Feeding Behavior, Habitat Use of the Angelfish by Gulf of California Marine Program

FEEDING BEHAVIOR; HABITAT USE, AND ABUNDANCE OF THE ANGELFISH Holacanthus passer (Pomacanthidae) IN THE SOUTHERN SEA OF CORTES

OCTAVIO ABURTOOROPEZA, ENRIC SALA AND CARLOS SANCHEZORTIZ This electronic reprint is provided by the author(s) to be consulted by fellow scientists. It is not to be used for any purpose other than private study, scholarship, or research. Further reproduction or distribution of this reprint is restricted by copyright laws. If in doubt about fair use of reprints for research purposes, the user should review the copyright notice contained in the original journal from which this electronic reprint was made.

Feeding behavior, habitat use, and abundance of the angelfish Holacanthus passer (Pomacanthidae) in the southern Sea of Cortés Octavio Aburto-Oropezaa , Enric Salab,c & Carlos Sánchez-Ortiza Departamento de Biolog´ıa Marina, Universidad Autónoma de Baja California Sur, La Paz, B.C.S. 23080. México b Scripps Institution of Oceanography, University of California at San Diego, La Jolla, CA 92093-0201, U.S.A. (e-mail: esala@coast.ucsd.edu) c Corresponding author

Received 13 March 1998

Accepted 27 July 1999

Key words: coprophagy, damselfish feces, omnivory, sex ratio, space partitioning Synopsis Feeding behavior and habitat use of the king angelfish, Holacanthus passer, was studied in the southern Sea of Cort´es, M´exico. H. passer fed on benthic communities (algae and sessile invertebrates) and in the water column (mainly feces from the damselfish Chromis atrilobata). Although there were not significant differences in feeding rate between sexes, coprophagy was more common in males, while grazing was more common in females. Spatial distribution of size classes followed a pattern of decreasing size with increasing depth. Feeding rate was significantly different among habitats: small females had a higher feeding rate on the bottom, big females and small males had similar feeding rates from the bottom to 3 m above the bottom, and big males had higher feeding rates from 5 m above the bottom to the surface. Habitat was clearly partitioned, and there was significant habitat overlap only between big females and small males. The abundance of H. passer was partly explained (34% of the total variance) by the abundance of the damselfish C. atrilobata. There was a clear trophic association between C. atrilobata schools and H. passer feeding damselfish feces in the water column. The sex ratio male : female of H. passer populations was > 1 at several sites, an unusual pattern for a protogynous fish. The sex ratio on the H. passer water column stock was also biased towards males at most sites. Although there is a positive relationship between C. atrilobata abundance and H. passer, there are factors other than damselfish abundance which cause this dominance of males.

Introduction The biology of angelfishes (Pomacanthidae) has generated great interest among coral reef ichthyologists (see review by Allen 1979). Their food habits are relatively well known, having been described as important sponge feeders (Randall & Hartman 1968, Dunlap & Pawlik 1996) and herbivores (Hiatt & Strasburg 1960, Randall 1967). Little attention, however, has been paid to the resource partitioning among size classes and sexes of angelfishes. Food habits of angelfishes have been studied mostly from stomach contents. This technique provides the best account of prey species,

but unless information of distribution of prey species is available, little can be said about the use of space by angelfishes. Stomach content analysis complemented with scuba diving observations provide a more thorough description of fish feeding ecology (e.g. Hourigan et al. 1989). Furthermore, in habitats with high spatial heterogeneity, the use of a single method may lead to erroneous conclusions about resource partitioning of fish species (Sala & Ballesteros 1997). The abundance and distribution of fishes is dependent on several distinct factors such as recruitment, habitat structure, food availability, and environmental factors (e.g. Jones 1991, Williams 1991). Most of the

436 investigations on the factors explaining the abundance of fishes have studied damselfishes and wrasses, and little attention has been paid to angelfish populations. Sex ratio of angelfish populations (proportion of sexes and sizes) appears to be determined by the mating system. Reproductive styles of angelfishes differ among genera, with the harem system common in Centropyge and Genicanthus, while monogamous pairing occurs in large Pomacanthus and many Holacanthus (Allen 1979). Most species of angelfish are protogynous hermaphrodites (Neudecker & Lobel 1982, Thresher 1984). No studies, however, have addressed the role of other factors, such as food availability, in structuring angelfish communities. The king angelfish, Holacanthus passer, ranges from the central Sea of Cortés to Ecuador and the Galápagos Islands (Thomson et al. 1979). Like most Pomacanthidae, H. passer is protogynous and males are generally larger than females. The reproductive unit of H. passer is the pair (Strand 1978, Moyer et al. 1983). Studies of stomach contents have revealed that H. passer is a diurnal grazer on sessile invertebrates (mainly sponges) and algae (Reynolds & Reynolds 1977, Bermúdez & Garc´ıa 1985, Pérez-España & Abitia-Cárdenas 1996), but can also be a plankton feeder (Strand 1978). The objectives of this study were to: (1) carry out in situ observations of H. passer feeding behavior; (2) describe the spatial distribution and habitat partitioning among size classes and sexes of H. passer; and (3) study the relationship between food availability and abundance and sex ratio of H. passer, in order to gain insight into the factors structuring H. passer communities. Materials and methods The study was carried out at seven sites on the southwestern coast of the Sea of Cortés, México (Figure 1). Los Islotes and Las Animas are islets exposed to strong, continuous tidal currents (Jiménez-Illescas et al. 1997). Underwater topography of both sites varies from steep vertical walls to gentle rocky slopes with sandy bottoms and fields of large boulders. Vertical walls were dominated by filter feeding invertebrates, mostly cnidarians (gorgonians, hydrozoans, and cup corals). Boulders were dominated mainly by algal turf and sparse coral heads (mostly Pocillopora elegans). Cabo Pulmo harbors extensive coral communities dominated by Pocillopora elegans, Porites californica and Pavona gigantea, over a series of granitic dikes

Figure 1. Location of the study sites. Circles are study sites on fields of large boulders; squares are sites on vertical walls. Sites in italics are study sites; the rest are sites from the fish monitoring from which we used data for the regression between Chromis atrilobata and Holacanthus passer density.

(Brusca & Thomson 1977). Punta Lobos, Pailebote, Punta Perico and Los Frailes are shallow sites with fields of large boulders colonized by algal turf. All underwater observations were made using SCUBA. Sampling was conducted in Winter of 1997–1998 at Los Islotes and in Winter of 1998–1999 at the other sites. Preliminary observations were made to identify potential prey of Holacanthus passer. Due to small size of organisms in benthic communities in the islands of La Paz, we could not identify in situ the different types of food H. passer ingested when grazing. We observed, however, that H. passer fed frequently in the water column, not as zooplanktivore, but eating feces of other fishes. We thus decided to group our observations of feeding behavior of H. passer in two categories: grazing and coprophagy. Distinction between sexes was based on color of pelvic fins (white in males, pale yellow

437 in females, Thresher 1984; and empirically verified by the authors). We grouped individuals into the following size classes: small females (140–200 mm total length), large females (> 200 mm), small males (150– 250 mm), and large males (> 250 mm). Estimation of fish size was determined using a plastic ruler attached to an acrylic sheet. The precision of our size estimates was validated prior to the study using plastic dummies of H. passer of different sizes. Only 4% of our estimates failed to assign fishes to their real size class. We quantified feeding rate of Holacanthus passer by following individual fish for 15 min and counting the number of bites for each of the two feeding categories (grazing and coprophagy) at Los Islotes. To test for differences in feeding rate between sex and feeding category, log-transformed data were analyzed using 2 factor ANOVA. When the interaction was significant, post-hoc multiple comparisons were tested using Tukey HSD tests. To determine spatial distribution of Holacanthus passer, we carried out visual censuses at Los Islotes using the technique of the stationary point (HarmelinVivien et al. 1985). This technique consists of counting the number of fishes in a 5 m radius within the first minute, and estimating their total length. Strand (1978) suggested a segregation of H. passer size classes in space, hence we decided to divide the water column into four habitats: bottom to 1 m above the bottom, 1–3 m above the bottom, 3–5 m above the bottom, and 5 m above the bottom to the surface. All censuses were carried out in areas between 8 and 12 m depth. Thirtysix replicate censuses were completed in each of the above habitats. To test for differences in density among habitats and size classes, log-transformed data were analyzed using 2 factor ANOVA. When the interaction was significant, post-hoc multiple comparisons were tested using Tukey HSD tests. To quantify feeding rate of Holacanthus passer in the different habitats, we followed individual fishes for 5 min (15 individuals of each size class) and counted the number of bites in each habitat at Los Islotes. To test for differences in feeding rate between size classes and habitats, log-transformed data were analyzed using 2 factor ANOVA. When the interaction was significant, post-hoc multiple comparisons were tested using Tukey HSD tests. Overlap among habitats in (1) species distribution and (2) feeding rate were determined as: !" " "pxhi − pyhi " , αH = 1 − 0.5

where pxhi and pyhi are (1) the proportions of abundance from visual census in the habitat hi for all size class pairs x, y; or (2) the proportions of feeding rate from visual census for all size class pairs x, y. These overlap indices vary from 0 (when the 2 size classes use totally different habitats) to 1 (when they use the same habitats in the same proportions). Following Keast (1978), an index value ≥ 0.6 was considered significant. Based on our results that show a trophic association between damselfishes and angelfishes (see Results), we hypothesized that the abundance of king angelfishes would increase with the abundance of damselfishes. To test this hypothesis we used data on fish abundance collected at 20 sites (Figure 1) during a monitoring of fish communities along the southern Sea of Cort´es (unpublished data). We carried out visual censuses using SCUBA diving to quantify the abundance of Chromis atrilobata (the most abundant damselfish in the region) and Holacanthus passer at each study site, using 50 m × 5 m line transects (n = 5 at each site) along which we counted all individuals of each species. We then performed a model II linear regression between C. atrilobata and H. passer abundance, to test whether increasing damselfish abundance causes increasing angelfish abundance. Our results at Los Islotes showed a sex ratio male : female > 1 in Holacanthus passer schools associated with Chromis atrilobata schools in areas with strong currents, and also that males tend to aggregate in the water column to eat damselfish feces. Since a sex ratio male : female > 1 is unusual for angelfishes (Allen 1979), we decided to investigate whether this sex ratio biased towards males was a consequence of the availability of planktivorous fish feces. We carried out visual censuses using SCUBA diving to quantify the abundance of C. atrilobata and the abundance and sex ratio of H. passer at each study site, using 50 m × 5 m line transects (n = 5) along which we counted and estimated the size of all individuals. We also assessed whether the proportion of H. passer feeding in the water column was a consequence of the presence of C. atrilobata schools. To study the association between C. atrilobata schools and H. passer, we counted the number of individuals and the sex of all H. passer encountered, and the number of individuals of each H. passer and C. atrilobata group. To test whether C. atrilobata abundance predicts the number of H. passer feeding in the water column, we carried out a non-linear regression between average size of C. atrilobata schools and proportion of H. passer

438 feeding in the water column. To test the hypothesis that increasing damselfish abundance causes increased ratio male : female in H. passer, a model II linear regression was estimated between C. atrilobata density and H. passer sex ratio. Results Holacanthus passer fed either in the water column (40.8% of total observations, n = 7138) or grazed on benthic communities (59.2% of total observations) at Los Islotes. Individuals feeding in the water column ate feces of scissortail damselfish, Chromis atrilobata (38.7%). We also observed groups of small H. passer females feeding on feces of the Cort´es rainbow wrasse, Thalassoma lucasanum (2.1%) and in two occasions we observed a small group of individuals feeding on feces of sea lions, Zalophus californianus (0.03%). Individuals of H. passer feeding in the water column searched for feces by swimming against the current and maintaining their position within schools of C. atrilobata. When an individual localized C. atrilobata feces, it swam readily to the feces, ingesting them by suction, then turned to look for more feces. When grazing on benthic communities, H. passer fed on 59.0% of the observations on the algal turf (where no individual species or algal types were identifiable in situ), with 0.2% of observed feedings occurring on identifiable macrozoobenthos [e.g. gorgonians (Leptogorgia rigida) and corals (Pocillopora elegans)]. H. passer were also observed feeding on cryptic sponges within broken P. elegans heads (0.01%). During the reproductive season of the damselfishes Microspathodon dorsalis and Abudefduf troschelli, H. passer also fed on demersal eggs of both species. H. passer grazed generally alone, seldom forming schools, except when feeding on demersal eggs when it joined multispecific schools of T. lucasanum, Johnrandallia nigrirostris, Bodianus diplotaenia, and Prionurus punctatus. Searching for benthic food consisted of swimming slowly, turning sideways, then extending the protractile mouth and ingesting prey. Holacanthus passer had an average feeding rate of 45.8 ± 3.6 (mean ± SE) bites 15 min−1 at Los Islotes. Although there were no significant differences in feeding rate between sexes and feeding habitats (benthos vs. water column), the two sexes fed at different rates on the two feeding habitats (significant sex×habitat interaction, Table 1). Males fed more in the water column

(52.3 ± 5.1 bites 15 min−1 ) than grazed (30.3 ± 5.2 bites 15 min−1 ), whereas females grazed (78.0 ± 9.9 bites 15 min−1 ) more often than fed in the water column (22.4 ± 2.9 bites 15 min−1 , p < 0.001). All H. passer found in the water column (≥1 m above the bottom) were associated with schools of Chromis atrilobata. The interaction between size and habitat was significant (Figure 2, Table 2), indicating that different size classes occupied habitats in a different way. Small females were more abundant closer to the bottom than in the other habitats (p < 0.001), and were not found > 3 m above the bottom in our censuses, Table 1. Holacanthus passer. Results of 2 factor ANOVA comparing feeding rate between sexes and feeding habitat (coprophagy and grazing). Factor

Sex Feeding habitat Sex × feeding habitat Error

1 1 1 152

0.198 0.023 12.475 0.306

0.647 0.076 40.775

0.422 0.782 <0.001

Figure 2. Holacanthus passer. Densities (mean ± SE) of size classes at each of the 4 depth-defined habitats considered in Los Islotes. Small females: 140–199 mm total length; big females: >200 mm; small males: 150–249 mm; big males: >250 mm. Table 2. Holacanthus passer. Results of 2 factor ANOVA comparing mean density between habitats and size classes. Factor

Habitat Size Habitat × size Error

3 3 9 564

0.97 0.16 0.71 0.04

24.22 3.99 17.70

< 0.001 0.008 < 0.001

439 Table 4. Holacanthus passer. Results of 2 factor ANOVA comparing feeding rate between habitats and size classes. Factor

Habitat Size Habitat × size Error

3 3 9 224

4.24 0.43 4.16 0.13

32.35 3.28 31.75

< 0.001 0.022 < 0.001

Figure 3. Holacanthus passer. Feeding rate (mean ± SE) of size classes at each of the 4 depth-defined habitats considered in Los Islotes. Size classes as in Figure 2. Table 3. Holacanthus passer. Habitat overlap (αH ) between size class pairs. Lower side of the matrix calculated for spatial distribution (density); upper side calculated for feeding rate. Small females: 140–199 mm total length; big females: >200 mm; small males: 150–249 mm; big males: >250 mm.

Small females Big females Small males Big males

Small females

Big females

Small males

Big males

— 0.50 0.64 0.21

0.44 — 0.86 0.49

0.48 0.91 — 0.36

0.19 0.45 0.36 —

although they were observed later feeding between 3 and 5 m above the bottom (Figure 3). Large females and small males were significantly more abundant from the bottom to 3 m above the bottom than from 3 m to the surface (p < 0.01). Big males followed a pattern opposite to that of small males, being significantly more abundant 3 m above the bottom (p < 0.001). Habitat overlap was significant (αH ≥ 0.6) only between small females and small males, and between big females and small males (Table 3). Feeding rate at Los Islotes decreased from the bottom to 5 m above the bottom (Figure 3). The different size classes showed significantly different feeding rates among habitats (significant size × habitat interaction, Table 4). Small females showed a dramatic decrease in feeding rate from the bottom to 5 m above the bottom (p < 0.001). Big females had similar feeding rates from the bottom to 5 m above the bottom, and had a significant lower feeding rate from 5 m above the bottom to the surface (p = 0.016). Small males had similar

Figure 4. Relationship between Chromis atrilobata density and H. passer density in fields of big boulders and vertical walls, between 5 and 20 m depth. The straight line is the linear regression, and the dashed lines are the 95% confidence intervals.

feeding rates from the bottom to 3 m above the bottom, and a significant lower feeding rate from 3 m above the bottom to the surface (p = 0.01). Big males had a higher feeding rate from 5 m above the bottom to the surface (p < 0.001). Feeding rate overlap (αH ) was highly significant between big females and small males (Table 3). The abundance of Chromis atrilobata partly explained the total abundance of Holacanthus passer (linear regression, F = 14.917, p = 0.0006; Figure 4), although it only explained 34% of the variance of H. passer abundance. The percentage of H. passer populations in the water column associated to C. atrilobata schools was ≥ 50% at all sites were C. atrilobata was present (Figure 5). The percentage of H. passer in the water column increased with increasing size of damselfish groups until a threshold about 100 damselfish group−1 was reached [non-linear regression: −7 y = 9.83 × 10−5 (1 − e−2.71×10 x ), r 2 = 0.865]. Sex ratio of Holacanthus passer at the different study sites varied from 0.5 to 2 (Table 5). Three out of seven sites had a sex ratio (males : females) >1, and

440 omnivore (Pérez-España & Abitia-Cárdenas 1996). During the present study we observed that coprophagy, mostly on feces of the damselfish Chromis atrilobata, was very important in H. passer feeding. This behavior was not observed before for H. passer, although previous reports of plankton feeding might have included consumption of fish feces. C. atrilobata is the most abundant fish species in shallow waters in La Paz Bay (Sánchez-Ortiz et al. 1997), forming large schools in sites subjected to strong currents. Although feces as fish food are thus abundant in the study area, only Prionurus punctatus (Acanthuridae), other than H. passer, was observed to feed on C. atrilobata feces. Another pomacanthid, Centropyge interruptus, has been reported to feed on feces of four species of zooplanktivorous fish (Moyer & Nakazono 1978). Coprophagy appears to be a common feeding style among fishes in coral reefs (Robertson 1982), but not in rocky reefs. Bailey & Robertson (1982) showed that protein and lipid content of fish feces are equal to or exceed those of non-fecal food (i.e. zooplankton, coral tissue, algae). Bailey & Robertson compared levels of protein and ash of algae from the southern Sea of Cortés (Montgomery & Gerking 1980) as indicators of the difference in potential nutritional values of feces and non-fecal food, and showed that fecal food (especially from zooplanktivores and some carnivores) may provide more energy than algae (see also Robertson 1982) for fishes. Energetic requirements differ among sexes in many fish species (e.g. Goldschmid & Kotrschal 1981, Hoffman 1983). Differences in use of food resources among sexes in Holacanthus passer might have been caused by diet shifts during ontogeny (Gerking 1994). However, observations other than coprophagy, such as formation of schools in order to consume demersal eggs

Figure 5. Relationship between mean number of Chromis atrilobata per school and percentage of the H. passer in the water column.

the linear regression between Chromis atrilobata density and H. passer population sex ratio was not significant (F < 0.001, p = 0.985, r 2 < 0.001). Groups of H. passer feeding in the water column showed male : female ratio >1 in five out of six sites, although the linear regression between Chromis atrilobata density and H. passer sex ratio in the water column was not significant (F = 0.169, p = 0.720, r 2 = 0.078). Discussion Fishes of the family Pomacanthidae have three basic feeding styles: predation on sessile invertebrates (mostly sponges), herbivory, and planktivory (e.g. Randall 1967, Randall & Hartman 1968). Holacanthus passer in the Sea of Cort´es has been identified as a sponge feeder (Reynolds & Reynolds 1977), an algivore (Berm´udez & Garc´ıa 1985), and also a generalist

Table 5. Holacanthus passer. Density of Chromis atrilobata (mean number of individuals 250 m−2 , SD in parenthesis), sex ratio of H. passer and sex ratio of H. passer groups in the water column, at each study site. N = number of observations. Site

Las Animas Pailebote Punta Lobos Los Frailes Cabo Pulmo Punta Perico Los Islotes

Chromis atrilobata density 410 (348.5) 443 (195.1) 163 (114.7) — — — 345.2 (171.11)

H. passer

H. passer water column

Sex ratio

2.02 0.83 1.32 0.47 0.76 1.00 1.60

368 77 109 22 30 96 440

3.07 1.25 1.39 0.83 — 1.87 3.25

301 36 86 11 0 66 264

441 of damselfishes indicates that H. passer has a highly opportunistic feeding ecology. This schooling behavior was also observed by Montgomery (1981), who suggested that schooling overwhelms defensive efforts by territorial damselfishes. Consideration of both spatial distribution and feeding rate indicates clear differences in resource use among size classes of Holacanthus passer, although they may overlap in some cases (mainly between large females and small males). Generally, the population was clearly stratified in the following way: small females exploited the bottom, mostly by grazing; large females and small males coexisted ≤ 3 m from the bottom; and large males dominated the upper water column ≥ 3 m above the bottom, feeding mainly on feces of zooplanktivorous fish. Further experimental studies are required to ascertain the factors and interactions which maintain this stratification. The results of this study indicate that Holacanthus passer abundance and habitat use in the southern Sea of Cort´es is partly dependent on the abundance of planktivorous fishes, particularly of the damselfish Chromis atrilobata. The number of C. atrilobata per school is a good predictor of the proportion of H. passer in the water column. It has been shown that planktivorous fishes are abundant where there are currents and that, below a threshold in water motion, the stronger the current speed the higher the abundance of planktivorous fishes (Stevenson 1972, Thresher 1983, Hobson 1991). This suggests that current speed may be also a good predictor of H. passer abundance and feeding behavior. However, our results also show that if there are no damselfishes, there are still H. passer, and that males go to bottom, which means that planktivorous fish are not necessary for H. passer presence in one habitat. The male : female ratio > 1 is an unusual pattern in a protogynous fish where we would predict a small number of males with a harem of females or a system of couples (e.g. Moyer et al. 1983, Shapiro 1988, Cole & Shapiro 1992). Pomacanthids also have populations with dominance of females (e.g. Moyer 1984, Hourigan & Kelley 1985). Moyer et al. (1983) described foraging groups of up to 100 male H. passer and associated them with breeding. However, we have observed male groups in the water column during all year for several years, and do not agree with the hypothesis that male groups are associated to spawning. Our results show that male H. passer dominate the water column, feeding upon damselfish feces. High abundance of damselfishes and, subsequently, of high

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