Energy balance and ovulation: small cages versus natural habitats

Abstract

In the laboratory, ovulation is suppressed when a mammal is in negative energy balance whether that state is caused by inadequate food intake, excessive locomotor activity or heavy thermoregulatory costs. In this paper, knowledge generated in the laboratory about the link between ovulation and energy balance is examined in relation to the kinds of energetic challenges mammals actually face in natural habitats. When viewed in that context, several conclusions can be drawn. First, females ovulate whenever extant energetic conditions permit unless the process is blocked by non-metabolic stress, social cues or a predictive seasonal cue such as photoperiod. In the latter case, most mammals show at least a seasonal tendency in their reproduction and the majority do not use a predictive cue; they reproduce opportunistically in relation to seasonal variation in the energetic characteristics of their environment. Second, the widely held assumption that a female's fat reserves must exceed a critical level in order that she may ovulate finds no support in the literature dealing with natural populations. Third, the surprisingly rapid responsiveness of the gonadotrophin releasing hormone (GnRH) pulse generator to energetic manipulation probably reflects the study of animals that are in a pure survival mode. Fourth, the complexity of the energetic challenges mammals face in the wild suggests that there are probably multiple metabolic and neural pathways coupling ovulation to energy balance and that these pathways are probably characterized by considerable overlap and redundancy. Thus, fifth, to develop a more realistic overview of these pathways there is a need for experimental designs that present mammals with the kinds of complex challenges they actually face in the wild habitats in which they evolved.

The pattern of ovulation in the southern African spiny mouse (Acomys spinosissimus)

“…The paired female, however, showed elevated FPM concentrations on the last sampling day and we may have missed the luteal phase because faecal sampling was conducted only every second day. Body mass and age of a female are important factors governing the reproductive process (Bronson 1998). It is, however, unlikely that these affected our results.…”

Fat Is Sexy for Females but Not Males: The Influence of Body Reserves on Reproduction in Snakes (Vipera aspis)

“…These animals also display ability to cancel, increase, or decrease reproductive effort at a later stage long after the initiation of reproduction per se. In this sense, capital breeding mammals may be similar to male asp vipers: individuals with more body reserves are more likely to reproduce, but do not require a threshold level of reserves to initiate reproduction (Bronson, 1998; this paper). Thus, they do not satisfy the "threshold" criterion for capital breeding (Stearns, 1992).…”

“…For example, several mammals are classified as typical capital breeders (Festa-Bianchet et al, 1998) but recent reviews on captive and natural populations of mammals found no support for the widely accepted "adaptationist argument that females should delay ovulation until they have sufficient energy reserves to support pregnancy and lactation" (Bronson, 1998;Schneider, Zhou, and Blum, 2000). These animals also display ability to cancel, increase, or decrease reproductive effort at a later stage long after the initiation of reproduction per se.…”

“…The energetics of reproduction has been a central theme in the ecological study of life history variation (Hirshfield and Tinkle, 1975;Morris, 1987Morris, , 1992Winkler and Wallin, 1987;Stearns, 1992;Monaghan and Nager, 1997), and more recently this topic has become an important focus in behavioral endocrinology (Cherel, Mauget, Lacroix, and Gilles, 1994;Bronson, 1998). It is obvious that organisms cannot reproduce in the total absence of energy reserves (Frish, 1978;Frish and McArthur, 1974), but the relationship between the amount of energy reserves and reproductive output (or effort) is complex and varies among species.…”

Glucogenic supply increases ovulation rate by modifying follicle recruitment and subsequent development of preovulatory follicles without effects on ghrelin secretion

“…Leptin has a reciprocal regulatory relation with ghrelin, a messenger coming directly from the gastrointestinal tract (Kalra et al 2005). Nutrition is hypothesized to be regulated by cholecystokinin, leptin and insulin, decreasing food intake and ghrelin, and increasing food intake (Bronson 1998). Cholecystokinin and ghrelin regulate food intake in the short term, whereas leptin and insulin regulate food intake over longer periods (Gorissen et al 2006).…”