Sex differences in the effects of captivity on hippocampus size in brown-headed cowbirds (Molothrus ater obscurus).

Abstract

In brood parasitic cowbirds, hippocampus (Hp) size is correlated with environmental spatial memory demands. Searching for host nests is the presumed causal factor influencing cowbird Hp size, because Hp volumes vary across species, sexes, and seasons according to nest-searching participation. Brownheaded cowbirds have female-only nest searching and, at least in the eastern subspecies, a larger Hp in females than in males, suggesting that nest searching influences cowbird Hp size. We predicted that female brown-headed cowbirds housed in aviaries lacking host nests would have a smaller Hp than wild-caught females whereas males would be unaffected. We found that the Hp was smaller in captive females, but not males, compared to their wild-caught counterparts. This did not appear to be due to general effects of an impoverished environment on all brain regions. Our results imply that interruption of nest searching in cowbirds prevents seasonal increase in Hp size in females. Future studies should isolate which behavioral differences between wild and captive birds contributed to captivity-induced changes in Hp volume in females while not affecting males. Keywordscowbird; hippocampus; sex differences; brain plasticity; brood parasitism Variation in environmental spatial demands is related to variation in hippocampus (Hp) size among closely related species, between sexes, and across seasons in mammalian, avian, and reptilian species. For example, food-storing behaviors in birds (Clayton, 1995a;Hampton, Sherry, Shettleworth, Kurgel, & Ivy, 1995;Hampton & Shettleworth, 1996;Healy & Krebs, 1992;Krebs, Sherry, Healy, Perry, & Vaccarion, 1989;Sherry, Vaccarino, Buckenham, & Herz, 1989;Volman, Grubb, & Schuett, 1997) and rodents (Jacobs, 1992;Jacobs & Spencer, 1994), foraging-related rate of movement in lacertid lizards (Day, Crews, & Wilczynski, 1999), home-range size in voles (Gaulin, 1992;Jacobs, Gaulin, Sherry, & Hoffman, 1990 Sherry, Jacobs, & Gaulin, 1992), and breeding-habitat complexity in petrels (Abbott, Walsh, Storey, Stenhause, & Harley, 1999) are all associated with enlarged Hp size, presumably due to the demands of spatial memory. In addition, seasonal variation in food-storing demands is associated with seasonal changes in Hp volume (Smulders, Sasson, & DeVoogd, 1995) in black-capped chickadees and rodents (Jacobs, 1996). Males have a larger Hp than females in a vole species in which males have larger home ranges but not in vole species that do not have sex differences in home range (Gaulin, 1992). These results provide evidence that environmental or experiential seasonal changes can alter Hp volume and that natural and sexual selection on a variety of spatial-related skills has produced a larger Hp in some species or sexes than in others.Although correlations of Hp volume with ecological demands for spatial ability are numerous, the specific mechanisms that contribute to such adult variation in the volume of the Hp are not well understood. We do know that species-specific reactions to spatial experience...

Is bigger always better? A critical appraisal of the use of volumetric analysis in the study of the hippocampus

“…This is a problem as one current method of measuring the Te in the literature is to estimate Te volume only on sections of tissue on which the Hp has also been measured (e.g. Sherry et al 1993;Cristol et al 2003;Day et al 2005Day et al , 2008. Since the Te is longer than the Hp, this means that parts of the Te that are anterior and posterior to the Hp may not have been included in the calculation.…”

Female cowbirds have more accurate spatial memory than males

“…We did not find a significant effect of breeding condition for any of the factors measured (table 1 and figure 2). However, because captivity may differentially affect the hippocampus, we cannot preclude the existence of seasonal differences in free-living birds [17]. Regardless, where sex differences in spatial cognition are found in animals, it is usually males who have better spatial ability [3].…”

Region-specific neuron recruitment in the hippocampus of brown-headed cowbirdsMolothrus ater(Passeriformes: Icteridae)

“…Adult neurogenesis is regulated by internal and external factors such as species, sex, singing activity, social environment, environmental conditions, hormones, seasonality, photoperiod, stress, aging and activity levels (Patel et al 1997;Adar et al 2008;Day et al 2008;LaDage et al 2009LaDage et al , 2010LaDage et al , 2011Delgado-Gonzalez et al 2011;Yamamura et al 2011;Maruska et al 2012;Onksen et al 2012;Alward et al 2014). In food caching bird species neuron recruitment is also regulated by experiences with food caching and retrieval (Clayton & Krebs 1994;Clayton 1995aClayton , 1996Patel et al 1997).…”

“…However, it is still unclear whether the regulatory mechanism of this seasonal change in the brain is related to photoperiod, experience or hormonal changes that coincide with changes in season and/or experience. Restricting experiences such as food caching or nest searching reduces Hp plasticity, including new cell recruitment (Day et al 2008;LaDage et al 2009). Here, captivity, even within natural conditions, may have restricted experiences that would lead to greater DCX+ cells, and therefore it is not possible to know the absolute extent of new cell recruitment that can happen without any captivity.…”