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Predator-prey interactions between the corallivorous snail Coralliophila abbreviata and the carnivorous deltoid rock snail Thais deltoidea.

Coral reefs in the Florida Keys have become highly degraded in recent decades, prompting efforts to reestablish populations of vital reef-accreting corals to restore reef structure and ecological function. However, predation on these corals by the corallivorous gastropod Coralliophila abbreviata has been a substantial and chronic impediment to these restoration efforts. We conducted laboratory experiments to determine whether Thais deltoidea, a carnivorous gastropod that commonly occurs with C. abbreviata, is a predator of C. abbreviata. We demonstrated that T. deltoidea readily preys upon C. abbreviata and preferentially targets smaller individuals, a foraging behavior that may optimize the energy gained due to reduced handling and consumption times. If this trophic relationship proves ecologically relevant, understanding the predator-prey dynamics between these species could ultimately aid in the development of a comprehensive coral reef restoration strategy for Florida.

Coral reefs in the Florida Keys, like those elsewhere in the Caribbean, have progressively degraded in recent decades due to a wide range of stressors (1). Staghorn coral Acropora cervicornis (Lamarck, 1816), and elkhorn coral Acropora palmata (Lamarck, 1816), in particular, have undergone a precipitous decline that has culminated in these species being listed as threatened under the U.S. Endangered Species Act (2). These coral species are fundamental to a healthy coral reef ecosystem, as they are particularly important for the accretion of new reef and provide structural habitat for a variety of fishes and invertebrates. Their reestablishment is now widely viewed as the first step in attempts to restore Florida's reefs. A concerted effort is being directed at restoring depleted acroporid coral populations using primarily A. cervicornis colonies propagated within a network of nurseries established along the south Florida reef tract (3). Predation by the corallivorous gastropod Coralliophila abbreviata (Lamarck, 1816), however, has profoundly affected the health and survival of the nursery-propagated colonies as well as the remnant wild colonies (4, 5, 6). In addition to the effects of its predation, C. abbreviata can introduce disease among colonies of both A. cervicornis and A. palmata (7). Direct removal has been suggested as a necessary measure to ensure both the survival of transplanted nursery colonies and the persistence of wild coral recruits (8, 9, 10). Although this method has been proven to reduce the impact of predation by C. abbreviata at the level of individual acroporid coral colonies, it would undoubtedly prove to be prohibitively labor-intensive for large-scale restoration (10). Therefore, the development of a comprehensive coral reef ecosystem restoration strategy, which includes the restoration of acroporid coral colonies on a large scale, must also address the effects of predation by C. abbreviata.

Very little effort has been directed at examining potential predators of C. abbreviata, and nothing is known about how predation upon C. abbreviata affects coral reef community structure. The only quantitative evaluation of predation on C. abbreviata of which we are aware is a laboratory study that demonstrated that the Caribbean spiny lobster Panulirus argus (Latreille, 1804) had great difficulty consuming even the average size C. abbreviata inhabiting Florida Keys reefs (11). The snapping shrimp Synalpheus fritzmuelleri Coutiere, 1909, has been observed to prey on a congener of C. abbreviata (12), and suggested predators of C. abbreviata include tetraodontid fishes and octopuses (6).

Thais deltoidea (Lamarck, 1822) is a carnivorous gastropod that preys on other molluscs and commonly occurs with C. abbreviata on high-relief, spur-and-groove reefs in the Florida Keys (13, 14), yet little is known about its role in the trophic structure of coral reef ecosystems. Because this snail is a potential predator of C. abbreviata, the extent to which this trophic interaction may influence local abundance of C. abbreviata merits further investigation to broaden our understanding of how this trophic interaction potentially affects coral reef ecosystem function and resiliency. Herein, we detail our observations of the predator-prey dynamics between T. deltoidea and C. abbreviata in the laboratory. We describe the basic feeding technique of T. deltoidea on C. abbreviata and quantify its size-specific and seasonal feeding rates.

We opportunistically collected T. deltoidea and C. abbreviata from along the Florida Keys reef tract from October 2012 through July 2013. Individuals were maintained in our laboratory (segregated by species) in 356-1 rectangular tanks in a flow-through seawater system. We conducted 34 predator-prey trials from November 2012 through August 2013. Each trial was conducted in a 21-1, closed-system glass tank (20 cm W x 40 cm L x 25 cm H) maintained at ambient seasonal water temperatures, salinities, and natural light-dark cycles; a data logger (HOBO Model UA-002-64, Onset Computer Corp., Bourne, MA) was used to record temperature. For each trial, one T. deltoidea and four different-sized C. abbreviata were placed in a tank for 30 d or until all the C. abbreviata had been consumed. Although the absolute densities of both species in our trials exceeded those reported in the wild, the relative densities approximated wild densities (14). T. deltoidea individuals were used in one trial only. During the course of our trials, we sometimes did not have enough untried C. abbreviata; hence, to ensure that we had enough prey individuals, those that had survived a trial were returned to a common pool of similar-sized individuals and possibly were used in subsequent trials. Though these individuals were not naive, the small size of the tanks in which the trials were conducted greatly reduced the effects of any escape behavior that prey individuals might have exhibited. Consequently, we are confident that reusing these individuals did not meaningfully affect our results. The 34 T. deltoidea individuals used in the trials ranged in size from 19.1 mm siphonal length (SL; the distance from the apex to the tip of the siphonal canal) to 44.8 mm SL (mean [+ or -] 1 SE = 33.0 [+ or -]1.1 mm SL). The 136 C. abbreviata individuals ranged from 9.5 mm to 38.9 mm SL (mean [+ or -] 1 SE = 19.5 [+ or -] 0.52 mm SL). The size ranges of both species bracketed the size ranges reported for the Florida Keys reef tract (14, 15). In each trial, the largest of the four C. abbreviata was approximately equal in SL to the T. deltoidea. We observed each trial daily during daylight hours and recorded any predation that had occurred since the previous observation. We defined a predation event as aperture-to-aperture contact (16) between individuals of T. deltoidea and C. abbreviata. A predation event was deemed successful or unsuccessful after the T. deltoidea individual had disengaged from the C. abbreviata individual. A predation event was considered successful if the C. abbreviata individual had been consumed, leaving the empty shell and operculum. A predation event was considered unsuccessful if the C. abbreviata individual was alive after the T. deltoidea individual disengaged from it. For each predation event, we recorded the SL of both snails and the consumption time of successful predation events (i.e., days from engagement to disengagement).

These predator-prey trials clearly demonstrated that Thais deltoidea readily prey upon Coralliophila abbreviata under our laboratory conditions. We observed at least one attempted predation event in 27 of the 34 trials (79.4%). In 12 of the 27 trials (44.4%), T. deltoidea consumed all four of the C. abbreviata. Among the 27 trials, we observed 73 successful and 10 unsuccessful predation events, although we acknowledge that some additional unsuccessful predation events may have occurred overnight between observations. T. deltoidea exhibited size-specific, prey selection behavior, as they clearly targeted the smaller individuals of C. abbreviata first (Fig. 1A). In addition, the relative difference in SL between T. deltoidea and C. abbreviata influenced the probability of a successful predation event (Fig. 1B). Not surprisingly, the larger the C. abbreviata prey, the longer it took the T. deltoidea to consume it (Fig. 2). The mean ([+ or -] 1 SE) consumption time of successful predation events was 2.85 d ([+ or -] 0.15), and consumption times ranged from 1 to 5 d. This behavior was similar to that which was observed in an intertidal congener of T. deltoidea, which exhibits size- and species-specific predation behavior that presumably maximizes energy gained per unit of handling time (17). It is reasonable to expect that T. deltoidea also exhibits this optimal foraging behavior and preferentially targets smaller C. abbreviata individuals, which would reduce consumption time. But our results also suggest that C. abbreviata may attain a size-related release from predation by T. deltoidea, although we note that T. deltoidea can grow larger than the largest individuals used in our experiment (14). We also suspect that T. deltoidea can probably distinguish between prey species, so we do not yet know if C. abbreviata is a preferred prey item.

The frequency of predation events and the consumption times of successful ones varied seasonally. Predation rates during trials conducted from June through August 2013 (mean [+ or -] 1 SE water temperature = 27.5 [+ or -] 0.8 [degrees]C) were more than four times greater than those in trials conducted from October 2012 through April 2013 (mean [+ or -] 1 SE water temperature = 22.3 [+ or -]1.0 [degrees]C) (Fig. 3A). Consumption time was also significantly shorter during the trials conducted in the warmer months (Fig. 3B). Such seasonal differences in the feeding rates of gastropods have been reasonably well documented and are associated with temperature-related physiological energetics (18). Water temperatures in our seawater system during trials conducted during June-August were similar to those at a site on the offshore reef tract (mean [+ or -] 1 SE = 27.0 [+ or -] 0.6 [degrees]C). Water temperatures in our system during October-April were slightly lower than those we measured on the reef tract when we conducted the trials during those months (mean [+ or -] 1 SE = 25.4 [+ or -] 1.0 [degrees]C). Consequently, the water temperatures under which we conducted our trials from October through April may have exacerbated the differences in seasonal predation rates that might characterize this predator-prey relationship on the Florida reef tract.

Although our results suggest that T. deltoidea can prey upon C. abbreviata in the laboratory, our findings do not allow us to answer a host of questions about the occurrence and/or nature of this interaction in the wild, nor to which extent it may shape the coral reef community, in particular, the ability to reduce predation on scleractinian coral by C. abbreviata. Our observations suggest a size-related and seasonal component to this trophic dynamic, but they likely only hint at the complexity of the relationship. Predator-prey dynamics, particularly those in systems with high trophic connectivity, are shaped by numerous direct and indirect mechanisms (17, 19, 20) that we did not test. In addition to the complex prey-selection behavior that gastropods display, this trophic relationship is probably also shaped by the complexity of the coral reef habitat, which directly affects encounter rates (21). Synoptic surveys of the benthic fauna along the Florida Keys reef tract revealed that the two species commonly occupy different areas in the same coral reef habitat (14). C. abbreviata was most often observed near or on coral colonies, whereas T. deltoidea was most commonly seen on algal turf-covered reef substrate (14). Nevertheless, on a few occasions we have observed both species occupying the same Acropora cervicornis colonies; and in one instance, we noted T. deltoidea actively preying on a C. abbreviata on a colony (Fig. 4).

Although our laboratory and in situ observations have yielded intriguing insights into the trophic dynamics of these two species, evaluating the nature of this relationship will require further in-depth experimentation to elucidate how and to which extent this relationship may shape the function of coral reef ecosystems. If it proves ecologically relevant, it has important implications for the rapidly expanding coral reef ecosystem restoration projects in south Florida. These restoration efforts have largely focused on restoring reef structure by outplanting coral (primarily A. cervicornis) that has been propagated and grown in a network of coral nurseries along the south Florida reef tract. But these efforts have been undertaken largely without directly addressing critical ecological processes fundamental to coral reef ecosystem function. Predation and disease-induced mortality on outplanted corals caused by C. abbreviata are two such processes that have proved particularly challenging (7, 8, 9, 10). Factors that could mitigate these impacts must be addressed if coral restocking is to prove successful. If T. deltoidea can indeed mitigate the effect of predation by C. abbreviata on corals in the wild, it could be used in coral reef restoration to enhance survival of corals, either by allowing restorers to outplant corals in locations with a naturally high abundance of T. deltoidea, or--if the strategy proved ecologically unsound--by enhancing its abundance at restoration sites through translocation. Ultimately, the manipulation of the trophic relationship between Thais deltoidea and Coralliophila abbreviata could constitute a significant component of a comprehensive coral reef restoration strategy for Florida.

Acknowledgments

This project was funded by the Florida Fish and Wildlife Conservation Commission. We thank John Hunt, Steve Geiger, Kate Lunz, Bland Crowder, and anonymous reviewers who contributed valuable insights that improved the manuscript.

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WILLIAM C. SHARP (*) AND GABRIEL A. DELGADO

Florida Fish and Wildlife Conservation Commission, Fish and Wildlife Research Institute, 2796 Overseas Highway, Suite 119, Marathon, Florida 33050

Received 27 May 2015; accepted 13 July 2015.

(*) To whom correspondence should be addressed. E-mail: bill.sharp@myfwc.com
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Author:Sharp, William C.; Delgado, Gabriel A.
Publication:The Biological Bulletin
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Date:Oct 1, 2015
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