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Nematocyst Replacement in the Sea Anemone Aiptasia Pallida Following Predation by Lysmata Wurdemanni: an Inducible Defense?

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Nematocyst Replacement in the Sea Anemone Aiptasia Pallida Following Predation by Lysmata Wurdemanni: an Inducible Defense? NEMATOCYST REPLACEMENT IN THE SEA ANEMONE AIPTASIA PALLIDA FOLLOWING PREDATION BY LYSMATA WURDEMANNI: AN INDUCIBLE DEFENSE? by Lucas Jennings A Thesis Submitted to the Faculty of The Charles E. Schmidt College of Science in Partial Fulfillment of the Requirements for the Degree of Master of Science Florida Atlantic University Boca Raton, Florida August 2014 ACKNOWLEDGEMENTS The author would like to thank his wife, Rachel Jennings and daughter Kathryn Jennings for their understanding, support and encouragement. Committee members Dr. Susan Laramore, Dr. Clayton Cook and Dr. Joshua Voss provided help and support throughout this process. Dr. Shirley Pomponi and Dr. John Scarpa contributed use of equipment and facilities. Support from the Broward Shell Club and Proaqutix was also greatly appreciated. iii ABSTRACT Author: Lucas Jennings Title: Nematocyst Replacement in the Sea Anemone Aiptasia pallida Following Predation by Lysmata wurdemanni: An Inducible Defense? Institution: Florida Atlantic University Thesis Advisor: Dr. Susan Laramore Degree: Masters of Science Year: 2014 The sea anemone Aiptasia pallida is a biological model for anthozoan research. Like all cnidarians, A. pallida possesses nematocysts for food capture and defense. Studies have shown that anthozoans, such as corals, can rapidly increase nematocyst concentration when faced with competition or predation, suggesting that nematocyst production may be an induced trait. The potential effects of two types of tissue damage, predator induced (Lysmata wurdemanni) and artificial (forceps), on nematocyst concentration was assessed. Nematocysts were identified by type and size to examine the potential plasticity associated with nematocyst production. While no significant differences were found in defensive nematocyst concentration between shrimp predation treatments versus controls, there was a significant difference in small-sized nematocyst in anemones damaged with forceps. The proportions of the different types of nematocysts iv between treatment types were also found to be different suggesting that nematocyst production in A. pallida is a plastic trait. v NEMATOCYST REPLACEMENT IN THE SEA ANEMONE AIPTASIA PALLIDA FOLLOWING PREDATION BY LYSMATA WURDEMANNI: AN INDUCIBLE DEFENSE? List of Tables ................................................................................................................... viii List of Figures .................................................................................................................... ix Introduction ......................................................................................................................... 1 Inducible defenses ........................................................................................................... 2 Production of new defensive structures .......................................................................... 3 Increase in existing defensive structures ......................................................................... 4 Anthozoan defeNse ......................................................................................................... 5 Aiptasia pallida ............................................................................................................. 11 Lysmata wurdemanni .................................................................................................... 12 Hypotheses ........................................................................................................................ 14 Methods............................................................................................................................. 15 Animal Collection ......................................................................................................... 15 CharacterizaTion of the Aiptasia pallida Cnidom ........................................................ 16 Animal Acclimation ...................................................................................................... 17 Artificial predation ........................................................................................................ 19 Shrimp predation ........................................................................................................... 19 Nematocyst counts ........................................................................................................ 20 Results ............................................................................................................................... 23 Determination of Aiptasia pallida Cnidom ................................................................... 23 Overall MANOVAs and anovas .................................... Error! Bookmark not defined. vi Artificial Predation ........................................................................................................ 24 Shrimp Predation ........................................................................................................... 26 Artifical vs. shrimp predation........................................................................................ 26 Discussion ......................................................................................................................... 29 Conclusions ....................................................................................................................... 36 References ......................................................................................................................... 49 vii TABLES Table 1. Nematocyst size class designations…………………….……………………...37 Table 2. Summary of MANOVA and ANOVA statistics for nematocyst counts………38 FIGURES Figure 1. Induced spines in Membranipora membrancea from Harvell 1990………….39 Figure 2. Inducible shape of Chthamalus anisopoma from Lively 1986a.....……..…….40 Figure 3. Anatomy of a sea anemone from Shick 1991…………………………………41 Figure 4. Damage treatments used by Chornesky 1983………………………………...42 Figure 5. Means of different nematocyst types for tentacle data………….………...….43 Figure 6. Means of different nematocyst types for column data………………………..44 Figure 7. Means of different nematocyst types for whole anemone data…………...…..45 Figure 8. Total nematocyst means…….…………………………………………..…….46 Figure 8. Nematocyst proportions for each nematocyst type for tentacle data….……...47 Figure 9. Nematocyst proportions for each nematocyst type for column data….………48 INTRODUCTION Effective defenses against predation and competition are important for sessile or semi-sessile organisms, including anthozoans. The diversity of defensive strategies and morphologies suggest strong evolution pressure on these defensive traits among organisms who cannot simply avoid a predator or competitor by relocating. While it is difficult to show experimentally, it is generally agreed that the development of defenses is energetically costly (Tollrian and Harvell 1999). Due to these costs, an organism that possesses the ability to rapidly allocate energy to the development of defense only when needed is thought to have a selective advantage compared to the same organism with fixed defensive phenotypes (Schlichting 1986; Sultan 1987; Adler and Harvell 1990; Slattery et al. 2001). Species that invest in constitutive (fixed) defense must allocate energy to the production and maintenance of defensive structures or compounds at all times while those investing in plastic (induced) defenses forgo these costs until defense is needed (Karban and Baldwin 1997; Agrawal and Karban 1999). The development and/or increase of defensive structures only when needed are collectively characterized as inducible defenses. Inducible defense is a form of phenotypic plasticity where an interaction with a predator or competitor triggers a defensive phenotypic response within a short time frame (Trussell 1996; Tollrian and Harvell 1999; Trussell and Nicklin 2002). Researchers agree that an inducible defense is favored over a constitutive defense by 1 natural selection if (1) the risk of predation is variable in both time and place, and is occasionally intense, but does not result in the mortality of the prey species, (2) the production of the defense requires costs and, or, there are tradeoffs associated with the defensive phenotype, (3) the advantage of the defense outweighs any and all costs associated with the production of the plastic defense, and (4) cues for the plastic trait are reliable with the defensive phenotype only occurring in the presence of the appropriate predator (Harvell 1986; Lively 1986a; Sterns 1989; DeWitt et al. 1998; Tollrian and Harvell 1999). INDUCIBLE DEFENSES Inducible defenses are found in a wide variety of marine organisms both sessile and mobile. When faced with a competitor or predator, organisms that exhibit an inducible defense either (1) produce new structures or compounds that were not previously present such as spines (Harvell 1986) or (2) increase defensive structures that were previously present, for example shell thickening (Trussell 1996) or defensive nematocysts (Gotchfeld 2004). Examples of the production of new defensive structures include the production of defensive spines in a bryozoan (Harvell 1984), shell- dimorphism in an acorn barnacle (Lively 1986b) and the production of sweeper tentacles in anthozoans (Chornesky 1983). Examples of increases in defensive structures already present include increased shell thickness in a marine snail (Trussell 1996), the increase in secondary metabolites in soft coral (Slattery et al. 2001),
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