Diel distribution and site fidelity of Apogon imberbis in shallow rocky reefs in Corsica, France Patrick Webster, Kyle Swann, Michael Richtik-Rinaudo Abstract In the Mediterranean, only sparse information is available for temporal distributions of fish assemblages, particularly nocturnal ones, especially for shallow coastal habitats and rocky shores, where traditional fish surveying methods are impractical (Azzurro, 2007). One member of such assemblages is the cardinal fish Apogon imberbis (Perciformes: Apogonidae). Despite their prominence on reefs, Apogonids remain one of the least studied of the major families of reef fishes (Marnane and Bellwood, 2002). Given its abundance in the rocky reef and cave complexes of the Mediterranean, A. imberbis is a potentially important component of the nutrient flux into the food webs of these systems (Bussotti, 2002). While previous studies have established site fidelity in Apogonids on coral reefs, sometimes returning to their lairs from considerable distances (Marnane, 2000, Døving et al., 2006), no similar work has been done in the Mediterranean. Previous work shows that fish species inhabiting rocky crevices can have a significant impact on the import of nutrients into their resting environment, and the concentration of organic material in inshore rocky reefs (Bray, 1981 & 1986), and has been hypothesized on coral reefs (Marnane, 2000). Establishing the diel and homing behavior of A. imberbis could elucidate if similar ecological processes potentially occur in the Mediterranean. In this study we investigated both the diel distribution and site fidelity in A. imberbis in shallow rocky reefs around STARESO, Calvi, France during the month of October 2010. The presence of cardinal fish at the four study sites during the day was significantly greater than at night (χ 2, P << 0.001), with an average of 7.7 times more fish sighted during the day. The difference in distribution between day and night was not significantly different between any of the sampled sites (contingency analysis, α = 0.05, JMP 8). The distribution of A. imberbis around their lairs during the day was significantly different from the distribution of the fish at night (P = 0.03). They were predominantely associated with rocky substrate during the day (contingency analysis, P < 0.001), but utilized both rocky and P.oceanica substrates equally at night (χ 2, P = 0.38). Tagging of individual fish from showed that A. imberbis individuals are site specific on the level of the lair, and even to specific locations within that same lair, without effect from relocation. This study provides the first investigation of site fidelity of Apogonids in the Mediterranean, and the first study seeking to quantify the diel distribution of A. imberbis in the shallow rocky reefs of Corsica. Our results provide an important glimpse into the temporal patterns and behavior of A. imberbis, a first step towards understanding its potentially important ecological role in the shallow rocky reefs of the Mediterranean. Notes: This study represents the final project for the BIOE159 Marine Ecology of Corsica Field Quarter 2010, offered at UC Santa Cruz, presented by P.W., K. S., and M.R-R on December 11 th, 2010, in Santa Cruz, CA, based on research conducted at STARESO, Calvi, Corsica, France in October 2010. Introduction The study of fish community ecology has centered around three components to resource utilization and allocation namely trophic, spacial, and temporal patterns with a focus on the two former (Helfman, 1978). Temporal patterns, especially diel behaviors, are comparatively understudied, despite their importance for resource partitioning between members of fish communities (Helfman, 1978). In the Mediterranean, only sparse information is available for potential diel distributions, especially for shallow coastal habitats and rocky shores, where traditional fish surveying methods are impractical (Azzurro, 2007). With most research in these areas focusing on diurnal species, there is a distinct lack of data available on nocturnal fish assemblages (Marnane and Bellwood, 2002), and none in shallow rocky areas of the Mediterranean (Azzurro, 2007). One member of such assemblages is the cardinal fish Apogon imberbis (Perciformes: Apogonidae). Apogon imberbis is one of the most common fish in the rocky reef and shallow cave habitats of the Mediterranean, accounting in some instances for 85% of fish in shallow marine caves (Bussotti, 2002). Most Apogonids that have been studied are distinctly nocturnal (Hobson, 1965, Helfsman, 1978). However, while the nocturnal behavior of A. imberbis was first introduced over 40 years ago (Bussotti, 2003), much of the data available for the ecology of the species is anecdotal within the context of broader studies (Bussotti, 2003). Despite their prominence on reefs, Apogonids remain one of the least studied of the major families of reef fishes (Marnane and Bellwood, 2002). Given its abundance in the rocky reef and cave complexes of the Mediterranean, A.
imberbis is a potentially important component of the nutrient flux into the food webs of these systems (Bussotti, 2002). Previous work shows that fish species inhabiting rocky crevices and openings in the reefs ( lairs ) can have a significant impact on the import of nutrients into their resting environment, and the concentration of organic material in inshore rocky reefs (Bray, 1981 & 1986). It has also been suggested that Apogonids may increase energy and nutrients in the form of fish biomass and feces at specific, predictable sites in coral reefs (Marnane and Bellwood, 2002) influencing predator and detritivore communities (Marnane, 2000). While previous studies have established site fidelity in Apogonids on coral reefs, sometimes returning to their lairs from considerable distances (Marnane, 2000, Døving et al., 2006), no similar work has been done in the Mediterranean. One such study showed that A. imberbis will move from inside a cave to its entry at night (Bussotti, 2003), but its behavior over open rocky reefs is unknown. Establishing the diel and homing behavior in A. imberbis could elucidate if similar processes of nutrient concentration in daytime refuges by nocturnal species found in coral reef systems occur in Mediterranean rocky reefs. In this study we investigated both the diel distribution and site fidelity in A. imberbis. We tested three questions that could help to increase our knowledge of the potential ecologic impact of this abundant Mediterranean fish: 1. Is there a marked difference in distribution of A. imberbis between night and day? We hypothesized that A. imberbis will be Figure 1: Map of research area and overview of study sites, marked by flags. Distance from Jetty to Cave Complex is approximately 110m. Shaded area marks sample area around Cave Complex and Hotel (Google Earth, 2010).
found in higher numbers inside of lairs during the day than at night. 2. Do A. imberbis move away from the lair at night to forage, and do they display pronounced substrate specificity for foraging? We hypothesized that A. imberbis will be found further from the lairs at night than during the day, and that they would predominately venture over P. oceanica beds, based on our preliminary observations. 3. Are individual fish site specific? We hypothesized that individual fish will be site-specific, returning to the same lairs every day after foraging. STUDY SPECIES Material and Methods Apogon imberbis is widely distributed on rocky reefs throughout the Mediterranean and Eastern Atlantic, from Morocco to the Gulf of Guinea, including the Azores (Tortonese, 1975). It lives as a solitary individual or in large schools, and inhabits crevices in rocky reefs and marine caves during the day from shallow waters to depths of 200 meters (Bussotti 2003). STUDY SITE This study was conducted in Revellata Bay near Calvi, Corsica, France at STARESO (Université de Liège) from October 5-27 2010. The bay hosts rocky reefs and P. oceanica beds in shallow waters to 15+ meters. Our study area was focused on the North side of the STARESO jetty, from inside the harbor mouth to 120m North along the coast (Figure 1). This area is characterized by both natural and artificial hard substrate rocky reefs with cracks, crevices and caves sloping down from cliffs above, while extensive meadows of P. oceanica stretch from the rocks at approximately 8m depth. Four sites with recurrent Apogon individuals were identified (Figure 1): Cave Complex, a swim-through ( Cave ) located 100m from the harbor with two main chambers, a roof at 8 meters, and openings at 10 meters, coupled with a collection of cracks and crevices down a gulley from the cave towards the P. oceanica beds from 11m to 15m depth; Hotel, a collection of a few large boulders forming caves 60 meters from the harbor at the base of the rocky slope/p. oceanica junction at 8m depth; Jetty, a cave formed from the artificial boulders immediately off the cement platform on the North side of the STARESO harbor at 7m depth; and Harbor, a collection of cracks inside the harbor 20 meters from the diver s ladder. DIEL DISTRIBUTION Fish counts of all adult individuals at the four lairs were conducted in the morning or afternoon for daytime counts on 16 days from 10/7 to 10/25, and 8 nights from 10/9 to 10/22, while freediving or on SCUBA. Both during the day and at night, behavioral observations of cardinal fish were recorded at and between each lair. DISPERSAL AND SUBSTRATE SPECIFICITY The two most populous lairs, the Cave Complex and the Hotel, were chosen as sites to conduct transects. These sites were ideal because of their large number of regularly occurring adult fish, as well as the heterogeneity of the substrate surrounding the lair. The total area surveyed around the Hotel and Cave was 780m 2 (390m 2 at each site). A central transect (30m x 13m) was run down the middle of the areas, during the day and night at each site, on SCUBA. Apogon imberbis numbers and the substrate they were found over were recorded from the central lair, marking the center of the area, in 5m increments (0-5m, 5-10m, 10-15m). Fish were counted by a buddy team of divers, splitting
the area in two, each diver conducting a 30m x 6.5m transect. SITE FIDELITY We tagged fish using 3-4 multicolored beads threaded on monofilament line. Individuals were collected during the day at the Cave Complex using hand nets and brought to the surface, where two needles were pushed through the muscle in front of the first dorsal spine and a double overhand knot tied with the ends of the line to secure the tag. A total of 35 fish were captured and tagged in three tagging sessions. Different color combinations of beads were used to differentiate between individual fish, with one bead identifying the location of release (black for North, white for South). One fish caught near the Cave Complex was tagged with a different scheme, as it inhabited a specific crack which only had one fish sighted in it the entire study duration, dubbed Special. 10 fish and Special were immediately released back at their point of capture. A total of 12 fish were released North of the Cave Complex, six 30m away and six 75m away, in areas with conspecfics. Another 12 fish were released South, six at the Hotel 56m away, the rest at the Jetty 110m away. Resights were conducted subsequently the rest of the month, totaling 8 days, on SCUBA. Results DIEL DISTRIBUTION The presence of cardinal fish at the four lairs during the day was significantly greater than at night (χ 2, P << 0.001), with an average of 7.7 times more fish sighted during the day. The difference in distribution between day and night was not significantly different between any of the sampled sites (contingency analysis, α = 0.05, JMP 8) (Figure 2). DISPERSAL AND SUBSTRATE SPECIFICITY The distribution of A. imberbis around their lairs during the day was significantly different from the distribution of the fish at night, both at the Cave Complex (χ 2, P = 0.03) and at the Hotel (χ 2, P = 0.014). Fish radiated outwards from their respective lairs at night, with 28% of fish at the Cave Complex and 35% of fish at Figure 2: Frequency of fish observed at each study site between day (blue columns) and night (black columns). A. imberbis showed a significant preference for refuge in lairs during the day (P << 0.001). The difference between night and day counts was not significantly different between any of the four sites based on contingency analyses (α = 0.05, JMP 8).
Figure 3: Frequency of fish in 5 meter increments around Cave Complex (A) and Hotel (B) during day (blue columns) and night (black columns). The distributions were significantly different between day and night at the Cave (P = 0.03) and Hotel (P = 0.018). Figure 4: Frequency of fish observed over rocky substrate (grey columns) and P. oceanica (green columns) during day and night, with data from the Cave and Hotel combined. Rocky substrate was utilized more than P. oceanica during the day (P << 0.001). No significant difference was observed between substrates at night (P = 0.38) the Hotel found 10-15m away, compared to just 7% and 6% respectively during the day (Fig. 3A-B). They were predominantely associated with rocky substrate during the day (contingency analysis, P < 0.001), but utilized both rocky and P.oceanica substrates equally at night (χ 2, P = 0.38) (Figure 4). SITE FIDELITY Of the 11 fish that were released back at the Cave Complex ( In Place ), 4 were resighted the next day, including Special in the crack it was originally found in. An average of 40% of In Place fish were resighted the rest of the study, with a high of 6 and low of 3. The Special tagged fish was seen every day, except the last, in the same crack until the end of the study. Of the 12 fish tagged individually and released away from the Cave, 56m South and 30m North (N/S 1), all 12 were resighted in the Cave, including 11 the next day, with all 6 Southern fish and 5 of the Northern fish. The next day, the one Northern fish missing from the previous day was seen back at the Cave. An average of 67% of N/S 1 fish were seen back at the cave the rest of the study. Of the 12 fish that were released twice as far the next day, N/S 2, 8 were seen back at the Cave the next day, including 5 of the 6 Southern fish and 3 of the 6 Northern fish. By the end of the study, all 6 N/S 2 Southern fish were resighted, and 4 of the 6 N/S 2 Northern fish. An average of 64% of N/S 2 fish were seen in the Cave the rest of the study (Figure 5). When investigating the site specificity of the individual fish within the Cave itself, 10 of 11 identifiable fish
Figure 5: Frequency of tagged fish resighted at Cave Complex over time. No data was collected on 10/26 due to a mandatory rest day. (without scars) were resighted and located in the Cave. All except one were seen in the same chamber within the Cave, in the same general vicinity of their previous location over a two day period. Discussion DIEL DISTRIBUTION As expected of a nocturnal species (Hobson, 1965, Helfman 1975, Bussotti, 2002), A. imberbis were seen in much higher numbers in lairs during the day than at night. Interestingly, each site had similar differences of fish abundance between night and day, implying that the lair itself its size, location, depth, the number of fish that live there, or other factors did not significantly influence the dispersal of the fish at night. A. imberbis thus behaved very similarly from lair to lair, validating our assimilation of data from the Cave Complex and the Hotel to investigate substrate specificity and the dispersal of the fish from their lairs. DISPERSAL AND SUBSTRATE SPECIFICITY As we anticipated, fish radiated away from their lairs to forage at night. Previous work showed that A. imberbis appears to move a considerable distance from their refuge deep within caves at night, but stayed close to the entrance (Bussotti, 2003). Our results show that A. imberbis can and will forage individually and exposed far from their refuge substrate, like their coral reef counterparts (Marnane and Bellwood, 2002). During our preliminary observational work, A. imberbis were seen to forage over both rocky substrate and P. oceanica at night, though we hypothesized P. oceanica would form their predominant foraging ground, due to its abundance around our research areas. Our data suggest that these fish showed no substantial spacial bias for any particular microhabitat at night for their foraging bouts, contrary to our expectations, though in line with certain Apogonid species on coral reefs (Marnane and Bellwood, 2002). Anecdotal observations at night showed that A. imberbis were never seen much above the sea grass beds or rocky reef in the water column, unlike some other Apogonids (Marnane and Bellwood, 2002), but no formal attempt was made to investigate their vertical distribution. SITE FIDELITY Our results show that A. imberbis are site specific, like other Apogonids in coral reefs in Australia and Japan (Kamawura, 1985, Okuda
and Yanagisawa, 1996, Marnane, 2000, Marnane and Bellwood 2002). Tagging of individual fish from the Cave Complex showed that A. imberbis individuals are site specific on the level of the lair, and even to specific locations within that same lair. The Special tagged fish was a clear example of this precise homing behavior. One of the first fish caught and released back to a specific crack in the Cave Complex, Special was resighted there over a two week period, while leaving this lair at night. Mortality associated with tagging was difficult to quantify, as the disappearance of fish could have been due to the tagging and handling of the fish, selective predation on tagged individuals, as well as tag loss, emigration, or natural mortality (Marnane, 2000). Because only 6 of the 11 fish that were tagged and immediately released back at the Cave Complex were resighted subsequently, the mortality due to the tagging process may have been substantial in our study, at least in the first round of tagging. However, at least four of the original tagged fish were still alive two weeks after tagging, ensuing groups of tagged fish had much better survival - especially N/S 1, with 100% of fish resighted two days after tagging - and several fish were observed behaving normally with scars from detached tags. The release distance from the Cave did not influence the number of fish resighted back at the lair, with A. imberbis individuals foregoing suitable habitat containing conspecifics to return to their original lair, a behavior also noted in Apogonids in coral reefs (Marnane, 2000). A few fish were seen back in the Cave with scars from tagging, confounding whether we were observing fish that we had resighted previously or stragglers that had reappeared. A. imberbis appeared to be very territorial even within the Cave, many times facilitating their capture, as the placeholder would chase the other fish into awaiting nets. With 91% of fish observed over a two-day period remaining in the same location within the Cave, no matter their release distance, a complex process of homing in A. imberbis is apparent. SUMMARY AND FUTURE WORK This study provides the first investigation of site fidelity of Apogonids in the Mediterranean, and the first study seeking to quantify the diel distribution of A. imberbis in the shallow rocky reefs of Corsica. This study complements research done on the temporal patterns of A. imberbis in other regions of the Mediterranean (Bussotti, 2003), while providing a broader spatio-temporal view of the diel migration of A. imberbis in a previously unexamined environment (Azzurro, 2007). Moreover, diel behaviors in fishes are often species-specific (Arrington, 2003), making the study of such patterns in individual species, especially understudied nocturnal species (Marnane and Bellwood, 2002), an important step towards a broader understanding of temporal shifts in rocky reef assemblages. This study also serves as a first glimpse into the diel behavior of A. imberbis mirorring other Apogonid species in coral reefs (Marnane 2000). It is therefore likely that A. imberbis perform a similarly important ecological role in the concentration of biomass, recycling, and import of nutrients into their home refuges in the Mediterranean, as hypothesized in coral reefs (Marnane 2000, Marnane and Bellwood, 2002). With the possibility that Apogonids spend the majority of their adult life in the same refuges (Marnane 2000), and our results showing their precise homing within lairs themselves, A. imberbis individuals may have a significant effect on the detritivore and predator community structure of the reefs (Marnane, 2000), while providing a predictable source of nutrients for their individual rest sites (Bray, 1981 & 1986).
Future work should be done to establish the range that A. imberbis cover at night, perhaps using internal acoustic implants, a method employed in numerous studies of diel behavior (cf. Poulet et al., 2004, March et al., 2010). This method would allow precise, passive monitoring of range and dispersal rate in these fish. Future work should also be done to investigate nutrient intake by A. imberbis into their reef systems - using stomach content analysis and laboratory experiments (cf. Bray, 1986). This study provides complimentary data to the study of nutrient flux and the trophic impact of Apogonids on their daily rest sites in the Mediterranean (Bussotti, 2003), by establishing complex homing behavior in A. imberbis (Marnane, 2000, Marnane and Bellwood, 2002). We also provide new data on the diel behavior of A. imberbis, an important component of nocturnal fish assemblages in an overlooked environment (Azzurro, 2002, Bussotti, 2002, Bussotti, 2003). Hence, this study provides an important glimpse into the temporal patterns and behavior of A. imberbis, a first step towards understanding its potentially important ecological role in the shallow rocky reefs of the Mediterranean. Acknowledgements We would like to thank the staff at STARESO for their hospitality and equipment, both of which were instrumental in the success of this project. We would also like to thank Desirée Davis for her assistance with the tagging procedures. We are indebted to the BIOE159 instructors, Pete Raimondi and Giacomo Bernardi (and son), as well as to our TAs Jimmy O Donnell, Brenna Mahoney, and Alexis Jackson, for their guidance, wisdom, and assistance on this project. Works Cited Arrington, D.A., and Winemiller, K.O. (2003) Diel changeover in sandbank fish assemblages in a neotropical floodplain river, Journal of Fish Biology 63, 442-459 Azzurro, E., Pais, A., Consoli, P. and Andaloro, F. (2007) Evaluation day-night changes in shallow Mediterranean rocky reef fish assemblages by visual census, Marine biology 151, pp 2245-2253 Bray, R.N., Miller, A.C., and Geesey, G.G. (1981) The Fish Connection: A Trophic Link between Planktonic and Rocky Reef Communities?, Science, New Series, Vol. 214, No.4517, pp 204-205 Bray, R.N., Purcell, L.J. and Miller, A.C. (1986) Ammonium excretion in a temperate-reef community by a planktivorous fish, Chromis punctipinnis (Pomacentridae) and potential uptake by young giant kelp, Macrocystis pyrifera (Laminariales), Marine biology 90, pp 327-334. Bussotti S, Denitto F., Guidetti P., Belmonte G., (2002) - Fish assemblages of shallow marine caves in the Salento Peninsula (Southern Apulia., SE Italy). P.S.Z.N. Mar. Ecol., 23 (suppl.): 11-20. Bussotti, Simona, Guidetti, Paolo and Belmonte, Genuario (2003) 'Distribution patterns of the cardinal fish, Apogon imberbis, in shallow marine caves in southern Apulia (SE Italy)', Italian Journal of Zoology, 70: 2, 153 157 Charbonnel, E., Serre, C., Ruitton, S., Harmelin, J.G., and Jensen, A. (2002) Effects of increased habitat complexity on fish assemblages associated with large artificial reef units (French Mediterranean coast). ICES Journal of Marine Science, 59: S208 S213. Doving, Kjell B., Stabell, Ole B., Ostlund-Nilsson, Sara and Fisher, Rebecca (2006) Site Fidelity and Homing behavior in coral reef cardinal fish: Are they using olfactory Cues?, Chem. Senses 31: pp 265-272 Helfman, Gene S. (1978) Patterns of community structure in fishes: summary and overview, Env. Biol. Fish. Vol. 3, No. 1, pp. 129-14 Hobson, Edmund S. (1965) Diurnal-Nocturnal Activity of some Inshore Fishes in the Gulf of California Copeia, Vol 1965, No. 3, pp 291-302 Kuwamura, Tetsuo (1985) Social and reproductive behavior of three mouthbrooding cardinalfishes, Apogon doederleini, A. niger and A. notatus, Environmental Biology of fishes, Vol. 13,No. 1, pp 17-24 March, D., Palmer, M., Alos, J. Gran, A., and Cardona, F. (2010) Short-term residence, home range size and diel patterns of the painted comber Serranus scriba in a temperate marine reserve, Marine Ecology Progress Series, Vol. 400: pp 195-206 Marnane, M.J. (2000) Site fidelity and homing behavior in coral reef cardinal fishes, Journal of fish biology 57, 1590-1600 Marnane, M.J. and Bellwood, D.R. (2002) Diet and Nocturnal foraging in cardinalfishes (Apogonidae) at One Tree Reef, Great Barrier Reef, Marine Ecology Progressive Series, Vol. 231, pp. 261-268 Okuda, N. and Yanagisawa, Y. (1996) Filial cannibalism by mouthbrooding males of the cardinal fish, Apogon doederleini, in relation to their physical condition, Environmental Biology of Fishes 45: 397-404 Poulet, N., Arzel, C., Menad, S., Lek, S. and Arigellar, C. (2005) Diel Activity of adult pike perch Sander lucioperca(l.) in a drainage canal in the Meditterranean basin during spring, Hydrobiolgia 543: pp 79-90