Reproductive resilience to food shortage in a small heterothermic primate

Abstract

The massive energetic costs entailed by reproduction in most mammalian females may increase the vulnerability of reproductive success to food shortage. Unexpected events of unfavorable climatic conditions are expected to rise in frequency and intensity as climate changes. The extent to which physiological flexibility allows organisms to maintain reproductive output constant despite energetic bottlenecks has been poorly investigated. In mammals, reproductive resilience is predicted to be maximal during early stages of reproduction, due to the moderate energetic costs of ovulation and gestation relative to lactation. We experimentally tested the consequences of chronic-moderate and short-acute food shortages on the reproductive output of a small seasonally breeding primate, the grey mouse lemur (Microcebus murinus) under thermo-neutral conditions. These two food treatments were respectively designed to simulate the energetic constraints imposed by a lean year (40% caloric restriction over eight months) or by a sudden, severe climatic event occurring shortly before reproduction (80% caloric restriction over a month). Grey mouse lemurs evolved under the harsh, unpredictable climate of the dry forest of Madagascar and should thus display great potential for physiological adjustments to energetic bottlenecks. We assessed the resilience of the early stages of reproduction (mating success, fertility, and gestation) to these contrasted food treatments, and on the later stages (lactation and offspring growth) in response to the chronic food shortage only. Food deprived mouse lemurs managed to maintain constant most reproductive parameters, including oestrus timing, estrogenization level at oestrus, mating success, litter size, and litter mass as well as their overall number of surviving offspring at weaning. However, offspring growth was delayed in food restricted mothers. These results suggest that heterothermic, fattening-prone mammals display important reproductive resilience to energetic bottlenecks. More generally, species living in variable and unpredictable habitats may have evolved a flexible reproductive physiology that helps buffer environmental fluctuations.

Figure 1. Effect of food availability on body mass over (A) gestation and (B) lactation.

Body mass (±SEM) of females fed ad libitum (AL) and calorie restricted females (CR60) (A) during the two months following oestrus, and (B) during the 45 days after birth.

Figure 2. Effect of food availability to lactating mothers on offspring femur growth.

Femur length grew slower and less for pups reared by calorie restricted females (CR60, open circles, grey line) than for those reared by females fed ad libitum (AL, black dots, black line). Lines draw the growth curves estimated per treatment with 2-parameters Gompertz models.

Figure 3. Effect of food availability to lactating mothers on the variation of offspring body condition with age.

Non-linear temporal variation of log (body mass) residuals [adjusted for log (femur length)] of offspring from females fed ad libitum (AL, panel A) and from calorie restricted females (CR, panel B). The curve describing the age effect (solid line) was extracted from GAMMs. Dashed lines depict 2 standard error point-wise confidence bands, and black dots provide partial residuals. In panel A., red dashed line points the date at which body condition is above average, thereby signing a sustained high body mass increase relative to body size growth. In panel B., red dashed lines and bold labels delimit the period of delayed growth.