The importance of wild birds as potential vectors of disease has received recent renewed empirical interest, especially regarding human health. Understanding the spread of bacterial pathogens in wild birds may serve as a useful model for examining the spread of other disease organisms, both amongst birds, and from birds to other taxa. Information regarding the normal gastrointestinal bacterial flora is limited for the majority of wild bird species, with the few well-studied examples concentrating on bacteria that are zoonotic and/or relate to avian species of commercial interest. However, most studies are limited by small sample sizes, the frequent absence of longitudinal data, and the constraints of using selective techniques to isolate specific pathogens. The pathogenic genera found in the gut are often those suspected to exist in the birds' habitat, and although correlations are made between bacterial pathogens in the avian gut and those found in their foraging grounds, little is known about the effect of the pathogen on the host, unless the causative organism is lethal. In this review, we provide an overview of the main bacterial pathogens isolated from birds (with particular emphasis on enteropathogenic bacteria) which have the potential to cause disease in both birds and humans, whilst drawing attention to the limitations of traditional detection methods and possible study biases. We consider factors likely to affect the susceptibility of birds to bacterial pathogens, including environmental exposure and heterogeneities within the host population, and present probable avenues of disease transmission amongst birds and from birds to other animal taxa. Our primary aim is to identify gaps in current knowledge and to propose areas for future study.

Bacterial pathogens in wild birds: a review of the frequency and effects of infection.

Incubation is a vital component of reproduction and parental care in birds. Maintaining temperatures within a narrow range is necessary for embryonic development and hatching of young, and exposure to both high and low temperatures can be lethal to embryos. Although it is widely recognized that temperature is important for hatching success, little is known about how variation in incubation temperature influences the post-hatching phenotypes of avian offspring. However, among reptiles it is well known that incubation temperature affects many phenotypic traits of offspring with implications for their future survival and reproduction. Although most birds, unlike reptiles, physically incubate their eggs, and thus behaviourally control nest temperatures, variation in temperature that influences embryonic development still occurs among nests within a population. Recent research in birds has primarily been limited to populations of megapodes and waterfowl; in each group, incubation temperature has substantial effects on hatchling phenotypic traits important for future development, survival, and reproduction. Such observations suggest that incubation temperature (and incubation behaviours of parents) is an important but underappreciated parental effect in birds and may represent a selective force instrumental in shaping avian reproductive ecology and life-history traits. However, much more research is needed to understand how pervasive phenotypic effects of incubation temperature are among birds, the sources of variation in incubation temperature, and how effects on phenotype arise. Such insights will not only provide foundational information regarding avian evolution and ecology, but also contribute to avian conservation.

Ecological, evolutionary, and conservation implications of incubation temperature-dependent phenotypes in birds

The intestinal microbiota have now been shown to largely affect host health through various functional roles in terms of nutrition, immunity, and other physiological systems. However, the majority of these studies have been carried out in mammalian hosts, which differ in their physiological traits from other taxa. For example, birds possess several unique life history traits, such as hatching from eggs, which may alter the interactions with and transmission of intestinal microbes compared to most mammals. This review covers the diversity of microbial taxa hosted by birds. It also discusses how avian microbial communities strongly influence nutrition, immune function, and processing of toxins in avian hosts, in manners similar to and different from mammalian systems. Finally, areas demanding further research are identified, along with descriptions of existing techniques that could be employed to answer these questions.

Diversity and function of the avian gut microbiota

Bi ds e i an chemical compounds, though ornithologists rarely consider them. Avian odors, for example, are readily detectable to humans in at least 17 avian orders and 80 genera (Table 1; data from Weldon and Rappole 1997). Scents consist of volatile chemicals, and birds embrace a remarkable diversity of aromas, such as the musky plumage of storm-petrels (Hydrobatidae; Jacob and Zisweiler 1982); the tangerine-like perfume of Crested Auklets (Aethia cristatella; Humphrey and Phillips 1958); the acrid, sour odor of Hooded Pitohuis (Pitohui dichrous) and Variable Pitohuis (P. kirkocephalus; Dumbacher et al. 1992); the sweet and dusty fragrance of the Kakapo (Strigops habroptilus; Butler 1989, J. C. Hagelin pers. obs.); and the foul stench of the Hoatzin (Opisthocomus hoatzin; see Weldon and Rappole 1997). Birds also produce a variety of substances consisting of larger, less volatile compounds. Frequently odorless, these occur in various forms, such as saturated fatt y acids of uropygial gland secretions (Jacob and Zisweiler 1982, Sweeney et al. 2004) or toxins sequestered in plumage or skin (e.g., Dumbacher et al. 1992). Human detection of an avian compound clearly does not mean that it is important to a bird, unless this has been verifi ed experimentally. Here, we focus on two major types of adaptive functions that have been proposed for a variety of odors and other chemical substances that birds either produce themselves or sequester from secondary sources. First, avian compounds may serve as a chemical defense. This includes protection against predators, ectoparasites, and microbes and can involve substances that act as an interspecifi c deterrent or signal (e.g., Cott 1947, Swennen 1968, Dumbacher et al. 1992, Mouritsen and Madsen 1994, Douglas et al. 2001, Shawkey et al. 2003). Alternatively, some authors posit that avian compounds function as an intraspecifi c chemosignal, similar to those found in other vertebrates, such as mammals (e.g., Balthazart and Schoff eniels 1979; review in Roper 1999, Hagelin 2007). Recently, birds have been shown to recognize conspecifi c body odor (Hagelin et al. 2003) and personal body odor or mate odor (Bonadonna and Nevitt 2004). Some chemical signatures are even individually specifi c (e.g., Bonadonna et al. 2003a, b, 2004, 2007). The use of chemical signals in intraspecifi c communication has the potential to fundamentally alter how we interpret bird behavior. The idea is relatively new and challenges the traditional view that birds predominantly respond to their world through sight and sound. Birds readily respond to chemicals derived 1Department of Biology, Swarthmore College, 500 College Avenue, Swarthmore, Pennsylvania 19081, USA; and 2Department of Biology, Memorial University of Newfoundland, St. John’s, Newfoundland, A1B 3X9, Canada Julie C. Hagelin1,3 and Ian L. Jones2 BIRD ODORS AND OTHER CHEMICAL SUBSTANCES: A DEFENSE MECHANISM OR OVERLOOKED MODE OF INTRASPECIFIC COMMUNICATION? The Auk 124(3):741–761, 2007 © The American Ornithologists’ Union, 2007. Printed in USA.

https://bioone.org/journals/The-Auk/volume-124/issue-3/0004-8038(2007)124[741:BOAOCS]2.0.CO;2/BIRD-ODORS-AND-OTHER-CHEMICAL-SUBSTANCES--A-DEFENSE-MECHANISM/10.1642/0004-8038(2007)124[741:BOAOCS]2.0.CO;2.pdf

Bird odors and other chemical substances: a defense mechanism or overlooked mode of intraspecific communication?

The microbiome is a vital component to the evolution of a host and much of what we know about the microbiome derives from studies on humans and captive animals. But captivity alters the microbiome and mammals have unique biological adaptations that affect their microbiomes (e.g., milk). Birds represent over 30% of known tetrapod diversity and possess their own suite of adaptations relevant to the microbiome. In a previous study, we showed that 59 species of bird displayed immense variation in their microbiomes and host (bird) taxonomy and ecology were most correlated with the gut microbiome. In this Frontiers Focused Review, I put those results in a broader context by discussing how collecting and analyzing wild microbiomes contributes to the main goals of evolutionary biology and the specific ways that birds are unique microbial hosts. Finally, I outline some of the methodological considerations for adding microbiome sampling to the research of wild animals and urge researchers to do so. To truly understand the evolution of a host, we need to understand the millions of microorganisms that inhabit it as well: evolutionary biology needs wild microbiomes.

/pdf/evolutionary-biology-needs-wild-microbiomes-2xn310oivd.pdf

Evolutionary Biology Needs Wild Microbiomes.

Many birds initiate incubation before clutch completion, which results in asynchronous hatching. The ensuing within-brood size disparity often places later-hatched nestlings at a developmental disadvantage, but the functional significance of the timing of the onset of incubation is poorly understood. Early incubation may serve to maintain the viability of early-laid eggs, which declines over time owing to the putative effects of ambient temperature. An unexplored risk to egg viability is trans-shell infection by micro-organisms. We experimentally investigated the rate and magnitude of microbial trans-shell infection of the egg, and the relative effects of ambient temperature and micro-organisms on hatching success. We show that infection of egg contents is prevalent and occurs within the time required to lay a clutch. The probability of infection depends on the climatic conditions, the exposure period and the phylogenetic composition of the eggshell microbiota. We also demonstrate that microbial infection and ambient temperature act independently to reduce egg viability considerably. Our results suggest that these two factors could affect the onset of avian incubation in a wide range of environments.

/pdf/trans-shell-infection-by-pathogenic-micro-organisms-reduces-18qc8la22g.pdf

Trans–shell infection by pathogenic micro–organisms reduces the shelf life of non–incubated bird's eggs: a constraint on the onset of incubation?

Avian eggshells harbour microbes shortly after laying, and under appropriate ambient conditions they can multiply rapidly, penetrate through shell pores, infect egg contents and cause embryo mortality. We experimentally examined how incubation affects bacterial processes on the eggshells of pearl-eyed thrashers Margarops fuscatus nesting in tropical montane and lowland forests in Puerto Rico. Bacteria and fungi grew rapidly on shells of newly laid, unincubated eggs exposed to ambient conditions, but declined to low levels on shells of eggs incubated by thrashers. Divergence in bacterial growth between incubated and exposed eggs was more marked at the montane forest than at the lowland site. Pathogenic microorganisms became increasingly dominant on shells of exposed eggs, but these groups were relatively rare on incubated eggs, where more benign, less invasive groups prevailed. Some incubation during laying may be necessary to decrease the probability of trans-shell infection by reducing the growth of harmful bacteria and fungi on eggshells, although it may increase hatching asynchrony and the likelihood of brood reduction.

https://www.fs.fed.us/global/iitf/pubs/ja_iitf_2005_cook001.pdf

Incubation reduces microbial growth on eggshells and the opportunity for trans-shell infection

Many avian species initiate incubation before clutch completion, which causes eggs to hatch asynchronously. This influences brood competitive dynamics and often results in nestling mortality. The prevailing hypotheses contend that parents incubate early because asynchronous hatching provides fitness benefits to parents or surviving offspring. An alternative idea is that early incubation is the best of a bad job because of the costs of delaying incubation to the viability of first-laid eggs. To explore this, we examined the potential for microbial infection, and the relative effects of infection and suboptimal development temperatures on the viability of pearly-eyed thrasher (Margarops fuscatus) eggs. We exposed newly laid eggs for 5 days at either end of a tropical altitudinal gradient and cleaned shells of half the eggs to reduce microbial growth. Uncleaned eggs were infected more than were cleaned eggs, and infection was greater for eggs exposed at the cool, humid site than at the hot, less humid site. Parentally incubated eggs, however, were not infected, suggesting that incubation limits infection. The consequence of exposure to infection and high ambient temperatures was a dramatic reduction in viability; cleaned eggs held at the cool site had the highest hatching success, which was significantly greater than for uncleaned eggs at this site and for cleaned eggs held at the hot site. This provides the first evidence that microbes can infect unincubated eggs of a wild bird, and that infection and ambient temperature act independently to reduce hatching success. These factors could affect avian life-history strategies in diverse habitats. Key words: ambient temperature, egg viability, hatching asynchrony, onset of incubation, saprophytic microorganism, trans-shell transmission. [Behav Ecol]

https://www.fs.fed.us/global/iitf/pubs/ja_iitf_2005_cook002.pdf

Microbial infection affects egg viability and incubation behavior in a tropical passerine

Avian parents influence the onset of development, hatching synchrony, and likelihood of brood reduction through the onset of incubation. Studies testing adaptive functions of brood reduction assume that eggs are protected by their shells and waiting for parents to initiate incubation in a manner that creates optimal hatching patterns, but the viability of early laid eggs may diminish over time due to putative effects of ambient temperature. We tested effects of exposure to ambient temperature on the viability of un- incubated bird eggs using an altitudinal climate gradient in Puerto Rico: daily maximum temperatures nearly always exceed developmental zero in the lowland forest, whereas tem- peratures rarely exceed developmental zero in the cloud forest and at intermediate altitudes. We removed 382 freshly laid Pearly-eyed Thrasher (Margarops fuscatus) eggs, placed them in holding boxes at three sites for 1-7 days, and returned them to nests to be incubated. Additional control eggs (n 5 39) tested effects of both handling and movement on hatching success, and unmanipulated eggs (n 5 139) provided a measure of natural hatching success. Hatching success of control eggs (82.0%) and unmanipulated eggs (84.9%) did not differ, indicating no impacts of handling on hatchability. Hatching success of experimental eggs exposed for one day (78.6%) was high but declined very strongly after exposure for three days (41.9%), five days (11.5%) and seven days (2.1%). Hatchability of eggs held at the cloud forest did not differ from eggs held at the lowland site but was lower for eggs exposed at mid-elevation. Hatching success was positively related to minimum temperature and marginally related to mean temperature and proportion of time above developmental zero. Exposure duration, treatment site, and maximum temperature were the only significant effects identified by stepwise logistic regression. Eggs held at the lowland site had shorter developmental periods than eggs held at other sites. Most embryo mortality (80.8%) oc- curred at very early stages. Our results demonstrate that viability of unincubated eggs exposed to moist tropical conditions declines strongly but suggest that ambient temperature is not the sole cause. We compare rates of egg viability decline among species, examine alternative mechanisms for the loss of viability, and discuss the significance of egg viability on avian life histories.

https://www.fs.fed.us/global/iitf/pubs/ja_iitf_2005_beissinger001.pdf

Mark I. Cook

Papers

Trans–shell infection by pathogenic micro–organisms reduces the shelf life of non–incubated bird's eggs: a constraint on the onset of incubation?

Incubation reduces microbial growth on eggshells and the opportunity for trans-shell infection

Microbial infection affects egg viability and incubation behavior in a tropical passerine

The shelf life of bird eggs: testing egg viability using a tropical climate gradient