Mary Bomberger Brown

Ectoparasites Reduce Long-Term Survival of their Avian Host

Few field studies have evaluated whether ectoparasites affect the long-term survival of their adult host, although many studies have examined the impact of parasites on the host’s offspring. In the colonially nesting cliff swallow ( Hirundo pyrrhonota), we manipulated ectoparasite load (of cimicid bugs, fleas, and chewing lice) by fumigating adults and comparing annual survivorship of fumigated birds and nonfumigated control birds captured at the same time. Mark-recapture experiments over an 8-year period revealed that non-fumigated birds had an annual survivorship about 12% less than that of fumigated birds, on average, but the effects did not vary with colony size. Based on the difference in survivorship between fumigated and non-fumigated birds, we estimated that parasitized individuals had an annual survivorship of 0.38, compared with 0.57 for non-parasitized birds. The parasite-caused reduction in survivorship was the equivalent of the host losing up to one year of lifetime reproductive success. Ectoparasites did not preferentially infest hosts of lower quality, suggesting that all birds in the population were at potential risk of suffering parasitism and the resulting reductions in survivorship. Our results show that obligate ectoparasites such as fleas and lice impose a substantial long-term cost to their hosts and suggest that future studies of ectoparasitism should consider the parasites’ effect on annual survival of adult hosts.

Glucocorticoid Hormone Levels Increase with Group Size and Parasite Load in Cliff Swallows

Animals often cope with adverse events by releasing glucocorticoid hormones, which in turn promote increased energy assimilation. In captive animals, crowding also leads to increased glucocorticoid activity, probably because of increased levels of social competition. We investigated how group size and ectoparasite infestations affected endogenous levels of the glucocorticoid hormone, corticosterone, in colonial cliff swallows, Petrochelidon pyrrhonota, in southwestern Nebraska, U.S.A. Parasites were removed from some colonies by fumigating nests. Baseline levels of corticosterone in breeding adults varied significantly with whether parasites were present, colony size (measured by total number of active nests at a site) and nesting stage. Across all analyses, birds from fumigated colonies averaged significantly lower baseline levels of corticosterone. These levels in adults increased with colony size at nonfumigated sites, especially during the period when nestlings were being fed, but no relation or the opposite one was found for birds in fumigated colonies. Baseline corticosterone levels were unrelated to sex, age, body weight or testosterone levels in adults. Corticosterone concentrations tended to increase during a bad-weather event when food was scarce. Patterns in nestling and recently fledged juveniles were consistent with those in adults. The increased baseline levels of corticosterone in birds of larger colonies appear related to the larger number of parasites there. Higher levels of corticosterone probably facilitate increased allocation of time and energy to foraging and greater energy assimilation during challenging events such as bad weather, parasitism by blood-feeding bugs in large colonies and the period when young are becoming independent of their parents.

Weather-mediated natural selection on arrival time in cliff swallows (Petrochelidon pyrrhonota)

Abstract An unusually long period of cold weather in May 1996 caused extensive mortality among insectivorous cliff swallows (Petrochelidon pyrrhonota) in the northern and central Great Plains. We analyzed how viability selection affected spring arrival time in a migratory Nebraska population by comparing capture histories of survivors with those of birds known to have died and by documenting how arrival time changed in the year following the selection event. Surviving birds had significantly later first-capture dates (an index of arrival time) in the years prior to selection than those that died; a significant selection differential suggested directional selection for birds that arrived later. Colony sites were occupied significantly later following the selection event, and the distribution of first-capture dates in the season after selection was significantly shifted toward later arrivals. Offspring of the survivors tended to arrive later than birds of the same age prior to the selection event. While major weather-caused mortality events of this magnitude are rare in the study area, spells of cold weather severe enough to cause limited mortality are frequent in April and early May. At least 25 probable mortality events of varying severity were identified in the last 50 years based on climatological data. Periodic weather-mediated selection against early arrival constrains the cliff swallow’s breeding season and may partly prevent directional selection for earlier nesting.

Group size and ectoparasitism affect daily survival probability in a colonial bird

Little is known in general about how group size or ectoparasitism affect survival in colonial animals. We estimated daily within-season survival probabilities for nesting adult and recently fledged juvenile cliff swallows (Petrochelidon pyrrhonota) at 239 colonies from 1983 to 2003 in southwestern Nebraska, USA. Some colonies had been fumigated to remove ectoparasites. We conducted mark-recapture at each colony site to estimate daily survival. There were no systematic differences between males and females in daily survival. Adults and juveniles occupying parasite-free colonies had, on average, 4.4% and 62.2% greater daily survival, respectively, than their counterparts in naturally infested colonies. Daily survival of all birds increased with colony size for both parasite-free colonies and those under natural conditions, although the effect was stronger for adults at fumigated sites and for juveniles. Average daily survival probability for adults tended to increase during warmer and drier summers. Although daily survival varied at some sites over the course of the nesting cycle, there were no strongly consistent within-year temporal effects on survival. Even small differences in daily survival probability can translate into large effects on mean lifespan. The deleterious effects of ectoparasites on daily survival within the season represent a previously unknown cost of ectoparasitism. The increase in within-season survival with colony size reflects the net effects of many costs and benefits associated with colony size. Ectoparasitism is probably the most important cost that tends to partly balance the positive effects of large colonies. The greater survival of cliff swallows in the larger colonies is a previously unknown advantage of colonial nesting.

EMPIRICAL MEASUREMENT OF PARASITE TRANSMISSION BETWEEN GROUPS IN A COLONIAL BIRD

While epidemiological models have suggested that the spread of parasites and infectious diseases often depends critically on the extent of movement by infected individuals between populations, there is little empirical information for any organism on the frequency of between-group parasite transmission or how it varies spatially. The trans- mission of parasites between discrete social groups or populations may also help determine a hosts total parasite or pathogen exposure. We measured the introduction of parasitic bugs (Oeciacus vicarius) into colonies of Cliff Swallows (Petrochelidon pyrrhonota) by transient birds from outside each group. The transmission of bugs increased strongly as the size of a nesting colony increased. More total transients visited the larger colonies, and the direction of change in transient numbers and the numbers of bugs introduced at a site from week to week tended to vary together. Transients at large colonies were more likely to have pre- viously or subsequently visited other large, infested colonies. The greater likelihood of parasites being introduced into larger colonies by transient birds contributes to an increase in parasite load with increased colony size in Cliff Swallows.

The Risk of Flawed Inference in Evolutionary Studies When Detectability Is Less than One

Addressing evolutionary questions in the wild remains a challenge. It is best done by monitoring organisms from birth to death, which is very difficult in part because individuals may or may not be resighted or recaptured. Although the issue of uncertain detection has long been acknowledged in ecology and conservation biology, in evolutionary studies of wild populations it is often assumed that detectability is perfect. We argue that this assumption may lead to flawed inference. We demonstrate that the form of natural selection acting on body mass of sociable weavers is altered and that the rate of senescence of roe deer is underestimated when not accounting for a value of detectability that is less than one. Because mark‐recapture models provide an explicit way to integrate and reliably model the detection process, we strongly recommend their use to address questions in evolutionary biology.

NONPARAMETRIC ESTIMATION OF NATURAL SELECTION ON A QUANTITATIVE TRAIT USING MARK-RECAPTURE DATA

Abstract Assessing natural selection on a phenotypic trait in wild populations is of primary importance for evolutionary ecologists. To cope with the imperfect detection of individuals inherent to monitoring in the wild, we develop a nonparametric method for evaluating the form of natural selection on a quantitative trait using mark‐recapture data. Our approach uses penalized splines to achieve flexibility in exploring the form of natural selection by avoiding the need to specify an a priori parametric function. If needed, it can help in suggesting a new parametric model. We employ Markov chain Monte Carlo sampling in a Bayesian framework to estimate model parameters. We illustrate our approach using data for a wild population of sociable weavers (Philetairus socius) to investigate survival in relation to body mass. In agreement with previous parametric analyses, we found that lighter individuals showed a reduction in survival. However, the survival function was not symmetric, indicating that body mass might not be under stabilizing selection as suggested previously.

Ectoparasites cause increased bilateral asymmetry of naturally selected traits in a colonial bird

Abstract Parasitism has been shown to correlate with levels of bilateral symmetry in some organisms, with more asymmetric individuals often having more parasites. However, few studies have shown experimentally that parasitism directly causes increased asymmetry. By fumigating some cliff swallow (Petrochelidon pyrrhonota) colonies and leaving others untreated, we investigated experimentally whether ectoparasitism by the cimicid swallow bug led to higher levels of asymmetry in length of wings, outer tail feathers, and tarsus among juvenile and adult birds. Juveniles from fumigated colonies measured soon after fledging had significantly less asymmetry in wing and outer tail length than juveniles from nonfumigated colonies; asymmetry in tarsus length was unaffected by parasitism. Adults that had undergone one or more post‐juvenal molts on the wintering grounds showed no differences in asymmetry between those reared in fumigated vs. nonfumigated colonies. These results show that ectoparasitism directly leads to increased feather asymmetry in cliff swallows, probably through parasite‐induced nutritional stress. Because wing and tail asymmetry impair flight performance and reduce foraging efficiency, the increased asymmetry caused by parasites represents a fitness cost to cliff swallows. This is among the few experimental studies to show an effect of parasites on asymmetry of naturally selected characters.

Ecological correlates of buggy creek virus infection in Oeciacus vicarius, southwestern Nebraska, 2004

Abstract Buggy Creek virus (family Togaviridae, genus Alphavirus, BCRV) is an alphavirus within the western equine encephalitis virus complex whose primary vector is the swallow bug, Oeciacus vicarius Horvath (Hemiptera: Cimicidae), an ectoparasite of the colonially nesting cliff swallow, Petrochelidon pyrrhonota, that is also a frequent host for the virus. We investigated ecological correlates of BCRV infection in 100-bug pools at 14 different swallow colony sites in southwestern Nebraska from summer 2004, by using plaque assay on Vero cells to identify cytopathic virus and reverse transcription-polymerase chain reaction to identify noncytopathic viral RNA. We found 26.7% of swallow bug pools positive for BCRV, with 15.6% showing cytopathic (“infectious”) virus and 11.0% noncytopathic (“noninfectious”) viral RNA. The prevalence of cytopathic BCRV increased with cliff swallow colony size in the current year; the percentage of noncytopathic samples at a site did not vary with colony size in the current year but increased with the previous year’s colony size at a site. Active colony sites (those used by swallows) had higher percentages of cytopathic BCRV in bug pools than at inactive colony sites, but the reverse held for noncytopathic viral RNA. Nests that were occupied by birds at some time in the season had more pools with cytopathic BCRV than did inactive nests. Colonies used by birds for the first or second time had less virus in bugs than did sites that had had a longer history of bird use. The percentage of pools with BCRV was affected by whether bugs were clustering at nest entrances or distributed elsewhere on a nest. The prevalence of cytopathic samples decreased at inactive colony sites and increased at active sites over the course of the summer, whereas the reverse pattern held for noncytopathic samples. Noncytopathic bug pools seem to reflect infection patterns from a previous year. The results suggest that the birds play an important role in amplification of the virus and that the spatial foci of BCRV occurrence can be predicted based on characteristics of cliff swallow colonies and the cimicid bugs that are associated with them.

Phylogeographical structure and evolutionary history of two Buggy Creek virus lineages in the western Great Plains of North America

Buggy Creek virus (BCRV) is an unusual arbovirus within the western equine encephalitis complex of alphaviruses. Associated with cimicid swallow bugs (Oeciacus vicarius) as its vector and the cliff swallow (Petrochelidon pyrrhonota) and house sparrow (Passer domesticus) as its amplifying hosts, this virus is found primarily in the western Great Plains of North America at spatially discrete swallow nesting colonies. For 342 isolates collected in Oklahoma, Nebraska, Colorado and North Dakota, from 1974 to 2007, we sequenced a 2076 bp region of the 26S subgenomic RNA structural glycoprotein coding region, and analysed phylogenetic relationships, rates of evolution, demographical histories and temporal genetic structure of the two BCRV lineages found in the Great Plains. The two lineages showed distinct phylogeographical structure: one lineage was found in the southern Great Plains and the other in the northern Great Plains, and both occurred in Nebraska and Colorado. Within each lineage, there was additional latitudinal division into three distinct sublineages. One lineage is showing a long-term population decline. In comparing sequences taken from the same sites 8-30 years apart, in one case one lineage had been replaced by the other, and in the other cases there was little evidence of the same haplotypes persisting over time. The evolutionary rate of BCRV is in the order of 1.6-3.6x10(-4) substitutions per site per year, similar to that estimated for other temperate-latitude alphaviruses. The phylogeography and evolution of BCRV could be better understood once we determine the nature of the ecological differences between the lineages.