Offspring dependence on parental care and the role of parental transfer of oral fluids in burying beetles

Abstract

BackgroundImmature stages of many animals can forage and feed on their own, whereas others depend on their parents’ assistance to obtain or process food. But how does such dependency evolve, and which offspring and parental traits are involved? Burying beetles (Nicrophorus) provide extensive biparental care, including food provisioning to their offspring. Interestingly, there is substantial variation in the reliance of offspring on post-hatching care among species. Here, we examine the proximate mechanisms underlying offspring dependence, focusing on the larvae of N. orbicollis, which are not able to survive in the absence of parents. We specifically asked whether the high offspring dependence is caused by (1) a low starvation tolerance, (2) a low ability to self-feed or (3) the need to obtain parental oral fluids. Finally, we determined how much care (i.e. duration of care) they require to be able to survive.ResultsWe demonstrate that N. orbicollis larvae are not characterized by a lower starvation tolerance than larvae of the more independent species. Hatchlings of N. orbicollis are generally able to self-feed, but the efficiency depends on the kind of food presented and differs from the more independent species. Further, we show that even when providing highly dependent N. orbicollis larvae with easy ingestible liquefied mice carrion, only few of them survived to pupation. However, adding parental oral fluids significantly increased their survival rate. Finally, we demonstrate that survival and growth of dependent N. orbicollis larvae is increased greatly by only a few hours of parental care.ConclusionsConsidering the fact that larvae of other burying beetle species are able to survive in the absence of care, the high dependence of N. orbicollis larvae is puzzling. Even though they have not lost the ability to self-feed, an easily digestible, liquefied carrion meal is not sufficient to ensure their survival. However, our results indicate that the transfer of parental oral fluids is an essential component of care. In the majority of mammals, offspring rely on the exchange of fluids (i.e. milk) to survive, and our findings suggest that even in subsocial insects, such as burying beetles, parental fluids can significantly affect offspring survival.

Variation in mandible development and its relationship to dependence on parents across burying beetles

“…This finding rules out the possibility that serrations alone are responsible for the ability to self‐feed, and instead that they are necessary but not sufficient for survival without parents. Supporting this is recent data from Capodeanu‐Nägler, Prang, et al (), who present two relevant results on N. orbicollis . First, they show that N. orbicollis first instar larvae do attempt to self‐feed but do so very inefficiently and thus cannot survive to the second instar on their own.…”

“…However, although well developed, parenting is not necessarily obligatory and the extent that offspring depend on parental care varies (Smiseth, Darwell, & Moore, ; Trumbo, ). As well as variation in larval begging behavior (Smiseth et al, ), some larvae can survive from hatching without parents, while others will not survive past the first instar if parents are not present to feed (Capodeanu‐Nägler et al, ; Capodeanu‐Nägler, de la Torre, et al, ; Capodeanu‐Nägler, Eggert, Vogel, Sakaluk, & Steiger, ; Capodeanu‐Nägler, Prang, et al, ; Jarrett, Schrader, Rebar, Houslay, & Kilner, ). There are no major differences in feeding ecology between obligate and facultative care species (Capodeanu‐Nägler et al, ; Scott, ), making this an ideal system for comparative studies.…”

“…The phylogeny of Nicrophorus and its closest relatives suggests that several independent transitions between obligate and facultative care have occurred, although the exact patterns of these transitions remain unclear (Jarrett et al, ; Sikes & Venables, ; Trumbo, Kon, & Sikes, ). Recently, Capodeanu‐Nägler, Prang, et al () present evidence that first instars of the obligate care species N. orbicollis can survive without parents if provided with oral secretions from parents and are able to consume flesh directly from a carcass. Thus, the primary mechanism for dependence on parents is not actually a lack of ability to self‐feed, but the physiology of the offspring and the requirement for nutrients provided in parental regurgitations.…”

Constrained flexibility of parental cooperation limits adaptive responses to harsh conditions

“… 2018 ), N. orbicollis show obligate parental care, meaning that larvae depend on direct provisioning for survival (Trumbo 1992 ; Capodeanu‐Nägler et al. 2016 , 2018 ). Parental care is described as predominantly biparental on the basis that males and females typically overlap with each other in the posthatching stage (in 66% of cases; Benowitz and Moore 2016 ), and both sexes perform the full repertoire of parenting behaviors (Scott and Traniello 1990 ; Trumbo 1991 ; Scott 1998a ).…”

Survey of neurotransmitter receptor gene expression into and out of parental care in the burying beetle Nicrophorus vespilloides

“…Parents also perform direct parental care by feeding dependent, begging offspring predigested carrion. Further direct care for the offspring occurs by excreting enzymes into the larval cavity to preprocess food to make it easily digestible for offspring (Capodeanu‐Nägler et al., 2018 ). Parental care lasts for 3–4 days, and then, the parent(s) may disperse and the larvae continue to consume the carcass for another few days.…”