Direct and indirect costs of co-infection in the wild: Linking gastrointestinal parasite communities, host hematology, and immune function

Abstract

Most animals are concurrently infected with multiple parasites, and interactions among these parasites may influence both disease dynamics and host fitness. However, the sublethal costs of parasite infections are difficult to measure and the effects of concomitant infections with multiple parasite species on individual physiology and fitness are poorly described for wild hosts. To understand the direct and indirect physiological costs of co-infection, we investigated the relationships among gastrointestinal parasite richness, species identity, and abundance and host hematological parameters, body condition, and investment in lymphocyte defenses. Using aggregate-scale parasite data from African buffalo (Syncerus caffer), we found few direct or indirect associations between infection and hematology in male hosts, and no significant associations were observed in female hosts or with respect to body condition in either sex. These results suggest that only strong physiological effects are detectable with aggregate-scale parasite data, and that hematological variables may be more sensitive to changes in condition than standard body fat condition indices. Analyses accounting for parasite species identity in female buffalo revealed that different parasites show distinct relationships with host hematology, body condition, and immune investment. However, four of six species-specific associations were obscured when parasites were considered in combination. Overall, fitness-related physiological mediators such as hematological indices may provide assessments of direct and indirect effects of parasite infection, particularly when parasite species identity and community composition are considered.

Keywords: African buffalo; Condition; Helminth; Parasite species richness.

Graphical abstract

Figure 1

The proportion of male (n = 203) and female (n = 278) African buffalo infected with GI parasite communities of varying species richness.

Figure 2

The relationship between gastrointestinal parasite richness and MCV for male buffalo. Least squares means ± 1 standard error are shown. Letters designate significant differences among levels of GI parasite richness.

Figure 3

Body condition was lower in Cooperia-Haemonchus co-infected buffalo compared to uninfected and Cooperia-only singly-infected buffalo. Means ± 1 standard error are shown. Letters denote significant differences among groups.

Figure 4

The relationship between total and species-specific strongyle egg abundance and four hematological parameters: RBC (cells/uL × 10⁶), HG (g/dL), HCT (%), MCV(10⁻¹⁵L), and body condition for 23 female African buffalo. If total strongyle egg abundance was considered (left column), a significant correlation was detected between egg abundance and HCT. HCT, MCV, and body condition index were significantly correlated with Cooperia egg abundance (center column). HG, RBC, and body condition index were significantly correlated with Haemonchus egg abundance (right column). Significance is denoted by a large asterisk, and correlation coefficients (r) are displayed with significance level (^•<0.05, ^**<0.01).

Figure 5

Indirect costs of infection demonstrated by the relationships between total and species-specific strongyle egg abundance and lymphocyte investment for 23 female African buffalo (A). After accounting for total strongyle intensity, lymphocyte investment was significantly and negatively correlated with MCV, and positively correlated with body condition (B). Significance is denoted by a large asterisk. The correlation coefficient (r) is noted with significance level (^•<0.05, ^**<0.01).