Loren Merrill

Local host specialization, host-switching, and dispersal shape the regional distributions of avian haemosporidian parasites

Significance Within eastern North America, distributions of vector-transmitted haemosporidian blood parasites of birds, commonly known as “avian malaria parasites,” are associated with the distributions of their host species independently of direct effects of climate on potential vectors. Spatial analyses additionally indicated an absence of dispersal limitation for these parasites. Finally, host-breadth, ranging continuously from specialist to generalist, varies among parasite lineages and is dynamic within parasite assemblages over space and time. The distributions of avian haemosporidian parasites emphasize the ability of parasites to disperse across broad regions and to switch readily between hosts to become emerging infectious diseases. The drivers of regional parasite distributions are poorly understood, especially in comparison with those of free-living species. For vector-transmitted parasites, in particular, distributions might be influenced by host-switching and by parasite dispersal with primary hosts and vectors. We surveyed haemosporidian blood parasites (Plasmodium and Haemoproteus) of small land birds in eastern North America to characterize a regional parasite community. Distributions of parasite populations generally reflected distributions of their hosts across the region. However, when the interdependence between hosts and parasites was controlled statistically, local host assemblages were related to regional climatic gradients, but parasite assemblages were not. Moreover, because parasite assemblage similarity does not decrease with distance when controlling for host assemblages and climate, parasites evidently disperse readily within the distributions of their hosts. The degree of specialization on hosts varied in some parasite lineages over short periods and small geographic distances independently of the diversity of available hosts and potentially competing parasite lineages. Nonrandom spatial turnover was apparent in parasite lineages infecting one host species that was well-sampled within a single year across its range, plausibly reflecting localized adaptations of hosts and parasites. Overall, populations of avian hosts generally determine the geographic distributions of haemosporidian parasites. However, parasites are not dispersal-limited within their host distributions, and they may switch hosts readily.

Maternal Antibody Transfer Can Lead to Suppression of Humoral Immunity in Developing Zebra Finches (Taeniopygia guttata)

Maternally transferred antibodies have been documented in a wide range of taxa and are thought to adaptively provide protection against parasites and pathogens while the offspring immune system is developing. In most birds, transfer occurs when females deposit immunoglobulin Y into the egg yolk, and it is proportional to the amount in the female’s plasma. Maternal antibodies can provide short-term passive protection as well as specific and nonspecific immunological priming, but high levels of maternal antibody can result in suppression of the offspring’s humoral immune response. We injected adult female zebra finches (Taeniopygia guttata) with one of two antigens (lipopolysaccharide [LPS] or keyhole limpet hemocyanin [KLH]) or a control and then injected offspring with LPS, KLH, or a control on days 5 and 28 posthatch to examine the impact of maternally transferred antibodies on the ontogeny of the offspring’s humoral immune system. We found that offspring of females exposed to KLH had elevated levels of KLH-reactive antibody over the first 17–28 days posthatch but reduced KLH-specific antibody production between days 28 and 36. We also found that offspring exposed to either LPS or KLH exhibited reduced total antibody levels, compared to offspring that received a control injection. These results indicate that high levels of maternal antibodies or antigen exposure during development can have negative repercussions on short-term antibody production and may have long-term fitness repercussions for the offspring.

Immune function in an avian brood parasite and its nonparasitic relative.

Organisms that breed multiple times must trade off resources between current and future reproduction. In many species, sexual selection can lead to reduced levels of immune function in males because they invest heavily in current reproduction at the expense of self-maintenance. Much less is known about whether the same trend is seen in species such as the brood-parasitic brown-headed cowbird Molothrus ater (hereafter “cowbird”), in which females invest heavily in current reproduction. We examined two measures of immune function (bactericidal capacity of the plasma and the phytohemagglutinin swelling response) and baseline levels of corticosterone in both sexes of the cowbird and its nonparasitic relative the red-winged blackbird Agelaius phoeniceus (hereafter “redwing”) during the breeding and subsequent nonbreeding seasons. We found that female cowbirds exhibited significantly lower levels of both measures of immune function than did male cowbirds and female redwings during the breeding season but had comparable levels during the nonbreeding season. Female redwings, in contrast, exhibited higher or comparable levels of immune function when compared with male redwings during the breeding season. In conjunction with published accounts documenting significantly higher rates of mortality for female cowbirds compared with male cowbirds and the fact that female cowbirds produce very high numbers of eggs (25–65) in a single breeding season, our results suggest that female cowbirds invest heavily in current reproduction at the expense of self-maintenance.

Prevalence of avian haemosporidian parasites is positively related to the abundance of host species at multiple sites within a region.

Parasite prevalence is thought to be positively related to host population density owing to enhanced contagion. However, the relationship between prevalence and local abundance of multiple host species is underexplored. We surveyed birds and their haemosporidian parasites (genera Plasmodium and Haemoproteus) at multiple sites across eastern North America to test whether the prevalence of these parasites in a host species at a particular site is related to that host’s local abundance. Prevalence was positively related to host abundance within most sites, although the effect was stronger and more consistent for Plasmodium than for Haemoproteus. In contrast, prevalence was not related to variation in the abundance of most individual host species among sites across the region. These results suggest that parasite prevalence partly reflects the relative abundances of host species in local assemblages. However, three nonnative host species had low prevalence despite being relatively abundant at one site, as predicted by the enemy release hypothesis.

Breaking down seasonality: androgen modulation and stress response in a highly stable environment.

Previous studies show that most birds inhabiting temperate regions have well defined life history stages, and they modulate the production of testosterone (T) and corticosterone (CORT) in response to changes in seasonality. In this study we aimed to examine baseline and stress-induced levels of CORT and circulating T in relation with life history stages in the rufous-collared sparrow, Zonotrichia capensis. We carried out this study for a year in a population inhabiting riparian habitats in the Atacama Desert in Chile, one of the most climatically stable and driest places in the world. This environment shows minimal yearly change in average temperature and precipitation is virtually zero. We found individuals breeding, molting and overlapping breeding and molt year round, although most individuals were molting during March and in breeding condition during October. T levels were not related to individual breeding condition, and at population level they were not significantly different across sampling months. Baseline levels of CORT did not vary across the year. Stress-induced levels of CORT were suppressed during March when most of the birds were molting. This phenomenon was also observed in birds not molting during this period suggesting a mechanism other than molt in determining the stress-response suppression. Our results strongly suggest that in this study site, long-term extremely stable conditions could have relaxed the selective pressures over the timing of life history stages which was evidenced by the breeding and molt schedules, its overlap and endocrine profiles.

Pre and post-natal antigen exposure can program the stress axis of adult zebra finches: Evidence for environment matching

Both maternal exposure to stressors and exposure of offspring to stressors during early life can have lifelong effects on the physiology and behavior of offspring. Stress exposure can permanently shape an individuals phenotype by influencing the development of the hypothalamic-pituitary-adrenal (HPA) axis, which is responsible for the production and regulation of glucocorticoids such as corticosterone (CORT). In this study we used captive zebra finches (Taeniopygia guttata) to examine the effects of matching and mismatching maternal and early post-natal exposure to one of two types of antigens or a control on HPA axis reactivity in adult offspring. Prior to breeding, adult females were injected with lipopolysaccharide (LPS), keyhole limpet hemocyanin (KLH) or a control. Offspring of females in each of the three treatments were themselves exposed to LPS, KLH or a control injection at 5 and 28days post-hatch. When offspring were at least 18months of age, standardized capture and restraint stress tests were conducted to determine the impact of the treatments on adult stress responsiveness. We found significant interaction effects between maternal and offspring treatments on stress-induced CORT levels, and evidence in support of the environment matching hypothesis for KLH-treated birds, not LPS-treated birds. KLH-treated offspring of KLH-treated mothers exhibited reduced stress-induced CORT levels, whereas LPS-treated or control offspring of KLH-treated mothers exhibited elevated stress-induced CORT levels. Although the treatment effects on baseline CORT were non-significant, the overall pattern was similar to the effects observed on stress-induced CORT levels. Our results highlight the complex nature of HPA axis programming, and to our knowledge, provide the first evidence that a match or mismatch between pre and post-natal antigen exposure can have life-long consequences for HPA axis function.

Epaulet Size and Current Condition in Red-Winged Blackbirds: Examining a Semistatic Signal, Testosterone, Immune Function, and Parasites

Some sexually selected signals are thought to convey information about the current condition and genetic/epigenetic quality of the individual signaling, including the ability to resist parasites. However, it is unclear whether semistatic sexual signals that develop periodically and remain stable over protracted periods, such as avian breeding plumage, can relate to measures of current condition and health. We examined a semistatic signal (wing epaulet size) in male red-winged blackbirds (Agelaius phoeniceus) during the breeding season and looked for relationships between this trait and circulating testosterone (T), hematocrit, bacteria-killing ability (BKA) of the blood, and the infection status, richness, and abundance of four functional categories of parasite. We found that epaulet size was positively related to circulating levels of T and ectoparasite infections. We found no relationships between T and parasite infections. In adult males there was a negative relationship between T and BKA, whereas in yearling males there was no relationship. We found no evidence for a general reduction in immunocompetence in males with larger epaulets but rather an increase in susceptibility to specific types of parasites. Our results suggest that semistatic signals can be linked to measures of current condition, and we postulate that these relationships are modulated via activity levels related to breeding-season activities.

A blurring of life-history lines: Immune function, molt and reproduction in a highly stable environment

Rufous-collared sparrows (Zonotrichia capensis peruviensis) from valleys in the Atacama Desert of Chile, live in an extremely stable environment, and exhibit overlap in molt and reproduction, with valley-specific differences in the proportion of birds engaged in both. To better understand the mechanistic pathways underlying the timing of life-history transitions, we examined the relationships among baseline and stress-induced levels of corticosterone (CORT), testosterone, and bacteria-killing ability of the blood plasma (BKA), as well as haemosporidian parasite infections and the genetic structure of two groups of sparrows from separate valleys over the course of a year. Birds neither molting nor breeding had the lowest BKA, but there were no differences among the other three categories of molt-reproductive stage. BKA varied over the year, with birds in May/June exhibiting significantly lower levels of BKA than the rest of the year. We also documented differences in the direction of the relationship between CORT and BKA at different times during the year. The direction of these relationships coincides with some trends in molt and reproductive stage, but differs enough to indicate that these birds exhibit individual-level plasticity, or population-level variability, in coordinating hypothalamo-pituitary-adrenal axis activity with life-history stage. We found weak preliminary evidence for genetic differentiation between the two populations, but not enough to indicate genetic isolation. No birds were infected with haemosporidia, which may be indicative of reduced parasite pressure in deserts. The data suggest that these birds may not trade off among different life-history components, but rather are able to invest in multiple life-history components based on their condition.

Cultural Evolution and Long-Term Song Stability in a Dialect Population of Brown-Headed Cowbirds

Abstract. Knowing the extent to which the acoustic structure of songs is temporally stable is essential to understanding how cultural evolution affects song dialects in oscines. The acoustic structure of the most prevalent variant of the flight-whistle song recorded from male Brown-headed Cowbirds (Molothrus ater) in the Mammoth dialect (Mammoth Lakes, California) from 2005 to 2009 differed significantly and consistently from whistles recorded in 1989 and 1978–1985. The most common whistle variant in the 2005–2009 sample had structural features absent from whistles described in the earlier studies and overall was produced at a consistently lower acoustic frequency. Besides the emergence of this new variant sometime between 1989 and 2005, the prevalence of other variants of the whistle also changed from 1978 to 2009. Changes reported in other studies of cultural evolution in oscines have been based on lower-level structural elements (notes and syllables), whereas we found that entire songs appear to have evolved as cultural units or memes. We discuss possible mechanisms as to how these changes may have occurred. Despite these changes, the Mammoth whistle still retained the same basic three-syllable structure it had 31 years ago. This stability is notable because of the potential for extreme variation in whistle structure exemplified by the distinct whistles of nearby dialects in the region.

Incubation temperature impacts nestling growth and survival in an open-cup nesting passerine

Abstract For oviparous species such as birds, conditions experienced while in the egg can have long‐lasting effects on the individual. The impact of subtle changes in incubation temperature on nestling development, however, remains poorly understood, especially for open‐cup nesting species with altricial young. To investigate how incubation temperature affects nestling development and survival in such species, we artificially incubated American robin (Turdus migratorius) eggs at 36.1°C (“Low” treatment) and 37.8°C (“High” treatment). Chicks were fostered to same‐age nests upon hatching, and we measured mass, tarsus, and wing length of experimental nestlings and one randomly selected, naturally incubated (“Natural”), foster nest‐mate on days 7 and 10 posthatch. We found significant effects of incubation temperature on incubation duration, growth, and survival, in which experimentally incubated nestlings had shorter incubation periods (10.22, 11.50, and 11.95 days for High, Low, and Natural eggs, respectively), and nestlings from the Low treatment were smaller and had reduced survival compared to High and Natural nestlings. These results highlight the importance of incubation conditions during embryonic development for incubation duration, somatic development, and survival. Moreover, these findings indicate that differences in incubation temperature within the natural range of variation can have important carryover effects on growth and survival in species with altricial young.