Can Seeds Help to Expel Parasites? A Comment on the Garber-Kitron (1997) Hypothesis

Abstract

Like many other primates, moustached and saddle-back tamarins (Saguinus mystax and Saguinus nigrifrons; previously Saguinus fuscicollis nigrifrons: Matauschek et al. 2011) are seed dispersers for a large number plant species whose fruits they exploit for food (Culot 2009; Garber 1986; Knogge and Heymann 2003). Tamarins consistently swallow seeds (ca. 95 % of fecal samples contain seeds) that are often very large in relation to the tamarins’ body size (Garber and Kitron 1997; Knogge and Heymann 2003). Mean length and width of seeds (± SD) recovered from feces was 1.75 ± 0.59 cm (maximum: 2.35 cm) and 0.74 ± 0.32 cm (maximum: 1.31 cm) in Saguinus mystax, and 1.74 ± 0.56 cm (maximum: 2.33 cm) and 0.75 ± 0.31 cm (maximum: 1.35 cm) in S. nigrifrons (Knogge and Heymann 2003). Heymann (1992) speculated that large seeds may function physiologically as a kind of “roughage” and that the lack of continuous gut stimulation may be one cause of the high prevalence of gastrointestinal diseases in captive tamarins (Clapp et al. 1988; Gozalo and Montoya 1992), which contrasts to the low prevalence in wild tamarins (Wood et al. 1989). Seeds do not provide a nutritional benefit but rather are ballast that occupies much space in the gastrointestinal tract (Garber and Kitron 1997). Therefore, seeking an adaptive explanation of seed swallowing, Garber and Kitron (1997) proposed dislodging and expelling intestinal parasites, particularly the highly damaging acanthocephalan hookworm Prosthenorchis elegans, as the major function. Huffman (1997; see also Huffman and Caton 2001; Huffman et al. 1996) and Wrangham (1995) had provided evidence for the mechanical expulsion of parasites through swallowing of entire leaves in chimpanzees (Pan troglodytes). Garber and Kitron (1997) based their argument on the high prevalence (and lethality; Cosgrove et al. 1968) of Prosthenorchis elegans infections in captive tamarins and low prevalence in the wild. Under the Garber–Kitron hypothesis, the following predictions can be made: At the group level, the prevalence of infections with Prosthenorchis elegans should correlate negatively with the proportion of fecal samples per group that contain seeds. At the individual level, individuals infected with Prosthenorchis elegans should swallow seeds more often than noninfected individuals. Because rates of seed swallowing itself are difficult to determine, I use the number of fecal samples per individual containing seeds as a surrogate variable. I used data from field studies of a population of Saguinus mystax and S. nigrifrons at the Estacion Biologica Quebrada Blanco (EBQB), in northeastern Peruvian Amazonia since 1994 to test these predictions.