Relationships between egg-recognition and egg-ejection in a grasp-ejector species

Abstract

Brood parasitism frequently leads to a total loss of host fitness, which selects for the evolution of defensive traits in host species. Experimental studies have demonstrated that recognition and rejection of the parasite egg is the most common and efficient defence used by host species. Egg-recognition experiments have advanced our knowledge of the evolutionary and coevolutionary implications of egg recognition and rejection. However, our understanding of the proximate mechanisms underlying both processes remains poor. Egg rejection is a complex behavioural process consisting of three stages: egg recognition, the decision whether or not to reject the putative parasitic egg and the act of ejection itself. We have used the blackbird (Turdus merula) as a model species to explore the relationship between egg recognition and the act of egg ejection. We have manipulated the two main characteristics of parasitic eggs affecting egg ejection in this grasp-ejector species: the degree of colour mimicry (mimetic and non-mimetic, which mainly affects the egg-recognition stage of the egg-rejection process) and egg size (small, medium and large, which affects the decision to eject), while maintaining a control group of non-parasitized nests. The behaviour of the female when confronted with an experimental egg was filmed using a video camera. Our results show that egg touching is an indication of egg recognition and demonstrate that blackbirds recognized (i.e., touched) non-mimetic experimental eggs significantly more than mimetic eggs. However, twenty per cent of the experimental eggs were touched but not subsequently ejected, which confirms that egg recognition does not necessarily mean egg ejection and that accepting parasitic eggs, at least sometimes, is the consequence of acceptance decisions. Regarding proximate mechanisms, our results show that the delay in egg ejection is not only due to recognition problems as usually suggested, given that experimental eggs are not touched significantly more often. Thus, the delay in egg ejection is mainly the consequence of a delay in the decision to eject, probably triggered by mechanical constraints imposed by eggs that are harder to eject (i.e. larger). Our results offer important information on the relationships between recognition and ejection and contribute to a better understanding of host defences against brood parasites.

Rejection of parasitic eggs: an updated terminology for a complex process

“…This use of these terms is sometimes imprecise and confusing, so they deserve to be clarify considering recent findings on egg rejection. Today we know that egg rejection is a complex and sequential process in which decision-making occupies a prominent place, and where several stages can be differentiated: recognition, decision and action itself (Stokke et al 2005, Antonov et al 2009, Soler et al 2012, 2017, Ruiz-Raya et al 2015. First, the host needs to realize that its nest has been parasitized, and identify which eggs are theirs and which is a foreign egg.…”

“…Finally, the specific response behaviour must be carried out. Although egg-recognition abilities of hosts have been frequently studied from egg-rejection rates (Davies and Brooke 1989a, Marchetti 2000, Soler et al 2000, Lahti and Lahti 2002, Avilés et al 2004, Spottiswoode and Stevens 2011, recent experimental evidence has confirmed that egg rejection does not necessarily follow egg recognition and that acceptance decisions occur (Soler et al 2012, 2017, Ruiz-Raya et al 2015. Therefore, recognition abilities should not be inferred from the final host response, but they need to be studied separately, which requires a delimitation of terms as accurate as possible.…”

“…On the other hand, the term recognition would imply the association of a previously processed stimulus with a foreign (or own) egg (Table 1), which will trigger the host response as it will be crucial for the decision stage. Interestingly, recent studies have used certain host behaviours such as the eggpecking behaviour or the occurrence of egg touches to infer egg recognition, independently of the final host response (Soler et al 2012, 2017, Ruiz-Raya et al 2015.…”

“…Therefore, terms like preference and choice (Table 1) deserve to be considered in the context of egg rejection and need to be incorporated to the scientific terminology in order to gain a better understanding of the specific host responses. The term motivation, the host's tendency to assume the potential costs of egg rejection under certain parasitism conditions (Table 1), has become a crucial concept in the psychology of decisionmaking, and recent studies suggest that host motivation (or rather, the lack of motivation) is, at least sometimes, behind egg acceptance shown by some host species (Soler et al 2012, 2017, Ruiz-Raya et al 2015. The inclusion of the concept of motivation in studies on egg rejection is a turning point in our understanding of the host's response to the parasitic egg.…”

“…Information on the parasitism conditions is updated throughout the complete process of egg rejection, and hosts can be able to assess certain characteristics of the parasite egg both during the judgment stage and even once the foreign egg has been recognized. This aspect has been included in recent works focusing on the role of behaviours such as egg-touching or egg-pecking (Soler et al 2012, 2017, Ruiz-Raya et al 2015, which could be used by hosts to gain information on some special characteristics of the parasitic egg. Therefore, terms related to these assessment mechanisms should undoubtedly be included in any attempt to establish an updated terminology on host response.…”