Multiple parasitism reduces egg rejection in the host (Acrocephalus arundinaceus) of a mimetic avian brood parasite (Cuculus canorus).

Abstract

A host that has been targeted by an avian brood parasite can recover most of its potential fitness loss by ejecting the foreign egg(s) from its nest. The propensity for some hosts to engage in egg rejection behavior has put selective pressure on their parasites to evolve mimetic eggshells resembling the host’s own shell colors and maculation. In turn, hosts have counterevolved increasingly more sophisticated detection methods such as narrowing visual egg acceptance thresholds or using social cues to recognize parasitism. However, multiple cognitive mechanisms acting simultaneously could theoretically interfere with one another and ultimately decrease egg rejection accuracy, especially if these heuristics yield differing targets for rejection. By painting hosts own eggs, we studied a host species of the common cuckoo Cuculus canorus, the great reed warbler Acrocephalus arundinaceus, and tested its responses to the presence of “foreign” eggs of varying quantity, colors, and uniformity. Using reflectance spectra of egg background coloration and avian perceptual modeling, we then estimated the sensory thresholds triggering egg rejection by this host for each treatment. As previously reported, rejection rates were positively related to the perceptual distance between own and foreign eggs in the nests in all treatments. However, rejection thresholds were more permissive (error prone) both with greater proportions of foreign eggs per clutch and/or when the suite of foreign eggs was perceptually more variable within the nest. These results suggest that parasites, through multiple parasitism, can partially overcome the evolution of hosts’ recognition of mimetic parasite eggs.

Proximate predictors of variation in egg rejection behavior by hosts of avian brood parasites.

“…The effect of clutch size (and, thus, the parasite-to-host egg ratio) on egg rejection appears to vary between studies and species. On the one hand, multiple parasitism (higher ratio) has been shown to reduce the rejection of parasitic eggs (Bán et al, 2013;Manna et al, 2019;Moskát et al, 2009;M. Stevens et al, 2013) supporting the hypothesis that the ability of hosts to reject eggs is compromised because multiple eggs can be perceived as the most different when using a discordancy-based egg rejection mechanism (but see Lang, Bollinger, & Peer, 2014).…”

“…For example, some hosts use the range and distribution of egg colors and patterns in the nest to make rejection decisions (Bán, Moskát, Barta, & Hauber, 2013;Moskát, Avilés, Bán, Hargitai, & Zölei, 2008). The variation of egg color in a clutch may be driven by the extent of the host's intraclutch variability (Moskát et al, 2008) or differences in the parasite-tohost egg ratio, due to single vs. multiple parasitism and/or variation in host clutch size (Manna et al, 2019;Moskát et al, 2009;Stevens, Troscianko, & Spottiswoode, 2013, but see Lang, Bollinger, & Peer, 2014). Hosts may respond differently to nests with varying parasite-to-host egg ratio not only because of the variation in color, but also because of the Weber's law, which posits that the ability of animals to discriminate between stimuli depends on the stimulus proportionality (Stevens, 1975).…”

“…Stevens, Troscianko, & Spottiswoode, 2013). The variation of egg color in a clutch may be driven by the extent of the host’s intraclutch variability (Manna et al, 2019; Moskát, Avilés, Bán, Hargitai, & Zölei, 2008) or differences in the parasite-to-host egg ratio, owing to single versus multiple parasitism and/or variation of host clutch size (Moskát et al, 2009; M. Stevens et al, 2013, but see Lang, Bollinger, & Peer, 2014).…”

“…Stevens, Troscianko, & Spottiswoode, 2013). The variation of egg color in a clutch may be driven by the extent of the host's intraclutch variability (Manna et al, 2019;Moskát, Avilés, Bán, Hargitai, & Zölei, 2008) or differences in the parasite-to-host egg ratio, owing to single versus multiple parasitism and/or variation of host clutch size (Moskát et al, 2009;, but see Lang, Bollinger, & Peer, 2014). Hosts may respond differently to nests with varying parasite-to-host egg ratio not only because of the variation of color but also because of Weber's law, which posits that the ability of animals to discriminate between stimuli depends on the stimulus proportionality (S. S. Stevens, 1975).…”

Quintuple parasitism of a great reed warbler nest by common cuckoos

“…Due to the longstanding high local parasitism rate, it would have been expected that, under strong selective pressure, great reed warblers would recognize multiple parasitic eggs and remove these eggs from their nests. However, previous studies conducted locally have shown that multiple parasitism, instead of functioning as a cue that the nest was parasitized, reduces egg rejection rates by the host (Manna et al, 2019;Moskát et al, 2009). These results show that great reed warblers reject foreign eggs based on their discordance to the rest of the eggs within the nest, rather than truly recognizing their own eggs, and multiple parasitism can even double the breeding success of common cuckoos per host nest by increasing the tolerance of the hosts toward dissimilar looking eggs (Moskát et al, 2009).…”