UC Davis

Anthropogenic land-use change and agricultural intensification have caused extensive ecological change on a global scale, especially during the last 50 years. This has coincided with large declines in avian abundance, especially among farmland-associated and grassland birds. There is increasing awareness of the negative ecological and environmental effects of the widespread use of pesticides and other anthropogenic chemicals across entire landscapes. Neonicotinoid insecticides in particular are associated with population declines in insectivorous birds due to pesticide-mediated reductions in food supply, and may exasperate declines in species that are of conservation concern. The direct and indirect effects of agricultural land-use change are complex, may be synergistic with other threats, and it is often difficult to untangle their individual contributions to biodiversity loss. As a discipline, conservation physiology aims to unmask effects that are not otherwise apparent with traditional methods used in applied conservation biology. For addressing questions of how species respond to anthropogenic land-use change, measures of individual body condition and behavior may be more sensitive for assessing habitat quality than are broad metrics of population size or species’ presence.

In this dissertation, I test the impacts of neonicotinoid pesticides and available foraging habitat, by combining movement behavior, individual health measures, and pesticide exposure, in the Tricolored Blackbird (Agelaius tricolor). Chapter 1 establishes pesticide exposure in Tricolored Blackbirds as directly quantified from salvaged carcasses. Chapter 2 investigates how habitat characteristics influence Tricolored Blackbird health and body condition. Chapter 3 evaluates how Tricolored Blackbird foraging behavior was related to suitable foraging habitat availability. Historically, Tricolored Blackbirds were associated with wetland and grassland habitats throughout their range in California and adjacent states. In recent years, Tricolored Blackbirds have become increasingly associated with agricultural habitats for both foraging and nesting and form breeding colonies within a diverse range of landscape matrices. For this reason, Tricolored Blackbirds are an excellent study system for exploring questions about how species respond to anthropogenic habitat changes. This species is known to forage extensively in some crops such as rice and alfalfa, while other crops such as walnuts and almonds do not provide suitable foraging habitat for breeding birds. Previous research and anecdotal observations indicate the Tricolored Blackbird reproductive success is closely tied to the abundance of suitable insect prey in habitats surrounding breeding colonies. While adult Tricolored Blackbirds are granivorous to some extent, females need to consume insect prey during the egg-laying stage of reproduction and nestlings are obligately insectivorous.

To assess pesticide exposure levels in Tricolored Blackbirds in Chapter 1, carcasses were opportunistically salvaged from breeding colony locations during banding and other monitoring efforts throughout the species range. A liquid chromatography-mass spectrometry (LC-HRMS) assay was used to detect neonicotinoid insecticides and other compounds in adult liver tissue and whole-carcass homogenates of nestlings. Contrary to expectations, the results show that Tricolored Blackbirds showed little pesticide residue as directly measured from salvaged carcasses of both adults and nestlings. Only two out of the 85 samples showed detectable levels of any target compound. Specifically, one adult male and one nestling showed exposure to clothianidin, and both were salvaged from breeding colonies near or in dairies in Kern County. Birds may be coming into contact with our target compounds at a frequency that was not captured by our salvage sampling method. Environmental exposure may be higher at other times of the year outside the Tricolored Blackbird breeding season. This study only targeted neonicotinoid insecticides (and sulfoxaflor, a sulfoximine systemic insecticide), so further evaluation of exposure to other classes of pesticides is also necessary. Additional research is needed to understand if and how insecticide use on the landscape affects the insect prey base of Tricolored Blackbirds, and to better understand the observed neonicotinoid exposure in dairy-associated breeding colonies.

In Chapter 2, I tested how the amount of natural and agricultural foraging habitats surrounding Tricolored Blackbird breeding colonies affected bird health and condition. Assessments of habitat quality have frequently been done via simple abundance or occupancy measures, however, it is useful to establish a mechanistic relationship with habitat quality. Physiological indicators may show signs of poor or decreasing habitat quality before changes in population size are detected at a larger scale, which can provide key insights for how individuals respond to habitat availability in agricultural landscapes. Specifically, I quantified body mass, composite fat score, average hematocrit, the ratio of heterophils to lymphocytes (H-L ratio), estimated total white blood cells (WBC), and severity of Knemidokoptes spp. scaly-leg mite infestations that are frequently observed in Tricolored Blackbirds. Day of year, colony stage, and nest substrate explained much of the variation in individual bird health and condition metrics analyzed, with significant differences between males and females. Foraging habitat characteristics did not have significant overall effects on the health and condition measures used here. I found that birds nesting in freshwater emergent vegetation showed lower H-L ratios than did birds nesting in upland/terrestrial vegetation. Because higher H-L ratios are broadly correlated with higher glucocorticoid levels and can be used as a proxy measure of stress in wild animals, the results suggest that birds nesting in upland/terrestrial vegetation are in a heightened state of physiological stress compared to birds nesting in freshwater emergent vegetation. Birds sampled from colony locations with a greater proportion of suitable foraging habitat had significantly lower severity of foot mite infestations. While it is not currently known where or how Tricolored Blackbirds contract and/or spread these mites, these results indicate that habitat may play a role in their epidemiology. These results highlight the importance of conservation physiology in showing how individuals and populations are impacted by landscape characteristics beyond what can be shown by studies using only information on presence/absence or abundance of birds. While population presence (such as Tricolored Blackbird colony settlement) is an important metric, it is also important to understand the relative value of different habitat characteristics for individual bird health and condition.

Chapter 3 added to the results presented in Chapter 2 by exploring how the availability of suitable foraging habitat influenced foraging behavior of breeding Tricolored Blackbirds. Habitat quality is a central concept in ecological theory and also plays a valuable role in applied conservation management of threatened species. Foraging behavior and foraging bout length have been shown to correlate with food abundance or availability, and provide proxies for assessing food availability on a broad spatial scale. Recent advancements in tracking technology have provided powerful tools for understanding species’ responses to environmental change and other stressors through detailed tracking of foraging behavior and other movement patterns. The mechanisms by which agricultural intensification have caused population declines are complex with habitat loss and degradation, pesticide exposure, direct mortality, and other disturbances often acting synergistically on both individuals and populations. Tricolored Blackbirds have become increasingly associated with agricultural habitats in recent decades, and this species is sensitive to reproductive failure if there is not sufficient insect prey available across the foraging landscape. I aimed to test the effects of the proportions of natural and agricultural foraging habitats surrounding Tricolored Blackbird breeding colonies on individual bird foraging behavior. Specifically, I used automated radio telemetry to passively monitor presence-absence of tagged birds at Tricolored Blackbird breeding colonies to infer foraging bout lengths. I found that birds nesting in colonies surrounded by a higher proportion of suitable foraging habitat took significantly shorter foraging bouts than birds nesting in colonies surrounded by a lower proportion of suitable foraging habitat. Similarly, birds nesting in freshwater emergent vegetation took significantly shorter foraging bouts than birds nesting in upland/terrestrial vegetation. These foraging bout lengths would have allowed approximately 13.8 foraging bouts per hour for females during the nestling stage with 94% habitat suitable within 5 km of the colony (the highest values observed in my study) compared to approximately 9.5 foraging bouts per hour when only 44% of habitat within 5 km was suitable. This shows that habitat characteristics within and adjacent to the colony have a large influence on bird foraging bout length and presumed adult energy expenditure during the reproductive cycle, which strengthens the case for conservation actions that seek to enhance the habitats around Tricolored Blackbird breeding colonies.