Early warnings of environmental change on ecosystems: hormonally-mediated life-history decisions in seabirds

Biological indicator species can reveal consequences of changes in physical processes within the environment, through effects on their physiology, behaviour and population dynamics. Long-lived species tend to be positioned at the top of the food chain where they can act as indicators of environmental change occurring at lower trophic levels. During poor conditions, these long-lived top predators have been selected to prioritise their own survival above the current breeding attempt, in order to maximise lifetime reproductive success. Endocrine mechanisms involving corticosterone, the ‘stress hormone’, and possibly prolactin, the ‘parental hormone’, are involved in mediating the abandonment of breeding in response to environmental perturbations. This thesis aimed to assess what the breeding success of a top marine predator indicates about changes in the marine ecosystem and what mechanisms control changes in breeding success, using the black-legged kittiwake Rissa tridactyla as the model species. I combined population-level analyses of long-term datasets (1997–2010) of diet composition, adult body mass, breeding success and foraging behaviour from the Isle of May, National Nature Reserve, Firth of Forth, south-east Scotland (56° 11‘ N, 02° 33’ W) with an individual-level field experiment to simulate chronic stress. Kittiwakes breeding in the north-western North Sea depend primarily on adult (1+ group) lesser sandeels Ammodytes marinus at the start of the breeding season and subsequently switch to depend primarily on young of the year (0 group) sandeels. Analysis of the long-term data showed that the timing of the kittiwake breeding season has become later in recent years, whilst the timing of the switch from 1+ group to 0 group sandeels in the kittiwake diet has become earlier, which may suggest mismatches in the timing of prey availability and predator demand. Increasing proportions of clupeids (mainly sprat Sprattus sprattus) were seen in the diet and further years of study may reveal whether clupeids could be a beneficial alternative prey type for kittiwakes. Foraging trip duration was unrelated to diet composition, suggesting that the main prey types of kittiwakes do not differ in their distance from the colony. Whilst foraging trip duration during incubation was related to changes in adult body mass and hatching success, diet composition was unrelated. There was a weak effect of diet composition during chick-rearing on fledging success, mediated via changes in adult body mass. However, this effect was masked by a stronger, independent, negative effect of foraging trip duration during chick-rearing. To simulate chronic stress in kittiwakes, individuals were implanted with corticosterone, using Alzet® osmotic pumps, for a week at the end of incubation. The methodology applied to kittiwakes was based on a preliminary experiment carried out in Japanese quail Coturnix coturnix japonica. The body mass and prolactin concentrations of kittiwakes were unchanged after this treatment. Corticosterone concentrations had returned to pre-treatment values by the end of the treatment week, which may have been due to down-regulation or suppression of the stress response as a result of the treatment. Corticosterone-implanted males showed lower nest attendance than sham-implanted males but the opposite was true for females. Breeding success at the end of the season was lower in corticosterone-implanted birds, suggesting a prolonged effect of chronic stress. In order to investigate the effects of disturbance to a group or colony of birds prior to the capture of an individual, a preliminary experiment was also carried out to test the stress responsiveness of a captive bird, the Japanese quail. No increase in corticosterone concentrations was seen after a capture-restraint protocol and with increasing time since the group of birds was first disturbed. A suppressed stress response in this bird may be explained by long-term captivity or domestication. These results show that the breeding success of a top marine predator can indicate changes in the timing of prey availability and prey location, mediated through changes in adult body mass. I also found that changes occurring during the chick-rearing period contributed most to the outcome of the breeding season. Chronically elevated concentrations of corticosterone are important in the control of breeding success, whereas prolactin may only play a role close to the timing of breeding failure or after failure has occurred. This thesis demonstrates the need for continued long-term monitoring of wild populations and refining of experimental methodology to better understand the impacts of environmental change on top predators