• Schoenle, Laura A.
  • Kernbach, Meredith
  • Haussmann, Mark F.
  • Bonier, Frances
  • Moore, Ignacio T.


  1. Chronic, low‐intensity parasite infections can reduce host fitness through negative impacts on reproduction and survival, even if they produce few overt symptoms. As a result, these parasites can influence the evolution of host morphology, behaviour and physiology. The physiological consequences of chronic infection can provide insight into the processes underlying parasite‐driven natural selection.
  2. Here, we evaluate the physiological consequences of natural, low‐intensity infection in an avian host–parasite system: adult male red‐winged blackbirds (Agelaius phoeniceus ) infected with haemosporidian parasites. Chronic haemosporidian infection has previously been shown to reduce both reproductive success and survival in several avian species.
  3. We used antimalarial medications to experimentally reduce haemosporidian parasitaemia (the proportion of blood cells infected with haemosporidian parasites) and measured the effect of treatment on body condition, haematology, immune function, physiological stress and oxidative state.
  4. Treatment with an antimalarial medication reduced parasitaemia for the most prevalent haemosporidian parasites from the genus Plasmodium . Treatment also increased haemoglobin and haematocrit, and decreased red blood cell production rates. We detected no effect of treatment on body condition, immune metrics, plasma corticosterone concentrations, total antioxidant capacity or reactive oxygen metabolites.
  5. Our results suggest that the damage and replacement of red blood cells during infection could be important costs of chronic haemosporidian infection. Strong links between parasitaemia and the physiological consequences of infection indicate that even for relatively low‐intensity infections, measuring parasitaemia rather than only presence/absence could be important when evaluating the role of infection in influencing hosts’ behaviour, physiology or fitness.


Study population, field methods and housing

We captured 29 adult male red‐winged blackbirds in April–May 2015 using mist nets with a conspecific playback and decoy or a seed‐baited Troyer V‐top trap at the Queen's University Biological Station (44°34′02.3″ N, 76°19′28.4″ W) and on nearby private property in Elgin, Ontario (44°36′28.8″ N, 76°13′38.3″ W). This population has been known to have high prevalence of haemosporidian infection since the late 1980s (Weatherhead, 1990; Weatherhead & Bennett, 1991; Weatherhead, Metz, Bennett, & Irwin, 1993) and from 2013 to 2015, prevalence was over 90% (Schoenle, Schoepf, Weinstein, Moore, & Bonier, 2017). We housed birds at the Queen's University Biological Station in semi‐natural conditions using an outdoor aviary consisting of 30 large flight aviaries (6 × 2.5 × 2.5 m) with walls that were permeable to insects, including potential vectors of Haemosporida. We fed the birds a diverse diet ad libitum, including poultry starter, seed mix, mealworms, dragonflies, hard‐boiled egg and fruit (in addition to insects that entered the aviaries). Prior to the start of this study, the birds were included as the control group for a hormone‐manipulation study (see Appendix S1 for details).

Experimental design

To ensure that parasitaemia was similarly distributed in the control and antiparasitic medication groups, we collected a blood sample and assessed the birds’ total haemosporidian parasitaemia 2 weeks before the start of the experiment. We ranked the birds by parasitaemia, and starting with the two highest ranked birds, randomly assigned one bird to the medication group and the other to the control group. We repeated this for the two birds with the next highest rankings and continued until all birds were assigned to a treatment group. Then, one bird from the control group (N  = 14) and the antiparasitic medication group (N  = 15) was assigned to each aviary. Because we had an odd number of birds, one bird in the medication group was housed with a bird from a previous study. The birds acclimated in their new aviary for 1 week prior to the start of the experiment.

On the first day of the study, we collected a blood sample (details below), weighed each bird, and assessed furcular fat by assigning a score on a 0–5 scale (birds in this study ranged from 0 to 3) (Wingfield & Farner, 1978). We then orally administered 200 μl of either the control or medication treatment once per day for 3 days. We blood sampled and weighed each bird again 7 and 14 days later. Our protocol was modelled on treatments used in the veterinary, parasitology and ecology literature (Cranfield et al., 1994; Karell et al., 2011; Remple, 2004). On each of the 3 treatment days, we gave the control group 10% sugar water. On the first treatment day, we gave the medication group 0.68 mg Primaquine (Sigma‐Aldrich 160393) and 1.7 mg Chloroquine (Sigma‐Aldrich C6628) (doses estimated as 10 mg/kg Primaquine and 25 mg/kg Chloroquine, calculated for a 68 g bird) dissolved in 200 μl of 10% sugar water. On the second and third treatment days, we administered 0.68 mg Primaquine and 1.02 mg Chloroquine (10 mg/kg Primaquine and 15 mg/kg Chloroquine, calculated for a 68 g bird) dissolved in 200 μl of 10% sugar water. Primaquine targets parasites in the blood and other tissues, and, while intended for treatment of Plasmodium (World Health Organization, 1995), has been found to be effective against avian Plasmodium , Haemoproteus and Leucocytozoon (Graczyk, Shaw, Cranfield, & Beall, 1994; Marzal et al., 2005; Merino et al., 2000). Chloroquine targets blood‐borne Plasmodium parasites, but has been used effectively to treat all avian haemosporidian genera (Graczyk et al., 1994; Karell et al., 2011; Remple, 2004). Both Primaquine and Chloroquine have been used to treat birds for haemosporidian infections in ecological field studies and under veterinary supervision with no reported side‐effects (e.g. Graczyk et al., 1994; Karell et al., 2011; Redig, Talbot, & Guarnera, 1993; Remple, 2004). However, in mammals both medications can cause intestinal upset and in some humans, Primaquine can cause haemolytic anaemia (Baird, 2005; Baird & Hoffman, 2004).