Charles R. Brown

Ectoparasitism as a Cost of Coloniality in Cliff Swallows (Hirundo Pyrrhonota)

Colonially nesting Cliff Swallows (Passeriformes: Hirundo pyrrhonota) in southwestern Nebraska, USA, are commonly parasitized by hematophagous swallow bugs (Hemiptera: Cimicidae: Oeciacus vicarius) and fleas (Siphonaptera: Ceratophyllidae: Ceratophyllus celsus). We examined to what degree these ectoparasites represent a cost of coloniality for Cliff Swallows. The number of swallow bugs per nest increased significantly with Cliff Swallow colony size. Body mass of nestling swallows at 10 d of age declined significantly as the number of bugs per nestling increased. By fumigating half of the nests in some colonies, killing the bugs, and leaving half of the nests as nonfumigated controls, we showed that swallow bugs lower nestling body mass and nestling survivorship in large Cliff Swallow colonies but not in small ones. Bugs cost nestlings, on average, up to 3.4 g in body mass, and reduced survivorship by up to 50%. Parasitism by fleas showed no consistent relationship with colony size during the nestling period but increased significantly with colony size early in the season, when birds were first arriving in the study area. Fleas did not affect nestling body mass or survivorship and thus, unlike swallow bugs, are probably not important costs of coloniality to Cliff Swallows. Field observations and nest fumigation experiments showed that Cliff Swallows apparently assess which nests are heavily infested with swallow bugs early each spring and select parasite-free nests, leading sometimes to alternate-year colony site usage. Cliff Swallows were more likely to construct new nests (rather than reusing old ones) in large colonies than in small colonies, probably in response to heavier infestations of ectoparasites in the existing nests of large colonies.

Insulin secretion: Combined effects of phorbol ester and A23187

The effect of the ionophore, A23187, and/or the phorbol ester, 12-O-tetradecanoyl-phorbol-13-acetate (TPA), on insulin secretion were compared with those of glucose. Glucose induces a biphasic pattern of insulin secretion; A23187 a comparable initial spike but no second phase; and TPA a slowly progressive increase. Combined A23187 and TPA evoke a pattern similar to that induced by glucose. Forskolin enhances both phases of glucose- induced and of TPA-A23187-induced insulin secretion. These results are interpreted in terms of a model of cell activation in which two branches of the calcium messenger system, the calmodulin branch and the C-kinase branch, control, respectively, the initial and sustained phases of insulin secretion.

Rapid induction of inflammatory lipid mediators by the inflammasome in vivo.

Detection of microbial products by host inflammasomes is an important mechanism of innate immune surveillance. Inflammasomes activate the caspase-1 (CASP1) protease, which processes the cytokines interleukin (IL)-1β and IL-18, and initiates a lytic host cell death called pyroptosis. To identify novel CASP1 functions in vivo, we devised a strategy for cytosolic delivery of bacterial flagellin, a specific ligand for the NAIP5 (NLR family, apoptosis inhibitory protein 5)/NLRC4 (NLR family, CARD-domain-containing 4) inflammasome. Here we show that systemic inflammasome activation by flagellin leads to a loss of vascular fluid into the intestine and peritoneal cavity, resulting in rapid (less than 30 min) death in mice. This unexpected response depends on the inflammasome components NAIP5, NLRC4 and CASP1, but is independent of the production of IL-1β or IL-18. Instead, inflammasome activation results, within minutes, in an ‘eicosanoid storm’—a pathological release of signalling lipids, including prostaglandins and leukotrienes, that rapidly initiate inflammation and vascular fluid loss. Mice deficient in cyclooxygenase-1, a critical enzyme in prostaglandin biosynthesis, are resistant to these rapid pathological effects of systemic inflammasome activation by either flagellin or anthrax lethal toxin. Inflammasome-dependent biosynthesis of eicosanoids is mediated by the activation of cytosolic phospholipase A2 in resident peritoneal macrophages, which are specifically primed for the production of eicosanoids by high expression of eicosanoid biosynthetic enzymes. Our results therefore identify eicosanoids as a previously unrecognized cell-type-specific signalling output of the inflammasome with marked physiological consequences in vivo.

INTENSE NATURAL SELECTION ON BODY SIZE AND WING AND TAIL ASYMMETRY IN CLIFF SWALLOWS DURING SEVERE WEATHER

Extreme climatic disturbances provide excellent opportunities to study natural selection in wild populations because they may cause measurable directional shifts in character traits. Insectivorous cliff swallows (Petrochelidon pyrrhonota) in the northern Great Plains must often endure periods of cold weather in late spring that reduce food availability, and if cold spells last four or more days, mortality due to starvation may result. We analyzed morphological shifts associated with viability selection, and how patterns of bilateral symmetry were affected by survival selection, during a four‐day period of cold weather in 1992 and a six‐day period in 1996 in southwestern Nebraska. Birds that died during the cold were compared to those still alive when the severe weather ended. The event in 1992 killed relatively few birds, but the cold spell in 1996 killed thousands of cliff swallows and reduced their population by about 53%. Climatological records suggest that mortality events comparable to that of 1996 have occurred in only one other year since 1875. Larger birds were favored in the 1996 event. Selection was more intense in 1996 than in 1992 because of more stressful conditions in 1996. Directional selection gradient analysis showed that measures of skeletal body size (tarsus length, culmen width and length) and wing length were targets of selection in 1996. Survivors had lower wing and outer tail asymmetry, and wing and tail asymmetry were targets of selection in both events. Mortality patterns did not differ by sex, but older birds suffered heavier mortality; morphological traits generally did not vary with age. Nonsurvivors were not in poorer apparent condition prior to the weather event than survivors, suggesting that selection acted directly on morphology independent of condition. Selection on body size in cliff swallows was more intense than in studies of body size evolution in other bird species. Larger swallows were probably favored in cold weather due to the thermal advantages of large size and the ability to store more fat. Swallows with low asymmetry were favored probably because low asymmetry in wing and tail made foraging more efficient and less costly, conferring survival advantages during cold weather. This population of cliff swallows may have undergone relatively recent body size evolution.

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.

Choice of colony size in birds

Most populations of colonial birds exhibit extensive variation in colony size. Field studies over the last decade have shown that individual birds breeding in colonies of certain sizes are apparently more successful than those settling in colonies of other sizes, yet size variation persists. Enough information is now available to suggest four explanations for how birds choose colonies and why colonies vary in size.

Cliff Swallow Colonies as Information Centers

Colonies of cliff swallows (Aves: Hirundo pyrrhonota) appear to be information centers in which colony residents acquire information on the location of food sources. Individuals that have been unsuccessful on a foraging trip return to the colony, locate a successful forager, and follow that individual to a food source. Individuals often follow, and are followed by, their neighbors within the colony, possibly because neighbors can observe foraging success through food brought back to nestlings. All individuals are equally likely to follow others or be followed, and thus all individuals benefit from opportunities to receive information.

Immune Defense and Host Sociality: A Comparative Study of Swallows and Martins

Sociality is associated with increased risks of parasitism, predation, and social competition, which may interact because social stress can reduce immunity, and parasitized individuals are more likely to fall prey to a predator. A mechanism allowing evolution of sociality in spite of high costs of parasitism is increased investment in antiparasite defenses. Here we show that the impact of parasites on host reproductive success was positively associated with the degree of sociality in the bird family Hirundinidae. However, the cost of parasitism in highly colonial species was countered by high levels of T‐ and B‐cell immune responses. Investment in immune function among colonial species was particularly strong in nestlings, and among social species, this investment was associated with a relatively prolonged period of development, thereby leading to extended exposure to parasites. Thus, highly social species such as certain species of swallows and martins may cope with strong natural selection arising from parasites by heavy investment in immune function at the cost of a long exposure to nest parasites.

Laying Eggs in a Neighbor's Nest: Benefit and Cost of Colonial Nesting in Swallows.

Intraspecific brood parasitism (laying eggs in anothers nest) occurs widely in colonial cliff swallows (Passeriformes: Hirundinidae: Hirundo pyrrhonota). In colonies consisting of more than ten nests, up to 24 percent of the nests were sometimes parasitized by colony members. Laying eggs in a conspecifics nest may be a benefit of coloniality for parasitic individuals and simultaneously may represent a cost to host individuals within the same colony.

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.