Ectoparasites and their avian hosts in the forests of Monteverde, Costa Rica


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Ectoparasites and their avian hosts in the forests of Monteverde, Costa Rica

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Ectoparasites and their avian hosts in the forests of Monteverde, Costa Rica
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Ectoparásitos y sus aves hospederas en Monteverde, Costa Rica
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Ferguson, Grace E.
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The term ectoparasite is defined as any parasite that lives on the outside of its host. On avian hosts, they occupy either the skin or feathers, consuming blood and tissue to provide the necessary nutrients to live and reproduce. In return, these tiny residents can cause harm to their hosts by transmitting disease and damaging important tissues. What is yet to be fully understood about this relationship between these parasites and their hosts is whether or not there is a clear correlation between characteristics of the host and the number and type of ectoparasites it carries. The main question of this study was whether or not it is possible to predict the abundance of ectoparasites on birds based on a number of characteristics of the host including their diet, the level of forest the inhabit, their social interactions, and their taxonomy. I mist-netted birds at three forested sites in the Monteverde area, examining each bird caught for the number and type of parasites it carried, and compiled that information with other research on the species of birds caught to answer this central question. My findings indicate that birds who spend most of their time in pairs have fewer parasites and that birds who consume mostly fruits and insects are likely to carry more parasites on average, however the abundance of ectoparasites is generally very variable. In addition, birds in pairs are far less likely to have ectoparasites present, which suggests an ecological benefit to a paired behavior strategy. ( ,, )
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Los ectoparásitos son parásitos que están fuera del cuerpo del organismo hospedero. En las aves ellos se encuentran en la piel o en las plumas, consumiendo sangre y otros tejidos que proveen los nutrientes necesarios para su vida y reproducción. Los ectoparásitos pueden causar daños a sus hospederos al transmitir enfermedades y dañar sus tejidos. Lo que todavía no se entiende bien acerca de la relación entre ectoparásitos y aves es si existe alguna correlación entre las características de las aves con la cantidad y el tipo de ectoparásitos que llevan. La pregunta principal de este estudio fue si se puede predecir la abundancia de ectoparásitos en aves según ciertas características de los pájaros como su dieta, estrato del bosque en el que habita, interacciones sociales, y grupo taxonómico. Capturé aves en redes de niebla en tres sitios en Monteverde, examiné cada pájaro observando el número y tipo de parásitos que llevaba, y compilé esa información con otras fuentes sobre las especies capturadas. Mis hallazgos indican que los pájaros que permanecen en parejas tienen menos ectoparásitos y los pájaros que consumen principalmente frutos e insectos también llevan en promedio más ectoparásitos, sin embargo, la abundancia de ectoparásitos es por lo general muy variable. Además, los pájaros en parejas son menos propensos a llevar ectoparásitos, lo que sugiere un beneficio ecológico para este comportamiento.
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Student affiliation : Department of Environmental Science, Policy, and Management, College of Natural Resources; University of California, Berkeley
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Ferguson 1 Ectoparasites and their Avian Hosts in the Forests of Monteverde, Costa Rica Grace E. Ferguson Department of Environmental Science, Policy, and Management, College of Natural Resources University of California, Berkeley EAP Tropical Biology and Conservat ion Spring 2019 7 June 2019 ______________________________________________________________________________ AB STRACT The term ectoparasite is defined as any parasite that lives on the outside of its host . On avian hosts, they occupy either the skin or fe athers, consuming blood and tissue to provide the necessary nutrients to live and reproduce. In return, these ti ny residents can cause harm to their hosts by transmitting disease and damaging important tissues. What is yet to be fully understood about this relationship between these parasites and their hosts is whether or not there is a clear correlation between cha racteristics of the host and the number and type of ectoparasites it carries . The main question of this study was whether or not it is possible to predict the abundance of ectoparasites on birds based on a number of characteristics of the host including th eir diet, the level of forest the inhabit, their social interactions , and their taxonomy. I mist netted birds at three forested sites in the Mon teverde area, examining each bird caught for the number and type of parasites it carried, and compiled that info rmation with other research on the species of birds caught to answer this central question. My findings indicate that birds who spend most of th eir time in pa i rs have fewer parasites and that birds who consume mostly fruits and insects are likely to carry more parasites on average, however the abundance of ectoparasites is generally very variable. In addition, birds in pairs are far less likely to have ectoparasites present, which suggests an ecological benefit to a paired behavior strategy. Ectopar ásitos y sus aves hospeder a s en Monteverde, Costa Rica RESUMEN Los ectoparásitos son parásitos que están fuera del cuerpo del organismo hospedero. En las aves ellos se encuentran en la piel o en las plumas, consumiendo sangre y otros tejidos que proveen l os nutrientes necesarios para su vida y reproducción. Los ectoparásitos pueden causar daños a sus hospederos al transmitir enfermedades y dañar sus tejidos. Lo que todavía no se entiende bien acerca de la relación entre ectoparásitos y aves es si existe al guna correlación entre las características de las aves con la cantidad y el tipo de ectoparásitos que llevan. La pregunta principal de este estudio fue si se puede predecir la abundancia de ectoparásitos en aves según ciertas características de los pájaros como su dieta, estrato del bosque en el que habita, interacciones sociales, y grupo taxonómico. Capturé aves en redes de niebla en tres sitios en M onteverde, examiné cada pájaro observando el número y tipo de parásitos que llevaba, y compilé esa informaci ón con otras fuentes sobre las especies capturadas. Mis hallazgos indican que los pájaros que permanecen en parejas tienen menos ectoparásitos y los pájaros que

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Ectoparasites and Avian Hosts in Monteverde Ferguson 2 consumen principalmente frutos e insectos también llevan en promedio más ectoparásitos, sin emb argo, la abundancia de ectoparásitos es por lo general muy variable. Además, los pájaros en parejas son menos propensos a llevar ectoparásitos, lo q ue sugiere un beneficio ecológico para este comportamiento. Ectoparasites have accompanied their avian h osts for many millions of years, relying on their blood, feather, and skin tissue for survival and reproduction (Proctor and Owens 2000). Most ecto parasites have specialized to their hosts to the point that some can only survive without their host for short intervals, if at all (Schmidt and Roberts 2000). This not only strongly affect the diversity of ectoparasites, causing rapid speciation and limit ing genetic mixing between populations, but also reducing the ways in which ectoparasites can be transmitted between hosts (Schmidt and Roberts 2000). While ectoparasites can have major effects on their hosts by transmitting disease, reducing vigo r by dama ging feather and skin tissue , and even consuming nestlings in their entirety , they do not necessarily inhibit normal behavior or life processes and live as many as 80% of wild birds (Proctor and Owens 2000 ; McFarlin and Robinson 2011 ). The ectoparasites that specialize on these wild birds can come in many different shapes and sizes and each has a unique niche that it inhabits (Schmidt and Roberts 2000). Diptera from the Hippoboscidae family are one of these common avian ectoparasites, an d tend to live nea r the skin of the abdomen of birds to feed off of blood and are therefore also transmitters of blood borne diseases (Arnold 1968). In addition, there are Acarid mites , mostly in the family Proctophyllodidae which is a family of feather mi te that is predomi nantly associated with Passerine birds , though they have been documented on many orders (Mirnov et al. 2017). They live on feathers with strong veins in the area between barbs , feeding on feather tissue and debris (Mirnov et al. 2017). T h ere are also ticks (Acarina: Ixodidae) and avian chewing lice (Insecta: Phthiraptera) which occur in lower densities, but remain important members of the avian ectoparasite community (Arnold 1970; Clayton et al. 1992). The prevalence and role they play in the lives of birds around the world makes them a subject worthy of study , especially s ince the population distribution of avian ectoparasites is highly variable . Furthermore, understanding how ectoparasites affect bird communities could make it easier to understand how thes e interactions might change in a future where there is a general dec line in insect abundance and birds continue to face threats from habitat loss and changing climates. To help better understand this dynamic relationship, I asked the question: is it poss ible to predict ectoparasite presence and abundance on the birds ar ound Monteverde based on the characteristics of their hosts? For many of these ectoparasites, they cannot survive without their host (the avian chewing lice are an example of this according to Clayton and coworkers (1992)), so one of my hypotheses is that contact with nestlings and other birds in a flock will affect the number and diversity of ectoparasites on the birds. My other hypothesis rests with the ability of some ectoparasites to sur vive in leaf litter, nest material, and inside flowers (Schmidt and Roberts 2000), so therefore I hypothesized that the time birds spent in contact with these surfaces would impact the number and type of parasites on their bodies.

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Ectoparasites and Avian Hosts in Monteverde Ferguson 3 MATERIALS AND METHODS Mist netting I captured all of my birds for sampling using mist nets in 3 different forest s at different elevations in the Monteverde area: the Rachel and Dwight Crandell Reserve trails, the Monteverde Ecological Sanctuary, and the Santa Elena Reserve. T he timing of ope ning mist nets was very much dependent on weather conditions such as rain or lighting , making the actualized timing of opening and closing variable. In general, nets were opened between 5:15 am and 7:00am and closed sometime between 10 am a nd 11:00 am on t en days over the course of two weeks from May 12 th to May 26 th , accumulating approximately 50 hours spent mist netting. The majority of the time, four 12 meter nets were used, sometimes supplemented by a 6 meter net and sometimes by an addi tional three 12 meter nets. The placement of the nets was deliberate with the intention of catching the most birds, so nets were placed along parts of the trail where more birds were observed, or where nets had been successful in the past. Collection and Identification Every bird was first identified using The Second Edition of The Birds of Costa Rica by Richard Garrigues and Robert Dean, weighed using a spring scale. The examination of the bird included all parts of the bird, first with the naked eye an d later with a m agnifying visor to better view the smaller or more obscured ectoparasites. There was no strict allotted time, but each bird took approximately 5 10 minutes to examine fully. Here again, priority was placed on location of parasites rather th an following a s trict time regimen. In the case of ectoparasite presence, I used tweezers to remove a few individuals from the bird and placed them in a vial with 70% Ethanol solution to preserved. In some cases, the parasites were too scarce to sample, in which case I si mply made a note of their presence and number . In addition to parasites, data was taken on feather condition as an indication of timing of most recent molt, presence of brood patch to indicate whether the bird was currently sitting on a nes t . Mite Identif ication I placed the mites in the 70% Ethanol solution in small sealed vials until they could be identified. The identification process included extracting the mites from the vial with tweezer and placing them on a slide to be viewed unde r a compound mic roscope. The majority of the mites were clearly visible under 100x magnification. I then took pictures of each mite so that the photos could be grouped into fifteen different morphotypes plus at least one species of lice, one tick, and Hipp oboscid flies. M orphotypes were defined based on body shape, length, and hairs present. Analysis After accumulating all of the data and information, I compared mite presence and abundance on the birds based on diet, habitat, feather condition, and prese nce of brood pat ch. To analyze the number of ectoparasites on each bird beyond presence or absence, I assigned scores based on the estimated quantity of ectoparasites on each designated part of the body (head, body, tail, and wings). Anything under ten par asites received parasite load between ten and twenty compared the ave rage scores for each body part against the other factors such as forest level inhabited , diet, brood patch, and species . Any relevant information that could not be gathered in the field, such as behavior, diet, and niche occupied was gathered from A Guide to the Birds of Costa Rica by Stiles and Skutch (1989).

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Ectoparasites and Avian Hosts in Monteverde Ferguson 4 RESULTS In total, I captured 84 birds of 36 species from 14 families. Of the birds captured, there were six general diets, eight described niche categories, and three categories of social behavior. Out of 84 individuals, 6 5 (7 7.4 %) were observed to have at least one of the four different types of ectoparasites. F urther breaking it down into species, there were only four species with no observed parasites and a total of 11 species with less than 50% of individuals having ectoparasites (Table 1). There were five birds (6.0%) with flies and another five birds (6.0%) with lice (identified after collection and observation under a microscope), while the rest of the ectoparasites observed were mites on the feathers of the wings, back of the head or the body. Wings were the most likely to be infested with these mites, with 62 (73.8 % ) birds observed to have mites on the wings versus only eight birds (9.5%) having parasites on their bodies, 25 birds (29.8%) wi th mites on their heads, and 16 birds (19.0%) with mites on their tails. Table 1 : The percent frequency of presence of ectoparasites on each species of bird included in the study. The table is ordered alphabetically by family, wi th the number of individuals included in the average in the column labeled Family Species Ectoparasites Sample Size Cardinalidae Habia fuscicauda 100% 2 Cracidae Chamaepetes unicolor 100% 1 Emberizidae Arremon brunneinucha 100% 2 Emberi zidae Chlorospingus flavopectus 50% 2 Emberizidae Melozone leucotis 50% 2 Furnariidae Dendrocincla homochroa 100% 2 Furnariidae Margorornis rubiginosus 100% 1 Furnariidae Premnoplex brunnescens 25% 4 Furnariidae Sclerurus mexicanus 50% 2 Grallariidae Grallaria guatimalensis 100% 1 Momotidae Momotus coeruliceps 100% 1 Parulidae Basileuterus culicivorus 100% 1 Parulidae Basileuterus rufifrons 100% 1 Parulidae Basileuterus tristriatus 100% 1 Parulidae Myioborus torquatus 100% 1 Parulidae Seiurus au rocapilla 100% 1 Picidae Picoides fumigatus 100% 1 Pipridae Chiroxiphia linearis 67% 9 Strigidae Ciccaba virgata 100% 1 Trochilidae Amazilia saucerrottei 100% 3 Trochilidae Amazilia tzacatl 50% 2 Trochilidae Campylopters hemileucurus 100% 2 Trochili dae Eupherusa eximia 80% 5 Trochilidae Heliodoxa jacula 100% 1

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Ectoparasites and Avian Hosts in Monteverde Ferguson 5 Trochilidae Lampornis calolaemus 100% 5 Trochilidae Phaethornis guy 100% 3 Troglodytidae Henicorhina leucophrys 33% 3 Troglodytidae Henicorhina leucosticta 0% 2 Troglodytidae Thryophilus rufalbus 43% 7 Turdidae Catharus aurantiirostris 100% 1 Turdidae Catharus frantzii 100% 2 Turdidae Catharus fuscater 100% 1 Turdidae Catharus mexicanus 100% 3 Turdidae Myadastes melanops 0% 1 Turdidae Turdus assimilis 100% 1 Tyrannidae Empidonax fla vescens 0% 1 Tyrannidae Mionectes olivaceus 100% 5 Only eleven birds had a brood patch present, but eight of those eleven had parasites (72.7%). Of those with no brood patch, 57 out of 73 birds had parasites (78.1%). Looking at the social behavior, 34 o ut of 39 (87.2%) of solitary birds and 22 out of 27 (8 1.5%) social birds had ectoparasites while only 9 of 18 (50%) of paired birds were positive for ectoparasites. In diets, the carnivore and 100% of the eight Fructivore/Insectivores were observed to have ectoparasites while only 31 of the 45 Insectivores (6 8.9%) and two of the four Omnivores (50%) had any ectoparasites. Of the 19 birds with feathers in excellent condition, only 10 had parasites (52.6%), while birds who were molting or with feather in good or fair condition were 88.9%, 82.8% and 84.4% likely to have parasites, respectively. Lastly, nine of the 12 birds who regularly come into contact with the ground had ectoparasites (75%), while 23 of the 32 birds spending most of their time in the underst ory (71.9%) and 33 of the 40 birds living between the understory and the upper canopy (82.5%) had ectoparasites. After the identification of 15 Acarid mite morphotypes and one Louse morphotype, there was no morphotype that correlated directly to a species of bird , however the data indicate that there is so me connection between family and morphotype (Table 2). There is a morphotype called ur different families, but 71% of the birds carrying this morphotype belonged to the same family: Trochilidae (Table 2). Table 2 : Morphotype of Acarid mite (and one louse) on left with the family and species of bird from which the ectoparasite was extracted. Morph Family Species Louse Trochilidae Lampornis calolaemus Turdidae Catharus mexicanus Emberizidae Arremon brunneinucha Parulidae Myioborus torquatus Grallariidae Grallaria guatimalensis Mite 1 Troglodytidae Henic orhina leucophrys

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Ectoparasites and Avian Hosts in Monteverde Ferguson 6 Parulidae Basileuterus culicivorus Mite 2 Trochilidae Campylopters hemileucurus Emberizidae Arremon brunneinucha Turdidae Catharus mexicanus Turdidae Turdus assimilis Parulidae Basileuterus tristriatus Cardinalidae Habia fus cicauda Mite 3 Emberizidae Arremon brunneinucha Parulidae Basileuterus tristriatus Parulidae Seiurus aurocapilla Mite 4 Trochilidae Lampornis calolaemus Turdidae Turdus assimilis Mite 5 Trochilidae Campylopters hemileucurus Tyrannidae Mionect es olivaceus Mite 6 Pipridae Chiroxiphia linearis Trochilidae Campylopters hemileucurus Trochilidae Lampornis calolaemus Trochilidae Phaethornis guy Tyrannidae Mionectes olivaceus Pipridae Chiroxiphia linearis Pipridae Chiroxiphia linearis Pipridae Chiroxiphia linearis Pipridae Chiroxiphia linearis Mite 7 Trochilidae Lampornis calolaemus Trochilidae Amazilia tzacatl Furnariidae Dendrocincla homochroa Mite 8 Turdidae Catharus mexicanus Tyrannidae Mionectes olivaceus Mite 9 Furna riidae Sclerurus mexicanus Cardinalidae Habia fuscicauda Mite 10 Parulidae Basileuterus rufifrons Trochilidae Amazilia saucerrottei Mite 11 Furnariidae Sclerurus mexicanus Mite 12 Furnariidae Sclerurus mexicanus Tyrannidae Mionectes olivaceus M ite 13 Parulidae Myioborus torquatus Trochilidae Eupherusa eximia Trochilidae Eupherusa eximia Turdidae Catharus aurantiirostris

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Ectoparasites and Avian Hosts in Monteverde Ferguson 7 Mite 14 Trochilidae Campylopters hemileucurus Trochilidae Phaethornis guy Trochilidae Eupherusa eximia Emberizid ae Arremon brunneinucha Troglodytidae Thryophilus rufalbus Trochilidae Amazilia tzacatl Trochilidae Amazilia saucerrottei Mite 15 Troglodytidae Thryophilus rufalbus Troglodytidae Henicorhina leucophrys Cracidae Chamaepetes unicolor Turdidae C atharus fuscater Trochilidae Phaethornis guy Trochilidae Heliodoxa jacula Troglodytidae Thryophilus rufalbus Trochilidae Amazilia saucerrottei Turdidae Catharus aurantiirostris In the next section, bird characteristics were compared against th e average scores of approximate parasite number (from zero to three) to reveal patterns in the number of parasites on each bird. When these average scores were compared against bird diet, birds eating predominantly fruits and insects had, on average, more parasites between the four parts of their bodies, followed by the birds only eating nectar (Fig. 1). In a comparison of average scores to niche space, birds who came regularly come into contact with the ground had fewer average parasites than those who spe nt much of their lives in shrubs or trees (Fig. 2). In the final comparison of average scores to social behavior, birds living in pairs had fewer parasites than both birds who are solitary or social (meaning living in flocks of 3 or more) (Fig. 3).

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Ectoparasites and Avian Hosts in Monteverde Ferguson 8 Fi g. 1 : Comparison of bird diet categories to the average score of each body part to reveal the total average score for each diet category. The Fructivores/Insectivores have a cumulat ive average score of 4.25, which would correspond to a number of parasites over 50. Meanwhile, the Fructivores have a cumulat ive average score of 1.8, which corresponds to between 15 and 20 parasites per bird on average. Fig. 2 : Comparison of bird niche categories to the avera ge score of each body part to reveal the total average score for each niche category. The cumulative average score of birds spending significant time in contact with the ground is significantly lower than bir ds of both other categories. 1 0,1778 0,0952 1,375 0,4222 0,619 0,5 1,2 2,375 1,2222 1,8095 1 0,6 0,5 0,1778 0,381 0 0,5 1 1,5 2 2,5 3 3,5 4 4,5 5 Carnivore (n=1) Fructivore (n=5) Fructivore/ Insectivore (n=8) Insectivore (n=45) Nectivore (n=21) Omnivore (n=4) Average Cumulative Score Dominant Diet Tail Wings Head Body 0,12 0,08 0,21 0,41 0,62 0,5 1,29 1,54 1,43 0,12 0,41 0,18 0 0,5 1 1,5 2 2,5 3 Ground to Lower Canopy Understory Understory to Middle Canopy Average Cumulative Score Niche Tail Wings Head Body

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Ectoparasites and Avian Hosts in Monteverde Ferguson 9 Fig . 3 : Comparison of b ird social behavior categories to the average score of each body part to reveal the total average score for each niche category . The cumulative average score of paired birds is significantly lower than both the social and solitary birds, with a score less than two. DISCUSSION To review , the main question of the study was whether or not it is possible to predict presence and appro ximate number of ectoparasites on birds in the Monteverde area based on physical, behavioral, a nd taxonomic characteristics of the birds themselves . According to a past study done in this area, ectoparasites were more likely found on species living in fore sted habitats and species with life strategies that included excessive contact with leaf litter or flowers (such as nectivorous hummingbirds and ground dwelling birds) ( McFarlin and Robinson 2011) . In addition, the natural history of many of the families o f ectoparasites indicate that their presence on birds would be related to the amount of time bi rds spent in contact either with other birds or with substrates that could provide habitat for the ectoparasites between hosts. For these reasons, I hypothesized that it would indeed be possible to find connections between the physical, behavioral, and tax onomic characteristics of the birds and the number of ectoparasites . My results indicate that while ectoparasite populations are varied and diverse on the birds included in this study, there are some avian characteristics that are indeed correlated to ecto parasite populations. First, there were a number of species of which none of the individuals captured had ectoparasites, while there were also a majority of species in which every bird captured had ectoparasites present. This indicates that there is at lea st some connection between species and ectoparasite populations. The additional analysis of mite morphotype and bird species or family showed no strong correlation in the majority of cases. This could indicate that mite species are less closely associated to specific species than I predicted, but it could also be the result of difficulty in properly classifying morphotypes. When considering avian diet, niche, and contact with nests, there was less clear of a correlation between these factors and presence or number of ectoparasites. This suggests that the 0,125 0,111 0,152 0,375 0,482 0,697 1,208 1,519 1,576 0,125 0,222 0,424 0 0,5 1 1,5 2 2,5 3 Pairs Social Solitary Average Cumulative Score Social Category Tail Wings Head Body

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Ectoparasites and Avian Hosts in Monteverde Ferguson 10 ectoparasites I ob served do not spend a significant amount of time apart from their hosts. In fact, there were, on average, more parasites observed on birds that rarely come into contact with the ground, whi ch indicates that my prediction that ectoparasites might be transfe rred through leaf litter was not supported. Going on, b irds with new feathers that had little to no sign of damage experienced few er instances of parasitism when compared to birds in the pr ocess of molting or with more damage to their feathers . This result could either indicate that newer feathers are less likely to have ectoparasites or that ectoparasites contribute to feather damage, both of which have scientific support (Jovani and Serrano 2001; Schmidt and Roberts 2000). The strongest connection found was between the social behavior of the bird and presence and abundance of ectoparasites. In this case, both solitary and social birds experienced similar amounts of parasites at similar rat es, while birds who lived in pairs not only have fewer average par asites but were also less likely to have parasites in general. This suggest a connection between pair behavior and protection from parasites and may indicate grooming as an important functio n of the pair strategy. A future study might further analyze this pair relationship. In conclusion, my hypothesis that it would be possible to predict ectoparasite presence and number based on physical, behavioral, and taxonomic characteristics of the bird s of Monteverde, Costa Rica, was only partially supported with on ly a few of the characteristics studied showing strong correlations to parasite distribution. In a future study, it might be beneficial to consider other factors specific to individual birds to assess variation between individuals of the same species or wi th similar natural histories. Going forward, this study has shed some light on the connection between the birds of Monteverde and their ectoparasites, but there is still much to learn and man y more factors involved in this complicated relationship. AC KNOWLEDGEMENTS I would very much like to thank Federico Chinchilla for assisting me every day with the mist netting and parasite collection. His presence (and coffee) was an enormous help and I really verde Institute and Santuario Ecológico Monteverde for allowing me to use their space for mist netting and a big thanks to Luisa Moreno and the high school students of the Amigos del Ambiente for letting me join them at the Santa Elena Reserve for mist net ting in the cloud forest. Thanks to Frank Joyce and Katy VanDeusen for introducing me to the world of Costa Rican birds. Lastly, thank you to UC EAP for such a wonderful experienc e. LITERATURE CITED Arnold, A., K . 1970 . Notes on a vian e ctoparasites f rom Costa Rica. l. Acarina and Diptera. Revista de Biología Tropical, 16(2) : 259 265. Clayton, D., G . , R., & Price, R. 1992 . Comparative e cology of Neotropical b ird l ice (Insecta: Pht hiraptera). The Journal of Animal Ecology, 61 (3) : 781 . Dube, W. C., Hund, A. K., Turbek, S. P., & Safran, R. J. 2018 . Microclimate and host body condition influence mite population growth in a wild bird ectoparasite system. International Journal for Parasi tology: Parasi tes and Wildlife,7 (3), 301 308.

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Ectoparasites and Avian Hosts in Monteverde Ferguson 11 Evans, B., & Taylor, E. 2000 . Factors affecting parasite abundance on birds. UCEAP Spring 2000 Co urse Book. Jovani, R., & Serrano, D. 2001 . Feather mites (Astigmata) avoid mounting wing feathers of passerine birds. Animal Behaviour,62 (4) : 723 727. Knee, W. 2006 . Keys to the f amilies and g enera of b lood and t issue f eeding m ites a ssociated with Albertan b irds. Canadian Journal of Arthropod Identification . Mironov, S. V., Literak, I., Sychra, O., & Capek, M. 2 017 . Feather mites of the subfamily Proctophyllodinae (Acari: Proctophyllodidae) from passerines (Aves: Passeriformes) in Costa Rica. Zootaxa,4297 (1) . McFarl in, M., & Robinson, J. 2011 . Bird ectoparasitic survey and possible community implications for alt ered habitats in San Luis, Costa Rica . UCEAP Spring 2011 Course Book. Proctor, H., & Owens, I. 2000 . Mites and birds: Diversity, parasitism and coevolution. Trends in Ecology & Evolution , 15(9) : 358 364. Prahl, L. 2006 . Determining avian vulnerability to ectoparasites using morphological and natural history traits . CIEE Fall 2006 Course Book . Schmidt, D.G., & Roberts, S.L. 2000 . Foundations of Parasitology . New York: Mc McGraw Hill.

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Ectoparasites and Avian Hosts in Monteverde Ferguson 12 APPENDIX Table ( Fig ) . 4 : A list of the species collected, their collection date, the bird weight, and the site in which they were collected. (MVI= Monteverde Institute , Rachel and Dwight Crandell Reserve trails, SM= Santuario Ecológico Monteverde, and SER= Santa Elena Reserve) Da te Collected Bird Number weight (g) Species Name 5/14/19 MVI 01 27.50 Thryophilus rufalbus 5/16/19 MVI 02 30.00 Thryophilus rufalbus 5/16/19 MVI 03 4.50 Eupherusa eximia 5/16/19 MVI 04 18.00 Chiroxiphia linearis 5/16/19 MVI 05 5.00 Lampornis calolaemu s 5/16/19 MVI 06 42.50 Melozone leucotis 5/16/19 MVI 07 25.00 Thryophilus rufalbus 5/16/19 MVI 08 4.75 Lampornis calolaemus 5/16/19 MVI 09 162.00 Momotus lessonii 5/16/19 MVI 10 32.00 Catharus mexicanus 5/16/19 MVI 11 27.50 Thryophilus rufalbus 5/16 /19 MVI 12 28.00 Thryophilus rufalbus 5/16/19 MVI 13 20.00 Chiroxiphia linearis 5/16/19 MVI 14 31.00 Catharus mexicanus 5/16/19 MVI 15 13.00 Campylopters hemileucurus 5/16/19 MVI 16 57.00 Arremon brunneinucha 5/16/19 MVI 17 22.00 Thryophilus rufalbus 5/18/19 SM 01 18.00 Chiroxiphia linearis 5/18/19 SM 02 27.50 Thryophilus rufalbus 5/18/19 SM 03 4.50 Amazilia tzacatl 5/18/19 SM 04 5.50 Amazilia tzacatl 5/18/19 SM 05 3.50 Eupherusa eximia 5/18/19 SM 06 16.00 Henicorhina leucosticta 5/18/19 SM 07 1 3.00 Basileuterus rufifrons 5/18/19 SM 08 18.00 Chiroxiphia linearis 5/18/19 SM 09 16.00 Chiroxiphia linearis 5/18/19 SM 10 36.50 Habia fuscicauda 5/18/19 SM 11 35.50 Habia fuscicauda 5/18/19 SM 12 450.00 Ciccaba virgata 5/21/19 SM 13 17.00 Chiroxiph ia linearis 5/21/19 SM 14 38.50 Dendrocincla homochroa 5/23/19 SM 15 16.00 Henicorhina leucosticta

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Ectoparasites and Avian Hosts in Monteverde Ferguson 13 5/23/19 SM 16 18.50 Chiroxiphia linearis 5/23/19 SM 17 5.00 Amazilia saucerrottei 5/23/19 SM 18 5.50 Amazilia saucerrottei 5/23/19 SM 19 47.50 Melozone leucotis 5/23/19 SM 20 17.50 Chiroxiphia linearis 5/23/19 SM 21 4.50 Eupherusa eximia 5/23/19 SM 22 5.00 Amazilia saucerrottei 5/23/19 SM 23 11.50 Basileuterus culicivorus 5/23/19 SM 24 18.00 Chiroxiphia linearis 5/23/19 SM 25 45.50 Dendrocincla hom ochroa 5/23/19 SM 26 5.00 Eupherusa eximia 5/24/19 SM 27 17.00 Seiurus aurocapilla 5/24/19 SM 28 28.00 Catharus aurantiirostris 5/25/19 SER 01 18.50 Chlorospingus flavopectus 5/25/19 SER 02 9.20 Campylopters hemileucurus 5/25/19 SER 03 6.40 Phaethorn is guy 5/25/19 SER 04 4.70 Lampornis calolaemus 5/25/19 SER 05 5.30 Lampornis calolaemus 5/25/19 SER 06 6.40 Phaethornis guy 5/25/19 SER 07 5.00 Eupherusa eximia 5/25/19 SER 08 17.50 Premnoplex brunnescens 5/25/19 SER 09 45.90 Arremon brunneinucha 5 /25/19 SER 10 30.00 Sclerurus mexicanus 5/25/19 SER 11 4.30 Lampornis calolaemus 5/25/19 SER 12 11.90 Mionectes olivaceus 5/25/19 SER 13 30.50 Catharus mexicanus 5/25/19 SER 14 10.20 Catharus mexicanus 5/25/19 SER 15 27.00 Catharus frantzii 5/25/19 S ER 16 69.30 Turdus assimilis 5/25/19 SER 17 15.50 Henicorhina leucophrys 5/25/19 SER 18 33.10 Myadastes melanops 5/25/19 SER 19 14.50 Premnoplex brunnescens 5/25/19 SER 20 18.70 Henicorhina leucophrys 5/25/19 SER 21 12.00 Basileuterus melanotis 5/25/ 19 SER 22 600.00 Chamaepetes unicolor 5/25/19 SER 23 98.00 Grallaria guatimalensis 5/25/19 SER 24 30.00 Catharus fuscater 5/26/19 SER 25 5.00 Phaethornis guy 5/26/19 SER 26 5.00 Heliodoxa jacula

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Ectoparasites and Avian Hosts in Monteverde Ferguson 14 5/26/19 SER 27 20.00 Mionectes olivaceus 5/26/19 SER 28 20.00 Mionectes olivaceus 5/26/19 SER 29 30.00 Margorornis rubiginosus 5/26/19 SER 30 28.00 Sclerurus mexicanus 5/26/19 SER 31 15.00 Mionectes olivaceus 5/26/19 SER 32 17.50 Premnoplex brunnescens 5/26/19 SER 33 17.50 Premnoplex brunnescens 5/26/19 SER 34 20.50 Mionectes olivaceus 5/26/19 SER 35 14.50 Chlorospingus flavopectus 5/26/19 SER 36 18.70 Henicorhina leucophrys 5/26/19 SER 37 35.00 Picoides fumigatus 5/26/19 SER 38 30.50 Catharus frantzii 5/26/19 SER 39 20.00 Empidonax flavescens T able ( Fig . ) 5 : Sample name, family, common name, and score assigned ba sed on approximate number of parasites S ample Name Family Species Common name Body Head Wings Tail MVI 01 Troglodytidae Rufous and white Wren 0 0 0 0 MVI 02 Troglodytidae Rufous and white Wren 0 0 0 0 MVI 03 Trochilidae Stripe tailed Hummingbird 0 0 0 0 MVI 04 Pipridae Long tailed Manak in 0 0 2 0 MVI 05 Trochilidae Purple throated Mountain gem 0 0 2 0 MVI 06 Emberizidae White eared Ground Sparrow 0 0 0 0 MVI 08 Trochilidae Purple throated Mountain gem 0 3 3 0 MVI 09 Momotidae Blue crowned Motmot 0 0 2 1 MVI 07 Troglodytidae Rufous a nd white Wren 0 0 0 0 MVI 10 Turdidae Black headed Nightingale Thrush 0 2 3 0 MVI 11 Troglodytidae Rufous and white Wren 0 0 0 0 MVI 12 Troglodytidae Rufous and white Wren 1 2 2 0 MVI 13 Pipridae Long tailed Manakin 0 0 2 0 MVI 14 Turdidae Black he aded Nightingale Thrush 0 3 3 2 MVI 15 Trochilidae Violet Sabrewing 0 0 3 2 MVI 16 Emberizidae Chestnut capped Brush Finch 1 1 2 1 MVI 17 Troglodytidae Rufous and white Wren 0 0 1 1 SER 01 Emberizidae Common Chlorospingus 0 0 0 0

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Ectoparasites and Avian Hosts in Monteverde Ferguson 15 SER 02 Trochilidae V iolet Sabrewing 0 1 2 0 SER 03 Trochilidae Green Hermit 0 1 3 0 SER 04 Trochilidae Purple throated Mountain gem 0 0 3 0 SER 05 Trochilidae Purple throated Mountain gem 0 0 3 0 SER 06 Trochilidae Green Hermit 0 0 1 0 SER 07 Trochilidae Stripe tailed Hu mmingbird 0 1 1 0 SER 08 Furnariidae Spotted Barbtail 0 0 0 0 SER 09 Emberizidae Chestnut capped Brush Finch 0 2 1 0 SER 10 Furnariidae Tawny throated Leaftosser 0 0 0 0 SER 11 Trochilidae Purple throated Mountain gem 0 0 2 0 SER 12 Tyrannidae Olive striped Flycatcher 0 0 3 0 SER 13 Turdidae Black headed Nightingale Thrush 0 2 2 0 SER 14 Parulidae Collared Redstart 0 2 3 0 SER 15 Turdidae Ruddy capped Nightingale Thrush 0 1 2 0 SER 16 Turdidae White throated Thrush 0 1 2 0 SER 17 Troglodytidae Gr ey breasted Woodwren 0 2 2 0 SER 18 Turdidae Black faced Solitaire 0 0 0 0 SER 19 Furnariidae Spotted Barbtail 0 0 3 0 SER 20 Troglodytidae Grey breasted Woodwren 0 0 0 0 SER 21 Parulidae Three striped Warbler 0 0 3 1 SER 22 Cracidae Black Guan 0 0 0 3 SER 23 Grallariidae Scaled Antpitta 1 2 3 0 SER 24 Turdidae Slaty backed Nightingale Thrush 0 2 2 2 SER 25 Trochilidae Green Hermit 0 2 1 1 SER 26 Trochilidae Green crowned Brilliant 2 0 1 0 SER 27 Tyrannidae Olive striped Flycatcher 0 1 2 0 SER 28 Tyrannidae Olive striped Flycatcher 0 0 3 0 SER 29 Furnariidae Ruddy Treerunner 0 0 3 0 SER 30 Furnariidae Tawny throated Leaftosser 0 0 3 0 SER 31 Tyrannidae Olive striped Flycatcher 0 2 0 0 SER 32 Furnariidae Spotted Barbtail 0 2 0 0 SER 33 Furnari idae Spotted Barbtail 0 0 0 0 SER 34 Tyrannidae Olive striped Flycatcher 0 0 0 0 SER 35 Emberizidae Common Chlorospingus 0 2 3 0 SER 36 Troglodytidae Grey breasted Woodwren 0 0 0 0 SER 37 Picidae Smokey Brown Woodpecker 2 0 1 0 SER 38 Turdidae Ruddy c apped Nightingale Thrush 0 0 2 0 SER 39 Tyrannidae Yellowish Flycatcher 0 0 0 0 SM 01 Pipridae Long tailed Manakin 0 0 2 0

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Ectoparasites and Avian Hosts in Monteverde Ferguson 16 SM 02 Troglodytidae Rufous and white Wren 0 2 1 1 SM 03 Trochilidae Rufous tailed Hummingbird 0 0 0 0 SM 04 Trochilidae Rufous tailed Hummingbird 0 0 1 1 SM 05 Trochilidae Stripe tailed Hummingbird 0 0 2 1 SM 06 Troglodytidae White breasted Woodwren 0 0 0 0 SM 07 Parulidae Rufous capped Warbler 0 0 3 0 SM 08 Pipridae Long tailed Manakin 0 0 0 0 SM 09 Pipridae Long tailed Man akin 0 0 2 0 SM 10 Cardinalidae Red throated Ant Tanager 0 1 2 2 SM 11 Cardinalidae Red throated Ant Tanager 0 0 1 0 SM 12 Strigidae Mottled Owl 1 0 0 0 SM 13 Pipridae Long tailed Manakin 0 0 0 0 SM 14 Furnariidae Ruddy Woodcreeper 1 0 0 0 SM 15 Trog lodytidae White breasted Woodwren 0 0 0 0 SM 16 Pipridae Long tailed Manakin 0 0 0 0 SM 17 Trochilidae Steely vented Hummingbird 0 2 1 0 SM 18 Trochilidae Steely vented Hummingbird 0 0 3 1 SM 19 Emberizidae White eared Ground Sparrow 0 0 1 0 SM 20 Pip ridae Long tailed Manakin 0 0 2 0 SM 21 Trochilidae Stripe tailed Hummingbird 0 0 2 0 SM 22 Trochilidae Steely vented Hummingbird 0 3 1 0 SM 23 Parulidae Golden crowned Warbler 0 0 2 1 SM 24 Pipridae Long tailed Manakin 2 0 2 0 SM 25 Furnariidae Rudd y Woodcreeper 0 0 2 0 SM 26 Trochilidae Stripe tailed Hummingbird 0 0 3 2 SM 27 Parulidae Ovenbird 0 0 1 0 SM 28 Turdidae Orange billed Nightingale Thrush 0 0 3 0


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