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Mechanisms of Parasitism in a Thermophilic MECHANISMS OF PARASITISM IN A THERMOPHILIC ANT, MELOPHORUS ANDERSENI ____________ A Thesis Presented to the Faculty of California State University Dominguez Hills ____________ In Partial Fulfillment of the Requirements for the Degree Master of Science in Department of Biology ____________ by Sara S. Hu Summer 2017 Dedicated to my mom. ii ACKNOWLEDGEMENTS Thank you to the National Science Foundation (IRES) for funding; CSIRO Darwin for providing excellent research resources and facilities while in Australia; my collaborators Drs. Ben Hoffmann, Adrian Smith, and Andrew Suarez; my lab mates in Australia, Erica Parra, Abe Perez, and Júlio Chaul; and my advisor, Dr. Terry McGlynn for all the feedback, support and guidance. iii TABLE OF CONTENTS PAGE DEDICATION ................................................................................................................... ii ACKNOWLEDGEMENTS .............................................................................................. iii TABLE OF CONTENTS ................................................................................................... iv ABSTRACT ....................................................................................................................... vi CHAPTER 1. INTRODUCTION ...........................................................................................................1 Statement of Collaboration ......................................................................................3 2. LITERATURE REVIEW ................................................................................................4 Study Organisms .....................................................................................................4 Social Parasitism .....................................................................................................5 3. METHODOLOGY ..........................................................................................................7 Study Sites ...............................................................................................................7 Colony Establishment and Survival .........................................................................7 Activity ....................................................................................................................8 Foraging Behavior .................................................................................................10 Running Speed .......................................................................................................10 Chemical Mimicry .................................................................................................11 Analysis..................................................................................................................12 4. RESULTS ......................................................................................................................13 Colony Establishment and Survival .......................................................................13 Activity ..................................................................................................................14 Foraging Behavior .................................................................................................22 Running Speed .......................................................................................................23 Chemical Mimicry .................................................................................................24 iv CHAPTER PAGE 5. DISCUSSION ...............................................................................................................29 Colony Establishment and Survival .......................................................................29 Activity ..................................................................................................................31 Foraging Behavior .................................................................................................34 Running Speed .......................................................................................................37 Chemical Mimicry .................................................................................................40 6. CONCLUSION .............................................................................................................42 REFERENCES ..................................................................................................................43 v ABSTRACT Ants have sophisticated, well-developed recognition systems that allow them to defend their nests. However, some organisms have evolved strategies to infiltrate ant colonies and exploit resources. Melophorus anderseni establish nests near their host, Iridomyrmex reburrus and parasitically raid host brood. We examined colony establishment and foraging behavior of M. anderseni to test three possible mechanisms that may facilitate interspecific nest raiding behavior: running speed, thermal tolerance, and chemical mimicry. We found that M. anderseni use a combination of the three mechanisms in order to exploit their host. My collaborators, Benjamin D. Hoffmann, Adrian A. Smith, and Andrew V. Suarez contributed to the chemical data and analyses portion of this thesis. Details of their collaboration can be found in the Statement of Collaboration subsection of Chapter 1. 1 CHAPTER 1 INTRODUCTION The evolution and maintenance of animal societies rely on the ability to distinguish group members from strangers. This form of behavioral discrimination allows group members, who are often kin, to direct costly beneficial behavior towards group individuals and exclude or defend against non-group individuals. Consequently, there is selective pressure for social and colonial organisms across taxa to possess well-developed recognition systems (Fletcher and Michener 1986; Gamboa et al. 1986; Hamilton 1987; O’riain and Jarvis 1997; Sherman et al. 1997; Starks 2004). Ants have finely tuned recognition systems (Lehav et al. 1999; Thomas et al. 1999; Wagner et al. 2000; Greene and Gordon 2007), which act as the mechanistic basis for their social organization, territoriality, and colony defense (Hölldobler and Wilson 1990; Stuart and Herbers 2000; Larsen et al. 2016). Nest defense is essential for sustaining the stability and survival of colonies (D’Ettorre and Lenoir 2010; Sturgis and Gordon 2012). However, many organisms have evolved strategies to penetrate these highly protected social fortresses (Lenoir et al. 2001; D’Ettorre et al. 2002; Akino 2008; Nash and Boomsma 2008). Social parasites use diverse strategies to deceive and exploit their hosts (Buschinger 1986; D’Ettorre and Heinze 2001; Buschinger 2009; Rettenmeyer et al. 2011). Chemical deception is often used by social parasites as a means of infiltrating host colonies (Lenoir et al. 2001). Agosti (1997) noted an unusual behavior in Melophorus anderseni, whereby M. anderseni workers ride on the back of a host ant. Agosti (1997) 2 suggested that M. anderseni were “hugging” and “rubbing” the Iridomyrmex sanguineus worker while riding its back in order to acquire its distinct smell (cuticular hydrocarbons). Distinct cuticular hydrocarbons used for nestmate recognition (Bonavita- Cougourdan et al. 1987; Lehav et al. 1999; Lucas et al. 2005) are adopted by ant and non- ant social parasites in order to cloak their presence from hosts (Franks et al. 1990; Lenoir et al. 1997; Akino et al. 1999; Lambardi et al. 2007; Hojo et al. 2014). Melophorus anderseni nest on the outskirts of Iridomyrmex sanguineus nests (Agosti 1997). Agosti (1997) noted M. anderseni make their way through guarded nest entrances as solitary foragers and steal brood from highly aggressive I. sanguineus. In 2014, during field observations of meat ant nests in Darwin, Australia, Melophorus anderseni were found robbing brood from another species, Iridomymrmex reburrus, which led to this study. Melophorus anderseni are a thermophilic species with exceptional heat tolerance like others in its genus (Christian and Morton 1992; Hoffmann 1998; Muser et al. 2005; Schultheiss and Nooten 2013). Ecologically similar thermophilic species have longer legs and high running speed (Hurlbert et al. 2008; Sommer and Wehner 2012). So, it is possible that thermal tolerance and high running speed allow M. anderseni to avoid conflict and escape attacks from their host. In this study, we examined colony establishment and foraging behavior of M. anderseni to evaluate three possible mechanisms that may facilitate interspecific nest raiding behavior of M. anderseni: thermal tolerance, running speed, and chemical mimicry. To accomplish this, we measured daily activity patterns and running speeds of 3 each species and compared the cuticular hydrocarbon profiles of these two species to congeners in the community to determine if chemical mimicry is occurring in this system. Statement of Collaboration My collaborators contributed most to the chemical data and analyses portion of this thesis. Benjamin D. Hoffmann (CSIRO Tropical Ecosystems Research Centre, Darwin, NT, AU) marked and measured distances for the Iridomyrmex nests and Melophorus queens discovered at Humpty Doo, sampled ants from Melville Island, Darwin (outside of CSIRO), and Gunlom Falls in Kakadu National Park, and sent the samples to Adrian A. Smith (North Carolina Museum of Natural Sciences, Raleigh, NC, USA). Adrian A. Smith performed the analyses of the hydrocarbon profiles at Andrew V. Suarez’s lab located at the University of
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