THE PENNSYLVANIA STATE UNIVERSITY SCHREYER HONORS COLLEGE DEPARTMENT OF BIOLOGY HIDDEN DIVERSITY OF BRAIN WORMS IN ZOMBIE ANTS HALEY DEMARTIN SPRING 2018 A thesis submitted in partial fulfillment of the requirements for a baccalaureate degree in Biology with honors in Biology Reviewed and approved* by the following: David Hughes Associate professor of Entomology and Biology Thesis Supervisor James Marden Professor of Biology & Assoc. Director, Huck Institutes of the Life Sciences Honors Adviser * Signatures are on file in the Schreyer Honors College. i ABSTRACT Ants, as one of the oldest and most diverse groups of social animals on Earth, can provide insight into various parasite-host relationships. Studying ants and their interactions with parasites over evolutionary time can advance our knowledge of the spread of disease throughout a society in general. In this research paper, I focus on worms infecting ants. The principal parasitic worms affecting ants are in the phylum Nematoda and the classes of Cestoda and Trematoda. Much of the previous research endeavors that have been completed on the study of worms infecting ants have been lost to time and language. The time and effort dedicated by other scientists to the study of this important relationship needs to be unearthed and that is what I attempted to do in this paper. Therefore I conducted a detailed library study of the diversity of worm parasite in ants, which involved extensive exploration of both the non-digitized corpus and non-English language corpus. Not only did I find more ant-worm parasite association records than previously known, but also I uncovered many significant records of parasite prevalence and distribution. My work lays the foundation for more research that can now be done on this subject. Furthermore, my work will hopefully resolve the ecological drivers of ant-parasite relationships and their evolutionary implications. ii TABLE OF CONTENTS LIST OF FIGURES ..................................................................................................... iii LIST OF TABLES ....................................................................................................... iv ACKNOWLEDGEMENTS ......................................................................................... v Introduction .................................................................................................................. 1 Materials and Methods ................................................................................................. 5 Results .......................................................................................................................... 7 Discussion .................................................................................................................... 21 Conclusion ................................................................................................................... 33 BIBLIOGRAPHY ........................................................................................................ 34 iii LIST OF FIGURES Figure 1. Number of times ant species are reported as a host to a worm. ................... 7 Figure 2. Visual Representation of Prevalence Distribution Data ............................... 8 Figure 3. Number of Ants Investigated in Each Study ................................................ 9 Figure 4 Papers Accessible on the Internet. ................................................................. 9 iv LIST OF TABLES Table 1: List of Trematodes Infecting Ants ................................................................. 10 Table 2: List of Cestodes Infecting Ants ..................................................................... 12 Table 3: List of Nematodes Infecting Ants .................................................................. 14 Table 4. Ant Host Biodiversity .................................................................................... 17 v ACKNOWLEDGEMENTS I would like to thank David Hughes and Jim Marden for reading my thesis and giving me comments. This research project could not have been done without the help of David Hughes who has been a great mentor and leader to me during my time working in the Hughes Lab. I thank everyone in the Hughes Lab who has helped me with this project. 1 Introduction The ubiquity and the abundance of ants living on the Earth’s surface are remarkable. According to a calculation done by Hölldobler and Wilson (1994), if there are one million trillion insects alive on earth, and if 1% of these insects are ants, and if individual workers weigh on average 1-5 mg, then the total weight of all the ants in the world is approximately equal to the total weight of all of the people in the world. While ants account for less than 2% of all insect species, they are the dominant fauna of all terrestrial ecosystems and they make up almost 70% of individual insects in tropical forests (Hölldobler and Wilson 1994). The dominance of ants in their environment leads them to be very involved in the lives and evolution of many other organisms. One relationship that has been studied extensively is the relationship between ants and their parasites. Ants can be a host to many kinds of organisms including viruses, bacteria, fungi, protozoa, flagellates, helminths, mites, Hymenoptera, and other types of insects (Schmid-Hempel 1998). Ants are of the most advanced type of social insects because they have the three biological traits that researchers use to define eusociality: the adults care for the young; two or more generations of adults live together in the same nest; and the members of each colony are divided into castes -a reproductive caste and a nonreproductive caste (Schmid-Hempel 1998). Eusociality makes ant colonies profitable targets for parasites because of the high density and high relatedness of ants in each colony (Schmid-Hempel 1998). Some of the qualities that make ant colonies profitable hosts also make them a difficult host for parasites to invade. Just as ants are diverse, so are the organisms that parasitize them. Therefore, parasites of ants use various strategies for infection. For example, parasites often target larvae and pupae as prime hosts which are often infected not by direct exposure to the parasite but through contamination of their food or nest material by other workers. 2 Bacteria and spores of fungi can remain infective for years and produce infections with few outward symptoms. A nematode infection occurs when the infective-stage nematode invades the host either by directly penetrating the cuticle or through natural openings, like the mouth, when the ant ingests an egg as food. Several rhabditidae nematodes have been reported in ants. Poinar (1975) grouped nematodes according to whether they are phoretic, facultative, or obligatory parasitic. Phoretic nematodes are not known to be associated with ants. The facultative nematodes are able to complete their life cycle outside the host. In insects they can be found in the body cavity, intestinal tract, pharyngeal and other glands or in the trachea. Obligate parasitic nematodes cannot live without a host and have no free-living stages. Generally these species are found in the insect’s body cavity; some may be found in the intestinal tract and reproductive system. A nematode’s life cycle can include intermediate hosts but they tend to have few host species. Several rhabditid nematodes have been reported from ants. Typically they parasitize the pharyngeal glands in the head of their host. Examples are Caenorhabditis dolichura (Janet 1983) in Formica fusca (Nickle and Ayre 1966), in Camponotus herculeanus and Acanthomyops claviger (Wahab 1962), and in other ants. Trematodes are a class of parasitic flatworms known as flukes. Parasitic trematodes use multihost life cycles involving two to three hosts in which molluscs serve as the first intermediate hosts and vertebrates serve as final hosts (Barger and Fellis, 2002). Krull and Mapes are credited with being the first to reveal the life cycle of a well-studied trematode, Dicrocoelium dendriticum (1952, 1953). They discovered that the adult D. dendriticum lays its eggs in the liver or bile-duct of certain mammals. The eggs are transferred to the first intermediate host, a mollusc through the feces of 3 the mammal. The infected snails produce slime balls which contain the trematode which by then has developed from eggs into cercariae. Ants are the second intermediate host and become infected because they use snail slime balls as a source of water, so they end up ingesting the cercariae with the slime. While inside of the ant, the trematodes penetrate the ant’s stomach in and enter the hemocoel. From there, they move through the ant’s body to its brain where they develop into metacercarial cycts. When the trematodes are in the ant’s brain, they can cause the ant to behave differently than normal in order to facilitate the trematode’s passage to its final host, livestock like sheep. For example, the ant will become more sluggish and lose sensitivity to light. Both of these things will cause the ant to spend more time outside the nest and therefore be more likely to be eaten by grazing livestock so that the trematode can complete its lifecycle (Carney 1967, 1969). This is just one example of how parasitism by worms can change the ant behavior. Cestodes are a class of parasitic tapeworms that are known for living in the digestive tracts of vertebrates as adults and the bodies of other species of animals as juveniles. Parasitic cestodes