Is resilience a unifying concept for the biological sciences?

There is increasing interest in applying resilience concepts at different scales of biological organization to address major interdisciplinary challenges from cancer to climate change. It is unclear, however, whether resilience can be a unifying concept consistently applied across the breadth of the biological sciences, or whether there is limited capacity for integration. In this review, we draw on literature from molecular biology to community ecology to ascertain commonalities and shortcomings in how resilience is measured and interpreted. Resilience is studied at all levels of biological organization, although the term is often not used. There is a suite of resilience mechanisms conserved across biological scales, and there are tradeoffs that affect resilience. Resilience is conceptually useful to help diverse researchers think about how biological systems respond to perturbations, but we need a richer lexicon to describe the diversity of perturbations, and we lack widely applicable metrics of resilience.

House sparrows prioritize skin repair over constitutive innate immunity during long-term chronic stress.

The reactive scope model was created to address two major unanswered questions in stress physiology: how and when does the adaptive acute stress response turn into harmful chronic stress? Previous studies suggest that immunoenhancement should occur in reactive homeostasis (acute stress) and immunosuppression should occur in homeostatic overload (chronic stress). We used this dichotomy of immune function to further elucidate the transition from acute to chronic stress by treating house sparrows (Passer domesticus) with different intensities of chronic stress and then monitoring their immune function. By varying the number of stressors given per day and the length of chronic stress bouts over a period of 6 months, we produced four treatment groups: high, medium, and low stress, and captivity-only. We tracked immunity through the bacterial killing assay and monitored healing of a 4 mm skin biopsy punch. We hypothesized that higher-stress birds would repair their skin more slowly and have lower bacterial killing capacity. The opposite was true-high-stress birds initially repaired their skin fastest. Additionally, all birds dramatically reduced bacterial killing capacity after the biopsy and increased food-derived uric acid, suggesting increased energy acquisition and a shift in immune resources to a more immediate concern (healing). Once healing finished, only the high-stress birds were unable to recover circulating immune function, suggesting that the combination of high stress and an immune challenge pushed these birds into homeostatic overload. Prioritizing healing over other immunological processes might be the best defense for a bird in its natural habitat.

Mercury correlates with altered corticosterone but not testosterone or estradiol concentrations in common loons.

We investigated the relation between environmental mercury exposure and corticosterone concentrations in free-living adult common loons (Gavia immer). We determined blood and feather mercury concentrations and compared them to testosterone, estradiol, and stress-induced plasma corticosterone concentrations. Although neither testosterone nor estradiol correlated with Hg levels, there was a robust positive relation between blood Hg and stress-induced corticosterone concentrations in males, but not in females. The lack of an effect in females may have been due to overall less contamination in females. There were no significant correlations between feather Hg and stress-induced corticosterone in either sex. To help determine whether Hg had a causal effect on corticosterone, we investigated the impact of experimental Hg intake on the corticosterone stress response in captive juvenile loons. Juveniles were subjected to three different feeding regimes: 0, 0.4 and 1.2µg Hg (as MeHgCL)/g wet weight (ww) fish. We then measured baseline and 30min post-solitary confinement stressor corticosterone concentrations. The Hg fed chicks exhibited a decreased ability to mount a stress response. From these data, we conclude that Hg contamination does appear to alter the corticosterone response to stress, but not in a consistent predictable pattern. Regardless of the direction of change, however, exposure to mercury contamination and the resulting impact on the corticosterone stress response in common loons may substantially impact health, fitness and survival.

Evaluating the stress response as a bioindicator of sub-lethal effects of crude oil exposure in wild house sparrows (Passer domesticus).

Petroleum can disrupt endocrine function in humans and wildlife, and interacts in particularly complex ways with the hypothalamus-pituitary-adrenal (HPA) axis, responsible for the release of the stress hormones corticosterone and cortisol (hereafter CORT). Ingested petroleum can act in an additive fashion with other stressors to cause increased mortality, but it is not clear exactly why--does petroleum disrupt feedback mechanisms, stress hormone production, or both? This laboratory study aimed to quantify the effects of ingested Gulf of Mexico crude oil on the physiological stress response of house sparrows (Passer domesticus). We examined baseline and stress-induced CORT, negative feedback, and adrenal sensitivity in house sparrows given a 1% oil or control diet (n = 12 in each group). We found that four weeks on a 1% oil diet did not alter baseline CORT titers or efficacy of negative feedback, but significantly reduced sparrows' ability to secrete CORT in response to a standardized stressor and adrenocorticotropin hormone injection, suggesting that oil damages the steroid-synthesizing cells of the adrenal. In another group of animals on the same 1% oil (n = 9) or control diets (n = 8), we examined concentrations of eight different blood chemistry parameters, and CORT in feathers grown before and during the feeding experiments as other potential biomarkers of oil exposure. None of the blood chemistry parameters differed between birds on the oil and control diets after two or four weeks of feeding, nor did feather CORT differ between the two groups. Overall, this study suggests that the response of CORT to stressors, but not baseline HPA function, may be a particularly sensitive bioindicator of sub-lethal chronic effects of crude oil exposure.

To breed or not to breed: physiological correlates of reproductive status in a facultatively biennial iguanid.

It is unusual for seasonal breeders to frequently skip opportunities for reproduction. We investigated the relationship between physiological state and reproductive decision-making in Galápagos marine iguanas (Amblyrhynchus cristatus), a species in which females typically reproduce biennially, although the proportion of breeding individuals varies significantly across years. Nearly all adult-sized females initiated follicular development prior to the lekking period, but 38% of females resorbed all developing follicles 5-15 days before the start of copulations. Receptive and non-receptive females differed in reproductive hormones during the mate choice period. Testosterone peaked in receptive females immediately prior to copulation, indicating that testosterone or its derivative estradiol likely mediates female receptivity in Galápagos marine iguanas. Non-receptive females showed significant peaks in both testosterone and progesterone during follicular atresia, suggesting that these hormones may be involved in inhibiting vitellogenesis. Two to three weeks prior to the period of reproductive decision-making (and the onset of follicular atresia in non-receptive females) receptive females were in higher body condition, were developing larger follicles, and had lower levels of both baseline and stress-induced corticosterone. Reproduction is extremely costly in this long-lived species, and increases the likelihood of mortality in the year following breeding; females could therefore gain significant benefits from being attuned to indicators of reproductive success. We suggest that corticosterone may modulate reproductive decisions by altering individual sensitivity to both internal and external cues of the likelihood of successful reproduction.

Steroid hormone interrelationships with territorial aggression in an Arctic-breeding songbird, Gambel's white-crowned sparrow, Zonotrichia leucophrys gambelii.

The breeding season is very brief for arctic-breeding passerines, and any interruptions of parental care by aggressive interactions over territory may reduce reproductive success. We tested both the "testosterone insensitivity" and "corticosterone insensitivity" hypotheses in the arctic-breeding Gambel's white-crowned sparrow, Zonotrichia leucophrys gambelii. Additionally, we tested whether simulated territorial intrusions (STIs), known to stimulate increases in luteinizing hormone (LH) and testosterone (T) in mid-latitude breeding Z. l. pugetensis, would also be effective in either the early or late phases of the brief breeding season of Z. l. gambelii. Plasma levels of T and LH were high early in the breeding season and declined as egg laying began. Exposure of free-living males to 10 min of STI significantly increased LH but not T secretion. Nonetheless, the pituitary-gonadal axis is sensitive as jugular injection of gonadotrophin-releasing hormone increased plasma T at 10 min relative to saline-challenged controls. T implants failed to increase territorial aggression following STI during incubation. These data are consistent with the T insensitivity hypothesis and contrast sharply with the response of the southerly breeding subspecies, Z. l. pugetensis, in which the territorial response to T administration is retained throughout its relatively long breeding season. However, corticosterone implants during the incubation period decreased territorial aggression during STI. This responsiveness to corticosterone is not consistent with the corticosterone insensitivity hypothesis of stress modulation. Z. l. gambelii retain sensitivity to corticosterone levels that may occur naturally in response to environmental perturbations resulting in suppression of territorial behavior.

Effect of polar day on plasma profiles of melatonin, testosterone, and estradiol in high-Arctic Lapland Longspurs.

In polar habitats, continuous daylight (polar day) can prevail for many weeks or months around the summer solstice. In the laboratory, continuous light conditions impair or disrupt circadian rhythms in many animals. To determine whether circadian rhythms are disrupted under natural polar day conditions in a species that is only a summer resident in polar regions we analyzed diel rhythms in plasma concentrations of melatonin, testosterone (T), and 17-beta estradiol (E(2)) during the summer solstice in Arctic-breeding Lapland Longspurs (Calcarius lapponicus). We compared these profiles to those of conspecifics housed in outdoor aviaries at a mid-latitude site in Seattle, Washington, during spring, summer, fall, and winter. Under polar day conditions plasma melatonin concentrations of Lapland Longspurs were strongly suppressed, but still showed a significant diel rhythm. Likewise, plasma T in males, and E(2) in females, showed significant diel changes in Arctic birds. Lapland Longspurs housed at mid-latitude in Seattle showed high-amplitude melatonin cycles at all times of the year, and the duration of the nightly melatonin secretion was positively correlated with the duration of the dark phase. We found no diel changes in plasma T in Seattle males in May, but Seattle females showed significant day/night differences in plasma E(2) in May. The data suggest that even under polar day conditions diel rhythms can persist. The maintenance of hormone rhythms could provide a physiological basis to reports of rhythmic behavior in many birds during the Arctic summer.