Does a niche construction strategy adaptation really exist in brown-headed cowbirds?

Abstract

The subject of brood parasitism has become the focus of widespread attention for the numerous finely tuned adaptations that have been discovered in coevolving specialist brood parasite–host systems (Davies, 2000; Krüger, 2007; Soler, 2017a). A recent study by Antonson et al. (2022) claims to have found one of these fascinating adaptations, posing the exciting conclusion that brown-headed cowbird (Molothrus ater) chicks use a niche construction strategy (alteration of its own environment for its own fitness benefit) in prothonotary warbler (Protonotaria citrea) host nests. In this experimental study, the authors have found that the selective brood reduction strategy driven by cowbird nestlings is reducing, but not eliminating host broods. According to their interpretation, this appears to represent an adaptive niche construction strategy given the brood reduction results and that survival of cowbird nestlings is higher in broods of two warbler nestlings than when alone or in broods of four warbler nestlings. This is an intriguing possibility but does a niche construction strategy allowing the survival of two nestmates really exist in brown-headed cowbirds?

Niche construction is a mechanism whereby individuals actively manipulate their environment to obtain more appropriate conditions in which their possibilities of survival and reproductive success increase (Aaby & Ramsey, 2022; Odling-Smee et al., 2013; Trappes et al., 2022). In birds, nest building is a clear example of niche construction (Trappes et al., 2022). The strategy of the common cuckoo (Cuculus canorus) nestling, which soon after hatching evicts all host nestmates from the nest, allowing it to monopolize the feeding effort of its foster parents, can be considered another clear case of niche construction. Other brood parasites (non-evictors) share the nest with host nestlings, but usually, the parasitic nestling(s) outcompetes host nestlings. This also implies an active manipulation of their environment (the nest), and therefore, this strategy could also be considered niche construction. However, Antonson et al. (2022) suggest that in the brown-headed cowbird—protonotary warbler system, the brood parasite selectively manipulates brood reduction favouring the presence of two warbler nestlings in the nest. This suggestion is based on comparisons of data on nestling warbler mortality in four experimental groups, with two parasitized and two unparasitized treatments. However, the crucial prediction of the niche construction hypothesis—that is, that the cowbird nestling causes selective host brood reduction, allowing the survival of just two host nestlings—was not demonstrated.

In addition, this study selectively cites publications and raises several other key questions. Antonson et al. (2022) base their study on the ‘begging assistance hypothesis’ (Kilner et al., 2004), which states that brown-headed cowbird nestlings sharing the nest with host nestlings grow faster than cowbird nestlings raised alone because parasitic nestlings take advantage of the begging calls produced by host nestlings to procure resources. That is, begging displays of host nestlings compel their parents to increase the rate of food delivery, and this extra food would be consumed by the cowbird nestling due to its higher competitive ability (Kilner et al., 2004). In support of the hypothesis that parasitic nestlings need the assistance of host nestlings to secure a sufficient quantity of food, the authors cite all publications that have provided any kind of support for it, both before (Lichtenstein & Sealy, 1998) and after the hypothesis was proposed (Gloag et al., 2012; Hoover & Reetz, 2006; Kilner et al., 2004; Li & Hauber, 2021). One of these publications, Li and Hauber (2021), clearly stated that this hypothesis works only with midsized host species. Further, Gloag et al. (2012) reported that the begging assistance hypothesis was only supported in a small host species, but not in a larger one. Unfortunately, Antonson et al. (2022) did not mention any of the experimental studies that did not support the predictions of the begging assistance hypothesis in an evictor brood parasite (Grim et al., 2009; Hauber & Moskát, 2008; Martín-Gálvez et al., 2005). Antonson et al. (2022) also did not seem to be aware of other studies (e.g. Bolopo et al., 2015; Rivers et al., 2010; Soler & de Neve, 2013) and a review (Soler, 2017b) concluding that in several nest-sharing brood parasite species larger nestlings successfully compete for extra food, regardless of whether they are hosts or parasites. In their paper, Antonson et al. (2022) did not discuss how this crucial factor (i.e. the size of the parasitic nestling relative to the size of its host nestmates) affects which nestling gets the extra food because of the intense begging emanating from nests shared by the brood parasite and host nestlings. On the contrary, in several places of the manuscript, the authors generalized the begging assistance hypothesis to all nest-sharing brood parasites. They even cited a study by Gloag et al. (2012) that tested this hypothesis in two species of different sizes that are used as hosts by the shiny cowbird (Molothrus bonariensis). In the small-sized host (the house wren, Troglodytes aedon), predictions of the begging assistance hypothesis were supported, whereas in the large-sized host (the chalk-browed mockingbird, Mimus saturninus) the parasite nestling registered higher food intake, mass growth and survival when reared alone than when sharing the nest with host nestlings, contradicting the begging assistance hypothesis. Antonson et al. (2022) did not mention these results with the large host, nor did they discuss the conclusion of Gloag et al. (2012) stating that cowbird nestlings are negatively affected by the presence of host nestlings in nests of mockingbirds. In short, this bias in citing studies weakens the conclusions that can be drawn from this study (Bouter et al., 2016; Gøtzsche, 2022).

In addition, Antonson et al.'s (2022) study raises several other major questions. First, the niche construction mechanism is presented by the authors as a finely timed and balanced adaptation. The vital question here is how such a complex and finely tuned adaptation could have evolved in the brown-headed cowbird, given that it is an extremely generalist brood parasite belonging to a recent clade (Sorenson & Payne, 2002). While interactions in other brood parasite–host systems are highly coevolved, with brood parasites having specific adaptations to brood parasitism, parasitic cowbirds lack most of those specialized adaptive features (Mermoz & Ornelas, 2004). In addition, finely tuned adaptations to brood parasitism are expected to evolve mainly in specialist brood parasite species in which selection pressures are stronger and adaptations and counteradaptations are more likely to evolve (Davies, 2000). This raises the question of how a finely tuned adaptation such as the suggested niche construction strategy in the cowbird—protonotary warbler system, which implies selective brood reduction favouring the presence in the nest of just two warbler nestlings, could have evolved in the brown-headed cowbird, a brood parasite that frequently parasitizes seven or more species at a single site with the same female usually parasitizing multiple host species (Krüger, 2007). This fundamental question is not discussed by the authors.

Second, how could cowbirds cause brood reduction that leads to an optimal niche? Antonson et al. (2022) address this question by speculation using only their own results. However, how can it be assumed that cowbird nestlings are able to force the starvation and/or survival of the appropriate number of host nestlings when several studies (e.g. Ryser et al., 2016; Smith et al., 2017) have highlighted that nestlings have little or no control over food allocation by parents, including in a brood parasite—host system (Soler et al., 2017)? Likely, the death of protonotary warbler nestlings is the consequence of starvation because they are outcompeted by the cowbird nestling, which is larger in size (adult cowbirds 35–45 g, adult warblers 14–16 g; Antonson et al., 2022), thereby providing it with a clear advantage, given that parents in most species selectively feed larger nestlings, even when smaller nestlings beg more intensively (Caro et al., 2016; Soler et al., 2022). To satisfactorily address this problem of the effect of difference in size between host and brood parasite nestlings, an additional experimental group would be needed, with five warbler nestlings in which one of the warblers is twice the size of its nest mates.

The selective host brood reduction of just two nestlings may be a consequence of the size of the prothonotary warbler, which is a mid-sized host species whose provisioning capacity could be just sufficient to raise one cowbird and two warbler nestlings.

Third, Antonson et al. (2022) report that the parasitism rate in their study area was 60%, but they do not discuss the rate of multiparasitism (two or more parasite eggs per nest). This information is indispensable to determine the strength of selection pressures favouring the evolution of an optimal niche strategy, given that brown-headed cowbirds are four times larger than protonotary warblers. According to Hoover (2003), who worked in the same prothonotary warbler population, more than half of the parasitized nests (51.1%; extracted from table 1 in Hoover [2003]) have two or more cowbird nestlings, signifying that the major competitors of a cowbird nestling are not small-sized host nestlings but other large-sized cowbird nestlings. According to this information, it is difficult to imagine the selection of an optimal niche strategy based on the existence of only host nestlings as nestmates of just one cowbird nestling. This relevant point was neither mentioned nor discussed by the authors.

In summary, before proposing the attractive possibility that a niche construction strategy could have evolved in brown-headed cowbird nestlings, the authors must firstly demonstrate that parasitic nestlings are responsible for selective host brood reduction to get the optimal brood size for the parasitic nestling of just two host nestlings in the nest. Second, citation bias should be avoided, reconciling or explaining the evidence of other studies that contradict the claim of niche selection; and thirdly, address the three important questions that have not been mentioned or discussed in their article. Until these problems are resolved, the reader can consider that the results reported by Antonson et al. (2022), which they claimed to support the niche construction hypothesis, only support the begging assistance hypothesis and may be merely a consequence of the provisioning capacity of the mid-sized protonotary warbler hosts, which could be sufficient to raise one cowbird and two warbler nestlings.

Manuel Soler: Conceptualization; writing – original draft; investigation; writing – review and editing; visualization; funding acquisition.

There is no conflict of interest to disclose.