Microclimate and host body condition influence mite population growth in a wild bird-ectoparasite system

Parasite populations are never evenly distributed among the hosts they infect. Avian nest ectoparasites, such as mites, are no exception, as their distribution across the landscape is highly aggregated. It remains unclear if this pattern is driven by differences in transmission events alone, or if the environment that parasites inhabit after transmission also plays a role. Here, we experimentally examined the influence of the post-transmission microclimate, nest characteristics, and host condition on ectoparasite population growth in a bird-ectoparasite system. We infested barn swallow (Hirundo rustica erythrogaster) nests with a standardized number of Northern Fowl Mites (Ornithonyssus sylvarium) and analyzed both biotic (nestling mass, wing length, number of other arthropods present in the nest, and brood size) and abiotic (temperature, humidity, nest lining, nest dimensions, and substrate upon which the nest was built) predictors of mite population growth. Our results suggest that mite populations were most successful, in terms of growth, in nests with higher temperatures, lower humidity, few other arthropods, and hosts in good condition. We also found that nests built on wooden substrates support larger populations of mites than those constructed on metal or concrete. These findings lend insight into the factors that drive large-scale patterns of ectoparasite distributions.

Methods
Research took place at 24 b swallow breeding colonies located in Boulder County Colorado from May–August 2016. Adult barn swallows were captured using mist nets and each bird was given a USGS metal identification band and a unique combination of color bands. Breeding pairs were identified and assigned to nests through behavioral observations. All nests at each of the study colonies were monitored every other day to track lining activity, egg laying, and the hatching and growth of nestlings. This study was part of a larger experiment examining the role of genes and environment in color development in nestling barn swallows. For all experimental nests (n = 58), existing NFM were removed from nests using a heat disinfection method (Hund et al., 2015b) three days after clutch completion. Briefly, eggs were removed and a heat gun was used to heat all parts of the nests to 125 °C at least two times. The heating process took approximately 5 min. After the nests had cooled to < 29 °C, the eggs were returned to the nest. After nests were disinfected, they were re-infected with 100 live fieldcollected northern fowl mites (NFM). 

iButton DS1923 data loggers (Maxim Integrated) are miniature sensors (17.4 mm in diameter, and 6.4 mm in depth) that were used to track temperature and humidity throughout nestling development within a subset of our experimental nests (n = 38). iButtons were installed in the nest at the same time that NFMs were experimentally added to the nest (3 days after clutch completion). iButtons were placed in the nest cup between the feather lining and mud structure to capture the microclimate in which NFMs live. Nest temperature and humidity measurements were collected every 10 min for 14 days for a total of around 2024 measurements for each nest.

Nest parasites were counted in the field when nestlings were 12 days old. We counted 1) how many mites were on the field assistant's hand after being placed in the nest for 30 s, 2) the number of mites on each nestling, and 3) the number of mites in the container used to hold the nestlings. These three counts were added together and used as a proxy for mite population size in each nest. Similar methods have been used in previous studies and correlate with mite population counts from nests placed in Berlese funnels (Møller, 1990; Hund et al., 2015b). Whole nests containing iButtons were collected 10 days (range: 7–12) after nestlings fledged (unless a new clutch had already been started) and placed into Berlese funnels for 24 h to get a more precise measure of final mite population size (n = 20, seven nests failed and were not included, five had new clutches before collection and were not included). Arthropods that were collected from the Berlese funnels were then sorted and counted using a dissecting microscope, according to procedures used previously (Hund et al., 2015b). The samples were separated into two categories: NFMs and other arthropods. Other arthropod numbers were small enough that they were counted individually. The mite populations were variable, but some were large enough that individual counting would have been unmanageable; for this reason, the number of mites in each sample was estimated by volume. To do this, 100 mites were counted and put in a micro-centrifuge tube as a reference. Then, mites were added into a new tube until its volume was the same as that of the reference tube. Once all the mites in a nest were accounted for, the number of complete tubes was counted, and multiplied by 100 to get an estimate of mite population size for a given nest.

Nestling mass, right wing length, and the number of nestlings were measured for each nest on day 12. Nestling mass was measured in grams using an electronic balance ( ± 0.01 g, AWS-100). Flattened wing length was measured for the right wing in millimeters ( ± 0.5 mm) using a wing rule (AFO Banding Supplies). Nestling mass was divided by wing length to calculate individual body condition. Individual nestling body condition scores were used to calculate an average nestling body condition for each nest. Brood size consisted of the number of live nestlings on day 12.

On day 12 after hatching, nest lining (amount of feathers in the nest cup) was evaluated on a qualitative scale from zero to three (zero being no feather lining, three being so many feathers that they could barely fit in the nest cup). Nest dimensions were measured using a measuring tape and nest area was calculated by multiplying the widest point of the nest cup by the height of the nest. The substrate on which the nest was built was categorized as either wood, metal, concrete, or other.