Large-bodied gastric spirurids (Nematoda, Spirurida) predict structure in the downstream gastrointestinal helminth community of wild spiny mice (Acomys dimidiatus)

Abstract

The dominant helminths infecting spiny mice (Acomys dimidiatus) in the montane wadis of the Sinai Peninsula of Egypt are spirurid nematodes, notably Protospirura muricola and Mastophorus muris. Both are relatively large robust stomach worms that accumulate in hosts resulting in high worm burdens. To ascertain whether the presence of spirurid worms or their burdens alters the host's likelihood of infection with other helminth species, we analysed a database containing quantitative data on helminth parasites of these mice (n = 431). This comprised of worm burdens recorded during 4 surveys, conducted at 4-year intervals, in 4 wadis, during late summer of each year. The presence of spirurid worms did not significantly alter species richness with other helminth species nor the likelihood of mice carrying other nematode species. However, there was a significant association, particularly of P. muricola, with the presence of intestinal stages of cestodes, and with the acanthocephalan Moniliformis acomysi. After controlling for intrinsic and extrinsic factors, mice harbouring spirurid worms had greater worm burdens of other helminths compared with mice without spirurids. Moreover, spirurid worm burdens showed a significant positive covariation with similarly adjusted species richness of other helminths, non-spirurid helminths, non-spirurid nematodes, oxyuroid nematodes and intestinal stage cestode worm burdens. We interpret these results as an indication that the key driver for co-occurrence of spirurids with other helminths is likely to be transmission via common arthropod hosts (for cestodes and acanthocephalans), but also that mice carrying the heavier spirurid worm burdens become more susceptible to directly transmitted nematodes such as the Oxyuroidea.

Keywords: Acanthocephala; Acomys dimidiatus; Cestoda; Nematoda; Oxyuroidea; Spirurida; arthropod-mediated transmission; associations and interactions between helminth species; spiny mice.

Graphical abstract

Figure 1.

Frequency distribution of Protospirura muricola and Mastophorus muris worm burdens (A) and their combined biomass (B), the correlation between combined worm burdens and biomass (C) and an adult eastern (Egyptian) spiny mouse (Acomys dimidiatus) with inset a spiny mouse stomach containing over 30, mostly mature, P. muricola (D). Note that in (B), the abscissa is discontinuous, showing intervals of 10 mg in the mass classes nearest to the ordinate, then intervals of 50 mg and 500 mg, and in (D), the mouse and stomach are approximately of the same scale, the diameter of the standard size Petri dish containing the worms is 9.0 cm. The average body length (nose to anus) of adult mice was 111.7 ± 0.40 mm (n = 273), tail length 109.5 ± 0.93 (n = 206) and weight 39.7 ± 0.42 g (n = 272).

Figure 2.

Covariance of the residuals of the MSMs for the combined spirurid worm burdens with NSpir helminth species richness (A and B), NSpir helminth worm burdens (C and D) and oxyuroid worm burdens (E and F). The panels on the left (A, C and E) illustrate the predictions of the relevant models in Table 7; those on the right (B, D and F) show regressions of MSMs of NSpir helminth species richness (B; R² = 0.0234), NSpir helminth (D; R² = 0.0178) and oxyuroid (F; R² = 0.0104) worm burdens on the MSM for the combined spirurid worm burdens. The shaded areas show the 95% confidence region. For additional details, see text and Tables 7 and S4.

Figure 3.

Covariance of the residuals of the MSMs for the combined oxyuroid worm burdens with spirurid biomass.