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Senior Honors Theses Undergraduate Showcase

8-2014

Host Specificity and ctE oparasite Load of in Utila, Honduras

Courtney Miller University of New Orleans

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Recommended Citation Miller, Courtney, "Host Specificity and ctE oparasite Load of Bat Flies in Utila, Honduras" (2014). Senior Honors Theses. 63. https://scholarworks.uno.edu/honors_theses/63

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Host specificity and ectoparasite load

of bat flies in Utila, Honduras

An Honors Thesis

Presented to the Department of Interdisciplinary Studies

of the University of New Orleans

In Partial Fulfillment

of the Requirements for the Degree of

Bachelors of Interdisciplinary Studies,

with Honors

by

Courtney Miller

May 2014 TABLE OF CONTENTS

Acknowledgments...... ii List of Figures...... iii Abstract...... iv Chapters: 1. Introduction...... 1 2. Materials, Methods, and Results...... 6 3. Discussion...... 14 References...... 19

! i! ACKNOWLEDGEMENTS

I would like to acknowledge my advisor, Dr. Phil DeVries for introducing me to the world of and providing me with the resources I needed to study them. I am also grateful for the valuable lessons in ecology, which played a huge part in this paper, from my second reader, Dr. Jerome Howard. I would also like to thank Kanahau Research and Conservation Facility in Utila. Specifically, I would like to acknowledge Steven Clayson for showing such enthusiasm for getting covered in bat guano on a daily basis and for helping me overcome any and every obstacle during field work. Also, Andrea Martinez for inspiring my interest in and for making it possible for this study to take place.

! ii! LIST OF FIGURES

1. Table I...... 9 2. Table II...... 11 3. Table III...... 12 4. Table IV...... 13

! iii! ABSTRACT

Bat flies (Streblidae) are obligate blood-feeding ectoparasites of bats that display varying degrees of host specificity. A total of 265 streblid bat flies were collected from

122 bats belonging to the families Phyllostomidae and Natalidae from Utila, the smallest bay island of Honduras. Out of four host-parasite associations, three were considered primary. Out of the three bat analyzed, one had significantly lower parasite prevalence and another had significantly higher parasite load and intensity. Both male and female bats were equally likely to be infested and variables of parasite density did not differ amongst host sex for any species. However, one species of bat had a significantly larger number of male parasites than female parasites. No significant relationships were found between variables of parasite density and host body mass or bat health (indicated by the ratio of mass to forearm length). The roosting ecology of the two cave roosting species in the study was considered and despite no apparent lack of dispersal barriers, the bat flies exhibited consistent primary associations. Examination of similar host-parasite relationship has many implications in parasite-host relationships and coevolution.

Keywords: Streblidae, ectoparasitic infestations, parasite-host associations, Chiroptera, bat health, roosting ecology

! iv!

CHAPTER I

INTRODUCTION

Bat flies, , are obligate ectoparasites of bats. They are highly specialized hematophageous true flies found in the fur or on the membranous areas of their hosts. The two families, Streblidae and , are both most diverse in the tropic regions with streblids having greater richness is the Western Hemisphere (Dick &

Patterson 2006). Both bat and bat species can exhibit a wide variety of ecological, morphological, and behavioral differences. The nature of the associations between bat flies and their hosts provides many significant yet complicated avenues for exploration.

Due to their odd lifecycle, the bat flies’ habitat expands far beyond the host environment. They are holometabolous insects that exhibit adenotrophic viviparity. The adult female bat fly leaves the host to find a suitable area on the roost substrate to deposit its offspring. A single 3rd instar larva immediately forms a puparium after being deposited, spends three to four weeks in a pupal stage, then emerges as an adult fly seeking a host (Dick & Patterson 2006). It is also notable that there have been cases where adult male bat flies were observed off the host, specifically amongst pupae (Dick

& Patterson 2006). Considering that bat flies spend up to a third of their adult lifespans off of their hosts, one might suspect that this provides increased potential for associations with a variety of host species. In other words, bat flies may be obligate parasites of bats, but given their life cycle, they are not permanent parasites.

While known life-histories are relatively similar, the morphological and behavioral characteristics of bat flies can vary significantly. Specifically, streblids may differ greatly in size, body shape, eye reduction, and wing development. Bat flies have

! 1! strong tarsal claws used for gripping host fur. Some also have a ctendium along the top posterior margin of their head, and various amounts and distributions of setae. Some species exhibit a host-site preference for either fur or membranous areas, such as the wings, which often correspond to certain morphological characteristics (Dick and

Patterson 2006). In a study on the host and host-site specificity of 25 neotropical bat species and 32 bat fly species, functional wings were not associated with host-site preference, but only fur-specific species had ctenidia and long hind legs (ter Hofstede et al. 2004). Fly movement was also observed to be different in this study. Species with shorter legs were seen navigating through the fur while others, with longer legs were pushing to the surface and walking on top of the fur.

Bat hosts also vary significantly in terms of physical and behavioral characteristics. Roosting ecology has shown to be an important factor in parasite and host associations. Some bats use more permanent roosts such as caves, tree cavities, or rock crevices, while others seek refuge in temporary roosts such as foliage or exfoliating bark.

Bats also differ in their degree of roost fidelity, which is often related to the permanence of their roost and form of social organization (Kunz & Fenton 2005). A study conducted on 130 bat species with 116 bat flies species found that bats roosting in more permanent, enclosed structures had higher parasite densities, were infested with more parasite species, and were more likely to be infested (Patterson et al. 2007). Characteristics of both parasites and hosts may contribute to varying degrees of host specificity in parasites.

Host specificity measures the tendency of a parasite to inhabit a single host species and results from the co-existence of parasite and host over evolutionary time

(Dick & Patterson 2007). Host-parasite associations can be categorized as primary or

! 2! non-primary. More specifically, there are multiple degrees, or classifications, of host specificity. Monoxenous refers to a species of parasites that occur only on a single host species, oligoxenous refers to a parasite that occurs on two or more species of the same , and pleioxenous refers to the parasite occurring on two or more host genera in the same (Seneviratne et al 2009). Furthermore, the smaller range of hosts, or the higher degree of specificity, a parasite has will be phylogenetically more similar or have shared behavioral and ecological attributes (Whitfield 1979).

A recent study designed to eliminate cross-host contamination of parasites concluded that 27 out of 31 bat fly species in Paraguay were restricted to one host species (Dick 2007). Host specificity can be thought of as an emergent behavior selected to increase the fitness of ectoparasites by adapting to a more specialized existence as opposed to a generalized one. Host specificity is either a consequence of restricted dispersal ability or the result of coevolutionary host-parasite adaptations (Giorgi et al

2004). Therefore, examining highly host specific bat flies that do not have dispersal barriers can offer significant insight into how adaptation is promoted by evolutionary associations.

The harm a parasite inflicts on its host varies by individuals and groups. However, increased parasite load has the potential to decrease the health of a host either directly though disease, or indirectly through behavior modification. Organisms can either avoid or remove parasites to reduce these fitness costs. Grooming is the primary cause of bat fly mortality (Presley 2010), and bat species with high rates of groom more intensely than those with lower rates (ter Hofstede & Fenton 2005). In principle, extra

! 3! grooming effort is costly behavior because it reduces energy levels for other essential tasks such as foraging for food.

Previous studies have found varying impact of bats flies on their hosts. Research on 87 Rhinolophus mehelyi bats and their 1227 ectoparasites found that parasite load had no apparent impact on bat health (Sharifi et al 2013). However, for Sturnira lilium males, parasitism rates of a streblid bat fly correlated with significant weight loss (Linhares &

Komeno 2000). Analyzing parasite impact can provide insight into the nature of the parasite-host relationship in addition to potential knowledge of their adaptive history.

Parasites that have less impact on their host may be more adapted than those with greater impact since their survival depends upon their ability to avoid detection and removal from the host.

Previous research on 53 species of neotropical bats found that body mass was not correlated with prevalence or mean intensity of ectoparasite infestation (Patterson et al

2008). Another study found that bat flies did not discriminate between male and female bats when given the opportunity to choose a host (Dick and Dick 2006). Identifying and monitoring trends in parasite abundance and distribution can suggest mechanisms that facilitate the coexistence of parasite species as well as the coexistence of parasites and their hosts.

The specific objectives of this study include: identifying the ectoparasites of bats in the study area, quantifying parasite presence, determining primary and non-primary associations, and examining abundance and distribution of parasites in relation to the species, sex, and health of their hosts. The primary intention of this research is to contribute to knowledge on bat flies and their degrees of host specificity, explore the

! 4! ecology and behavior of these ectoparasites and their hosts, and discuss the importance of future research regarding host-parasite relationships.

! 5! CHAPTER 2

MATERIALS, METHODS, AND RESULTS

Study Site

Data were collected from 13 February to 10 March 2014 in the northeast region of

Utila, Bay Islands, Honduras, in a single cave system and from the area immediately surrounding it. The bay island of Utila is located approximately 18 km from the mainland port of La Ceiba and the total area is 49 km2. The environments on the island include mangrove forests, savannas, hardwood forests, and coastal ecosystems. Humidity is high year-round and the average temperature is 85°F. Utila experiences a rainy season from late October to early February accompanied by slightly cooler temperatures. The cave is approximately 80 feet deep with the entrance approximately 50 feet above sea level. It is located within a hardwood forest characterized by Cercropia trees, Bursera simaruba,

Thrinax radiate, Sabal palms, and Ficus aurea. The cave is also in close proximity to approximately 20 acres of land experiencing secondary succession.

Field Methods

The protocol for host and parasite processing was designed to minimize the likelihood of contamination, or the assignment of ectoparasites to the wrong host individual. In the cave, bats were collected with an extendable fishing net or by hand.

Upon capture, each bat’s pelage, wings, and membranous areas were thoroughly inspected and bat flies were removed by hand using soft forceps (Dittmar et al. 2009).

The bat flies were removed and placed in 95% ethanol (Dick 2013). Each vial was labeled with the host bat’s identification number. The bat was then placed in a clean cloth bag until processed.

! 6! A mist net was also set up on five occasions, usually from 1800 to 2100. On three evenings the mist net was placed at ground level, in front of and approximately 40 meters from the cave entrance. On the other two evenings the net was also placed at ground level, but adjacent to the side of the cave and approximately 50 meters from the entrance.

The net was checked every few minutes for captured bats. Once a bat was captured, it was placed in a clean cloth bag for no longer than ten minutes before being thoroughly examined for ectoparasites in the same manner carried out in the cave and then processed.

Upon processing, the following morphological data was collected from each bat: mass, right forearm length, right hind foot length, right ear length, noseleaf length (if applicable), and tail length (Reid 2009). Sex, reproductive status for females, age

(determined by a fused or unfused epiphyseal gap in the joints of the forth and fifth fingers), and location of capture were also noted. Bats were then marked to avoid recapture by trimming a small patch of fur on the right shoulder and released at their capture site (Stuckey 2009).

Any bat fly that was seen after inspection, or during processing, was not counted or collected. To avoid contamination, both the hand net and gloves were shaken and inspected between handing bats. As a bat was being removed from the mist net, the rest of the net was lowered to avoid multiple captures. In addition, as each bat was being untangled from the net, a second individual was monitoring the surrounding net.

Bats were identified to species according to Reid (2009). Bat flies were identified to genus according to Dick and Miller (2010), and then identified to species according to

! 7! identification keys in Wenzel (1976). The identity and sex of each ectoparasite was determined using light microscopy.

Statistical Analysis

Parasite prevalence, load and intensity were determined for each host species

(Bertola et al. 2005; Dick et al. 2003; Patterson et al 2008). Prevalence refers to percentage of bat infested by bat flies, parasite load refers to average number of bat flies per host individual, and intensity refers to the average number of bat flies per infested bat. These rates were also determined separately for male and female populations of each bat species. The significance of patterns of prevalence among host species and host sex were analyzed using Fisher’s exact test, parasite load was compared using an ANOVA, infestation intensity was compared using t-tests, and a binomial test was used to determine if parasite sex differed among hosts. The Pearson correlation coefficient was used to determine associations between body mass and parasite load (Komeno &

Linhares 1999). Bat health was indicated by the ratio of body mass to forearm length and was also compared to parasite load using the Pearson correlation coefficient (Sharifi et al.

2013).

A 5% cut-off rule was used to categorize host-parasite relationships as either primary or non-primary (Dick 2007). When 5% or more individuals of a specific parasite species is found on the same host species it is considered a primary association. Likewise, when a host species found with less than 5% of the total number of parasite individuals sampled of a species it is considered non-primary. This cutoff level is intended to eliminate spurious results due to small sample size, sampling error, or contamination events (Stamper 2012).

! 8! Results

A total of 265 bat flies belong to four species and two genera in the family

Streblidae were found on 122 adult bats comprising of four species (Table I). All but one species was found exclusively on one host species. dugesii Townsend was found on two bat species. However, 98% of the individuals were found on Glossophaga soricina, classifying it as a primary host, and only 2% were found on Lonchorhina aurita, classifying it as a non-primary host. In addition, the sample size was so low for L. aurita

(1) that it was not considered representative of the species. Also, Artibeus jamaicensis was found with 2 different species of bat flies, but one of them, Trichobius angulatus

Wenzel, had a sample size of only four. While it is considered a primary association according to the 5% cut off rule, it was not considered for further analysis. Primary associations were also found between, Trichobius galei Wenzel and Natalus mexicanus

(100%) and between Megistopoda aranea Coquillett and A. jamaicensis (100%).

TABLE I Summary of bat species and their ectoparasites collected in Utila, Honduras with!total! sample!size!(n)!and!prevalence!(percent!of!infested!bat!species)! !

! 9! All of the bat fly species and their associated hosts in this study were recently described for Honduras (although no sites on Utila were sampled) by Dick (2013), except for Trichobius angulatus Wenzel. Trichobius galei Wenzel, found on N. mexicanus, was the most abundant bat fly and constituted a significantly higher parasite load and parasite intensity compared to the parasite species found on G. soricina and A. jamaicensis. Not a single host of this bat fly was found without at least one parasite.

Prevalence was not significantly different between N. mexicanus and A. jamaicensis (p=1.000). However, prevalence for G. soricina was significantly different from both N. mexicanus and A. jamaicensis (p=0.001). Prevalence did not differ significantly among males and females of G. soricina (p=0.1928), N. mexicanus

(p=1.000), nor A. jamaicensis (p=0.5840). Also, in general, bat species with higher prevalence also had higher parasite load and intensity (Table II).

Parasite load was significantly different for all species; F (2.114)=47, p<0.001.

However, there was no overall difference in parasite load between males and females across species; F (1,114)=0.015, p =0.903. Also, the difference in parasite load between males and females across species is consistent; F (2,114)=0.645, p=0.527. N. mexicanus had significantly higher parasite load (Table II).

Parasite intensity was not significantly different between G. soricina and A. jamaicensis; t(89)=0.50, p=0.6199. Intensity was significantly different between G. soricina and N. mexicanus; t(89)=8.04, p<0.001. It was also significantly different for A. jamaicensis and N. mexicanus; t(58)=5.58, p<0.001. N. mexicanus had significantly higher parasite intensity (Table II). Parasite intensity was not significantly different between males and females of any species.

! 10! Parasite sex did not vary significantly among G. soricina and A. jamaicensis

hosts. However, male parasites were significantly more prevalent than female parasites

on N. mexicanus (p<0.001) (Table III).

TABLE II Ectoparasite prevalence (percent of infected bats), mean load (average number of parasite found on bat, and mean intensity (average number of parasites found on infested bats) for bat flies on male and female bat hosts. Number in parentheses refers to samples size

! 11!

TABLE III Numbers of males and females and the sex ratio of bat fly species !

There was no significant correlation between ectoparasite load and the physical condition of the bats. Specifically, there was no relationship between parasite load and bat body mass, nor between parasite load and the health indicator for any species. When bat species were examined by sex, there was still no relationship found between these variables (Table IV).

! 12! TABLE IV Correlation coefficients for parasite load and bat body mass and for parasite load and health of males and females of three bat species. No relationships showed significant Pearson correlations. !

.

! 13! CHAPTER 3

DISCUSSION

G. soricina had a lower proportion of infested individuals, or prevalence, than both A. jamaicensis and N. mexicanus. There was no preference for male or female hosts, similar to results reported by Patterson et al (2008). Parasite load and intensity were significantly higher for N. mexicanus. However, both variables were not significantly different between host sex of any species. In accordance with recent research, the bat flies in this study showed consistent primary associations and apparent parasite impact on bat health was minimal.

Research on a broader scale and with larger sample sizes of bat and bat fly species would establish host specificity based on a specificity index (SI). The SI is calculated for each host-parasite association and represents the proportion of individual ectoparasite species found on a particular host while accounting for the phylogeny of hosts (Aguiar and Antonini 2011, Dick and Gettinger 2014, Presley 2010, Stamper 2012). Considering the small number of host-parasite relationships in this study, calculating this value was not appropriate. However, it is relevant that the parasites observed were consistently associated with the same host. The one exception was a single T. dugesii found on the host, L. aurita, but this was considered cross contamination as this was the only time this bat species was found in the cave during the duration of the study (Table I). Based on patterns observed in this study it is likely that these bat fly species would have a relatively high SI if enough information were available to make the calculation possible.

There was a distinct bias in sex ratios among the parasites sampled. In the two species of parasites collected from the cave dwelling bats there were between 1.5 and 2

! 14! times more males than females. Male-biased sex ratio could be a result of pre-partum bias, selective grooming, difference in dispersal ability, male longevity, or sampling bias

(Dick & Patterson 2008). Further explanation of these varying sex ratios could provide a greater understanding of the life-history of bat flies.

These bat flies are shown to maintain primary associations despite the lack of dispersal barriers. The two cave roosting bats in this study were observed roosting amongst each other. Often N. mexicanus were observed roosting within clusters of G. soricina, in direct contact with heterospecific bats. However, this may have been a result of human disturbance. Nevertheless, different species groups of roosting bats were always within close proximity to each other. The limited cave openings required different bat species to use the same area to enter or exit the cave, and even when bats enter and exit at different times, they utilize the same flyway passages in the cave. Pupae of T. galei Wenzel are predominately found in the fly way passages in the cave and at times more than 20 meters from the nearest roosting bats (Dittmar et al. 2009). While a high presence in flyway passages may facilitate finding a host, it also allows opportunities for inhabiting non-primary hosts.

Since physical barriers to non-primary hosts are not apparently a factor here, the strong bat-bat fly relationships observed for the cave dwelling bats are likely attributed to the strong association of these species throughout evolutionary history. The roosting ecology or distribution of bat species could have influenced the specialization of their bat fly parasites. This study was conducted on an island, so physical isolation or migrations events may also have contributed to the strong primary associations observed in these

! 15! particular bat fly species. Limited number of sample species did not allow for the classification of bat flies as monoxenous or otherwise.

G. soricina and N. mexicanus are cave dwellers, while A. jamaicensis roosts in a variety of structures, primarily tree hallows, foliage and other forms of less permanent roosts. N. mexicanus, is specifically known for high roost fidelity (Dittmar et al. 2009).

Parasite differences between permanent & non-permanent roost structures were not explored in the primary methods and results sections due to lack of species variation and certainty in roosting habits. However, an unpaired t-test did show that parasite load did not vary significantly between cave roosting bats and non cave roosting bats; t(119)=1.3832, p=0.1692. However, parasite intensity was significantly higher for cave roosting bats; t(119)=2.9354, p=0.0040.

Hosts receive no known benefit from their ectoparasites (Dick et al 2003), yet this study and others showed no direct impact on bat health from parasites. A more holistic understanding of the impact parasites have on bat health could offer valuable information on the coevolution of particular host and parasites. There are many cases where parasites have evolved to use molecule mimicry, or similar immune signaling molecules, to avoid host immunosurveillance (Salzet et al. 2000). Some studies of bat flies suggest that this could be present and could possibly aid in the explanation of high host specificity (Dick

& Patterson 2007). Immunocompatibilty may also explain why there is no apparent impact on bat health.

Limitations

The primary limitations to this study were small sample sizes and a short duration for data collection. While the methods were carefully selected to best suit the study

! 16! design, they also had some drawbacks. Bat flies, especially streblids, are known to vacate the host when it is stressed (Dick 2007). Parasite density was most likely underestimated, although, the same person removed the parasites from all bats. The sampling effort, in terms of swiftness and thoroughness, was as consistent as possible. The host-site on the body was not taken into account because the bat flies were too mobile on the host to accurately judge their original location on the bat.

Many variables come into play when considering an organism’s health or well- being. Therefore, the estimation of health used in this and other studies may not be the most accurate indicator of the bats’ physical state. At the very least, it is a factor that should be monitored on a temporal scale. Parasite size should have also been taken into account when estimating parasite load, considering larger parasites may have a greater impact than smaller parasites. Overall, the study was relatively short and the data set would have benefited from a study that captured the bat populations at different seasons or for a longer amount of time.

Conclusion

Host-parasite systems are important to understanding community ecology and variation in biodiversity. Factors supporting host specificity along with information on historical, ecological, or physical isolation can contribute to understanding coevolution of host and parasites. The phylogeny for bat fly families is unresolved, but it could offer critical information regarding speciation among bat ectoparasites. Controlled experimental studies could also contribute a great deal to understanding host preference.

Despite their negative reputation, parasites play an important role in nature.

Parasites apply selective pressure on host populations by impacting fitness and

! 17! population dynamics, and in many cases attribute to the regulation of healthy host populations (Pilosof et al. 2012). Bats are well known for their significant ecological role as predators, pollinators, and seed dispersers. With both hosts and parasites in mind, the maintenance of all sources of biodiversity is essential for ecological stability.

While this was the first study undertaken on the bat and bat fly fauna in the cave on the island of Utila, it might be the beginning of more systematic and long-term research. The current research further solidifies the understanding of bat-bat fly associations by examining parasitism rates and parasite impacts on cave roosting and non-cave roosting bat species. Future exploration of host specificity of obligate ectoparasites can reveal important information regarding community structure, cospeciation and biodiversity, which all facilitate the conservation of healthy ecosystems.

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