The energetic cost of parasitism in a wild population.
ABSTRACT: Parasites have profound fitness effects on their hosts, yet these are often sub-lethal, making them difficult to understand and quantify. A principal sub-lethal mechanism that reduces fitness is parasite-induced increase in energetic costs of specific behaviours, potentially resulting in changes to time and energy budgets. However, quantifying the influence of parasites on these costs has not been undertaken in free-living animals. We used accelerometers to estimate energy expenditure on flying, diving and resting, in relation to a natural gradient of endo-parasite loads in a wild population of European shags Phalacrocorax aristotelis We found that flight costs were 10% higher in adult females with higher parasite loads and these individuals spent 44% less time flying than females with lower parasite loads. There was no evidence for an effect of parasite load on daily energy expenditure, suggesting the existence of an energy ceiling, with the increase in cost of flight compensated for by a reduction in flight duration. These behaviour specific costs of parasitism will have knock-on effects on reproductive success, if constraints on foraging behaviour detrimentally affect provisioning of young. The findings emphasize the importance of natural parasite loads in shaping the ecology and life-history of their hosts, which can have significant population level consequences.
Project description:Parasites often prompt sub-lethal costs to their hosts by eliciting immune responses. These costs can be hard to quantify but are crucial to our understanding of the host's ecology. Energy is a fundamental currency to quantify these costs, as energetic trade-offs often exist between key fitness-related processes. Daily energy expenditure (DEE) comprises of resting metabolic rate (RMR) and energy available for activity, which are linked via the energy management strategy of an organism. Parasitism may play a role in the balance between self-maintenance and activity, as immune costs can be expressed in elevated RMR. Therefore, understanding energy use in the presence of parasitism enables mechanistic elucidation of potential parasite costs. Using a gradient of natural parasite load and proxies for RMR and DEE in a wild population of breeding European shags (Phalacrocorax aristotelis), we tested the effect of parasitism on maintenance costs as well as the relationship between proxies for RMR and DEE. We found a positive relationship between parasite load and our RMR proxy in females but not males, and no relationship between proxies for RMR and DEE. This provides evidence for increased maintenance costs in individuals with higher parasite loads and suggests the use of an allocation energy management strategy, whereby an increase to RMR creates restrictions on energy allocation to other activities. This is likely to have fitness consequences as energy allocated to immunity is traded off against reproduction. Our findings demonstrate that understanding energy management strategies alongside fitness drivers is central to understanding the mechanisms by which these drivers influence individual fitness.
Project description:Environmental contaminants and parasites are ubiquitous stressors that can affect animal physiology and derive from similar dietary sources (co-exposure). To unravel their interactions in wildlife, it is thus essential to quantify their concurring drivers. Here, the relationship between blood contaminant residues (11 trace elements and 17 perfluoroalkyl substances) and nonlethally quantified gastrointestinal parasite loads was tested while accounting for intrinsic (sex, age, and mass) and extrinsic factors (trophic ecology inferred from stable isotope analyses and biologging) in European shags Phalacrocorax aristotelis. Shags had high mercury (range 0.65-3.21 ?g g-1 wet weight, ww) and extremely high perfluorooctanoic acid (PFOA) and perfluorononanoic acid (PFNA) residues (3.46-53 and 4.48-44 ng g-1 ww, respectively). Males had higher concentrations of arsenic, mercury, PFOA, and PFNA than females, while the opposite was true for selenium, perfluorododecanoic acid (PFDoA), and perfluooctane sulfonic acid (PFOS). Individual parasite loads (Contracaecum rudolphii) were higher in males than in females. Females targeted pelagic-feeding prey, while males relied on both pelagic- and benthic-feeding organisms. Parasite loads were not related to trophic ecology in either sex, suggesting no substantial dietary co-exposure with contaminants. In females, parasite loads increased strongly with decreasing selenium:mercury molar ratios. Females may be more susceptible to the interactive effects of contaminants and parasites on physiology, with potential fitness consequences.
Project description:Parasitic infection has a direct physiological cost to hosts but may also alter how hosts interact with other individuals in their environment. Such indirect effects may alter both host fitness and the fitness of other individuals in the host's social network, yet the relative impact of direct and indirect effects of infection are rarely quantified. During reproduction, a host's social environment includes family members who may be in conflict over resource allocation. In such situations, infection may alter how resources are allocated, thereby redistributing the costs of parasitism between individuals. Here, we experimentally reduce parasite burdens of parent and/or nestling European shags (Phalacrocorax aristotelis) infected with Contracaecum nematodes in a factorial design, then simultaneously measure the impact of an individual's infection on all family members. We found no direct effect of infection on parent or offspring traits but indirect effects were detected in all group members, with both immediate effects (mass change and survival) and longer-term effects (timing of parents' subsequent breeding). Our results show that parasite infection can have a major impact on individuals other than the host, suggesting that the effect of parasites on population processes may be greater than previously thought.
Project description:Flight is a key adaptive trait. Despite its advantages, flight has been lost in several groups of birds, notably among seabirds, where flightlessness has evolved independently in at least five lineages. One hypothesis for the loss of flight among seabirds is that animals moving between different media face tradeoffs between maximizing function in one medium relative to the other. In particular, biomechanical models of energy costs during flying and diving suggest that a wing designed for optimal diving performance should lead to enormous energy costs when flying in air. Costs of flying and diving have been measured in free-living animals that use their wings to fly or to propel their dives, but not both. Animals that both fly and dive might approach the functional boundary between flight and nonflight. We show that flight costs for thick-billed murres (Uria lomvia), which are wing-propelled divers, and pelagic cormorants (Phalacrocorax pelagicus) (foot-propelled divers), are the highest recorded for vertebrates. Dive costs are high for cormorants and low for murres, but the latter are still higher than for flightless wing-propelled diving birds (penguins). For murres, flight costs were higher than predicted from biomechanical modeling, and the oxygen consumption rate during dives decreased with depth at a faster rate than estimated biomechanical costs. These results strongly support the hypothesis that function constrains form in diving birds, and that optimizing wing shape and form for wing-propelled diving leads to such high flight costs that flying ceases to be an option in larger wing-propelled diving seabirds, including penguins.
Project description:Soaring flight is a remarkable adaptation to reduce movement costs by taking advantage of atmospheric uplifts. The movement pattern of soaring birds is shaped by the spatial and temporal availability and intensity of uplifts, which result from an interaction of local weather conditions with the underlying landscape structure. We used soaring flight locations and vertical speeds of an obligate soaring species, the white stork (Ciconia ciconia), as proxies for uplift availability and intensity. We then tested if static landscape features such as topography and land cover, instead of the commonly used weather information, could predict and map the occurrence and intensity of uplifts across Europe. We found that storks encountering fewer uplifts along their routes, as determined by static landscape features, suffered higher energy expenditures, approximated by their overall body dynamic acceleration. This result validates the use of static features as uplift predictors and suggests the existence of a direct link between energy expenditure and static landscape structure, thus far largely unquantified for flying animals. Our uplift availability map represents a computationally efficient proxy of the distribution of movement costs for soaring birds across the world's landscapes. It thus provides a base to explore the effects of changes in the landscape structure on the energy expenditure of soaring birds, identify low-cost movement corridors and ultimately inform the planning of anthropogenic developments.
Project description:Flapping flight is the most energetically demanding form of sustained forwards locomotion that vertebrates perform. Flock dynamics therefore have significant implications for energy expenditure. Despite this, no studies have quantified the biomechanical consequences of flying in a cluster flock or pair relative to flying solo. Here, we compared the flight characteristics of homing pigeons (Columba livia) flying solo and in pairs released from a site 7 km from home, using high-precision 5 Hz global positioning system (GPS) and 200 Hz tri-axial accelerometer bio-loggers. As expected, paired individuals benefitted from improved homing route accuracy, which reduced flight distance by 7% and time by 9%. However, realising these navigational gains involved substantial changes in flight kinematics and energetics. Both individuals in a pair increased their wingbeat frequency by 18% by decreasing the duration of their upstroke. This sharp increase in wingbeat frequency caused just a 3% increase in airspeed but reduced the oscillatory displacement of the body by 22%, which we hypothesise relates to an increased requirement for visual stability and manoeuvrability when flying in a flock or pair. The combination of the increase in airspeed and a higher wingbeat frequency would result in a minimum 2.2% increase in the total aerodynamic power requirements if the wingbeats were fully optimised. Overall, the enhanced navigational performance will offset any additional energetic costs as long as the metabolic power requirements are not increased above 9%. Our results demonstrate that the increases in wingbeat frequency when flying together have previously been underestimated by an order of magnitude and force reinterpretation of their mechanistic origin. We show that, for pigeons flying in pairs, two heads are better than one but keeping a steady head necessitates energetically costly kinematics.
Project description:In many animals, catabolic and anabolic periods are temporally separated. Migratory birds alternate energy expenditure during flight with energy accumulation during stopover. The size of the energy stores at stopover affects the decision to resume migration and thus the temporal organization of migration. We now provide data suggesting that it is not only the size of the energy stores <i>per se</i> that may influence migration scheduling, but also the physiological consequences of flying. In two subspecies of the northern wheatear <i>Oenanthe oenanthe</i>, a long-distance migrant, estimated energy stores at a stopover during autumn migration were positively related with both constitutive innate and acquired immune function, and negatively related with oxidative damage to lipids. In other words, migrants' physiological condition was associated with their energetic condition. Although time spent at stopover before sampling may have contributed to this relationship, our results suggest that migrants have to trade-off the depletion of energy stores during flight with incurring physiological costs. This will affect migrants' decisions when to start and when to terminate a migratory flight. The physiological costs associated with the depletion of energy stores may also help explaining why migrants often arrive at and depart from stopover sites with larger energy stores than expected. We propose that studies on the role of energy stores as drivers of the temporal organization of (avian) migration need to consider physiological condition, such as immunological and oxidative states.
Project description:Acquisition or loss of flying ability is evolutionarily linked with maximum life span (MLS) in mammals and birds. Although ecological factors, such as extrinsic mortality, may lead to either shortened or extended life spans through natural selection, MLS is influenced by complex molecular and metabolic processes, and the genetic changes associated with flying ability that have led to either a longer or shorter MLS are unknown. Here, we examine the parallel evolution of flight in mammals and birds and investigate positively selected genes at branches where either the acquisition (in little brown bats and large flying foxes) or loss (in Adélie penguins, emperor penguins, common ostriches, emus, great spotted kiwis, little spotted kiwis, okarito brown kiwis, greater rheas, lesser rheas, and cassowaries) of flight abilities occurred. Although we found no shared genes under selection among all the branches of interest, 7 genes were found to be positively selected in 2 of the branches. Among the 7 genes, only IGF2BP2 is known to affect both life span and energy expenditure. The positively selected mutations detected in IGF2BP2 likely affected the functionality of the encoded protein. IGF2BP2, which has been reported to simultaneously prolong life span and increase energy expenditure, could be responsible for the evolution of shortened MLS associated with the loss of flying ability.
Project description:To maximize fitness, flying animals should maximize flight speed while minimizing energetic expenditure. Soaring speeds of large-bodied birds are determined by flight routes and tradeoffs between minimizing time and energetic costs. Large raptors migrating in eastern North America predominantly glide between thermals that provide lift or soar along slopes or ridgelines using orographic lift (slope soaring). It is usually assumed that slope soaring is faster than thermal gliding because forward progress is constant compared to interrupted progress when birds pause to regain altitude in thermals. We tested this slope-soaring hypothesis using high-frequency GPS-GSM telemetry devices to track golden eagles during northbound migration. In contrast to expectations, flight speed was slower when slope soaring and eagles also were diverted from their migratory path, incurring possible energetic costs and reducing speed of progress towards a migratory endpoint. When gliding between thermals, eagles stayed on track and fast gliding speeds compensated for lack of progress during thermal soaring. When thermals were not available, eagles minimized migration time, not energy, by choosing energetically expensive slope soaring instead of waiting for thermals to develop. Sites suited to slope soaring include ridges preferred for wind-energy generation, thus avian risk of collision with wind turbines is associated with evolutionary trade-offs required to maximize fitness of time-minimizing migratory raptors.
Project description:Flapping flight is one of the most costly forms of locomotion in animals. To limit energetic expenditures, flying insects thus developed multiple strategies. An effective mechanism to reduce flight power expenditures is the harvesting of kinetic energy from motion of the surrounding air. We here show an unusual mechanism of energy harvesting in an insect that recaptures the rotational energy of air vortices. The mechanism requires pronounced chordwise wing bending during which the wing surface momentary traps the vortex and transfers its kinetic energy to the wing within less than a millisecond. Numerical and robotic controls show that the decrease in vortex strength is minimal without the nearby wing surface. The measured energy recycling might slightly reduce the power requirements needed for body weight support in flight, lowering the flight costs in animals flying at elevated power demands. An increase in flight efficiency improves flight during aversive manoeuvring in response to predation and long-distance migration, and thus factors that determine the worldwide abundance and distribution of insect populations.