The relationship of fleas and gerbils is paradoxical. Fleas should have adverse effects on gerbils due to the energetic costs of replacing the blood that they remove, yet adult gerbils in the laboratory do not show any. And still, gerbils spend long hours grooming. We suggest that the cost of bearing ecoparasites is found elsewhere. Gerbils typically face conflicting demands of food and safety. In response, gerbils use time allocation and vigilance to manage risk. We suggest that ectoparasites reduce the effectiveness of vigilance directed against predators, thereby increasing the cost of predation and forcing gerbils to reduce vigilance levels and rely more on time allocation. We tested these predictions in a large outdoor vivarium. We manipulated whether gerbils were infested with fleas, and we exposed gerbils to a (muzzled) fox. To quantify foraging behavior, we measured giving-up densities (GUDs) of gerbils in artificial food patches (seed trays), sampling bush and open microhabitats. We equipped trays with PIT tag readers that logged the duration of each forager’s visit to those resource patches. These data also allowed us to reconstruct harvest rate curves and partition GUDs into time allocation and vigilance.
Results/Conclusions

Gerbils experience higher GUDs in the presence of foxes, in the open microhabitat, and when they carried fleas. Furthermore, gerbils with fleas responded to foxes with especially high GUDs. Similarly, gerbils spent less time in resource patches when foxes were present, in the open microhabitat, and when they carried fleas. Again, the response to foxes was especially strong for gerbils with fleas. Finally, quitting harvest rates of gerbils increased when foxes were present, in the open microhabitat, and when they carried fleas, with responses to foxes being especially strong again for gerbils with fleas. The results demonstrate that the gerbils treat the burden of fleas as a substantial foraging cost, exceeding even the cost generated by foxes, because of the exaggerated response of flea-infested gerbils to predators. That is, gerbils with fleas are more scared. The harvest rate curves suggest that fleas drive gerbils to distraction and interfere with harvesting. Fleas likely interfere with the effectiveness of vigilance, as well, as evidenced by flea-infested gerbils managing risk from foxes solely by time allocation. Ectoparasites exact a large cost on gerbils by hindering their foraging aptitudes in the face of predators. Earlier studies often showed that the direct cost of ectoparasitism is slight; we demonstrate here that the indirect cost is substantial.