Flying on empty: Reduced mitochondrial function and flight capacity in food-deprived monarch butterflies

Mitochondrial function is fundamental to organismal performance, health,
and fitness – especially during energetically challenging events, such as
migration. With this investigation, we evaluated mitochondrial sensitivity
to ecologically relevant stressors. We focused on an iconic migrant, the
North American monarch butterfly (Danaus plexippus), and examined the
effects of two stressors: seven days of food deprivation, and infection by
the protozoan parasite Ophryocystis elektroscirrha (known to reduce
survival and flight performance). We measured whole-animal resting
metabolic rate (RMR) and peak flight metabolic rate, and mitochondrial
respiration of isolated mitochondria from the flight muscles. Food
deprivation reduced mass-independent RMR and peak flight metabolic rate,
whereas infection did not. Fed monarchs used mainly lipids in flight
(respiratory quotient 0.73), but the respiratory quotient dropped in
food-deprived individuals, possibly indicating switching to alternative
energy sources, such as ketone bodies. Food deprivation decreased
mitochondrial maximum oxygen consumption but not basal respiration,
resulting in lower respiratory control ratio (RCR). Furthermore, food
deprivation decreased mitochondrial complex III activity, but increased
complex IV activity. Infection did not result in any changes in these
mitochondrial variables. Mitochondrial maximum respiration rate correlated
positively with mass-independent RMR and flight metabolic rate, suggesting
a link between mitochondria and whole-animal performance. In conclusion,
low food availability negatively affects mitochondrial function and flight
performance, with potential implications for migration, fitness, and
population dynamics. Although previous studies have reported poor flight
performance in infected monarchs, we found no differences in physiological
performance, suggesting that reduced flight capacity may be due to
structural differences or low energy stores.