BULLETIN OF MARINE SCIENCE, 55(2-3): 1316-1323, 1994
GRAY TRIGGERFISH (BALISTES CAPRISCUS GMELIN) FEEDING FROM ARTIFICIAL AND NATURAL SUBSTRATE IN SHALLOW ATLANTIC WATERS OF FLORIDA
Frederic E. Vose and Walter G. Nelson
ABSTRACT Diets of gray triggerfish (Balistes capriscus Gmelin) collected on artificial and natural substrates were compared during a project investigating re-use of waste materials (stabili7.eu oil ash) as reef building materials. Gray triggerfish from natural reefs consumed relatively greater amounts of bivalves than those collected on artificial reefs. In contrast, gray triggerlish from artificial reefs consumed more barnacles than did their natural reef counterpalts. Tax- onomically, the food of fish from artificial reefs was more restricted than that of !ish from natural habitats. Results indicate, however, that gray triggerfish are not obligate feeders on well-armored prey as might be predicted from jaw morphology and dentition. In effect, these adaptations broaden the feeding niche of gray triggerfish, allowing feeding flexibility which includes both armored and unarmored invertebrate prey.
Fishes use artificial reefs as breeding sites and as structural refugia for escap- ing predation or for resting. Of additional importance, many fish feed on other animals attracted to or directly produced in association with the artificial struc- tures. Reef fish populations may be enhanced by increases in available food, however, the food pathways of artificial reefs are not well known (Bohnsack and Sutherland, 1985). Triggerfishes are important members of reef fish assem- blages found on artificial reefs in subtropical waters, and their feeding habits are of interest in determination of reef function. The main objective of the present study was to determine feeding habits in gray triggerfish and to compare diets of fish collected on artificial and natural reef substrates. The diet of gray triggerfish (Balistes capriscus) inhabiting artificial reefs is not well known, al- though observations of predation on sand dollars have recently been reported (Frazer et aI., 1991). Queen triggerfish (Balistes vetula) have been reported to feed on well-armored invertebrate prey (Randall, 1967), as have the balistids in general (Shipp, 1986), This research was undertaken as part of a project evaluating the suitability of stabilized oil ash waste as a building material for artificial habitats (Nelson ct aI., 1988; Metz and Trefry, 1988; Kalajian et aI., 1989; Vose, 1990; Nelson et aI., 1994). The period between reef deployment and collection of fish was short (17 months), and at the time of collection, the fouling cover of the artificial reef was dominated by barnacles, In contrast, previous observations from the nearby nat- ural reef fouling community indicated greater species richness of prey items. Thus, it was expected that the diet of Balistes capriscus inhabiting the artificial reefs would differ from that of fish collected on natural reefs (Ho: no difference in diet of gray triggerfish collected on artificial and natural reefs).
METHODS
Four experimental reefs were deployed in April 1987 approximately 2 km off the coast of Vero Beach, Florida (27°40'N, 80020'W) in 12.9 m of water on coarse shell-hash sediments (previously figured in Nelson et aI., 1988). The reef array included two reefs, each composed of 100 solid stabilized oil-ash blocks, and two reefs composed of 100 solid concrete blocks. The reef patches were approx- imately I m tall, with a footprint of 10 m2, and were located from 26-56 III apart.
1316 VOSE AND NELSON: GRAY TRIGGERFISH FEEDING 1317
Gray triggerfish were collected from both stabilized oil-ash reefs and concrete reefs to determine what prey were consumed and in what propOltions. Gray triggerfish are usually inactive at night, thus, all fish included in analysis were collected during the day to maximize the number of fish with recently consumed prey. Seventeen months after reef deployment (20 September 1988), 5-6 fish were speared from each artificial reef patch (N = 23). Seventy-two gray triggerfish were collected during the day by hook-and-linc and spear from limestone reefs (four stations) located in cquivalent water depth during April to September 1988. The majority of fish (13 of 19) selected for gut contents analysis were collected on natural ledges located within 4 km of the artificial reef site. The collection from natural reefs provided size frequency information for fish on natural reefs, which adequately sampled individuals within the same range of standard length (SL) of fish collected on the artificial reefs. Only those fish from natural reefs which fell within the same size range as fish from artificial reefs were examined (N = 19). Fish were held on ice until SL was measured to the nearest millimeter (within 3 h). Stomachs and intestines were then removed, fixed in 20% formalin, and after a minimum of 48 h transferred to 70% 2-isopropanol. Contents of the entire gastrointestinal tract were removed and iden- tified to the lowest possible taxonomic level under a dissecting microscope. Prey items were dried at 60°C in pre-weighed aluminum drying dishes. Percent frequency of occurrence (Hynes, 1950; Hyslop, 1980) and perccnt dry weight of prey items were calculated. Unidentifiable organic material (advanced state of digestion), sand, empty shells (from incidental sediment ingestion) and parasites were not included in calculations of percent dry weight. Dry weight data for gray triggerfish were arcsine transformed and statistically analyzed with one- way ANOYA. These data were used to test the null hypothesis that there were no significant differ- ences in percent dry weight of dominant prey items for individuals collected on artilkial or natural substrate.
RESULTS
A haphazard spearing of fish from artificial reefs yielded specimens ranging from 15.3-21.4 cm SL, with a mean of ] 8.7 ± 1.6 cm SL (Fig. Ia), which corresponded to the lower end of the distribution of individuals collected on natural reefs (Fig. I b). The mean SL of all gray triggerfish (N = 72) collected from natural limestone reefs was 23.8 ± 4.0 em, while individuals ranged from approximately 17-36 em (Fig. I b). Specimens from the larger natural reef col- lection which fell within the same range of SL as those collected on the artificial reefs (N = 19) had a mean of 20.0 ± 1.5 cm, and were selected for diet analysis. Two specimens from the artificial reef collection (N = 23) had no identifiable prey in their guts (only digested organic material), while all fish examined from daytime collections on natural reefs (N = 19) held identi fiable prey. Data sets were pooled within habitat (Table I). Gray triggerfish moved between individual artificial reefs, and there was similarity in fouling assemblages (Nelson et aI., this issue). Therefore, the fish collected from oil-ash and concrete reefs were pooled. Barnacles dominated the identifiable prey items (74.53% dry wt., 65% fre- quency of occurrence) from guts of gray triggerfish collected on artificial reefs. Barnacles constituted a proportionally higher dry weight per gut of individuals from artificial habitat when compared to natural habitat (one-way ANOVA, P < 0.05). In contrast, bivalves dominated the diet (44.13% dry weight, 100% fre- quency of occurrence) of specimens from natural reefs (Table I). Significantly higher proportions of bivalves were present in the guts of triggerfish collected on natural reefs compared to specimens collected on artificial reefs (one-way ANO- VA, P < 0.00 I). The dry weight of prey items such as barnacles and bivalves is CaCO) dominated, which may have overestimated their contribution to dietary intake relative to soft-bodied prey. However, similar methods were used for spec- imens from both habitats, and should not have influenced between habitat com- parIsons. Whole and fragmented polychaetes were observed in 6 I % of fish from artificial reefs, compared to 95% of fish collected from natural reef. Polychaetes contrib- uted ] .98% and 4.50% of total dry weight of identifiable prey items on artificial 1318 BULLETIN OF MARINE SCIENCE. VOL. 55, NO. 2-3, 1994
12 1 a 10 ARTIFICIAL REEF
8
6
4
(f) «--l 2 ::::) Cl 0 > ~ ~ ~ ~ ~ ~ ~ ~ 0 0 ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~
8
6
4
2
0 0 0 a ~ a ~ a ~ a 0 ~ ~ a ~ 0 ~ 0 a 0 a 0 tti I"- cO ci N .,t >Ii
Figure I. Length distribution of gray triggerfish (Batistes capriscus) collected from (a) artificial reefs and (b) natural reefs, Standard length was determined to the nearest mm. VOSE AND NELSON: GRAY TRIGGERFISH FEEDING 13]9
Tab]e 1. Summary of gut contents for gray triggerfish collected on artificial (N = 23) and natura] (N = 19) reefs. Tab]ed values are from pooled gut contents (within collection areas). Unidentified organic material, sediment (sand and empty shell) and parasites were not included in the calcu]ations of percent dry weights.
Arti llcial reds Natural reefs
% Dry % Freq. % Dry % Freq. Prey item # Taxa weight occur. # Taxa weight occur.
Cirripedia 3 74.53 65 4 17.7 89 Crust. fragments NA 3.07 30 NA 1.59 I] Amphipoda 2 0.01 35 5 0.27 58 Isopoda ] <0.01 4 2 0.04 2] Ostracoda I 0 13 I <0.01 21 Paguroidea 0 0 0 ] 0.47 5 Thalassinoidea 0 0 0 1 0.9 ]6 Portunidae ] 5.57 ]3 I 4.70 ] ] Xanthidae ] 1.67 ]3 ] 3.88 37 Majidae I 0.09 4 ] 5.39 ]6 Palinuridae 0 0 0 ] 2.61 5 Pinnotheridae 0 0 0 ] 0.03 5 Decapoda (zoeae) NA <0.0] 4 NA 0 0 Gastropoda 3 0.46 39 5 1.26 95 Bivalvia 6 9.45 87 9 44.13 100 Asteroidea 0 0 0 I 0.75 5 Ophiuroidea 0 0 0 ] 0.07 16 Echinacea 1 1.72 26 I 3.7] 16 Gnathostomata ] 0.17 4 ] 0.53 42 Holothuroidea I <0.01 4 ] 2.35 26 Polyehaeta 4 1.98 6] 6 4.50 95 Hydrozoa I 0.63 13 1 0.08 63 Bryozoa 2 0.19 44 I 0.31 53 Anthozoa 0 0 0 I 0.41 II Plantae 0 <0.01 9 3 0.18 53 Porifera 0 0 0 2 3.49 42 Urochordata I <0.01 9 2 0.02 26 Pisces (fish scales) NA 0.19 9 NA 0 0 Pisces (fish tissue) NA 0.20 4 NA 0 0 Foraminiferida ] 0.02 35 I 0.04 68 Unid. egg NA 0.03 17 NA 0 0 Total taxa 30 55 Organic material 100 100 Sediment 78 100 Parasites 87 89
NA = not available.
reefs and natural reefs, respectively (Table I). Percent dry weights of polychaetes per gut were not significantly different between the two collections of fish (one- way ANOYA). Mobile crustaceans, particularly decapod crabs, were secondary foods for fish collected from both artificial and natural reefs. Portunid crabs were consumed by 11-13% of all fish, making up 4.70-5.57% dry weight of prey items (Table 1). Xanthid crabs were found in 37% of fish from natural reefs, compared to only 13% of fish from artificial reefs. The families Majidae, Palinuridae and Pinnotheri- dae were all found in modestly higher frequency and weight in fish from natural reefs (Table 1). The diet of gray triggerfish included a wide variety of invertebrates (Table 1), but the food was heavily macerated making identification difficult. Due to fragmentation of prey, enumeration was not possible for some taxa, and we were 1320 BULLETIN OF MARINE SCIENCE, VOL. 55, NO. 2-3, 1994 unable to calculate indices of relative importance (IRI-Pinkas et a\., 1971). The diet of specimens from natural reefs was more varied than those from artificial reefs (Vose, 1990) representing a total of 30 and 55 taxa respectively (Table I). Four species of barnacles were identified from the intestinal tract of fish from natural substrate, as compared to three from artificial reefs. One barnacle genus, Chelonebia, occurs on the shells of turtles and decapods and was found only in guts of fish from natural reefs (Table I). Bivalve taxa were somewhat more varied in the diet of individuals which fed on natural substrate (natural-9 spp., artificial-6 spp.). Similarly, five gastropod taxa were found in guts of fish from natural reefs, compared to three gastropod taxa in guts of fish from artificial reefs (Table I). While no fish from natural reefs had fed on other fishes, a few triggerfish from artificial reefs had consumed fish (Table I). More groups of echinoderms were consumed on natural reefs. Fish from natural reefs fed on sea stars, sea cucumbers, brittle stars, sea urchins and sand dollars while those from artificial reefs consumed only sea urchins, sand dollars and sea cucumbers (Table 1). Although algae were detected in the guts of 9% of specimens from artificial reefs and 53% of those collected from natural reefs, they comprised <0.01 % and 0.18% by weight of items in the diet, respectively (Table I). Unidentifiable organic material, sand, empty shell (from sediments) and gas- trointestinal parasites were present in most fish examined (Table I). The organic material was primarily soft tissues of unknown origin found at the posterior end of the digestive tracts.
DISCUSSION Gray triggerfish are potentially important predators on hard bottom communi- ties of east central Florida. Gray triggerfish are diurnally active, as determined from day and night SCUBA observations combined with the examination of guts of specimens collected at night (data not presented). Smaller fish, ranging in size from 10-175 mm, may be found in association with pelagic Sargassum (Dooley, 1972). Dooley found that algae, hydroids, barnacles and polychaetes (decreasing order of frequency of occurrence) were important in the diet of small gray trig- gerfish. At approximately 16-17 cm SL, it appears that gray triggerfish colonize hard bottom habitat. Fishes collected from the natural reefs in this study had a size frequency distribution similar to previous reports (Bohnsack and Harper, 1988). On the artificial reefs, gray triggerfish collected were on the lower end of the size range displayed in the natural reef collection. Previously, limited quantitative information was available on the diet of the gray triggerfish in later stages of development. Gray triggerfish were reported to feed on decapod crustaceans (Sedberry, 1984), scyllarid lobsters (Barshaw and Spanier, 1994) and a variety of crustaceans and mollusks, many of which were planktonic (Nelson, 1988). A strong jaw and specialized dentition suggests Ba/- isles capriscus is adapted for feeding on well-armored invertebrate prey, but it is clearly not a specialized feeder. Instead, gray triggerfish are opportunistic feeders whose morphology provides the ability to feed on both unarmored and armored prey. Within the Balistidae, there is further evidence of a lack of feeding specializa- tion among species. For example, the queen triggerfish (Ba/isles velu/a) was re- ported to feed primarily on echinoids in the Caribbean (Randall, 1967) but was subsequently reported as having consumed crabs and chitons (Reinthal et aI., 1984), suggesting feeding flexibility similar to Balisles capriscus. Despite similar jaw and teeth morphology, two other West Indian species are listed by Randall VOSE AND NELSON: GRAY TRIGGER FISH FEEDING ]321
(1967) as preferring algae and plankton (Canthidermis suffiamen and Melichthys niger, respectively). Hobson (1974) also describes the plectognathic black durgon (Metichthys niger) as an omnivore feeding on plankton and benthic algae. It is clear that morphology of fishes, particularly with respect to the jaw and teeth, may not always be a good predictor of feeding ecology. This has also been sug- gested for blennioid fishes (Kortschal, 1989) where evolution of a biting jaw allowed some species to feed on a greater diversity of prey. The present data on gray triggerfish feeding are inconsistent with the hypothesis that morphological specialization (strong jaw and sharp cutting teeth) necessitates a narrow feeding niche. Diets of gray triggerfish from natural and artificial habitat were dissimilar. This may reflect differing availability of prey in the two habitats. For example, bivalves associated with hard substrate were a common food of gray triggerfish inhabiting both reef types, but were consumed in greater proportions by fish from natural reefs. Frequency of occurrence for bivalves was similar for the two habitats, but taxonomic richness was greater for fishes which fed on natural reefs. Studies of fouling communities noted only six bivalve species present on artificial reef sur- faces in July-October 1988 (Neth, 1991), which accounted for a small percentage of total cover. Fouling data are unavailable from actual fish collection locations on natural reefs, but a limited study of shallow water outcrops near Sebastian Inlet, Florida (approximately 24 km north of Vero Beach) yielded 10 bivalve species (W. G. Nelson, unpubl.). In December 1987, bivalves occurred on 16 of 21 rock samples collected from natural reefs south of Sebastian Inlet. These dif- ferences between fouling communities on artificial and natural substrate (for spe- cies richness and abundance of bivalves) probably affected diets of gray triggerfish inhabiting the two reef types. Feeding plasticity has allowed gray triggerfish colonists to shift their diet toward prey more readily available on the artificial reefs. Barnacles overwhelm- ingly dominated the diet of fish examined from artificial reefs. In contrast, bar- nacles were a secondary food of fish from natural reefs. Once again, this prob- ably reflects differences in prey availability; barnacles dominated the fouling cover of the artificial reefs (see Savercool, 1988; Neth, 1991; Nelson et aI., 1994). Barnacles, however, occurred on only 5 of 21 rock samples collected from natural reefs south of Sebastian Inlet (W. G. Nelson, unpubl.). The rela- tively young age of the artificial reefs may have indirectly affected gray trig- gerfish diets, as significant changes occurred in later successional fouling de- velopment (Neth, 1991). Batistes capriscus is a successful early colonizer of artificial reefs (Frazer et aI., 1991) in the eastern Gulf of Mexico. Similarly, Randall (1963) noted Balistes vetula colonized an artificial reef in the Virgin Islands within I week of deploy- ment. Gray triggerfish colonized artificial reefs offshore from Vero Beach, Florida within 30 days of reef deployment (Vose, 1990). Gray triggerfish readily shift their diet to available prey items upon locating a new habitat. By being able to prey on many different foods, individuals can easily adapt their diet to changes in food availability which occur during early stages of development in fouling assemblages on artificial structure. In summary, diets of gray triggerfish collected on artificial reefs were markedly different from the diets of fish from natural substrate. Attached fauna are the main food of gray triggerfish on both artificial and natural substrate, which demonstrates the importance of reef-produced prey items for this species. 1322 BULLETIN OF MARINE SCIENCE. VOL. 55. NO, 2-3. 1994
ACKNOWLEDGMENTS
We would like to thank the following persons for field assistance: E, Olsen, R, Gurlek, J, Morton, B. Trocine, D. Charvat, Q. Fong, G, Collins, P. Navratil, R. Krause, M. Maher and B. Vose, Dr. S, Bell graciously provided computer and laboratory support We also thank Dr. W, Lindberg and J. Loftin for reviewing an earlier version of this manuscript. The field work for this project was funded in part by Florida Power and Light, and scientific liaison was provided by Dr. R. Wilcox. This research partially fulfilled the requirements for the Ph.D. degree in Oceanography at the Florida Institute of Technology.
LITERATURE CITED
Barshaw, D. E. and E. Spanier. 1994. Antipredator behaviors of the Mediten'anean slipper lobster, Scylla rides latus, Bull. Mar. Sci. 55: 375-382. Bohnsack, J. A. and D. L Sutherland. 1985, Artificial reef research: a review with recommendations for future priorities. Bull. Mar, Sci. 37: 11-39. ---and D. E. Harper. 1988, Length-wcight relationships of selected marinc recf fishes from the southeastern United States and the Caribbean. NOAA Tech Memo. NMFS-SEFC-215, 3 J pp. Dooley, J, K. 1972. Fishes associated with the pelagic Sargassum complex, with a discussion of the Sargassum community, Contr. Mar. Sci. 16: 1-32. Frazer, T. K., W. J. Lindberg and G. R. Stanton, 1991. Predation on sand dollars by gray triggerfish, Ba/istes capriscus, in the Northeastern Gulf of Mexico. Bull. Mar, Sci. 48: 159-164. Hobson, E, S. 1974. Feeding relationships of teleostean fishes on coral rcefs in Kona, Hawaii. Fish. Bull. 72: 915-1030. Hynes, H. B. N. 1950. The food of the freshwater sticklebacks (Gasterosteus acu/eatus and Pygosteus pungitius), with a review of the methods used in the study of the food of fishes. J. Anim. Ecol. 19: 35-38, Hyslop, E. J. 1980. Stomach contents analysis-a review of methods and their application, J, Fish BioI. 17: 411-429. Kalajian, E. H., I. W. Duedall, C. S. Shieh and J. R. Wilcox. 1989. SOAR (Stabilized Oil Ash Reef) performance: an ocean alternative to landfills, Proceedings of the 6th Symposium on Coastal and Ocean ManagementJASCE, Charleston, South Carolina. Pp, 1102-1115. Kortschal, K. 1989, Trophic ecomorphology in eastern Pacific blennioid fishes: character transfor- mation of oral jaws and associated change of their biological roles. Env. BioI. Fishes 24: 199- 218. Metz, S. and J. H. Trefry. 1988. Trace mctal considerations in experimental oil ash reefs. Mar. Poll. Bull. 19: 633-636. Nelson, R. S. 1988. A study of the life history, ecology and population dynamics of four sympatric reef predators (Rhomboplites aurorubens. Lutjanus campechanus, Lutjanidae; Haemu/on me/an- urwn, Haemulidae; and Pagrus pagrus, Sparidae) on the East and West Flower Garden Banks, Northwestern Gulf of Mexico, Ph,D. Dissertation, North Carolina State University, Dept of Zo- ology, Raleigh, North Carolina, Pp, 194-196. Nelson, W. G., P. M. Navratil, D. M. Savercool and F. E. Vose. 1988. Short-term effects of stabilized oil ash reefs on marine benthos. Mar. Poll. Bull. 19: 623-{)27. ---, D. M. Savercool, T. E. Neth and J. L. Rodda. 1994. A comparison of the fouling community on stabilized oil-ash and concrete reefs. Bull. Mar. Sci. 55: 1303-1315. Neth, T. E. 1991. Comparison of longterm development of fouling communities and benthic infauna between stabilized oil ash and concrete reefs. M.S. Thesis, Florida Institute of Technology, Dept of Oceanography and Occan Engineering, Melbourne, Florida. 184 pp. Pinkas, L., M. S. Oliphant and I. L K. Inverson. 1971. Food habits of albacore, blucfin tuna and bonito in California waters. Dept Fish, Game Cal., Fish. Bull. 152: 1-105. Randall, J, E. 1963. An analysis of the fish populations of artificial and natural reefs in the Virgin Islands. Carib. J. Sci. 3: 31-47. ---. 1967. Food habits of reef fishes of the West Indies, Stud, Trop. Oceanogr. (Miami) 5: 665- 847. Reinthal, P N., B, Kensley and S, M. Lewis. 1984. Dietary shifts in the queen triggerfish, Batistes vetula, in the absence of its primary food item, Diadema antil/arum, Mar, Ecol. 5: 191-195, Savercool, D. M. 1988. A comparative study of the fouling communities on oil ash block and concrete block reefs off Vero Beach, Florida. M. S. Thesis, Florida Institute of Technology, Melbourne, Florida. 47 pp. Sedberry, G. R. 1984. South Atlantic OCS area, living marine resources study, Phase III, Volume I. Marine Resources Research Institute, South Carolina Wildlife and Marine Resources Dept, Charleston, South Carolina. 223 pp. vaSE AND NELSON:GRAY TRIGGERFISHFEEDING 1323
Shipp, R. L. 1986. Guide to the fishcs of the Gulf of Mexico. Marine Environmental Sciences Consortium of Alabama, Mobile, Alabama. 256 pp. Vose, F: E. 1990. Ecology of fishes on artificial and rock outcrop reefs off the central east coast of Florida. Ph.D. Dissertation, Florida Institute of Technology, Dept. of Oceanography and Ocean Engineering, Melbourne, Florida. xi+ 140 pp.
DATE ACCEPTED: May 10, 1993.
ADDRESSES: (F.E. V. and w.G.N.) Department of Oceanography and Ocean Engineering. Florida lnsti1!lte of Technology. 150 W. University Boulevard, Melbourne, Florida 32901; PRESENT ADDRESS: (F.E. v.) Department of Fisheries and Aquatic Sciences. University of Florida, 7922 N. W. 71st Street. Gainesville. Florida 32606.