How Important Are Hemoparasites to Migratory Songbirds? Evaluating Physiological Measures and Infection Status in Three Neotropical Migrants during Stopover

Abstract

Long-distance migrations are energetically expensive for many animals, including migratory songbirds. During these demanding journeys, birds likely face limitations in allocating resources to different physiological functions, including lipid reserves needed to fuel the migration and costly immune defense against pathogens. We sampled three species of long-distance migratory songbirds during their fall migration through coastal Georgia and quantified their body condition, subcutaneous fat reserves, and infection status with blood parasites (Hemoproteus and Plasmodium). We also quantified cellular immunity, on the basis of total and differential white blood cell counts, and estimated individual stress levels, using the heterophil∶lymphocyte (H∶L) ratio. We tested whether birds infected with blood parasites had decreased fat measures, poorer body condition, or increased stress levels (as reflected by H∶L ratios). We also examined relationships between immune cell profiles and the following variables: body condition, subcutaneous fat, infection status, age, and species. Infected birds did not show greater H∶L ratios, poorer body condition, or lower fat measures, but in one species infected individuals showed significantly elevated leukocyte counts. Although we found little evidence for negative relationships between immune cell counts and body condition or fat measures, as might reflect underlying trade-offs in resource allocation, our results concerning hemoparasites are consistent with past work and suggest that chronic hemoparasite infections might have minimal effects on the outcome of long-distance migratory flight.

The use of glucocorticoid hormones or leucocyte profiles to measure stress in vertebrates: What’s the difference?

“…Interestingly, these results have varied. Some researchers have reported that parasites elevate H/L or N/L ratios (Fokidis, Greiner, & Deviche, ; Shutler & Marcogliese, ; Wojczulanis‐Jakubas et al., ), whereas others found no evidence of such (Cornelius et al., ; Granthon & Williams, ; Krams et al., ; Shutler, Lowe, & Robinson, ; Sperry et al., ). We note, however, that the interpretation of leucocyte profiles in the context of parasites can be subject to the same difficulties outlined above for coloration (see also Blaustein et al., ); in other words, high H/L ratios have been interpreted by some researchers as heightened ability to control and clear parasite infections, and by others as evidence of active infection.…”

“…The hypothesis typically tested is that higher parasite loads are associated with higher H/L or N/L ratios (e.g. Cornelius, Davis, & Altizer, 2014;Wojczulanis-Jakubas, Jakubas, Czujkowska, Kulaszewicz, & Kruszewicz, 2012); some studies have incorporated additional variables such as moult (Pap et al, 2011), predation (Raffel, Hoverman, Halstead, Michel, & Rohr, 2010) or sex (Waterman, Macklin, & Enright, 2014) to investigate more complex relationships. Interestingly, these results have varied.…”

Links between blood parasites, blood chemistry, and the survival of nestling American crows

“…Results from other studies seeking links between these parameters and hemosporidian infections have also yielded inconsistent results. Some have documented positive correlations (e.g., in total WBC counts; Ots & Horak, 1998, lymphocytes;Ellis et al, 2014;Krams et al, 2013;Ots & Horak, 1998, and heterophils;Ellis et al, 2014;Krams et al, 2013), whereas others documented either no effect or a correlation in the opposite direction (e.g., in total WBC counts; Cornelius et al, 2014;Schoenle et al, 2017;Biard, Monceau, Motreuil, & Moreau, 2015, lymphocytes;Cornelius et al, 2014, heterophils, and H:L ratio;Cornelius et al, 2014;. Considered in concert, these inconsistencies indicate that links between hemosporidian infections and total WBC cell count, heterophils, and lymphocytes are context dependent and not generalizable across host-parasite systems.…”

“…The host immune response is energetically costly, using resources that could have been allocated to other functions (Cornelius et al, 2014). An over-reactive immune response can itself damage the host (Sorci, 2013).…”

“…They can have devastating impacts in naïve populations (Atkinson & Samuel, 2010), and many studies have reported negative associations with infection in endemic areas, including reductions in condition (Marzal, Bensch, Reviriego, Balbontin, & de Lope, 2008;Merino, Moreno, Sanz, & Arriero, 2000), antipredator behavior (Garcia-Longoria, Moller, Balbontin, de Lope, & Marzal, 2015;Mukhin et al, 2016), mating display behavior (Bosholn, Fecchio, Silveira, Braga, & Anciaes, 2016), survival (Asghar et al, 2015;Krams et al, 2013;Sol, Jovani, & Torres, 2003), and reproductive output (Asghar, Hasselquist, & Bensch, 2011;Knowles, Palinauskas, & Sheldon, 2010;Marzal et al, 2013;Merino et al, 2000). Other studies, however, have reported no associations-or even positive associations-with infection (Cornelius, Davis, & Altizer, 2014;Fargallo & Merino, 2004;Piersma & van der Velde, 2012;Podmokla et al, 2014;Zylberberg et al, 2015), or have reported effects that vary among host species (Atkinson & Van Riper, 1991;Ellis, Kunkel, & Ricklefs, 2014;Sorci, 2013), host population (Piersma & van der Velde, 2012), parasite species (Asghar et al, 2011;Lachish, Knowles, Alves, Wood, & Sheldon, 2011;Marzal et al, 2008), and characteristics of individual hosts (Hammers et al, 2016). As such, the extent to which the hemosporidians broadly constitute a selective pressure across different systems and contexts is unclear.…”