Investigating the effects of polycyclic aromatic hydrocarbon exposure on avian pre-migratory fuelling and migration
Long-distance avian migrants travel vast distances between their breeding and wintering grounds. Often this involves non-stop flights of thousands of kilometers without access to supplementary food or water. During these periods, birds rely almost exclusively on endogenously stored fuel to sustain several hours to days of migration flight. Accomplishing these extreme feats of endurance requires that birds rapidly accumulate fat stores prior to migration and at discrete sites (i.e., staging sites) along the migration route. Rapidly storing enough fat is crucial for long-distance migrants. Adequate fuel accumulation increases the probability of surviving migration. As well, fat deposition rates and departure fuel loads affect migration pace, and earlier arrival on the breeding grounds in the spring increases reproductive performance. As a result, impaired pre-migratory fuelling has been identified as an important factor in the ongoing declines of long-distance migratory bird populations. There is evidence to suggest that polycyclic aromatic hydrocarbons (PAHs), the toxic constituents of oil pollution, can impair refuelling physiology and limit pre-migratory fat accumulation. Despite this evidence, however, a link between PAH exposure and impaired pre-migratory fuelling had yet to be established. Therefore, the objectives of this research were (1) to directly assess whether PAH ingestion impairs pre-migratory fuelling, (2) to investigate the physiological mechanisms of PAH-induced pre-migratory fuelling impairment, and (3) to characterize the impacts of impaired fuelling on avian migration timing. My first objective was addressed using a captive dosing experiment. Sanderling (Calidris alba), a long-distance migratory shorebird, were orally dosed with environmentally-relevant PAH concentrations and mixtures. I found that oral exposure to PAHs during staging lowered Sanderling pre-migratory body mass gains, with individuals in the high dose group (dosed with 1260 µg PAH/kg-bw/day) gaining 4.4 ± 3.7 g less than controls. More specific investigations into the mechanisms underlying this result showed that serum bile acid concentrations and the hepatic mRNA expression of liver basic fatty acid binding protein 1 (Lbfabp) and hepatic lipase (Lipc) were reduced by PAH exposure. This suggested that sublethal PAH ingestion impaired fuelling by disrupting cholesterol and lipid homeostasis. These results confirmed that PAH exposure can limit deposition of the fuel loads that influence staging durations, departure decisions, and migratory speed. Therefore, further research was warranted to characterize the effects of PAH exposure and fuelling impairment on avian migration timing. For this work, I first examined the relationship between PAH contamination and staging site quality for fuelling shorebirds. I trapped Sanderling and Red knots (C. canutus) from six staging sites along the Texas and Louisiana Gulf Coast, which were variably affected by the Deepwater Horizon oil spill and which are susceptible to frequent and repeated oil pollution. Upon capture, I collected blood samples to measure Sanderling and Red knot plasma metabolite levels. I estimated PAH ingestion from foraging by measuring sediment total PAH concentrations at each site. Staging sites in Louisiana had the highest total sediment PAH concentrations (3.41 – 640 ng/g sediment). Metabolite data suggested that Sanderling in Louisiana exhibited the lowest refuelling rates, and both Sanderling and Red knots departed later than average from Louisiana. Next, I investigated the relationship between fuelling and migration timing in northward-migrating Sanderling using radio-telemetry techniques. I attached coded nanotags to Sanderling at the six Gulf of Mexico staging sites and at Chaplin Lake, Saskatchewan, a more northern staging site along Sanderlings’ migration route. Fuel loads were negatively correlated with stopover durations and departure dates at both sites. I also found that individuals that departed later from the Gulf of Mexico also arrived later and subsequently departed later from Saskatchewan. Model estimates suggested that a bird that was 5 g lighter at capture departed 2 days later from the Gulf of Mexico, arrived 1.5 days later in Saskatchewan, and then departed 16 hours later for its breeding grounds. There is thus evidence that fuel loads affect Sanderling migration timing and that slower birds do not catch up with earlier individuals. Fully understanding how PAHs affect pre-migratory fuelling, and ultimately avian populations, requires a mechanistic approach that links molecular-level events to adverse outcomes at the population-level. Therefore, the fourth objective of this research was to synthesize multiple datasets on how PAHs can affect avian pre-migratory fuelling into a biologically plausible mode of action that is useful to avian ecotoxicological risk assessment. This was accomplished by organizing the data of this thesis and existing knowledge into a putative adverse outcome pathway linking the molecular mechanisms underlying pre-migratory fuelling impairment to the effects of impaired fuelling on migratory bird populations. Organizing data into a progression of toxicity events increases our understanding of how PAHs and compounds with similar mechanisms of action can affect avian populations. Therefore, this thesis provides new information to guide avian ecotoxicological risk assessments and to increase our understanding of the toxicological threats to long-distance migratory bird populations.
polycyclic aromatic hydrocarbon, shorebird, migration, pre-migratory fuelling, staging
Doctor of Philosophy (Ph.D.)