Behavioral Ecology of Coral Reef Fishes at Spawning

Coral reef fishes aggregate to spawn on certain locations of reefs. This thesis is an extensive investigation of the behavioral and ecological relations between spawning reef fishes, predators and their environment at a spawning aggregation site. Many hypotheses have been proposed regarding the adaptive nature of different diel reproductive cycles observed in coral reef fishes. This study quantified the spawning patterns of eleven different reef fish species at one location (Johnston Atoll, Central Pacific), while making simultaneous measurements of the environmental factors likely to affect the spawning behavior of reef fishes. The environmental variables measured included time of day, tides, current velocity, current speed and abundance of piscivorous predators, and were correlated with observed spawning outputs through multifactorial analyses. High interspecific variability in spawning patterns was found among the eleven monitored species. The majority of species spawned at a specific time of the day, in agreement with the timing of spawning described at other locations, indicative of a fixed general response by fishes across distribution areas. Spawning of most fishes with daytime spawning peaks was correlated with local changes in current direction and predatory risks, showing responses designed to reduce the mortality of propagules and adults. Dusk-spawning species generally did not respond to changes in flow direction and predator abundance, most likely due to their short spawning periods and the reduced predatory pressures that occurred at dusk. Tides did not seem to be used exclusively as synchronizing cues to adult fishes for spawning. The influence of current speed in determining diel timing of spawning varied among species, with some species showing responses to current speed while others showed no response. Predation is a selective force hypothesized to influence the spawning behavior of coral reef fishes. This study describes and quantifies the predatory activities of two piscivorous and three planktivorous species at a coral reef fish spawning aggregation site in Johnston Atoll (Central Pacific). To characterize predator-prey relations, the spawning behavior of prey species was quantified simultaneously with measurements of predatory activity, current speed and substrate topography. Diel activity patterns and predator-prey relations varied among the predatory species analyzed. The activity patterns of piscivores, measured both as abundance and attack rates, were high during the daytime, decreased during the late afternoon hours and reached a minimum at dusk. The abundance of piscivores was significantly correlated with the abundance of prey for only one (Caranx melampygus) of the two piscivorous species, while the other species (Aphareusfurca) did not respond to prey abundance. The selection of certain prey species by piscivores was consistent with two different hypotheses: the satiation of predators and the differences in spawning behaviors among prey species. Two of the three planktivorous species fed most actively at dusk, and selected as prey those species of reef fishes that produced eggs of large size. The third planktivorous species fed at all times of the day. Spawning prey fishes were more abundant over substrates with complex topography where refuges from piscivores were abundant than over smooth substrates. Overall attack rates by piscivores on adult spawning fishes were higher than by planktivores feeding on recently released eggs. The diel spawning patterns displayed by reef fishes at the study site seem to be influenced by the diel activity and prey selection patterns of piscivores previously described. The highest diversity of prey species occurred at dusk, when piscivores were least abundant and overall abundance of prey fishes was lowest. The behavioral strategies used by the piscivore Caranx melampygus (Carangidae) while feeding on spawning aggregations of coral reef fishes were studied for two years at Johnston Atoll (Central Pacific). Visual behavioral observations revealed the existence of two different hunting behaviors employed by this predator. A 'midwater' hunting behavior, which consisted of midwater high speed attacks on spawning fishes, is typical of large sized transient predators and yielded a low capture success rate (2 %). An 'ambush' hunting behavior consisted of attacks on spawning fishes from hiding locations in the substrate, and yielded a much higher capture success rate (17 %). While ambushing their prey, C. melampygus displayed territorial aggressive behaviors toward other intruding conspecifics, defending a specific section of the reef. This specialized ambushing behavior is atypical of fast swimming carangids, but illustrates the behavioral flexibility of this predator. I suggest that the use of these two hunting behaviors by C. melampygus can potentially cause density-dependent mortality rates in prey communities, a demographic consequence previously attributed to the simultaneous action of various guilds of predatory species. Two species of trunkfishes (Ostraciidae) were observed spawning above a coral reef at Johnston Atoll (Central Pacific). This study analyzed the potential causes determining the difference in spawning ascent height in Ostracion meleagris (3.3 m average) and 0. whitleyi (1.5 m average). One hypothesis proposes that the risk of predation by piscivores influences how far each species can swim from the substrate, and that predation risk is greater for 0. whitleyi than 0. meleagris. Trunkfishes have an armoured exoskeleton and secrete an ichthyotoxic mucous under stress conditions, two defenses against predation. Because the two species used the same spawning grounds and spawned at approximately the same time, their size and toxicity levels were analyzed to assess their susceptibility to predation. Toxins were extracted from wild fishes and tested using a mosquitofish assay. Ostracion whitleyi was more toxic than 0. meleagris, refuting the predation-risk hypothesis. A second hypothesis proposes that long ascents are a way for spawning pairs to avoid disturbances by other male conspecifics. Observations of the spawning behaviours of the two species showed that male 0. meleagris were frequently involved in fighting episodes and showed high rates of male streaking (intruding nonpaired males attempting to fertilize eggs from spawning paired females), while none of these behaviours were observed in 0. whitleyi. The larger spawning height from the substrate may be an attempt by pairs of 0. meleagris to reduce the possibility of interference by other male conspecifics. Thus, the height of spawning ascents corresponds to the expectation from the male disturbance hypothesis, but not to the expectation of the predatory risk hypothesis. Thesis Supervisor: Lauren S. Mullineaux Title: Associate Scientist, Woods Hole Oceanographic Institution Acknowledgments At the present time my thesis has been written, defended and corrected. Six years of hard work have come to an end, and it is time to look back and acknowledge all the people who helped me in one way or another with my research and my life. I hope to not miss too many people, since there were so many of you who helped me pursue my dreams of becoming a marine ecologist. I have a large thesis committee, so bear with me. My advisor, Lauren Mullineaux, taught me all I know about the scientific method and encouraged me to move ahead with my research during obscure moments. Without her, I would have never finished this work. Phil Lobel gave me the opportunity of coming to WHOI, becoming a field ichthyologist and to work on Johnston Atoll. Judy McDowell was always a phone call away when I needed her, calm and optimistic. Andy Solow achieved what four different university courses were never able to accomplish, teach me statistics. Maybe the combination of infinite patience on his side and large doses of dark roasted coffee was the trick. Glenn Flierl graciously accepted being my MIT committee member, and greatly helped this thesis with most insightful comments of my work. Chris Petersen brought expertise on fish behavior to my committee, revised in detail all my manuscripts and always paid for our oriental food feasts. Two of my chapters are the result of conversations with him. I also wanted to thank to temporary members of my committee: Steve Bollens helped me pursue my interests in larval fish behavior, and Larry Madin, who's support as the head of the WHOI diving board was crucial for the completion of my field work. My thesis was done in two different laboratories, so many people have shared my messy desks. My work was always influenced by my friend David Mann, also my colleague, officemate, diving buddy and writing consultant. We managed to help each other in rough moments, fuel our interests for the study of fishes and laugh as much as possible in the process. In the early days Erich Horgan and John Barimo completed ichthyology laboratory, it was a pleasure to work with such an enthusiastic bunch of friends. For brief moments Carla Curran, Diana Ma and Alistair Economakis coincided with me in this lab. Later on I moved across the hallway to share a space with Ewann Bernston and Susan Mills, which provided me with friendship, support and chocolate during the process of writing up my thesis. Laughs were also abundant. David Mann, Gary Jaroslow, Deb Bidwell and Donald Kramer painfully read many rough drafts in Spanglish and improved my English. Conchita Avila and Annie Weisbrod helped me design the trunkfish toxicity protocol. I spent most of my time in first floor of the Redfield building, were the organismal biologists of WHOI are most commonly found: Rudi and Ami Scheltema, Stacy Kim, Jesus Pineda, Peter Tyack, Rebecca Thomas, Patrick Miller, Pam Arnofsky, Mircea Podar, Molly and Winkle. Richard Harbison and Jim Craddock deserve special attention for great friendships and for transmitting to me their passion for science and the oceans. If they are not doing molecular biology because they are not interested, younger generations should drop by their offices to learn something about how science should be. The WHOI education office always supported me, and I would like to specially thank Jake Peirson, Abbie Alvin and Julia Westwater, for dear friendships and support. Colleen Hurter from the MBL/WHOI library is one of the most hard working and efficient persons on this planet, and is a wonderful person too. I believe it is very easy to obtain a Ph.D. with such a supporting team on your side. But I also spent a lot of time at Johnston Atoll doing field work. Diving buddies were essential for my work with SCUBA, and I had the best ones: David Mann, Diana Ma, Alistair Economakis, Steve Oliver, John Barimo and Erich Horgan. Also a group of friends from Johnston Island, all excellent divers, was always ready to jump in the water if necessary, specially if it involved strong currents, sharks and spearing fishes: Gary McCloskey, GW, Kelly and Miguel Busquets, Dave Shogren, Jane Super and Mary Boyce. Roger DiRosa, Donna O'Daniel and Chris Depkin from the U.S. Fish & Wildlife were our friends and colleagues, and we helped each other studying either fish or birds. None of this work could have been possible without the help of vast amounts of money. A fellowship form La Fundacion "La Caixa" allowed me to come to the WHOI/MIT Joint Program and generously funded me for two years. Travel to Johnston Atoll, part of my salary and many oceanographical toys were funded by the following grants to P.S. Lobel: U.S. Army Chemical Material Destruction Agency (via NOAA Sea Grant NA90-AA-D-SG535 and the Office of Naval Research N00014-91-J-1591 and N00014-92-J-1969) and the U.S. Army Legacy Resource Management Program (DAMD 17-93-J-3052). Finally the WHOI education office covered my tuition for a few years and paid for my attendance to scientific meetings. Funds were also received from the Thomas F. Westcott Fund for WHOI / MIT Joint Program Students, WHOI Sea Grant project R/B134-PD, Coastal Research Center and Copeland Family Foundation. I have left for now some of the most important people to me during these years, which were essential for my completion of my doctorate: my friends. You can easily recognize them, they are all fun loving open people with great hearts. I will first list Deb Bidwell, who recently entered my life like a hurricane and gave me the necessary energy to finish my thesis. She makes me happy and I am looking forward to many new adventures in her company. From my arrival to Woods Hole, Gary Jaroslow shared with me the good and bad moments, amplifying the first and soothing the last. I am honored we can call each other friends. In a similar role, I have to include the 'old guard' from Woods Hole: Javier Escartin, Dan Torres, The Weidmans, Joe & Cecilia Lacasce, David & Amy Mann, Miguel & Kathleen Goni, Dan & Haiga Lizarralde, Xavi Garcia, Connie Hart and Margie Oleksiak, the greatest group of friends a crazy spaniard lost in New England could ask for. But I also want to thank Gaspar Taroncher, Ee Lin Lim, Nancy Parmentier, Rob & Kahmla Evans, Deana Erdner, Jake, Anna Maria Peirson and family, Abbie Jackson, Julia Westwater, Rich & Judy Harbison, #2, Sonsoles Gonzalez, Ghislaine Llewelyn, Lisa & Jason Moore, Gustavo & Aria Arrizabalaga, David West, Nicole Duhamel, Kate Lindner, Christina Sun, Stacy Kim, Ewann Agenbroad, Dan Lindstrom, Ishi Buffin, Dana Stuart, Vicki Tauxe, Sheri Hall, Glenn Crossin, Lihini Aluwihare, Bill Shaw, Debbie Hassler, Karie Slavik, Pablo Canales, Shannon Wagner, Max, The Jovines, Rebecca Thomas, Flip Williams and the WHUF crowd, since they were all important friends to me at some point of my career, and still are. From Spain, I have to thank Carlos Hermida, Maite Cendan and Chema Velasco, que siempre me animaron a perseguir mis suefios pese que ello supusiese interponer un oceano entre nosotros. Espero pagarles con creces en el futuro proximo. Finally I want to thank my family. I shared with them unique moments while diving in Menorca and fishing up the mountains of Spain, which obviously influenced the topic of this thesis. My mother, Elena Bizcarrondo, not only allowed me, but encouraged me to pursue my dreams and interests. My father, Jose Maria Sancho, is the one that took me to a fishing derby when I was 6, and bought me a speargun at the age of 8. I could have never asked for anything else.