American Society of Naturalists

A membership society whose goal is to advance and to diffuse knowledge of organic evolution and other broad biological principles so as to enhance the conceptual unification of the biological sciences.

“The enemy within: how does a bacterium inhibit the foraging aptitude and risk management behavior of Allenby’s gerbils?”

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Douglas F. Makin, Burt P. Kotler, Joel S. Brown, Mario Garrido, and Jorge F. S. Menezes (Dec 2020)

The behaviorally mediated indirect effects that endoparasites have on their host may be as large as the direct effects

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Allenby’s gerbil (<i>Gerbillus andersoni allenbyi</i>). <br />(Credit: Douglas F. Makin)
Allenby’s gerbil (Gerbillus andersoni allenbyi).
(Credit: Douglas F. Makin)

Allenby’s gerbils are commonly infected with the Mycoplasma haemomuris-like bacteria which has been demonstrated empirically to carry relatively low direct physiological costs (i.e. mild nutrient deficiencies). However, are there indirect ecological consequences of infection that affect the ability of gerbils to forage optimally and manage predation risk within their environment? We tested two alternatives: 1) does a nutrient deficiency lead to infected gerbils increasing their foraging effort and taking more risks while foraging to make up for any energetic shortfalls? 2) Alternatively, does infection lead to lethargy, whereby sick gerbils are compromised in their ability to harvest food efficiently and avoid predators? To address these questions, we compared the risk management strategies and foraging behavior of infected and non-infected gerbils. Infected gerbils were compared at two levels, those acutely infected (i.e. peak infection loads) and those with chronic infections (i.e. low infection loads). Our findings indicated that infected gerbils incurred dramatically higher foraging costs, including less efficient foraging, diminished effectiveness of vigilance and increased predation rates. Surprisingly, chronically infected gerbils experienced higher ecological costs than acutely infected gerbils. This suggests that the debilitating effects of infection occur gradually, with a progressive decline in the quality of time allocated to activities. Overall, our findings highlight how small direct physiological costs can give rise to large indirect ecological costs. Moreover, similar to predators which have both direct lethal effects and indirect effects on prey (i.e. perceived predation risk), endoparasites affect hosts not only by killing them (direct costs), but also through altering their interactions with predators, resources and landscape features (i.e. indirect costs).


Barn owl (<i>Tyto alba</i>).<br />(Credit: Douglas F. Makin)
Barn owl (Tyto alba).
(Credit: Douglas F. Makin)

Abstract

Microbes inhabiting multi-cellular organisms have complex, often subtle effects on their hosts. Gerbillus andersoni allenbyi are commonly infected with the Mycoplasma haemomuris-like bacteria, which may cause mild nutrient (choline, arginine) deficiencies. However, are there more serious ecological consequences of infection such as effects on foraging aptitudes and risk management? We tested alternatives: 1) nutrient compensation hypothesis, does nutrient deficiency induce infected gerbils to make up for the shortfall by foraging more and taking greater risks? or 2) lethargy hypothesis, do sick gerbils forage less, and are they compromised in their ability to detect predators or risky microhabitats? We compared the foraging and risk management behavior of infected and non-infected gerbils. We experimentally infected gerbils with the bacteria, which allowed us to compare between non-infected, acutely infected (peak infection loads), and chronically infected (low infection loads) individuals. Our findings supported the lethargy hypothesis over the nutrient compensation hypothesis. Infected individuals incurred dramatically elevated foraging costs, including less efficient foraging, diminished “quality” of time spent vigilant, and increased owl predation. Interestingly, gerbils that were chronically infected (lower bacteria load) experienced larger ecological costs than acutely infected individuals (i.e. peak infection loads). This suggests that the debilitating effects of infection occur gradually, with a progressive decline in the quality of time gerbils allocated to foraging and managing risk. These increased long-term costs of infection demonstrate how small direct physiological costs of infection can lead to large indirect ecological costs. The indirect ecological costs of this parasite appear much greater than the direct physiological costs.