribbean mullid, FEMALES MA L.ES Parupeneus maculatus.

FIGURE 4. Lunar periodicity of gonad development: N indicates individuals collected during the nonrepro­ ductive season; R indicates individuals collected during SPAWNING BEHAVIOR OF ACANTHURIDS the reproductive season, December through May. Total number of fish studied was 140 females and 89 males; Three species of acanthurids spawned the number beside each symbol indicates the number in during the same time period as the previously the sample. 1 = fish collected 1-7 days after the full described fishes during March and April moon; 2 = fish collected 8-14 days after the full moon; 3 = fish collected 15-23 days after the full moon; 1975. A small aggregation of about a dozen 4 = fish collected 24 days after and up until the next individuals swam together until they sud­ full moon. denly darted upward a few meters, spawned

FIGURE 5. Chaetodon mu/ticinctus spawning. The female on the farthest right with a male behind. The sex of the third individual is not known. 200 PACIFIC SCIENCE, Volume 32, April 1978

and descended in unison. I noted several such over the same spot and courtship was directed group spawnings of Acanthurus nigrorus, toward enticing a female to a specific tall Ctenochaetus strigosus, and Zebrasoma flave­ rock/coral in the immediate territory, scens. Their reproductive behavior did not chaetodontids spawned wherever they might differ significantly from the reproductive be in a general home range without apparent behavior of acanthurids as described by orientation to specific reef structures. Randall (1961b). Spawning did, however, take place on the seaward side of the reef. Reese (1975) has described other aspects of chaetodontid behavior. The taxonomic relationship of the DISCUSSION Pomacimthidae and Chaetodontidae has The schedule of reproduction among been teviewed by Freihofer (1963) and Bur­ Hawaiian reef fishes reflects adaptation to a gesS (1974)., variety of ecological factors. Diel periodicity It is well known that chaetodontids, like appears to be influenced primarily by the many other fishes, transform into nocturnal balance between the threats ofdiurnal plank­ coiorations. Although the full significance of tivores feeding on eggs and newly hatched these nocturnal colors remains uncertain, larvae and crepuscular piscivores attacking the fact that chaetodontids wait until dUsk spawning adults. Spawning at dusk involves to spawn agrees with Hobson's (1974) con­ minimal risk to eggs and larvae, but it is the tehtion that recognition is important duhng time of peak predation upon adult fishes. both day and night. Hobson (1974) suggests: Lunar reproductive synchrony further reduces "It is logical that diurnal fishes would employ the probability of predation oil individuals viSual clues to identify one another. But the by creating a swamping effect [the selfish distinctive nocturnal colorations of many herd hypothesis, see Reaka (1976)]. The tide chaetodontids suggest that members of some is outgoing during evenings shortly before a species need to recognize each other after full moon and may aid in removal of eggs dark as well. Nocturnal colorations that and larvae from the immediate vicinity ofthe occur among chaetodontids in Kona reef where they are exposed to reef plank­ (Hawaii) tend to accentuate a contrast, thus tivores. The annual peak in reproductive ~aking them more visible at lower light activity is correlated with a shift in ocean levels. Although the nocturnal colorations of current that retains pelagic larvae around some fishes, such as those that become mot­ the islands and ensures their return to tled, make them more difficult to see in the Hawaiian reefs. These various factors exert tlark (Schroeder 1964), certain chaetodontids their influence at different times (diel, lunar, in Kona seem to be effecting a nocturnal and annual) and result in selection for display" (p. 1022). Since at least three reproductive cycles that overlap in many species spawn during dusk, these low-light­ ways. Their relative effects on timing, how­ level, color-contrasting displays may aid in ever, are probably not as distinct as the mate recognition. Probably the situation is categories presented below might imply. similar in other species that change color when spawning at low light levels. Although, Reproductive Behavior and Coloration I noted color changes in these fishes when ed-at-dusk,-Lam_noLiamiliar Pomacanthids and chaetodontids exhibited enough with their nocturnal colorations to similar reproductive behavior and a mating evaluate the similarities. position that is unlike other fishes whose behavior has been described. One difference Diel Reproductive Periodicity between chaetodontids and pomacanthids is that the chaetodontids did not restrict their Diurnal planktivores are adapted for activity to specific locations on the reef. plucking small prey from midwater, while Whereas Centropyge potteri always spawned nocturnal planktivores, such as apogonids Reproductive Behavior of Centropyge potteri-LoBEL 201

light combined with sunlight just before sunset is sufficient for fishes to recognize

TIDE PATTERNS ON FULL MOON DAYS mates, spawn, and also avoid potential pred­ JANUARY TO MAY 1974 ators, but is not enough for planktivorous fishes, requiring high visual acuity, to con­ 2 tinue foraging. ...,.: The threat from predators may partially .... explain why a prominent reef structure :I: Cl towering in the home range of Centropyge W :I: potteri is important. While spawning in

...J midwater, they were still close to a reef « 9 0 shelter to which they darted between en­ .... counters, after spawning, and when disturbed by other fishes. Similar orientation to a tall reef structure has been reported for Hypo­ 0600 I 00 1800 0000 TIME plectrus chlorurus (Serranidae) when spawn­ ing (Barlow 1975). FIGURE 6. Tide patterns during the full moon of the months January until May 1974. These patterns are The importance of such a towering coral/ representative, showing the general retreating tide in the rock is evident on patch reefs, where it may evening and a morning increasing tide. be one factor limiting the number ofspawning males. A male on a patch reef controlled a and some holocentrids, possess large mouths limited area and consequently access to and feed mainly on large plankton prey resident females, while mostly pairs occurred (Hobson 1974, Hobson and Chess 1976). on extensive reefs. Since females spawn only By dusk, most diurnal planktivores have once nightly, the males on patch reefs very descended to the reef for the night (Collette probably enjoy a greater reproductive and Talbot 1972, Domm and Domm 1973, success. This aspect of the biology of C. Hobson 1972). Spawning at dusk may reduce potteri should be further examined experi­ the probability of eggs being eaten in two mentally. ways: (1) there are few active planktivores Spawning during the daytime is known to and (2) any planktivores that are still active occur among some pomacentrids, labrids, may be quickly satiated by the simultaneous and scarids (Helfrich 1958, Meyer 1977, spawning by many fishes. In addition, there Moyer 1975, Moyer and Bell 1976, Potts was an outgoing tide during the time of 1974, Reinboth 1973, Roede 1972, Sale 1971, spawning of this study, which may aid in Youngbluth 1968). Pomacentrids protect sweeping eggs and larvae from the reef and their nests against predators, and labrids and from the grasp of planktivores that are still scarids release large numbers of eggs. Active active (Figure 6). At this time the difference predation of labrid eggs by planktivorous in the height of the tide from high to low was pomacentrids has been described by Meyer greatest, which may influence the rate of (1977). Eggs may be less likely to be eaten flow. In the mornings the tide was incoming. if they are toxic [as is known only for some The reproductive activity of broadcast- tetraodontiform fishes and a cottid, Pillsbury --spawning-species-was-not-evi-dentin-theleer--C-1957J-j-orflmrrarrhe water's surface wnere . areas where there were planktivores or other few fishes feed. The eggs of some nesting species spawning. The avoidance response pomacentrids and balistids hatch predom­ by spawning fishes to planktivores has also inantly during the dark (Allen 1972, Lobel been reported by Hobson (1965). Twilight is and Johannes 1977). The eggs of the poma- a visually difficult time for most reef fishes centrid Amphiprion clarkii hatch between and is when predation is at its peak (Hobson 34 and 70 min after sunset (Moyer and Bell 1972, 1974, Munz and McFarland 1973). It 1976). These fishes would also share the may be that the low level of reflected moon- advantages of fishes spawning at this time. 202 PACIFIC SCIENCE, Volume 32, April 1978

TABLE 4

FISHES WITH PELAGIC LARVAE SHOWN TO HAVE A PEAK SPAWNING SEASON BETWEEN DECEMBER AND JUNE IN HAWAII

FAMILY SPECIES AUTHORITY

Acanthuridae Acanthurus triostegus sandvicensis Randall 1961a Blenniidae Entromacrodus marmoratus Strasburg 1953 Istiblennius zebra Strasburg 1953 Chaetodontidae Chaetodon miliaris Ralston 1975, 1976 Engrau1idae Stolephorus purpureus Leary, Murphy, and Miller 1975 Kuhliidae Kuhlia sandvicensis Tester and Takata 1953 Labridae Labroides phthirophagus Youngb1uth 1968 Muraenidae Gymnothorax eurostus Gosline and Brock 1960 Pomacanthidae Centropyge potteri This study Pomacentridae Abudefdufabdominalis Helfrich 1958 Chromis ovalis Swerd10ff 1970 Chromis verator Swerdloff 1970 Dascyllus albisella Stevenson 1963 Eupomacentrus fasciolatus (= Pomacentrus jenkinsi) Gosline 1958

NOTE: This table lists only those species with pelagic larvae. Spawning has been said to occur throughout the year in many of these fishes; however, all have been reported with peak reproductive seasons at this time. Details will be presented elsewhere (Lobel and Reaka 1977). All species listed are endemic to Hawaii except G. eurostus and E. fasciolatus. Lunar Reproductive Periodicity with 20 of 34 of the nests hatching within I week of the full moon. Two other poma- Annual and lunar spawning seasons have centrids also have spawning peaks on about been described for many temperate zone the full moon (Moyer 1975, Moyer and Bell fishes (e.g., Schwassman 1971), but reports 1976). Johannes at Palau has determined full on the spawning periods of tropical fishes are moon spawning synchrony for the nesting scattered and few. triggerfish, Pseudobalistes flavimarginatus In the Society Islands, Ctenochaetus (Lobel and Johannes 1977) Lunar periodicity striatus and Zebrasoma scopas spawned at has also been suggested for Extremeus micro­ dusk within 5 days preceding the full moon, pus and Gnathodon speciosus (Carangidae) and Acanthurus triostegus sandvicensis also in Hawaii (Watson and Leis 1974). Kuhlia spawns on a lunar cycle (Randall 1961a, b). sandvicensis (Kuhliidae) is also suspected of Randall and Randall (1963) suggest~d that spawning near the time of full moon in spawning occurred for Scarus rupripinne Hawaii (Tester and Takata 1953). In addition, (Sacridae) during the full moon and possibly many marine are known to during the new moon in the Caribbean Sea. spawn during the full moon (Korringa 1947). Roede (1972) reported that peak reproduc- An explanation fully accounting for a peak tive activity for seven Caribbean labrids was period of spawning and hatching eggs during pronounced at the full moon. She also found dusk on evenings of the first quarter to full two other lower peaks during the lunar moon is difficult to construct, however, month, and she suggests that propagation several nonexclusive potential factors may ----iin-these-labrids-may-continue-t-hroughout-be-i-nv01vecli-:-:------­ the month but with increased activity during I. Reduced threat to eggs and larvae due the full moon period. Abudefdufabdominalis to midwater planktivores which are gener- (Pomacentridae) spawned during full and ally inactive by dusk. new moon phases in Hawaii (Helfrich 1958), 2. Eggs and larvae swept out to sea with as does Amphiprion spp. (Pomacentridae) at retreating tide. Enewetak Atoll (Allen 1972). Allen (1972) 3. Lunar periodicity may act as a cue reported 26 of 34 spawnings of Amphiprion synchronizing simultaneous reproductive spp. 6 days before or after the full moon, readiness within a species. Reproductive Behavior of Centropyge potteri-LoBEL 203 o SOUTHWEST CURRENT

rc)\

GYRALS ~RM

FIGURE 7. Generalized direction ofocean currents as interpreted from the data of Barkley, Ito, and Brown (1964). The northwest current with gyrals forming in the lee ofthe island of Hawaii occurs during the peak spawning season, December to June. The shift to the southwest current direction begins in June and lasts until December; eventually, it connects with the equatorial current (Jones 1968). 4. Lunar periodicity may serve to syn­ related with an abundance of all species' chronize spawning of several species to eggs (Watson and Leis 1974). Water temper­ create a swamping effect, quickly satiating atures were also at their lowest during the any planktivores that may still be active. reproductive peak in the Caribbean (Munro 5. Since most larvae are photopositive, the et al. 1973). Watson and Leis suggested that full moonlight may stimulate larvae to these physical changes in Hawaii reflect a swim toward the surface, thus preventing shift in ocean currents and such a shift may them from settling back to the reef where increase the retention of pelagic eggs and they may be trapped and eaten (Allen larvae near the Hawaiian Islands (see also 1972). Jones 1968, Sale 1970). This is being further examined by Lobel and Reaka (1977) using Annual Reproductive Periodicity the results of drift-bottle experiments by Barkley, Ito, and Brown (1964). Full moon While tropical fishes are generally believed phases during this season were associated --to-spawn-throughout-the-year;-a-sprin-g-with-p-ea-Ic-tidaI-crran-ge-s--and-during thIs study ·­ spawning peak during February through spawning occurred at dusk, which coincided April is evident among Caribbean reef fishes with an outgoing tide. (Munro et al. 1973). My observations suggest The seasonal change of ocean current that reproductive activity in several Hawaiian direction has been assessed by the recovery reef fishes also peaks in the spring from of drift bottles released in the vicinity of the December until June (Table 4). During this island of Hawaii (Barkley, Ito, and Brown period in Hawaii there were generally lower 1964) (Figure 7). The current drift is roughly surface temperatures and salinities that cor- parallel to the Hawaiian Islands from January 204 PACIFIC SCIENCE, Volume 32, April 1978

until June. The direction begins to shift after The populations ofreefs which are adapted June from the predominantly northwest to unique situations are confronted with parallel direction to a drift primarily to the the problem of conserving their pelagic southwest. This southwesterly current even­ stages contrary to dispersing larvae into the tually becomes part of the north equatorial major ocean current systems. Since many current (Jones 1968). The northwesterly reef possess a pelagic stage in their current direction and effects of tidal changes life history, this selection pressure may be that run parallel to the shore create pockets widespread where we find organisms (1) of eddies between the islands where larvae restricted to specific environmental circum­ may accumulate. Additionally, surface cur­ stance, (2) in specific and very isolated places rent gyrals form in the lee of the island such as Hawaii, and/or (3) in a situation of Hawaii, the southernmost island in the where the results of competitive interactions Hawaiian Archipelago. These gyrals move depend upon a large number of recruits along with the northwest current, and (e.g., Sale 1974, 1977). Synchronization of organisms trapped within may be easily reproduction with ocean currents favoring transported along the island chain (J ones return of larvae to home reefs may be one 1968). The effectiveness of surface current mechanism by which reduced dispersal is gyrals in trapping pelagic larvae has been accomplished. If the different ecological set­ suggested by the distribution of acanthurid ting in Hawaii favors natural selection of larvae; Sale (1970) found larval acanthurids those taxa with a mechanism assuring return that were swept past an island every 5 to 6 of larvae to suitable reefs, we may expect a days as a gyral rotated. Species with pelagic peak reproductive season between December offspring dispersed into the ocean during and June to be evident among those species the period June until December may have especially suited to Hawaiian habitats. If this their progeny dispersed to the north equato­ proves true, we may predict such seasonality rial current. Thus, they may not contribute at least among the recognized endemic significantly at that time to the repopulation species [29 percent of the fishes (Randall of the Hawaiian fauna. 1976; see also Gosline 1968)], which are The changing seasonal current pattern among the most numerous on Hawaiian reefs. may reflect the possibility for flow to be stronger and more westerly in July to ACKNOWLEDGMENTS December; however, a random component of flow may be predominant at any time Many people generously aided me during (anonymous reviewer, personal communica- my study while I was an undergraduate at the tion). The variability in the seasonality of University of Hawaii. I am most grateful to these patterns is not yet known. Even so, George S. Losey and Leighton R. Taylor, Lobel and Reaka (1977) show that the num- who guided my research and study. My ber ofdrifting objects lost from or retained in consistent diving companions helped not Hawaiian waters during the two seasons are only in the field, but also in the interpretation statistically significantly different. Marjorie of what we saw: Paul Allen, Paul Atkins, Reaka and I are presently evaluating the Joe Bauer, Sally Bauer, Ed Baughman, general applicability of the hypothesis for Deetsie Chave, John Earle, Denny Gorlick, ---~tfie fauna in HawaIi anaeJ.sewnere. rue-face-Dan 1ohnsnII-,-Steve-RaIston-;-and-most­ that 12 of the 14 species so far reported especially Janie Culp. Ed Baughman and (Table 4) are taxonomically recognized Ha- John Earle were also generous with the use waiian endemics emphasizes the limited of their boats. Research at Enewetak Atoll, distribution of these fishes. Knowledge of Marshall Islands, was supported by the Mid­ how widespread this phenomenon is among Pacific Marine Laboratory (S. V. Smith, Hawaiian aquatic animals requires con- Director). Equipment and laboratory space siderably more data on the reproductive was provided freely by the Department of seasonality of both endemics and more Zoology, the Hawaii Cooperative Fishery widely ranging species. Unit, and the Waikiki Aquarium, University Reproductive Behavior of Centropyge potteri-LoBEL 205

of Hawaii. Interisland travel was made DAVIS, W. P., and R. S. BIRDSONG. 1973. possible by Doug Pendleton, Marine Pro­ Coral reef fishes which forage in the water grams, University of Hawaii. I would also column. Helgolander wiss. Meersunters. like to thank Edmund Hobson, John Ran­ 24: 292-306. dall, Marjorie Reaka, Ross Robertson, Peter DOMM, S. B., and A. J. DOMM. 1973. The Sale, and John Stimson for their aid and sequence of apearance at dawn and dis­ comments. Karen Cheng, Kathie Cunning­ appearance at dusk of some coral reef ham, and Arila Kourany kindly typed vari­ fishes. Pac. Sci. 27: 128-135. ous versions of the manuscript. To all, my FREIHOFER, W. C. 1963. Patterns ofthe ramus sincere Aloha. This project was prepared in lateralis accessorius and their systematic partial satisfaction of requirements for the significance in teleostean fishes. Stanford Honors Program, University of Hawaii, Ichthyol. Bull. 8:81-189. 1975. A portion of this study was presented GOSLINE, W. A. 1958. The nature and evolu­ at the Cornell University Mini-Symposium tion of the Hawaiian inshore fish fauna. on coral reef fishes, 1976. Proc. Eighth Pac. Sci. Congr. 3: 347-357. ---. 1968. Considerations regarding the evolution of Hawaiian animals. Pac. Sci. 22:267-273. LITERATURE CITED GOSLINE, W. A., and V. E. BROCK. 1960. ALLEN, G. R. 1972. Anemonefishes, T.F.H. Handbook of Hawaiian fishes. University Publications, Neptune, N. J. 288 pp. of Hawaii Press, Honolulu. 378 pp. BARKLEY, R. A., B. M. ITO, and R. P. BROWN. HELFRICH, P. 1958. The early life history and 1964. Releases and recoveries of drift reproductive behavior of the Maomao, bottles and cards in the central Pacific. U.S. Abudefduf abdominalis (Quoy and Gai­ Fish Wildl. Servo Spec. Sci. Rep. 492. mard). Ph.D. Thesis. University ofHawaii, BARLOW, G. W. 1975. On the sociobiology Honolulu. ofsome hermaphroditic serranid fishes, the HOBSON, E. S. 1965. Diurnal-nocturnal Hamlets, in Puerto Rico. Mar. BioI. activity of some inshore fishes in the Gulf 33: 295-300. of California. Copeia 1965: 291-302. BAUER, J. A., and G. KLAY. 1974. Pygmy ---. 1968. Predatory behavior of some angels spawn. Octupus 1: 5. shore fishes in the Gulf of California. U.S. BREDER, C. M., and D. E. ROSEN. 1966. Fish Wildl. Serv., Res. Rep. 73. 92 pp. Modes of reproduction in fishes. Natural ---.1972. Activity ofHawaiian reeffishes History Press, New York. 941 pp. during the evening and morning transitions BURGESS, W. E. 1974. Evidence for the eleva­ between daylight and darkness. Fish. Bull. tion to family status of the angelfishes U.S. 70:715-740. (Pomacanthidae), previously considered to ---. 1974. Feeding relationships ofteleos­ be a subfamily of the butterflyfish family, tean fishes on coral reefs in Kona, Hawaii. Chaetodontidae. Pac. Sci. 28: 57-71. Fish. Bull. U.S. 72:915-1031. CHAVE, E. H., and D. B. ECKERT. 1974. HOBSON, E. S., and J. R. CHEss. 1976. Trophic Ecological aspects of the distribution of interactions among fishes and zooplankters fishes at Fanning Island. Pac. Sci. 28: 297­ near shore at Santa Catalina Island, Cali­ -11. f()rnia-:-F-ish-:-BuH-:-B-:-S-:-7H69-598c:-.-- CLARKE, T. A. 1970. Territorial behavior and JONES, R. S. 1968. Ecological relationships population dynamics of a pomaceateid in Hawaiian and Johnston Island Acan­ fish, the Garibaldi, Hypsypops rubicuada. thuridae (surgeonfishes). Micronesica 4: Ecol. Mongr. 40: 189-212. 309-361. COLLETTE, B. B., and F. H. TALBOT. 1972. KORRINGA, P. 1947. The moon and periodi­ Activity patterns of coral reef fishes with city in breeding marine animals. Ecol. emphasis on nocturnal-diurnal change­ Monogr. 17:349-381. over. Nat. Hist. Mus. Los Ang. City Sci. LEARY, D. F., G. 1. MURRHY, and M. MILLER. Bull. 14:98-124. 1975. Fecundity and length at first spawn- 206 PACIFIC SCIENCE, Volume 32, April 1978

ing of the Hawaiian anchovy, or Nehu demic. M.S. Thesis. University of Hawaii, (Stolephorus purpureus Fowler) in Honolulu. 102 pp. Kaneohe Bay, Oahu. Pac. Sci. 29: 171-180. ---.1976. Age determination ofa tropical LOBEL, P. S. 1975. Hawaiian angelfishes. reef butterflyfish utilizing daily growth Marine Aquarist 4: 30-41. rings of otoliths. Fish. Bull. U.S. 74: 990- LOBEL, P. S., and R. E. JOHANNES. 1977. 994. Nesting behavior and larvae of triggerfish RANDALL, J. E. 1961a. A contribution to the (Balistidae). Manuscript. biology of the convict surgeonfish of the LOBEL, P. S., and M. L. REAKA. 1977. Syn- Hawaiian Island, Acanthurus triostegus chronization ofreproduction with seasonal sandvicensis. Pac. Sci. 15: 215-271. currents as a mechanism for endemism in ---. 1961b. Observations on the spawning Hawaiian marine fauna. Manuscript. of surgeonfishes (Acanthuridae) in the MEYER, K. A. 1977. Reproductive behavior Society Islands. Copeia 1961 :237-238. and patterns of sexuality in the Japanese ---. 1976. The endemic shore fishes ofthe labrid fish Thalassoma cupido. Jap. J. Hawaiian Islands, Lord Howe Island and Ichthy. 24: 101-112. Easter Island. Colloque Commerson 1973, MOYER, J. T. 1975. Reproductive behavior O.R.S.T.O.M. Travaux et Documents of the damselfish Pomacentrus nagasa- 47: 49-73. kiensis at Miyake-jima, Japan. Jap. J. RANDALL, J. E., and H. RANDALL. 1963. The Ichthy. 22: 151-163. spawning and early development of the MOYER, J. T., and L. J. BELL. 1976. Repro- Atlantic parrotfish, Sparisoma rubripinne, ductive behavior of the anemonefish Am- with notes on other scarid and labrid phiprion clarkii at Miyake-jima, Japan. fishes. Zoologica 48 :49-61. Jap. J. Ichthy. 23: 23-32. REAKA, M. L. 1976. Lunar and tidal periodi- MUNRO, J. L., V. C. GAUT, R. THOMPSON, city ofmolting and reproduction in stoma- and P. H. REESON. 1973. The spawning topod crustacea: a selfish herd hypothesis. seasons of Caribbean reef fishes. J. Fish. BioI. Bull. 150:468-490. BioI. 5: 69-84. REESE, E. S. 1973. Duration of residence by MUNZ, F. W., and W. N. McFARLAND. 1973. coral reef fishes on "home" reefs. Copeia The significance of spectral position in the 1973: 145-149. rhodopsins oftropical marine fishes. Vision ---. 1975. A comparative field study ofthe Res. 13: 1829-1874. social behavior and related ecology of reef MYRBERG, A. A., JR., B. D. BRAHY, and A. R. fishes of the family Chaetodontidae. Z. EMERY. 1967. Field observations on repro- tierpsychol. 37: 37-61. duction of the damse1fish, Chromis multi- REINBOTH, R. 1973. Dualistic reproductive lineata (Pomacentridae), with additional behavior in the protogynous Tha- notes on general behavior. Copeia 1967: lassoma bifasciatum and some observations 819-827. on its day-night changeover. HelgoHinder PILLSBURY, R. W. 1957. Avoidance ofpoison- wiss. Meersunters 24: 174-191. ous eggs ofthe marine fish, Scorpaenichthys ROEDE, M. J. 1972. Color as related to size, marmoratus, by predators. Copeia 1957: sex, and behavior in seven Caribbean 251-252. labrid fish species. Studies Fauna Curacao --~.P0-Ffs,&-W-;-1-9+4~'Fhe-e0l0r-ati0n-ana-its--41-7-1-264.,--.------­ behavioral significance' in the corkwing SALE, P. F. 1970. Distribution oflarval Acan- wrasse, Crenilabrus melops. J. Mar. BioI. thuridae off Hawaii. Copeia 1970: 765- Assoc. 54: 925-938. 766. RALSTON, S. V. D. 1975. Aspects of the age ---. 1971. The reproductive behavior of and growth, reproduction and diet of the the pomacentrid fish, Chromis caeruleus. millet-seed butterflyfish Chaetodon miliaris Z. tierpsychol. 29: 156-164. (Pisces: Chaetodontidae), a Hawaiian en- ---. 1974. Mechanisms of co-existence in Reproductive Behavior of Centropyge potteri-LOBEL 207

a guild of territorial fishes at Heron SWERDLOFF, S. N. 1970. The comparative Island. Proc. Second Internat. Coral Reef biology of two Hawaiian species of the Symp. 1: 193-206. damselfish Chromis (Pomacentri­ ---. 1977. Maintenance of high diversity dae). Ph.D. Thesis. University of Hawaii, in communities. Am. Nat. Honolulu. 111: 337-359. TESTER, A. L., and M. TAKATA. 1953. Con­ SCHROEDER, R. E. 1964. Photographing the tribution to the biology of the aholehole, night creatures of Alligator Reef. National a potential baitfish. Industrial Research Geographic Magazine 125: 128-154. Advisory Council Grant, Final Rep. 29. SCHWASSMAN, H. O. 1971. Biological 54 pp. rhythms. Pages 371-416 in W. S. Hoar and WALTERS, C. K. 1967. Nest guarding be­ D,-J. Randall, eds. Fish physiology. Vol. havior of the male Maomao, Abudefduf 6::'Academic Press, New York. abdominalis. M.S. Thesis. University of STEVENSON, R. A. 1963. Life history and Hawaii, Honolulu. behavior of Dascyl/us a/bisel/a, a poma­ WATSON, W., and J. M. LEIS. 1974. Ichthyo­ centrid fish. Ph.D. Thesis. University of plankton of Kaneohe Bay, Hawaii. Hawaii, Honolulu. UNIHI-Seagrant Rep. 75-01. STRASBURG, D. W. 1953. The comparative YOUNGBLUTH, M. J. 1968. Aspects of the ecology of two salarine blennies. Ph.D. ecology and ethology of the cleaning fish, Thesis. University of Hawaii, Honolulu. Labroides phthiaophagus Randall. Z. tier­ psychol. 25 :915-932.