Charles M. Bishop

The trans-Himalayan flights of bar-headed geese (Anser indicus)

Birds that fly over mountain barriers must be capable of meeting the increased energetic cost of climbing in low-density air, even though less oxygen may be available to support their metabolism. This challenge is magnified by the reduction in maximum sustained climbing rates in large birds. Bar-headed geese (Anser indicus) make one of the highest and most iconic transmountain migrations in the world. We show that those populations of geese that winter at sea level in India are capable of passing over the Himalayas in 1 d, typically climbing between 4,000 and 6,000 m in 7–8 h. Surprisingly, these birds do not rely on the assistance of upslope tailwinds that usually occur during the day and can support minimum climb rates of 0.8–2.2 km·h−1, even in the relative stillness of the night. They appear to strategically avoid higher speed winds during the afternoon, thus maximizing safety and control during flight. It would seem, therefore, that bar-headed geese are capable of sustained climbing flight over the passes of the Himalaya under their own aerobic power.

Helping effort increases with relatedness in bell miners, but 'unrelated' helpers of both sexes still provide substantial care

Indirect fitness benefits from kin selection can explain why non-breeding individuals help raise the young of relatives. However, the evolution of helping by non-relatives requires direct fitness benefits, for example via group augmentation. Here, we examine nest visit rates, load sizes and prey types delivered by breeding pairs and their helpers in the cooperatively breeding bell miner (Manorina melanophrys). In this system, males remain in their natal colony while young females typically disperse, and helpers of both sexes often assist at multiple nests concurrently. We found extremely clear evidence for the expected effect of genetic relatedness on individual helping effort per nest within colonies. This positive incremental effect of kinship was facultative—i.e. largely the result of within-individual variation in helping effort. Surprisingly, no sex differences were detectable in any aspect of helping, and even non-relatives provided substantial aid. Helpers and breeders of both sexes regulated their provisioning effort by responding visit-by-visit to changes in nestling begging. Helping behaviour in bell miners therefore appears consistent with adaptive cooperative investment in the brood, and kin-selected care by relatives. Similar investment by ‘unrelated’ helpers of both sexes argues against direct fitness benefits, but is perhaps explained by kin selection at the colony level.

Hibernation in an Antarctic Fish: On Ice for Winter

Active metabolic suppression in anticipation of winter conditions has been demonstrated in species of mammals, birds, reptiles and amphibians, but not fish. This is because the reduction in metabolic rate in fish is directly proportional to the decrease in water temperature and they appear to be incapable of further suppressing their metabolic rate independently of temperature. However, the Antarctic fish (Notothenia coriiceps) is unusual because it undergoes winter metabolic suppression irrespective of water temperature. We assessed the seasonal ecological strategy by monitoring swimming activity, growth, feeding and heart rate (f H) in N. coriiceps as they free-ranged within sub-zero waters. The metabolic rate of wild fish was extrapolated from f H recordings, from oxygen consumption calibrations established in the laboratory prior to fish release. Throughout the summer months N. coriiceps spent a considerable proportion of its time foraging, resulting in a growth rate (Gw) of 0.18±0.2% day−1. In contrast, during winter much of the time was spent sedentary within a refuge and fish showed a net loss in Gw (−0.05±0.05% day−1). Whilst inactive during winter, N. coriiceps displayed a very low f H, reduced sensory and motor capabilities, and standard metabolic rate was one third lower than in summer. In a similar manner to other hibernating species, dormancy was interrupted with periodic arousals. These arousals, which lasted a few hours, occurred every 4–12 days. During arousal activity, f H and metabolism increased to summer levels. This endogenous suppression and activation of metabolic processes, independent of body temperature, demonstrates that N. coriiceps were effectively ‘putting themselves on ice’ during winter months until food resources improved. This study demonstrates that at least some fish species can enter a dormant state similar to hibernation that is not temperature driven and presumably provides seasonal energetic benefits.

Eco-Virological Approach for Assessing the Role of Wild Birds in the Spread of Avian Influenza H5N1 along the Central Asian Flyway

A unique pattern of highly pathogenic avian influenza (HPAI) H5N1 outbreaks has emerged along the Central Asia Flyway, where infection of wild birds has been reported with steady frequency since 2005. We assessed the potential for two hosts of HPAI H5N1, the bar-headed goose (Anser indicus) and ruddy shelduck (Tadorna tadorna), to act as agents for virus dispersal along this ‘thoroughfare’. We used an eco-virological approach to compare the migration of 141 birds marked with GPS satellite transmitters during 2005–2010 with: 1) the spatio-temporal patterns of poultry and wild bird outbreaks of HPAI H5N1, and 2) the trajectory of the virus in the outbreak region based on phylogeographic mapping. We found that biweekly utilization distributions (UDs) for 19.2% of bar-headed geese and 46.2% of ruddy shelduck were significantly associated with outbreaks. Ruddy shelduck showed highest correlation with poultry outbreaks owing to their wintering distribution in South Asia, where there is considerable opportunity for HPAI H5N1 spillover from poultry. Both species showed correlation with wild bird outbreaks during the spring migration, suggesting they may be involved in the northward movement of the virus. However, phylogeographic mapping of HPAI H5N1 clades 2.2 and 2.3 did not support dissemination of the virus in a northern direction along the migration corridor. In particular, two subclades (2.2.1 and 2.3.2) moved in a strictly southern direction in contrast to our spatio-temporal analysis of bird migration. Our attempt to reconcile the disciplines of wild bird ecology and HPAI H5N1 virology highlights prospects offered by both approaches as well as their limitations.

Fatty acid binding protein in heart and skeletal muscles of the migratory barnacle goose throughout development

The long-distance migratory flights of birds are predominantly fueled by the oxidation of fatty acids, which are sourced primarily from extracellular adipose stores. These fatty acids have to be transported, via the circulatory system, to the mitochondria of the active muscles. An important facilitator of fatty acid transport within the cytoplasm of muscle cells is fatty acid binding protein (FABP), which serves as an intracellular carrier of long-chain fatty acids. In mammals, the muscular FABP content is related to the fatty acid oxidation capacity of the tissue. The aim of this study was to measure FABP in samples taken from the cardiac, pectoralis, and semimembranosus muscles of a long-distance avian migrant, the barnacle goose (Branta leucopsis), at various stages of development. Western blot analysis identified a single goose muscle protein of 15 kDa that was able to bind fatty acids and showed a 66% cross-reactivity with antibodies against human heart-type FABP. Captive goslings showed no significant changes in FABP content of either the heart (62.6 +/- 10.6 microgram/g wet wt) or the semimembranosus muscle (8.4 +/- 1.9 microgram/g wet wt) during development. However, in both peripheral and deep sites within the pectoralis muscle, FABP content of samples taken from captive goslings were approximately 10-fold higher throughout development and reached values of 30-40 microgram/g wet wt in fledging goslings at 7 wk of age. A further twofold higher value was seen in wild but not in captive goslings immediately before migration (12 wk of age). Similarly, FABP content was significantly higher in pectoralis samples taken from wild adults (94.3 +/- 3.6 microgram/g wet wt) compared with those from captive adults (60.5 +/- 3.6 micro/g wet wt). These results suggest that the experience of flight activity may be of critical importance in achieving maximal expression of FABP in the pectoralis muscles of postfledging and mature geese immediately before migration.The long-distance migratory flights of birds are predominantly fueled by the oxidation of fatty acids, which are sourced primarily from extracellular adipose stores. These fatty acids have to be transported, via the circulatory system, to the mitochondria of the active muscles. An important facilitator of fatty acid transport within the cytoplasm of muscle cells is fatty acid binding protein (FABP), which serves as an intracellular carrier of long-chain fatty acids. In mammals, the muscular FABP content is related to the fatty acid oxidation capacity of the tissue. The aim of this study was to measure FABP in samples taken from the cardiac, pectoralis, and semimembranosus muscles of a long-distance avian migrant, the barnacle goose ( Branta leucopsis), at various stages of development. Western blot analysis identified a single goose muscle protein of 15 kDa that was able to bind fatty acids and showed a 66% cross-reactivity with antibodies against human heart-type FABP. Captive goslings showed no significant changes in FABP content of either the heart (62.6 ± 10.6 μg/g wet wt) or the semimembranosus muscle (8.4 ± 1.9 μg/g wet wt) during development. However, in both peripheral and deep sites within the pectoralis muscle, FABP content of samples taken from captive goslings were ∼10-fold higher throughout development and reached values of 30-40 μg/g wet wt in fledging goslings at 7 wk of age. A further twofold higher value was seen in wild but not in captive goslings immediately before migration (12 wk of age). Similarly, FABP content was significantly higher in pectoralis samples taken from wild adults (94.3 ± 3.6 μg/g wet wt) compared with those from captive adults (60.5 ± 3.6 μg/g wet wt). These results suggest that the experience of flight activity may be of critical importance in achieving maximal expression of FABP in the pectoralis muscles of postfledging and mature geese immediately before migration.

The paradox of extreme high-altitude migration in bar-headed geese Anser indicus

Bar-headed geese are renowned for migratory flights at extremely high altitudes over the worlds tallest mountains, the Himalayas, where partial pressure of oxygen is dramatically reduced while flight costs, in terms of rate of oxygen consumption, are greatly increased. Such a mismatch is paradoxical, and it is not clear why geese might fly higher than is absolutely necessary. In addition, direct empirical measurements of high-altitude flight are lacking. We test whether migrating bar-headed geese actually minimize flight altitude and make use of favourable winds to reduce flight costs. By tracking 91 geese, we show that these birds typically travel through the valleys of the Himalayas and not over the summits. We report maximum flight altitudes of 7290 m and 6540 m for southbound and northbound geese, respectively, but with 95 per cent of locations received from less than 5489 m. Geese travelled along a route that was 112 km longer than the great circle (shortest distance) route, with transit ground speeds suggesting that they rarely profited from tailwinds. Bar-headed geese from these eastern populations generally travel only as high as the terrain beneath them dictates and rarely in profitable winds. Nevertheless, their migration represents an enormous challenge in conditions where humans and other mammals are only able to operate at levels well below their sea-level maxima.

Frigate birds track atmospheric conditions over months-long transoceanic flights

Understanding how animals respond to atmospheric conditions across space is critical for understanding the evolution of flight strategies and long-distance migrations. We studied the three-dimensional movements and energetics of great frigate birds (Fregata minor) and showed that they can stay aloft for months during transoceanic flights. To do this, birds track the edge of the doldrums to take advantage of favorable winds and strong convection. Locally, they use a roller-coaster flight, relying on thermals and wind to soar within a 50- to 600-meter altitude band under cumulus clouds and then glide over kilometers at low energy costs. To deal with the local scarcity of clouds and gain longer gliding distances, birds regularly soar inside cumulus clouds to use their strong updraft, and they can reach altitudes of 4000 meters, where freezing conditions occur.

Evidence for a respiratory component, similar to mammalian respiratory sinus arrhythmia, in the heart rate variability signal from the rattlesnake, Crotalus durissus terrificus

SUMMARY Autonomic control of heart rate variability and the central location of vagal preganglionic neurones (VPN) were examined in the rattlesnake (Crotalus durissus terrificus), in order to determine whether respiratory sinus arrhythmia (RSA) occurred in a similar manner to that described for mammals. Resting ECG signals were recorded in undisturbed snakes using miniature datalogging devices, and the presence of oscillations in heart rate (fh) was assessed by power spectral analysis (PSA). This mathematical technique provides a graphical output that enables the estimation of cardiac autonomic control by measuring periodic changes in the heart beat interval. At fh above 19 min-1 spectra were mainly characterised by low frequency components, reflecting mainly adrenergic tonus on the heart. By contrast, at fh below 19 min-1 spectra typically contained high frequency components, demonstrated to be cholinergic in origin. Snakes with a fh >19 min-1 may therefore have insufficient cholinergic tonus and/or too high an adrenergic tonus acting upon the heart for respiratory sinus arrhythmia (RSA) to develop. A parallel study monitored fh simultaneously with the intraperitoneal pressures associated with lung inflation. Snakes with a fh<19 min-1 exhibited a high frequency (HF) peak in the power spectrum, which correlated with ventilation rate (fv). Adrenergic blockade by propranolol infusion increased the variability of the ventilation cycle, and the oscillatory component of the fh spectrum broadened accordingly. Infusion of atropine to effect cholinergic blockade abolished this HF component, confirming a role for vagal control of the heart in matching fh and fv in the rattlesnake. A neuroanatomical study of the brainstem revealed two locations for vagal preganglionic neurones (VPN). This is consistent with the suggestion that generation of ventilatory components in the heart rate variability (HRV) signal are dependent on spatially distinct loci for cardiac VPN. Therefore, this study has demonstrated the presence of RSA in the HRV signal and a dual location for VPN in the rattlesnake. We suggest there to be a causal relationship between these two observations.

How Bar-Headed Geese Fly Over the Himalayas

Bar-headed geese cross the Himalayas on one of the most iconic high-altitude migrations in the world. Heart rates and metabolic costs of flight increase with elevation and can be near maximal during steep climbs. Their ability to sustain the high oxygen demands of flight in air that is exceedingly oxygen-thin depends on the unique cardiorespiratory physiology of birds in general along with several evolved specializations across the O2 transport cascade.

Spatial dynamics of bar-headed geese migration in the context of H5N1

Virulent outbreaks of highly pathogenic avian influenza (HPAI) since 2005 have raised the question about the roles of migratory and wild birds in the transmission of HPAI. Despite increased monitoring, the role of wild waterfowl as the primary source of the highly pathogenic H5N1 has not been clearly established. The impact of outbreaks of HPAI among species of wild birds which are already endangered can nevertheless have devastating consequences for the local and non-local ecology where migratory species are established. Understanding the entangled dynamics of migration and the disease dynamics will be key to prevention and control measures for humans, migratory birds and poultry. Here, we present a spatial dynamic model of seasonal migration derived from first principles and linking the local dynamics during migratory stopovers to the larger scale migratory routes. We discuss the effect of repeated epizootic at specific migratory stopovers for bar-headed geese (Anser indicus). We find that repeated deadly outbreaks of H5N1 on stopovers during the autumn migration of bar-headed geese could lead to a larger reduction in the size of the equilibrium bird population compared with that obtained after repeated outbreaks during the spring migration. However, the opposite is true during the first few years of transition to such an equilibrium. The age-maturation process of juvenile birds which are more susceptible to H5N1 reinforces this result.