Phylogenetic and Habitat Influences on Mating System Structure in the Humbug Damselfishes (Dascyllus, Pomacentridae)

BULLETIN OF MARINE SCIENCE. 57(3): 637~52. 1995

PHYLOGENETIC AND HABITAT INFLUENCES ON MATING SYSTEM STRUCTURE IN THE HUMBUG DAMSELFISHES (DASCYLLUS, POMACENTRIDAE)

John Godwin

ABSTRACT The darnselfish genus Dascyllus contains nine species and exhibits protogynous sex change and/or functional gonochorism with variation both interspecifically and possibly intraspecifically between habitats. The genus can be divided into three species complexes and along lines of both descent and body size: 1) five species in two species complexes (complexes I and 2) are relatively small-bodied, closely associate with branching coral throughout life, and commonly exhibit resource defense polygyny and associated protogynous sex change, 2) three species in a third species complex (complex 3) reach larger body size, closely associate with branching coral only as juveniles, and do not exhibit resource defense polygyny, and 3) D. ftavicaudus, a large-bodied member of the otherwise small-bodied species complex 2. Das- cyllus ftavicaudus and D. albisella (complex 3) are both large bodied, but differ in their responses to habitat type. Dascyllus flavicaudus shows differences in sex ratio, space use and mating system between a discontinuous coral cover habitat (female-biased sex ratio, resource defense polygyny) and continuous coral cover habitat (non-biased sex ratio, no resource defense polygyny) while D. albisella does not (non-biased sex ratio, no apparent resource defense polygyny in either habitat type), suggesting that both ecological factors and phylogenetic history influence these characters.

Emlen and Oring (1977) proposed that the dispersion of resources critical to the limiting sex, usually females, is a major determinant of mating system structure. Males monopolizing critical resources may also gain exclusive mating access to females (resource-defense polygyny), giving such males high reproductive success. However, phylogenetic history can be very important in shaping and con- straining adaptation. It has become increasingly apparent that modern character states such as mating system responses to ecological factors can be profitably considered in a phylogenetic context (Brooks and McLennan, 1991). This paper concerns variation in mating system structure in a genus of Indo- Pacific damselfishes, the Dascyllus. The Dascyllus consists of nine species distributed across the tropical Indo-Pacific from the Red Sea to Hawaii (Fig. la-c; Randall and Allen, 1977). These small planktivores all exhibit a strong association with live branching coral during at least the juvenile stage of their life history. The eggs are demersal and parental care is provided solely by males. This is one of the better studied genera of coral reef fishes and has been the subject of approximately 40 papers including many related to reproductive and feeding ecology, mating and social behavior, and protogynous sex change (in addition to papers cited below: see: Holzberg, 1973; Jones, 1988; Sale, 1971a, 1971b, 1972a, 1972b, 1976; Shpigel and Fishelson, 1983; Sweatman, 1983, 1985, 1988). The genus can be divided into three species complexes on the basis of morphology, biogeography, and striking coloration differences (affinities and character similarities described in Randall and Allen, 1977). I will refer to these as the aruanus, reticulatus, and trimaculatus complexes respectively (groups 1-3 from abstract) for the most geographically widespread member species of each (Fig. 1, aruanus complex: D. aruanus, D. melanurus; reticulatus complex: D. reticulatus, D. cameus, D. marginatus, D. fiavicaudus; trimaculatus complex: D. trimaculatus, D. albisella, D. strasburgi; Fig. 2).

637 638 BULLETIN OF MARINE SCIENCE, VOL. 57, NO, 3, 1995

aruanus complex '::, ··:9::::::::::::::::::::::::::-:·:····

reticulatus complex

.-:.. .-:0-:·:-:-:-:-:·:-:-:-:-:-:·:-:-:-'·'. .. - .

trimaculatus complex

" > D. strasburgi

Figure 1. Distributional maps for species complexes within the genus Dascyllus.

The reticulatus and aruanus complexes are both small-bodied, reaching maximum sizes of approximately 65-70 mm SL. The exception is D. flavicaudus, a member of the reticulatus complex which reaches at least 90 mm SL. The three species of the trimaculatus complex reach greater maximum body sizes (100-110 GODWIN: MATING SYSTEMS IN DASCYLLUS DAMSELFISHES 639

species body size sex change

Figure 2. Hypothesized relationships between Dascyllus species complexes. Body size: "I.:'-large bodied, "s"-small bodied; Sex change: "y"-species exhibits sex change, "n"-species has been studied but functional sex change has not been described, ?-species has not been studied. (*Diagnosis of sex change in D. flavicaudus is from this paper). mm SL). This length difference represents an approximate four to fivefold difference in body mass. Both protogynous hermaphroditism and apparent functional gonochorism are exhibited in the Dascyllus. Protogynous sex change was first documented for the genus in D. aruanus (Fricke and Holzberg, 1974; Coates, 1982) and subsequently in two members of the reticulatus complex, D. reticulatus (Schwarz, 1980; Schwarz and Smith, 1990) and D. marginatus (Shpigel and Fishelson, 1986). Functional protogynous sex change has not been described in the trimaculatus complex despite some study of social systems and ecology in D. trimaculatus and D. albisella (Stevenson, 1963; Barash, 1980; Godwin, this paper). No published information is available for D. carneus, D. strasburgi, or D. melanurus, although in Madang, Papua New Guinea D. melanurus appears to have a similar social organization to D. aruanus and thus probably exhibits sex change (pers. obs.). Functional protogynous sex change in Dascyllus species appears to be associated exclusively with a haremic polygynous mating system in which males defend coral heads on which females are resident (Fricke and Holzberg, 1974; Coates, 1982; Schwarz and Smith, 1990; Shpigel and Fishelson, 1986). For purposes of this paper, sex change is considered primarily as a consequence of this type of mating system. Elsewhere (Godwin, in prep.), I describe an unusual form of sex change (intermediate between pre- and post-maturational) in D. albisella and more directly address the evolution of sexual patterns in the genus. Based on findings to date, the distribution of resource defense polygyny and sex change in the Dascyllus fall along lines of both body size and descent (Fig. 2). Relationships among the three species complexes are not known. The relationships among species complexes depicted in Figure 2 are based on the interpretation of meristic character data which follows (data from Randall and Allen, 1977). These data suggest two alternate topologies depending on the characters used. Similarities in modal numbers of pectoral rays and especially soft dorsal rays suggest a closer relationship between the reticulatus and trimaculatus complexes, while modal gill raker counts on the first arch suggest a closer relationship between the aruanus and trimaculatus complexes. However, comparisons of gill raker counts between species are confounded by an influence of body size. In 640 BULLETIN OF MARINE SCIENCE, VOL. 57, NO.3, 1995 examining correlations between meristic characters within individuals (raw data provided by H. Randall and G. Allen), I found significant positive relationships between standard length and gill raker counts within several Dascyllus species: D. aruanus (upper limb gill rakers: r = 0.252, P < 0.001; lower limb gill rakers: r = 0.175, P = 0.007, N = 241), D. reticulatus (upper limb gill rakers: r = 0.020, P = 0.833, lower limb gill rakers: r = 0.362, P < 0.001, N = 112), D. trimaculatus (upper limb gill rakers: r = 0.532, P = 0.012, lower limb gill rakers: r = 0.624, P = 0.002). Gill raker counts therefore do not appear to be useful indicators of phylogenetic relationships in Dascyllus. No significant correlations were found between standard length and either soft dorsal or pectoral ray counts for any Dascyllus. These data therefore tentatively support an initial separation between the aruanus complex and the lineage leading to the rcticulatus and trimaculatus complexes, followed by a later separation of the reticulatus and trimaculatus lineages (Fig. 2). While more data are clearly necessary to firmly re- solve the subgeneric relationships here, the important point for purposes of this study is the relationship that is not supported: a closer affinity between the aruanus and reticulatus complexes than between either complex and the trimaculatus complex. Taken together, these data suggest that the ancestral Dascyllus was small- bodied and sex changing. This would require one transition to produce the large- bodied trimaculatus complex rather than two transitions from a large-bodied an- cestor to produce the predominantly small-bodied aruanus and reticulatus complexes. I propose two alternative hypotheses here to account for the observed patterns of body size and sex change in Dascyllus. These hypotheses were proposed a posteriori for most of the genus as information was available for D. aruanus, D. reticulatus, D. marginatus, D. trimaculatus, and D. albisella. Information was not available for D. flavicaudus and predictions were therefore a priori with respect to this critical test species. Individuals of small Dascyllus species are typically restricted to coral heads where these heads are spatially separated. This restricted mobility has been as- cribed to predation pressure limiting movement between corals (Fricke, 1980; Shpigel and Fishelson, 1986), although such movement does occur (Coates, 1982). A coral head represents a discrete, defensible resource for males (Fricke, 1980). A male monopolizing a coral head and excluding other males also monopolizes mating access to resident females and realizes high reproductive success (Fricke and Holzberg, 1974). Fricke (1980) considered this mating system a resource defense polygyny in which males defend a discrete resource to which females are attracted. Neither i) the relative influences of coral characteristics versus resident male characteristics on choice of a coral by individual females, or ii) the degree to which female movement may be constrained by males have been addressed. These issues are beyond the scope of this paper. Polygynous mating on male-monopolized coral heads should create a large variance in male reproductive success with large male~ having high reproductive success and small males having little or none. The expected reproductive success for an individual should therefore be greater in female function at small size and male function at large size. The size advantage hypothesis (Ghiselin, 1969; War- ner, 1975) predicts that this situation will select for protogynous sex change as is observed in D. aruanus, D. marginatus, and D. reticulatus. This "monopolization" hypothesis is essentially the hypothesis tested for intraspecific mating system variation in D. marginatus by Fricke (1980) restated to also address interspecific variation in the genus and the occurrence of functional sex change. The hypothesis makes two predictions. The first is that with an increase in the size of GODWIN: MATING SYSTEMS IN DASCYILUS DAMSELFlSHES 641 the coral resource beyond that which is effectively defensible by a single male, a mating system shift from resource defense polygyny to a more polygynandrous or promiscuous system should be observed (and is: Fricke, 1980; Shpigel and Fishelson, 1986). The second prediction is that with an evolutionary increase in body size, female mobility will also increase. Consequently, female monopoliz- ability will decrease and the same mating system shift observed intraspecifically with an increase in coral size will be observed interspecifically with an increase in body size. An alternate non-adaptive hypothesis postulates that space use and sexual pattern are unrelated to body size, being instead more related to phylogenetic affinities. This "phylogenetic inertia" hypothesis predicts that space use and sexual pattern will be conserved within species complexes in this genus. Both hypotheses are supported by the published data. The Dascyllus known to exhibit resource defense polygyny and functional sex change are small-bodied, but are also related by descent within their respective species complexes (Fig. 2). Species in the trimaculatus complex are both large and related by descent. The influences of body size and phylogeny are thus completely confounded. In order to separate the influences of body size and phylogeny, it was necessary to study D. fiavicaudus. This species reaches a large body size (90 mm SL), but definitely appears to be most closely related to the small-bodied species of the reticulatus complex (Randall and Allen, 1977). The monopolization hypothesis predicts that D. fiavicaudus will not show resource defense polygyny or undergo sex change because with large body size females will gain higher mobility and move over areas too large to be monopolized by individual males. This is predicted to elim- inate conditions which select for sex change. In contrast, the phylogenetic inertia hypothesis predicts that D. fiavicaudus will exhibit the same space use patterns as closely related species in the reticulatus complex and commonly undergo sex change.

MA TERlALS AND METHODS

Study Locations.-I made behavioral observations and collections of D. albisella at four locations in Kaneohe Bay and at Manana Is. on Oahu between August 1987 and May 1992. Kaneohe Bay is a large embayment enclosed by a shallow barrier reef. The sample locations were patch reefs within the bay which rise to within 1 m of the surface. They consist of dead coral rubble tops and steeply sloping sides with a mixture of coral rubble and dense coral cover (primarily Porites compressa and Montipora verrucosa) to a depth of 8-10 m, where they give way to muddy bottom. The Sampan reef is a small patch reef in a channel through the barrier reef. Water depth here is 2-3 m and the reef consists of a 8 X 10 m patch of P. compressa and scattered heads of the coral Pocillopora eydou.xi immediately adjacent on sandy bottom. The total area of this reef is approximately 250 m2• I also made observations and collections of D. albisella at Manana Island off the east coast of Oahu in an area of 5-9 m depth characterized by a hard, reef rock substratum, isolated heads of mainly P. eydou.xi, some Porites lobata, and little or no other cover. I found Dascyllus albisella only around the larger Pocillopora and Porites heads in this area. I observed and collected Dascyllus flavicaudus at several sites on the north shore of Moorea in August 1990. These included two continuous cover sites on inshore fringing reefs and several discontinuous cover sites in grooves of the reef slope spur and groove zone outside the reef crest. The continuous cover sites (Pihaena Pt. and Maharepa, 17°29'S, 149°50'W) were characterized by broken to continuous cover of the coral Montipora verrucosa in 2-12 m depth. These two sites differed in population density. Pihaena Pt. had a large colony of approximately 160 individuals resident in an approximately 16 by 20 m area centered around a large Montipora head. I mapped the areas used by five males and five females during single 15-min observation periods at this site. Maharepa had approximately 20-25 resident fish in a mapped area on the reef slope extending 30 m along the shore and from the edge of the reef flat down the reef slope 10 m. The discontinuous cover sites were characterized by relatively little cover except widely scattered large heads of P. eydou.xi. It was from these heads that I sampled the D. fiavicaudus groups in this study. I did not observe spawnings during 642 BULLETIN OF MARINE SCIENCE, VOL. 57, NO.3, 1995

this period, but females had large vitellogenic eggs and visited nests which males had prepared and over which they exhibited the courtship and territorial signal jump behavior (Reese, 1964; Sale, I972a). I collected Dascyllus aruanus in the Marianas Islands (Guam) in April 1988, the Society Islands (Moorea) in August 1990, and the Marshall Islands (Majuro) in September 1992. The Guam collections were at Ypao beach, Thmon Bay (l3"23'N, 144°45'E). This site was characterized by extensive and continuous thickets of staghorn Acropora coral in 1-2 m depth. The Moorea collections were on an inshore fringing reef at Pihaena Pt. in 1m depth (described above). The Marshall Islands collections were on a lagoonal patch reef at 5-10 m depth in the southern end of the Majuro lagoon (7°9'N, 171°12'E). This reef was characterized by essentially continuous cover of Porites finger coral. I collected Dascyllus trirrwculatus from the continuous cover habitat site at Pihaena Pt., Moorea described above in August, 1990 and made casual observations of this species in both continuous and discontinuous cover sites on Moorea, as well as in Guam, Majuro, and Madang, Papua New Guinea. Collection and Sex Determination Methods.-I collected fish for determinations of population sex and size distributions in two different ways. I collected D. aruanus, D. albisella, D. jlavicaudus, and D. trirrwculatus at night either snorkeling or using SCUBA and handnets. I attempted to avoid collection bias by locating individual fish with the flashlight beam and ignoring any other individuals encountered until the focal fish was either captured or lost. I collected D. albisella at Manana Is., Oahu and D. jlavicaudus in the outside barrier reef habitat in Moorea during daylight hours by driving them into the coral heads they resided around, covering the corals with a net, and anesthetizing the fish with 2- methyl quinoline (quinaldine). I made sexual identifications by examining the sexually dimorphic genital papilla (Thresher, 1984) and gametes (extruded with gentle pressure on the abdomen: Fricke, 1980). Marking and Observations.-I marked individual fish by clipping varying combinations of dorsal, pelvic, and/or anal fins with a standard single-hole paper punch. This did not appear to affect their swimming, feeding, or general activity. I followed individuals at approximately 4-5 m distance for varying time budget periods over mapped areas using snorkel or SCUBA. I determined space use patterns of male and female D. albisella with IS-min focal-individual-observations of marked and unmarked fish on the Sampan channel reef in Kaneohe Bay. I mapped the areas used by three males and five female D. jlavicaudus at Maharepa, Moorea during three IS-min focal-individual-observation periods per fish and the areas used by five males and five females at Pihaena Pt., Moorea during one IS-min focal-individual-observation period per fish. These observations began 1-3 days after capture, marking and release and extended over 3-7 days. Histology.-I fixed gonads in either 10% buffered formalin or Bouin's solution, dehydrated in either a graded ethanol or ethanol/butanol series, and infiltrated and embedded with paraffin. I sectioned gonads transversely at 8-10 !Lmand stained with hematoxylin and eosin. Statistical Analysis.-I performed statistical analyses by hand according to Zar (1984) or using Systat 5.1 for the Macintosh personal computer. I used Pearson product moment correlation coefficients to assess associations between variables and two sample t-tests to test for size differences between males and females. I assessed the power of the Chi-square tests used to detect significant deviations from I: I sex ratios with power analyses as described by Cohen (1969).

RESULTS AND DISCUSSION

This section reviews published information and presents new data on sex ratio and space use patterns of Dascyllus species in both continuous and discontinuous coral cover habitats. The emphasis is on comparing patterns in D. flavicaudus, the large-bodied member of the otherwise small-bodied reticulatus complex, and the large-bodied D. albisella (large-bodied trimaculatus complex). This emphasis is intended to contrast the patterns shown by these species in the context of the monopolization and phylogenetic inertia hypotheses presented above. Both sex ratio and space use are taken as indicators of mating system structure and are therefore covered together for each species. Summary mating system and sex ratio information in different habitat types from both this study and previously-published studies is presented in Table 1. Detailed sex ratio and body size data for various Dascyllus species from this study are presented in Table 2. Dascyllus flavicaudus and D. albisella show similar sex ratio and space use patterns in continuous cover habitats, but differ in discontinuous cover habitats. I therefore GODWIN: MATING SYSTEMS IN DASCYUUS DAMSELASHES 643

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Figure 3. Size distributions by sex for Dascyllus arnanus, D. ftavicaudus, and D. trimaculatus at Pihaena Pt., Moorea. Females shown in clear bars, males in filled bars. describe sex ratio and space use in continuous cover habitats first to underscore the species differences in discontinuous cover habitats. Sex Ratio and Space Use Patterns in Continuous Coral Cover Habitats.-DAs- CYLLUSFI.AVICAUDUS.The sex ratios for D. flavicaudus in the two continuous cover sites examined were not significantly female-biased: 1.21 (number of females per male) at Pihaena Pt. and 1:1 at Maharepa. Male body sizes were significantly greater than females at Pihaena Pt., but with a large overlap (Fig. 3). Patterns of space use by males and females were apparently similar at the two sites despite a difference in total number of resident animals (~160 at Pihaena and 20-25 at Maharepa based on marklresightings). Males aggressively defended small nest site areas and made feeding excursions into the water column. Females ranged 646 BULLETIN OF MARINE SCIENCE. VOL. 57. NO.3. 1995

Q 0 I----l 2m

Figure 4. Reef areas used by individual male and female Dascyllusjiavicaudus at Maharepa. Moorea. Male areas shown by solid lines. female areas shown by dashed lines.

freely over the reef, swimming 2-4 m above the coral in a loose feeding school. This space use difference was more pronounced at Pihaena Pt. than Maharepa, where males made longer duration feeding excursions. Figure 4 illustrates the composite areas used by three males and five females at the Maharepa site. I did not encounter or capture approximately half the resident individuals in repeated night collecting trips, so the figure does not represent the areas used by all D. flavicaudus at the Maharepa site. The areas used by different males overlap and the areas used by females could overlap the areas used by more than one male. Two of the five marked females were approached aggressively during observation periods by the marked 85 mm male whose area of activity is depicted on the center left of Figure 4, but all five were courted at least once by a different resident male. This courting occurred within the area used by the marked 85 rom male. The D. flavicaudus observations from continuous cover sites indicate that in this habitat type: i) females did not significantly outnumber males, ii) males and females had broadly overlapping home ranges, and iii) females did not restrict and/or were not restricted in their movements to areas defended by individual males. DASCYLLUS ALB/SELlA. Collections of this species in the continuous cover habitat of Kaneohe Bay, Oahu produced sex ratios ranging from 0.73 to 1.17 (females/ male), but none showed a significant female bias (Table 2, X2 test, P > 0.05). This is also the case if the Kaneohe Bay collections are lumped (147 males, 158 females, X2 test, P > 0.05). This result differs from that of Stevenson (1963) who found significantly female-biased sex ratios in D. albisella (Waikiki, Oahu: 202 males, 254 females [1:1.26, X2 = 5.930, P < 0.05]; Kaneohe, Oahu: 90 males, 177 females [1:1.97, X2 = 28.34, P < 0.001]). This difference is difficult to account for, but may be due to differing collection methods (poisoning, spearing, trapping in Stevenson's study) introducing either a male bias in this study or female bias in Stevenson's study. The difference could also result from Steven- son's inclusion of small individuals in the Kaneohe collection (starting at 50-55 mm SL) while I counted only individuals of a size from which gametes could be expressed. Individuals less than approximately 65 mm do not appear to spawn, suggesting that they should not be considered in the operational sex ratio. Figure 5 shows the sex by size distribution for D. albisella on the Sampan channel reef, which was representative. Males were significantly larger than fe- GODWIN: MATING SYSTEMS IN DASCYUUS DAMSELFISHES 647

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Figure 5. Size disttibution by sex for Dascyllus albisella at Sampan Channel site, Kaneohe Bay, Oahu. Females shown in clear bars, males in filled bars. males (Table 2), but with a broad size overlap. This was also observed in two other Kaneohe Bay collections and suggested in a third (Barrier Reef site, t-test, P == 0.069). Barash (1980) observed space use by male and female D. albisella at Maui, Hawaii. He found that females moved in groups over areas of reef which encom- passed the nest sites and territories of many males. I observed the same patterns of space use in continuous cover habitats generally and in particular with marked individuals on the Sampan reef in Kaneohe Bay, Oahu. Female D. albisella spent virtually all of their time well off the bottom (1-3 m) and moved freely over the reef as part of a loose feeding school. In habitats where water depth was greater (10-30 m), I observed feeding schools as much as 8-10 m above the bottom. The location of feeding schools appears to be determined by current direction and schools are typically upcurrent with respect to the area used by colonies in D. albisella. As with D. flavicaudus, the important point regarding space use by female D. albisella in continuous cover habitats is that individual females did not restrict and/or were not restricted in their movements to areas defended by individual males. Supporting this interpretation was the frequent observation of females vis- iting the nests of several neighboring males in quick succession (within approx. 1-3 min) and then rejoining the feeding school. Also, I observed individual females move between and lay eggs in the nests of two different males during single spawning bouts on rare occasions (N == 2). DASCYLLUS ARUANUS AND DASCYLLUS TRIMACULATUS. These two species exhibited similar sex ratio patterns in continuous cover habitats to those described above for D. flavicaudus and D. albisella (Tables 1, 2). Male D. aruanus were signifi- 648 BULLETIN OF MARINE SCIENCE, VOL. 57, NO.3, 1995 cantly larger than females in the four sites I sampled (Table 2, Fig. 3a). This was not the case for D. trimaculatus at the Pihaena Pt. site (Table 2, Fig. 3c), a result which is difficult to account for given the samples sizes of 20 and 21 individuals and significantly larger male body sizes observed in other Dascyllus species. I did not make space use observations on marked D. aruanus or D. trimaculatus individuals, but more casual observations suggested the same pattern of sex differences described above for D. albisella and D. fiavicaudus in this habitat type. It is important to note here that power analyses revealed the sex ratio comparisons discussed above and presented in Table 2 to be statistically weak. With one exception (Manana Is. #3, 40% power), none of these chi-square tests had greater than 20% power to detect deviations from a 1:1 sex ratio (20% probability of producing a significant result assuming an actual female bias existed in the population sampled). The finding of no female biases in the sex ratios should therefore be regarded with caution. The important point, however, is that even if the small biases in the sampling represent actual female biases in the continuous cover habitat population sex ratios, these biases are small when compared to the 1:3 to 1:6 sex ratios found for small haremic groups in Dascyllus species (Tables 1, 2; discussion below). Based on the information presented above, both D. fiavicaudus and D. albisella are similar to other Dascyllus species studied in sex ratio patterns, space use, and probably overall mating system structure in continuous cover habitats. Fricke (1980) experimentally demonstrated a mating system shift from resource defense polygyny on small standardized coral units (defensible by single males) to a promiscuous system on large standardized coral units (too large to be defended by single males) in D. marginatus. This result was supported by descriptive work in D. marginatus, where female-biased, haremic groups were found on medium sized corals with three to seven individuals (Fricke, 1980), but less female-biased groups were found on larger corals occupied by more than nine individuals. Shpi- gel and Fishelson (1986) described haremic social structures for both D. aruanus and D. marginatus in discontinuous cover habitats, but "lek-based" systems in continuous cover habitats. Sex ratios which are not strongly female-biased and a lack of resource defense polygyny in continuous cover habitats appear to be conserved characteristics of Dascyllus mating systems. An apparent exception is seen with D. reticulatus in a continuous cover habitat at Lizard Island, Great Barrier Reef (Schwarz, pers. corom.), where harem polygyny appears to occur despite coral cover being relatively continuous. It would be interesting to determine whether heterogeneity in coral cover type (i.e., species, morphology) creates monopolizable "patches" that Dascyllus are attracted to even when coral cover is continuous. The next section describes an apparent lack of conservation across the genus of haremic mating structures and female-biased sex ratios in discontinuous cover habitats.

Sex Ratio and Space Use Patterns in Discontinuous Coral Cover Habitats.- Strongly female-biased sex ratios, resource defense polygyny, and protogynous sex change in Dascyllus species are known primarily from habitats characterized by both i) discontinuous coral cover and ii) corals small enough to be effectively monopolized by single large males (Table 1, but note D. reticulatus exception above). I found the same patterns in this study for the large-bodied member of the reticulatus complex, D. fiavicaudus, but not for the trimaculatus complex species, D. albisella. DASCYUUSFLAV1CAUDUS.Adult D. fiavicaudus were found almost exclusively in large heads of Pocillopora eydouxi located in the reef groove discontinuous cover GODWIN: MATING SYSTEMS IN DASCYLLUS DAMSELFISHES 649 habitat on Moorea. All the D. flavicaudus of four groups containing four or more individuals were captured and sexed. The largest individuals in three of these groups were 80-85 mm males. The largest individual in a fourth group appeared to be female, based on genital papilla morphology, but histological examination of the gonad showed that it was changing sex as it contained oocytes in several stages of atresia as well as proliferating spermatogenic tissue. In another group, the largest individual was a 77 mm male, but the next four largest fish were not captured. The largest group captured, with 13 individuals, contained five males. The largest resident fish was a male and the other four males were spread through the group size hierarchy (males: 87, 78, 76, 74, 70 mm; females: 80, 77, 75, 74, 73, 71, 70, 68 mm). Three other groups were observed, but not captured. Relative size was assessed visually and an individual was considered a male if it showed the characteristic male signal-jump behavior. Based on these criteria, one group contained a male and four females, a second group had a male and two females, and the third group had two males and two females. All fish fed in the water column 1-3 m above their resident coral and retreated to the coral when approached by a diver. During this retreat, the largest or only resident male consistently performed signal jumps. The sex ratios in this habitat did not show a statistically significant female bias when those groups that were completely collected and sexed were considered individually, but the bias is significant if these groups are lumped (8 males: 23 females; X2 = 5.828, P < 0.025). DASCYLLUS ALB/SELLA. Five D. albisel/a groups from the discontinuous cover habitat at Manana Is., Oahu ranged in size from eight to over 30 individuals (Table 1; not all the individuals in the largest group were collected and the actual group size was estimated at 35-40). Despite the range in group size, sex/size ratios and space use appeared similar between groups and also similar to patterns described above from continuous coral cover habitats in D. albisel/a. Sex ratios were not significantly different from 1:1, males were significantly larger than females, and males did not appear to monopolize areas containing females. As in continuous cover habitats, females fed well off the bottom in a loose school and males defended nest site areas on the substratum within 3-4 m of the coral heads. Observations of the two large groups preceding capture and the results of a separate study following spawning in this location (Danilowicz, 1995), indicated that many males defended nests with eggs around the coral in each of these groups (10-11 in the largest group), indicating that spawning was not monopolized by one or a few males. Monopolization and Phylogenetic Inertia Hypotheses for Dascyl/us Sexual Pat- terns.- The monopolization hypothesis proposed that small body size limits the mobility of females in the aruanus and reticulatus complexes, restricting them to coral heads (in most habitats) which can be monopolized by males. Females of species in the trimaculatus complex are much larger and consequently have greater relative mobility, which precludes their monopolization since the areas they use are also much larger. The prediction for small species that a shift to promiscuous (Fricke, 1980) or lek-based (Shpigel and Fishelson, 1986) mating should be observed in habitats where corals are too large to be monopolized by a single male is borne out by previous descriptive and experimental work, but was made previously by Fricke (1980) and is a posteriori in the context of this study. The major a priori prediction tested in this study concerns the large-bodied member of the predominantly small-bodied reticulatus complex, D. flavicaudus. The monopolization hypothesis predicts that large body size in D. flavicaudus should 650 BULLETIN OF MARINE SCIENCE, VOL. 57. NO.3, 1995 increase female mobility, preventing monopolization of access to females by large males and the development of resource defense polygyny. This prediction was not supported. Dascyllus flavicaudus did exhibit resource defense polygyny in a discontinuous cover habitat. This test case therefore provides no evidence that an increase in body size influences interspecific variation in mating system structure. Such an effect might still be worth investigating in other groups where large size differences are observed within genera or families (e.g., Paracirrhites hawkfishes: P. arcatus, P. forsteri, P. hemistictus). The phylogenetic inertia hypothesis proposed that body size was irrelevant and predicted that mating system responses to habitat and sexual patterns would be conserved within species complexes. This prediction was supported both by patterns in D. flavicaudus and the lack of a shift in space use patterns despite the presence of what appeared to be a monopolizable resource for the large-bodied trimaculatus complex member D. albisella in the discontinuous coral cover habitat. A difference between D. flavicaudus and the members of the trimaculatus complex is also supported by the observation that D. flavicaudus groups were centered around P. eydouxi heads in the reef slope discontinuous cover habitat of Moorea, while a few meters away D. trimaculatus spread over larger areas at the sides of the reef grooves. However, the possibility that D. flavicaudus excludes D. trimaculatus from P. eydouxi heads cannot be rejected. Detailed observations of both species and removal experiments in this habitat would be especially useful. Adaptation to the most commonly encountered environment may preclude short-term adjustments to an unusual environmental situation. Fricke (1979) did not find shifts from the typical monogamous mating system structure in the pro- tandrous anemonefish Amphiprion akallopisos in an unusual habitat where host anemones were distributed contiguously rather than the usual situation of isolated anemones. The finding that A. akallopisos did not develop the predicted polygynous mating system was attributed to a lack of behavioral flexibility. This may also be the case for D. albisella, where males do not appear to alter their behavior to monopolize a resource critical to females even when this appears possible (based on the ability of male D. flavicaudus to do so). The isolated coral habitat is rare in the Hawaiian Islands and D. albisella may lack the behavioral flexibility take advantage of it. This type of difference in reaction to a similar environment between related species is considered evidence for phylogenetic constraints on a trait, just as differences in a trait manifested between environment types within a species can be evidence for adaptive responses (pp. 83-84, Brooks and Mc- Lennan, 1991). A conclusion of phylogenetic constraint with respect to the space use of male D. albisella explicitly assumes that these males would realize a benefit through monopolization of isolated corals. This has not been shown and would at least require comparing male mating success in natural and experimental haremic mating situations produced through male removals.

ACKNOWLEDGMENTS

I am grateful for the assistance of the faculty, staff, and students at the Hawaii Institute of Marine Biology, University of Guam Marine Laboratory, Lizard Island Research Station, and the Christensen Research Institute. Special thanks are due D. Gochfeld, B. Danilowicz, B. Tyler, R. Pyle, M. Lutnesky, C. Fiedler, J. Mendez, E. Gardner, G. Losey Jr., and E. Reese for help in the field and constructive criticism; H. Randall and G. Allen for kindly sharing their Dascyllus morphological data; and to C. Petersen, A. Schwarz, P. Sikkel, and one anonymous reviewer whose comments greatly improved the manuscript. This is contribution #966 of the Hawaii Institute of Marine Biology. GODWIN: MATING SYSTEMS IN DASCYLLUS DAMSELFISHES 651

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DATEACCEPTED:March 7, 1995. 652 BULLETIN OF MARINE SCIENCE, VOL. 57, NO.3, 1995

ADDRESS: Hawaii Institute of Marine Biology, University of Hawaii at Manoa, P.O. Box /346, Kaneohe, Hawaii 96744-1346; PRESENT ADDRESS: Institute of Reproductive Biology, Patterson Lab- oratories, University of Texas at Austin, Austin, Texas, U.S.A. 78712, ph: (5/2) 47/-1 I /3, FAX: (5/2) 47]-9651, E-mail: [email protected].