The Role of Chemical Signals on the Feeding Behavior of the Crown-Of-Thorns Seastar, Acanthaster Planci (Linnaeus, 1758)
Total Page：16
File Type：pdf, Size：1020Kb
THE ROLE OF CHEMICAL SIGNALS ON THE FEEDING BEHAVIOR OF THE CROWN-OF-THORNS SEASTAR, ACANTHASTER PLANCI (LINNAEUS, 1758) BY CIEMON FRANK CABALLES A thesis submitted in partial fulfillment of the requirements for the degree of MASTER OF SCIENCE IN BIOLOGY UNIVERSITY OF GUAM SEPTEMBER, 2009 AN ABSTRACT OF THE THESIS of Ciemon Frank Caballes for the Master of Science in Biology presented 25 September, 2009. Title: The Role of Chemical Signals on the Feeding Behavior of the Crown-of- Thorns Seastar, Acanthaster planci (Linnaeus, 1758) Approved: ______________________________________________________________ Peter J. Schupp, Chairman, Thesis Committee Coral reefs are among the world’s most diverse and productive ecosystems, but at the same time also one of the most threatened. Increasing anthropogenic pressure has limited the resilience of reefs to natural disturbances, such as outbreaks of crown-of- thorns seastar, Acanthaster planci. A. planci is a corallivore known to inflict large-scale coral mortality at high population densities and continues to be a reef management problem despite previous control efforts. There has been no active control of A. planci populations on Guam since the 1970’s despite recent surveys showing that A. planci outbreaks continue to damage large areas of reef and is one of the primary sources of coral mortality around Guam. Large aggregations of up to 522 individuals/ha of reef were observed to feed mainly on Acroporids, especially encrusting Montipora and branching Acropora. Preferential feeding by A. planci, even at moderate densities, causes differential mortality among coral species, which can exert a major influence on community structure. Despite this, the underlying mechanisms involved in this feeding behavior are still poorly understood. The role of chemical signals from the coral prey and chemoreception by A. planci is important in understanding prey location, prey discrimination, and the formation of aggregations. Several experiments were set-up to test these stages of A. planci feeding. Choice assays were conducted in a Y-maze and in situ, using extracts or compounds incorporated into agar-based gels at natural concentrations. Y-maze assays in the laboratory showed that A. planci individuals were attracted to crude extracts of Montipora sp., Acropora surculosa, and Pocillopora eydouxi, but did not show preference for extracts of Porites rus, Porites cylindrica, and Diploastrea heliopora. Further analyses of extracts reveal that the variability of betaine concentrations between coral species was not consistent with observed feeding preferences. Moreover, the 90% aqueous MeOH fraction of A. surculosa was the most active in terms of chemoattraction. Previously identified feeding attractants (i.e. a- linolenic acid and betaine) also elicited chemotaxis in Y-maze assays. In field experiments, betaine was shown to be effective in attracting A. planci from longer distances, while a-linolenic acid was more effective in short distances. In a natural setting, chemoreception by A. planci is largely influenced by the solubility of these compounds and the local hydrodynamic conditions. Furthermore, extraoral predation presumably results in tissue damage and decompartmentalization, which induces enzymatic cleavage of dimethylsulfoniopropionate in zooxanthellae to dimethyl sulfide and acrylic acid. Laboratory choice assays show that these cleavage products attract A. planci and could explain why individuals tend to aggregate toward colonies with partial mortality when feeding, rather than feed on intact colonies. Taken together, these results clearly indicate that chemical signals influence the feeding behavior of A. planci at different stages: first, A. planci actively use chemical signals to locate prey from a distance and find favorable substrata; secondly, short-distance and contact chemoreception is used in prey discrimination and in determining which colonies are most palatable; and lastly, predation by A. planci facilitates chemical reactions that produce chemoattractive compounds and increase concentrations of attractants present in coral. Knowledge on the role of chemical signals on the feeding behavior of A. planci will be applicable in designing traps or bait stations as alternative tools in the control and management of outbreaks. TO THE OFFICE OF GRADUATE SCHOOL AND RESEARCH The members of the committee approve the thesis of Ciemon Frank Caballes presented 25 September, 2009. ____________________________________ Dr. Peter J. Schupp, Chairman ____________________________________ Dr. Laurie J. Raymundo, Member ____________________________________ Dr. Alexander M. Kerr, Member ____________________________________ Dr. Ross H. Miller, Member Accepted: ____________________________________ ` __________________ Elise Ralph, Ph.D. Date Dean, Graduate School and Research TABLE OF CONTENTS Abstract Approval Page Title Page Acknowledgments ……………………………………………………………………….. i Table of Contents ……………………………………………………………………....... iii List of Tables …………………………………………………………………………….. vi List of Figures ……………………………………………………………………………. vii CHAPTER 1 General Introduction 1.1 Threats to coral reefs ………………………………………….…. 1 1.2 General biology of Acanthaster planci …………………………... 2 1.3 A. planci outbreaks: Causes and consequences ………………….. 4 1.4 Objectives ………………………………………………………... 11 1.5 Significance of the study ………………………………………… 12 CHAPTER 2 Distribution and Characteristics of A. planci Aggregations 2.1 Introduction ……………………………………………………… 14 2.2 Methods ………………………………………………………….. 16 2.2.1 Study Sites ………………………………………………... 16 2.2.2 Broadscale: Manta Tow Surveys …………………………. 17 2.2.3 Finescale: Belt Transect Surveys ………………………… 19 2.2.4 Data Analyses …………………………………………….. 20 2.2.5 Collection of A. planci …………………………………… 21 2.3 Results …………………………………………………………… 23 2.3.1 Abundance and Distribution of A. planci ………………… 23 2.3.2 Coral Mortality …………………………………………... 24 2.3.3 Feeding Preferences ……………………………………… 25 2.3.4 Size Class of Outbreak Populations ……………………… 25 2.3.5 Collection of A. planci …………………………………… 26 2.4 Discussion ………………………………………………………... 37 CHAPTER 3 Prey Discrimination and Chemoreception 3.1 Introduction ……………………………………………………… 46 3.2 Methods ………………………………………………………….. 48 3.2.1 Study Organisms …………………………………………. 48 3.2.2 Y-maze Specifications and Extract Diffusion Experiment ... 49 3.2.3 Choice Assays ...................................................................... 51 3.2.4 Statistical Analyses .............................................................. 52 3.3 Results …………………………………………………………… 55 3.3.1 Diffusion of Extracts in the Y-maze ..................................... 55 3.3.2 Coral Extract Choice Assays ……………………………... 55 3.4 Discussion ………………………………………………………... 60 CHAPTER 4 Chemical Analysis of Coral Extracts 4.1 Introduction ……………………………………………………… 65 4.2 Methods ………………………………………………………….. 67 4.2.1 Study Organisms ................................................................. 67 4.2.2 Extraction Procedure .......................................................... 68 4.2.3 Determination of Natural Concentrations of Extracts ........ 69 4.2.4 Choice Assays with Extract Fractions ................................ 69 4.2.5 Extract Partitioning ……………………............................. 70 4.2.6 Quantification of Betaine Concentrations ........................... 71 4.2.7 Statistical Analyses ……………………………………….. 71 4.3 Results …………………………………………………………… 73 4.3.1 Natural Concentration of Extracts ……………………….. 73 4.3.2 Choice Assays with Extract Fractions …….……………... 73 4.3.3 Characterization of Extracts ………………..……………. 74 4.3.4 Betaine Concentration …………………………... 74 4.4 Discussion ………………………………………………………... 81 CHAPTER 5 Effectiveness of Identified Feeding Attractant Compounds 5.1 Introduction ……………………………………………………… 86 5.2 Methods ………………………………………………………….. 88 5.2.1 Chemical Reagents ……………………………………….. 88 5.2.2 Laboratory Feeding Assays ………………………………. 88 5.2.3 Field Feeding Assays …………………………………….. 90 5.2.4 Field Trapping Experiments ……………………………… 92 5.2.5 Statistical Analyses ……………………………………….. 93 5.3 Results …………………………………………………………… 96 5.3.1 Laboratory Feeding Assays …………………………...….. 96 5.3.2 Field Feeding Assays …………………………………….. 96 5.3.3 Field Trapping Experiments ……………………………… 98 5.4 Discussion ………………………………………………………... 102 CHAPTER 6 Chemoattraction and the Formation of Aggregations 6.1 Introduction ……………………………………………………… 107 6.2 Methods ………………………………………………………….. 111 6.2.1 Study Organisms …………………………………………. 111 6.2.2 Chemical Reagents ……………………………………….. 111 6.2.3 Choice Assays …………………………………………….. 112 6.2.4 Statistical Analyses ……………………………………….. 114 6.3 Results …………………………………………………………… 115 6.4 Discussion ………………………………………………………... 117 CHAPTER 7 Synthesis and Implications 7.1 General Discussion and Summary ……………………………….. 123 7.2 Research Implications …………………………………………… 133 7.3 Management Implications ……………………………………….. 134 Literature Cited ................................................................................................................. 137 LIST OF TABLES Table 1 ANOVA Table of A. planci abundance and distribution ……………….. 27 Table 2 SRH-ANOVA Table of field feeding preferences …………………….... 33 Table 3 Collection of A. planci individuals from several outbreak sites around Guam ……………….……………………………. 36 Table 4 Mean crude extract concentrations of selected scleractinian corals ……………………………………………………… 77 Table 5 Proportion of hydrophilic and lipophilic components in selected coral species ………………………………………………… 79 Table 6 Concentration of betaine