Immune response varies with rate of dispersal in invasive cane toads (Rhinella marina)

Abstract

What level of immunocompetence should an animal maintain while undertaking long-distance dispersal? Immune function (surveillance and response) might be down-regulated during prolonged physical exertion due to energy depletion, and/or to avoid autoimmune reactions arising from damaged tissue. On the other hand, heightened immune vigilance might be favored if the organism encounters novel pathogens as it enters novel environments. We assessed the links between immune defense and long-distance movement in a population of invasive cane toads (Rhinella marina) in Australia. Toads were radio-tracked for seven days to measure their activity levels and were then captured and subjected to a suite of immune assays. Toads that moved further showed decreased bacteria-killing ability in their plasma and decreased phagocytic activity in their whole blood, but a heightened skin-swelling response to phytohemagglutinin. Baseline and post-stress corticosterone levels were unrelated to distance moved. Thus, long-distance movement in cane toads is associated with a dampened response in some systems and enhanced response in another. This pattern suggests that sustained activity is accompanied by trade-offs among immune components rather than an overall down or up-regulation. The finding that high mobility is accompanied by modification of the immune system has important implications for animal invasions.

Figure 1. Toad in motion.

Female cane toad (Rhinella marina) bearing a 3g radio-transmitter on a bead chain belt.

Figure 2. Cane toad blood cells.

Giemsa-stained cane toad blood smear with representative selection of blood cell types. Letters to the upper left of cells denote: (B) basophil, (E) eosinophil, (L) lymphocyte, (N) neutrophil, (r) erythrocyte, and (t) thrombocyte. Scale bar in the lower right indicates 10 µm.

Figure 3. Bacteria-killing ability of toad plasma.

After 60E. coli (closed, solid) plasma from toads that had moved further during the previous week was less bactericidal, than was plasma from more sedentary toads. The ability of toad plasma to kill O. anthropi (open, dashed) was unaffected by the distance the toad had moved.

Figure 4. Phagocytic activity of toad whole blood.

Luminescence (RUL = relative luminescence units) profiles of blood from toads that moved greater than the mean distance (995 m) (dashed line) and less than the mean distance (solid line). Distance groupings are for graphical purposes only; in our statistical analyses, we treated distance moved as a continuous variable.

Figure 5. Skin swelling induced by phytohemagglutinin (PHA).

Comparison between toads that had moved greater than the mean distance (995 m) (dashed line) and less than the mean distance (solid line) over the previous week. “% swelling” indicates the relative difference in web thickness between a toe web injected with PHA and a control web injected with saline. Distance groupings are for graphical purposes only; in our statistical analyses, we treated distance moved as a continuous variable.

Figure 6. Relationship between a conglomerate immune measure and distance moved.

Immune PC1 values of individual cane toads regressed on the total distances moved by those animals during seven days of prior radio-tracking. Positive values of PC1 indicate toads with poor bacteria-killing and phagocytosis scores, low neutrophil levels, and a large skin-swelling response to phytohemagglutinin.