Ectoparasite abundance and d iversity on farm a nim als in Monteverde and San Luis along an elevation g radient Sarah Callahan Department of Ecology and Evolutionary Biology University of California, Los Angeles EAP Tropical Biology and Conservation Program, Fall 2016 16 December 2016 ABSTRACT Abundance and diversity of arthropods are largely dependent on climate Elevation gradients provide different microclimates that can support a unique number and variety of species. In order to test the effect of elevation on abundance and diversity of arthropod ectoparasite s I collected samples on four different farms: Life Monteverde and Benito in Monteverde at about 1,800 m and Le lo Ma far m in San Luis around 700 m. At each elevation, I compared abundance and diversity of ectoparasites on dogs and cattle. I found a presence of Ctenocephalides and Pulex fleas on dogs, and 22 different morphospecies of ticks on cattle. Trends in the data show a higher abundance of fleas and a greater diversity of tick morphospecies sampled at low elevation. It is likely that ectoparasites will experience a change in abundance and distribution among and between elevations as global warmi ng continues to adjust microclimates. Therefore, it is important to understand their current abundance and distribution to best prepare for the effects of climate change. Additionally, d ata from goat samples collected on the farms in Monteverde reveal a pr esence of Damalinia caprae lice. The higher number of adult and total lice on Life Monteverde indicate s a more established population than the nymph dominated population on goats at Benito This difference in abundance is due to differing ectoparasite control practices and living conditions of animals on each farm. Difference in lice abundance between farms at the same elevation is evidence that ectoparasite abundance can be controlled through best practice management. Abundancia y d iversidad de ectoparsitos en a nimales de f incas e n Monteverde y San Luis RESUMEN La abundancia y diversidad de artrpodos dependen mucho del clima. Los gradientes de elevacin proveen diferentes microclimas que pu eden mantener una nica y variada composicin de especies. Para evaluar el efecto de la elevacin en la abundancia y diversidad de artrpodos ectoparsitos, yo recolect muestras en cuatro diferentes fincas: Life Monteverde y de Benito Guindon en Monteverd e a alrededor de 1800 msnm, y las de Lelo Mata y Tima Sales en el Valle de San Luis, cerca de los 700 msnm. En cada elevacin, yo compar la abundancia y diversidad de ectoparsitos en perros y vacas. Detect pulgas de Ctenocephalides y de Pulex en perros y 22 morfo especies de garrapatas en las vacas. Las tendencias en los datos muestran mayor abundancia de pulgas y mayor variedad en las morfoespecies de garrapatas muestreadas a menor elevacin. Es de esperar que los ectoparsitos cambien en abundancia y distribucin dentro y entre elevaciones a medida que contine el calentamiento global. Es importante entender sus distribuciones actuales y prepararse para los efectos de cambio de clima. Adicionalmente, datos
de muestreos en cabras en Monteverde revel la presencia de piojos Damalinia caprae El mayor nmero de piojos adultos y nmero total de piojos en Life Monteverde, indica una poblacin mejor establecida que la poblacin dominada por ninfas encontrada en la finca de Benito Guindon. Esta diferencia en a bundancia se debe a diferencia en prcticas de control sobre ectoparsitos, as como condiciones generales de los animales. Diferencias en abundancia de piojos entre las fincas a la misma elevacin es evidencia que su abundancia puede ser controlada median te buenas prcticas de manejo. The rising global temperature is altering the distribution of microclimates which is in turn affecting the distribution of many organisms. It is predicted that changes in temperature, precipitation, humidity and other c limatic factors will affect the reproduction and population dynamics of parasite arthropod vectors of disease (Gage et al 2008). Increasing temperatures are projected to expand the distribution of these arthropods, and with the m, the diseases they carry, which could endanger host communities parasitized by these vectors ( Zamora Vilchis et al 2012). Historically the low temperature climate of the high elevations helps to reduce the abundance of parasite vectors. Other factors such as reduced habitat, reduced resource diversity, and reduced primary productivity at high elevations also contribute to the lack of arthropods (Zamora Vilchis et al 2012; McCoy, 1990). In contrast, the higher temperatures and higher humidity in lowland areas provide an ideal environment for reproduction of these disease carrying parasites However, the rising global temperatures are causing the disappearance of the factors that have kept ectoparasites out of the lowlands. This could lead to an increased prevalence of parasitic arthropods at higher elevations ( Zamora Vilchis et al 2012). Parasites affect all mammal species, and can be especially troublesome for domesticated mammals. Ectoparasites can be present on the surface of the entire body of farm animals such as cattle, goats, and even cats and dogs. Because t hese an imals live in such close quarters, ectoparasites are easily transferred among individuals (Poissant et al 2008). Farmers need to know which species are currently parasitizing their animals, and what species are likely to parasitize them in the future in order to control parasite populations If not controlled, the ectoparasite load on an animal will begin to affect i ts health, resulting in losses of livestock production including milk, meat, and pelt sales that exceed $2.26 billion annually (Byford et al 1992). Additionally, this topic is relevant to human health, as some ectoparasites are known to be vectors of dise ase that affect humans For example, a specific type of flea called the Pulex irritans is able to feed from a variety of mammals, including cats, dogs, goats and humans, and also has been known to transmit plague which is a zoonotic disease that can be tra nsferred to human beings (Bitam et al 2009). Additionally, ticks from the genus Ixodes which are often present on cattle and other livestock, can cause Lyme disease in humans (Kasper, 2015). It is even easier for diseases caused by ectoparasites to be tr ansferred between domesticated animal populations to wild ones, introducing a new source of problems regarding controlling ectoparasites and disease in the wild. However, farmers have the power to control the transmission of ectoparasites on their farm animals, lessening the impact on wildlife and the chances of transmitting disease. Through certain management practices, such as burning and clearing fields of poten tial ectoparasite harboring vegetation creating larger living spaces and grazing areas to limit contact between
animals, and regularly grooming and treating animals for ectoparasites ectoparasite populations can better avoided or controlled (Texas A&M Agrilife Extension, 2016 ; Smith, 2010 ) A study by Stanko and others (2002) found that host density has a major influence on the species richness of ectoparasite communities. This emphasizes the importance of keeping populations at low density by providing adequate sized living spaces. Additionally, insecticide treatments such as sprays, dips, pour ons, dust, and others are also important for controlling ectoparasite population numbers ( Cornell Department of Entomology, 2016 ) It is important for farmers to become educated about the time of the year that is most effective to administer specific ectoparasite treatments, the safest and most effective dosage for each and the frequency with which to treat their animals to achieve the most effective results As the weather changes and distribution of these ectoparasites adjusts over time, this could result in a newfound struggle to control population s of ectoparasites. There is not much literature on ectoparasite abundance and diversity on farm ani mals at different elevations. It is important to recognize current abundance and diversity patterns in order to better understand environmental preferences of ectoparasites, and how the changing climate could affect these patterns in the future. Past studi es support a correlation between arthropod abundance and elevation, though I could not find any literature about the effect of elevation gradient on ectoparasite s specifically This led me to ask whether ectoparasite abundance and diversity does differ bet ween high and low elevation. Due to the fact that it is more difficult for most arthropods to survive in a high elevation environment with lower humidity, cooler temperatures, and reduced resource diversity (Zamora Vilchis et al 2012; McCoy, 1990), I predict ed that the abundance and diversity of ectoparasites on animals would be lower at high elevation farms and higher at low elevation farms. Additionally, because previous studies indicate a correlation between host dens ity and ectoparasite diversity and livestock management recommends frequent ectoparasite treatment, I predicted that animals on same elevation farms with larger living spaces more recent ectoparasite treatment would sustain lower ectoparasite abundance and diversity. MATERIALS AND METHODS STUDY SITES -Between the dates of 21 November 2016 to 26 I collected samples on four different farms in Monteverde, Puntarenas, Costa Rica. This includes Life Monteverde (High 1) (High 2) in Monteverde at about 1,800 m a nd Lelo Ma (Low 1) s farm (Low 2) in San Luis around 700 m. STUDY SUBJECTS -Dogs Goats Cattle Life Monteverde (High 1) 3 5 Benito Guindon (High 2) 1 5 4 Lelo Ma ta (Low 1) 4 5 Tim Sayles (Low 2) 2 6
SAMPLING METHOD S -DOGS -I ran a thin pronged lice brush through the hair on the rear end of the dog, and placed my finger on any fleas on the comb. I then pinched the fleas and place d them in a small plastic tube filled with alcohol to kill and preserve them. I repeated this process a total of 5 times on the rear end of the dog, and 3 times near the h ead and collar area. If the dog hair was too long to pass through the comb, I would spend no more than 5 minutes searching through the hair near the rear end and another 5 minutes searching near the head and collar a rea for a total of 10 minutes per dog. CATTLE -To sample the coat, I ran the thin back, and used a plastic Ziploc bag to collect the sample of hair and ectoparasites off the brush. I This process resulted in a total of 4 brush samples from each cattle. In order to remove ticks embedded in the skin, I used tweezers to collect ticks off the entirety of the body, focusing on the most areas with the highest concentration of ticks: on the udder and the rear end underneath the tail. I then placed the ticks in and small plastic tubes filled with alcohol. GOATS I used the same method used to sample the coat of the cattle. IDENTIFYING/CATEGORIZING ECTOPARASITES -I viewed all of the ectoparasites in a P etr i dish with alcohol under a dissecting microscope from 10x to 40x magnification. I identified fleas and lice to genus level using identification charts and descriptions from the Chittagong Veterinary School, and Cornell University Veterinary Entomology websites ( Cornell Department of Entomology, 2016 ; Texas A&M Agrilife Extension, 2016 ). I categorized ticks into morphospecies using shape, design and coloration. RESULTS DOGS Both higher elevation farms had a smaller average number of fleas per dog than the lower elevation farms. The averages show a difference of 5.83 more fleas per dog at low elevation farms (Figure 1 ). Both Ctenocephalides and Pulex genera of fleas were present at high and low elevation although the Ctenocephalides genus was absent at a high elevation farm, and the Pulex genus was absent at a low elevation farm. There were more individuals of both species found at low elevation compared to high elevation and about twice as many Ctenocephalides than Pulex individuals (Table 1 ). There was an average of 11 fleas per dog across the entire sample size and a single dog sampled on Low 1 with a fle a abundance value of 33; three times the av erage flea abundance (Figure 2 ). This indiv idual accounted for 30% of the total fleas collected.
Figure 1. Dog Flea Abundance. Shows the average number of fleas collected off each dog at each farm. High 1 and High 2 are shown first followed by Low 1 and Low 2 averages. Finally, the total flea per dog average of high elevation and low elevation farms is presented. Table 1 : Dog Fle a Species Diversity. Shows the number of Ctenocephalides and Pulex individuals on each farm. Farm Ctenocephalides Pulex High 1 10 8 High 2 0 2 Low 1 33 20 Low 2 17 0 Figure 2 Distribution of Fleas on Dogs. Shows the total number of fleas sampled from each dog on each far m. CATTLE There was a lower number of tick morphosp ecies present at high elevation than at low elevation. There were also fewer unique morphospecies found on the high elevation farm than the low elevation farms (Table 2). There were only 2 overlapping morphospecies of tick between 8,6 4 14,75 10,5 7.5 13.33 0,0 5,0 10,0 15,0 20,0 25,0 30,0 Average Number of Fleas High 1 High 2 Low 1 Low 2 Avg High Avg Low 10 9 7 4 8 14 33 4 15 6 0 5 10 15 20 25 30 35 Number of Fleas Individual Dogs High 1 High 2 Low 1 Low 2
the low elevation farms. There were 7 morphospecies total found at h igh elevation with 3 species only found at this elevation, and 19 morphospecies total found at low elevation with 15 species only found at this elevation with an overlap of 4 species between the two elevations. The average number of tick species at each pe r cattle was 1.72 at low elevation, and 1.75 at high elevation, resulting in .03 more at low elevation. The average number of unique tick species per cattle was 1.36 at low elevation and .75 at high elevation, resulting in 0.61 more at low elevation (Table 3). Of the 22 morphospecies collected, only 9% of the species were present on all three farms, 14% were present on two farms, and 77% were present on only one farm. Table 2: Number of Morphospecies of Ticks on Cattle Per Farm. Shows number of different morphospecies and unique morphospecies of ticks collected off cattle on each farm Farm # Species #Unique Species High 1 7 3 Low 1 8 4 Low 2 14 11 Table 3: Tick Species Presence. Shows the number of species sampled off cattle at each elevation, the number of species found at both and the number of unique species found at each, and their averages for each elevation. Elevation # Species Average # Species # Unique Species Average # U nique Species High 7 1.75 3 0.75 Low 19 1.72 15 1.36 GOATS There were approximately twice as many lice collected on High 1 than on High 2 with an average number of 10.6 lice per goat on High 1 and 5.4 lice per goat on High 2. There were about 4.5 times more adult Damalinia caprae lice on High 1 than High 2, and a similar number of Damalinia caprae nymphs present on High 2 and High 1. On High 1, the ratio of adults to nymphs was about 2:1, and on High 2, the ratio was about 1:2 (Figure 3 ) The distribution of lice on goats shows an average of 8 lice per goat. There were three individuals on High 1 with higher than average lice abundances of 10, 18, and 20. There was one individual on High 2 with an above average lice abundance value, 18. There was only one goat with a lice abundanc e value of 0, sampled on High 2 (Fig ure 4).
Ectoparasite Abundance and Diversity Along an Elevation Gradient Callahan 7 Figure 3 Goat Lice Abundance and Diversity. Shows the total number of lice sampled at each life stage on goats at each farm, both at high elevation. The graph also shows the total average lice per goat on each farm. Figure 4 Distribution of Lice on Goats Shows the total number of lice sampled from each goat on each farm at high elevation DISCUSSION DOGS The general trend of higher abundance of fleas sampled on the lower elevation farms supports my prediction and could be due to a difference in environmental factors. Higher elevations are cooler, and experience more fluctuations in temperature than the warmer, and more stable temperatures found at lower environments (McCoy, 1990) According to Haas (1965), fleas ex perience the highest proliferation rates in locations with a warm, stable climate, and high percent relatively humidity. These environmental aspects are more consistent with the climate at lower elevations, which is likely why there was a higher abundance of fleas at low elevation in this study. Damalinia caprae 36 D. caprae nymph 17 Damalinia caprae 8 D. caprae nymph 19 High 1 10.6 High 2 5.4 0 5 10 15 20 25 30 35 40 Number of Lice High 1 High 2 Averages 18 10 4 20 1 3 18 5 1 0 0 5 10 15 20 25 Number of Lice Individual Goat High 1 High 2
Ectoparasite Abundance and Diversity Along an Elevation Gradient Callahan 8 Though both species of fleas are present at both elevations, one high elevation farm only had Pulex fleas present, while another farm only had Ctenocephalides present (Table 1) This shows a slight preference for survival of one species over the other on different farms. A previous study by Duyck and collaborators (2006) about climatic niche partitioning of fruit flies found that some climatic niches were able to promote coexistence between four fly species. Resea rchers discovered that each fly species exhibited a clear preference for a specific climate based on the tolerances limits of each species. This ultimately led to niche segregation at each environment, allowing the four species to share a general area with unique preference for specific microclimates. This same pattern of niche partitioning could be occurring between Ctenocephalides and Pulex fleas along the elevation gradient, resulting in a d ifferent abundance of each at different elevation s The data also shows that the total species abundance between the two species was about the same at high elevation, but that Ctenocephalides fleas greatly outnumber ed Pulex fleas at low elevation. In a previous study on flea species infestations on dogs, it was found that 65.1% of the dogs were infested with Ctenocephalides alone, while only 18.6% of dogs were infested by Pulex alone. An even fewer percentage of dogs were infested with both species of flea (Yore et al 2013). This also found that Ctenoceph alides were the most abundant species of flea It is likely that this genus is better equipped to outcompete Pulex fleas, which is why my data shows twice as many Ctenocephalides individuals than Pulex individual s found on dogs (Table 1) This emphasizes the importance of understanding diversity of ectoparasites in order to best control a specific population. CATTLE Low ele vation farms had a greater number and average number of morpho species as well as a greater number and average number of unique morpho species only found at that elevation when compared to the high elevation farms (Table 3). This higher diversity of species supports my prediction and is likely due to the fa ct that the environment at lower elevation s is w armer and more humid (McCoy, 1990) In order to survive, ticks need a humidity levels above their critical equilibrium humidity. They are dependent on moist microenvironments, which help prevent total body water loss and drops in hemolymph volume at low hu midity (Hair et al 1975). In a similar study of insects along an elevation gradient, it was found that maximum species richness was most often documented at the lowest elevation sampled (McCoy, 1990). E vidence also suggests that species turnover at relatively high rates is more plausible at lower elevations, further supporting its higher species richness (McCoy, 1990). This could also be because of larger number of herbivorous insect larvae, parasitoids, and insect predators are more abundant at higher elevations (McCoy, 1990). This helps support my data showing that there is higher tick morpho species abundance at lower elevations where the higher humidity provides a more favorable environment and there a re fewer insect predators. There was a greater percentage of morpho species that were present at just one farm than those that were present on multiple farms, with an ov erlap of 2 morphospecies between low elevation farms, and 4 morphospecies between high and low elevation. This lack of overlap between tick morpho species on different farms is likely due to the fact that cattle from different farm environments are not in direct contact with each other and have limited roaming range, so there is no direct cat tle to cattle transmission of ticks between cattle at different farms. They would have to be transmitted by some other source that is able to travel between different farm environments, such as another wild mammal. Even in this case, there are other factor s such as
Ectoparasite Abundance and Diversity Along an Elevation Gradient Callahan 9 climate and predation that could limit a during or after transmission The presence of specific species at each elevation provides further insight into area specific tick diversity There were only 3 species of tick that were foun d only at high elevation in contr ast with 15 species found only in low elevation. This supports my prediction based on the hypothesis that the environment at low elevation is much more favorable for tick survival, allowing higher carrying capacity of ticks, more species diversity, and higher rates of species turnover (McCoy, 1990). It is likely that more of these species would be present at high elevation if they were able to survive in that climatic niche. GOATS Goats sampled on High 1 had about twice as many adult lice as nymph lice and goats on High 2 had about t wice as many nymphs as adults. The se patterns are inverses of each other, indicating that each farm lice population was at a different point in the ir life cycle at the time of sampling. The nymphs were between 10 20 days old at the time of sampling and are not able to reproduce and the adult lice were more than 35 days old with developed ovipositors and are therefore able to reproduce (Murray and Gordon, 1968) The fact that there were more adults on and a greater total number of lice on High 1 indicates that this lice population is older and therefore more esta blished. The large amount of reproductive adults on this farm indicates a mature population with a potential for exponential population growth. Due to the fact that lice reach reproductive maturity after 35 days combined with the amount of mature lice present, it is likely that that population had been reproducing for numerous months On High 2, the greater presence of lice nymphs than adults indicates a more newly introduced lice population. The presence of more nymph lice under 20 days old than adult lice over 35 days old indicate that this population is most likely a newer population that has not been reproducing for more than a few months. Th ough both farms are at a similar elevation with similar climate, th ere were almost twice as many lice on High 1 than High 2 (Fi gure 3). This coul d have been due to a variety of factors, such as size of indoor living space, density of goats, amount of time spent outdoors, and frequency and intensity of ectoparasite treatme nt ( Smith, 2010). The farm, High 1, had 14 goats total that live d in an outdoor enclosure of about 2 00 square meters The second farm, High 2, had 24 adult goats that lived in an outdoor area of more than 20,000 square meters High 2 had 100 times more square meters than High 1 for less than two times the amount of goats. Also, the goats at High 2 are let out to graze all day, and only brought in at night, while the goats at High 1 are let out an average of 6 hours per day Additionally, the indoor livin g area was relatively small on High 1, and larger on High 2. Consistent with my prediction, smaller indoor and outdoor areas and less time spent outside likely contribute to why goats on High 1 had higher lice counts than those on High 2. Higher concentrations of animals in smaller conditions allows for more contact, which results in more opportunities for transmission of lice between individuals. Also, less time spent outside means that th e goats have less sun exposure. According to Smith (2010), sun exposure can be a method for driving out overheated lice. As supported by my findings, in order to achieve best control of ectoparasite abundance, indoor and outdoor living spaces should be plenty large enough for the population of hosts to av oid transmission by contact. At the time I took the samples, the goats on High 1 had not been treated for lice in over a year using the injectable deparasitizer, Interex However, the goats on High 2 had been treated
Ectoparasite Abundance and Diversity Along an Elevation Gradient Callahan 10 about 2 weeks before I had taken my s amples. The internal deparasitizer BioMac, used by High 2 aims to kill adult lice by putting chemicals in the blood that kill the lice that feed on it. However, the eggs are not killed by this treatment, which is why I saw a higher abundance of nymphs 14 days later. Because lice eggs hatch into nymphs after 10 days, it is important to treat the animal again between 10 and 20 days later so that you make sure to kill all of the nymph lice before they turn into reproductive adults. The difference in abundance of lice and the time since anti ectoparasite treatments shows the importance in treatment in maintaining ectoparasites at a lower abundance and provides support to my prediction In general, treatments should be administered on time and in the correct qu antity in accordance with the instructions in order to best control ectoparasites. Lastly, understanding the life cycle of the ectoparasites that inhabit each animal and the way that the medication rids of these pests could reveal additional methods to bes t control the population, such as administering anti parasite medication 10 20 days after the initial dose, or allowing goats to gra ze for longer in the sun to drive out lice ( Smith, 2010 ). I observed a pattern of individual goats and dogs carrying an exponentially greater ectoparasite load than average Certain individual goats carried more than twice the average number of lice, and an individual dog carried three times as many fleas than average. This could be explained by the lifecycle a nd behavior of lice and fleas. Both of these ectoparasites lay eggs on their host, and those eggs hatch and begin feeding off the host. Unless their current host is in contact with a mor e desirable host or the flea population has reached carrying capacity, it is likely that the ectoparasites would remain concentrated on the single host. Previous research has shown that ectoparasites do also exercise host preference. This usually depends on host temperature conditions, skin thickness and texture, extensiv ene ss of peripheral circulation, consistent hair growth, and well regulated body temperature (Prasad, 1987 ; Prasad, 1969 ). Additional variables, including h ormones, sex, and health of a host can also affect ectoparasite preference (Ali et al 1966 ; Ferrari et al 2003 ). These factors would allow the population of ectoparasites to proliferate on specific individuals, resulting in much larger abundance than average. It is likely that these desired hosts are vectors for transmission of ectoparasites to other indi viduals. In a past study of transmission of lice to between goats, Hallam (1985) found that goats could be infested with lice from another individual f rom as few as 14 days of contact After 13 weeks of contact, there was a relatively similar abundance of l ice on each individual within t he sample group. This idea of ectoparasites spreading from one heavily infested individual to others likely happens in a similar manner for most ectoparasites. Some, such as fleas that can jump, may be able to spread more qui ckly and exercise more host preference than those that are la rgely stationary, such as lice. This emphasizes the importance of administering frequent treatmen ts to all animals to avoid heavily concentrated parasite loads and tran smission of lice to other individuals. GENERAL As climate change continues to alter and adjust species distribution, ectoparasites will likely begin to move to a higher elevation, similar to the adjustment patterns seen in plants and other animals ( Lenour et al 2008). With the c hanging distribution of these ectoparasites comes a change in distribution of the diseases associated with them. This creates new challenges for farmers, especially those at high elevation in dealing with a high er abundance and new diversity of ectoparasites This could cause a decline in health of animals caused by ectoparasite load, resulting in livestock profit loss (Byford et al 1992). It also could result in greater presence of
Ectoparasite Abundance and Diversity Along an Elevation Gradient Callahan 11 disease that affects not only livestock, but also wild animals, and even humans (Bitam et al 2009). However, with the proper knowledge and res ources, ectoparasite populations can be efficiently controlled (Smith, 2010). This study provides information regarding the abundance and diversity of fleas, ticks, and lice on farms at two elevations, which can provide insight into how the distribution of ectoparasites may change as a result of climate change causing warming of higher elevations in the future. E ctoparasites have the potential to be the subject of applicable studies in the future. The correlation between specific microclimates and ectoparasite diversity and abundance could be better established if ectoparasites and temperature, humidity and climate stability data were collected at farms. Also, it would be insightful to study the impact of ectoparasites on animals by quantifying the number and diversity of ectoparasites on an animal and measuring its vital signs to determining if there is a correlation between ectoparasite load and general health o f the animal. ACKNOWLEDGEMENTS Thank you to the farm owners Guillermo Vargas Benito Guindon, Lelo Mata, and Tim Sayles for letting me take samples from their animals and the Monteverde Institute for letting me use their lab space Thank you to Eric McAdam, Flix Salazar, and Federico Chinchilla for helping me to collect dozens of ectoparasites off sometimes uncooperative animals, and for the patience and guidance from my professors, Federico Chinchilla, Andrs Camacho, Frank Joyce, Emi lia Triana, Sof ia Arce Flores, and Justin Welch. Special thanks to the Segura Vega Family for hosting and supporting me during this project and making me feel so welcome! Lastly, thanks to my parents for making this incredible experience possible for me. SOURCES CITED Ali, Sami R., and Gordon K. Sweatman. 1 966 Effect of age, sex, and hormone treatment of the mouse on the level of infestation by R hipicephalus sanguineus larvae. The Journal of Parasitology 407 412. Bitam, Idir 2010 Fleas and flea borne diseases. Inte rnational J ournal of I nfectious D iseases 14.8 : e667 e676. Byford, R. L., M. E. Craig, and B. L. Crosby 1992 A Review of Ec toparasites and Their Effect on Cattle Production. Journal of Animal Science 70 : 597. Web. Cornell De partment of Entomology. Veterinary Entomology. Arthropod Identification Cornell n.d. Web. 14 Dec. 2016. D uyck, P Pat rice D and S Quilici. 2 006 Climatic niche partitioning following successive invasions by fruit flies in La Runion Journal of Animal Ecology 75.2 : 518 526.
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