Infected honeybee foragers incur a higher loss in efficiency than in the rate of energetic gainby D. Naug

Biology Letters

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than in the rate of energetic gain

Infected honeybee foragers incur a higher loss in efficiency

Dhruba Naug , 20140731, published 5 November 2014102014 Biol. Lett.

Supplementary data html http://rsbl.royalsocietypublishing.org/content/suppl/2014/11/04/rsbl.2014.0731.DC1. "Data Supplement"

References http://rsbl.royalsocietypublishing.org/content/10/11/20140731.full#BIBL

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Cite this article: Naug D. 2014 Infected honeybee foragers incur a higher loss in efficiency than in the rate of energetic gain.

Biol. Lett. 10: 20140731. http://dx.doi.org/10.1098/rsbl.2014.0731

Animal behaviour

The foraging behaviour of an animal is fundamentally driven by its nutritional and energetic state. Parasites, by drawing nutrition and eliciting energetically on November 6, 2014http://rsbl.royalsocietypublishing.org/Downloaded from Electronic supplementary material is available at http://dx.doi.org/10.1098/rsbl.2014.0731 or via http://rsbl.royalsocietypublishing.org.Author for correspondence:

Dhruba Naug e-mail: dhruba@colostate.eduSubject Areas: behaviour, health and disease and epidemiology

Keywords: optimal foraging, currency, energetics, life history, honeybees, diseaseReceived: 11 September 2014

Accepted: 15 October 2014rsbl.royalsocietypublishing.orgexpensive immune responses, can therefore alter the foraging behaviour of their hosts [1]. Behavioural alterations, including those related to foraging, as consequences of parasitism and disease have been extensively studied, but only rarely have these changes been explored from the perspective of an optimal foraging framework [2]. Optimal foraging models, which use appropriate currencies and cost–benefit functions based on several parameters and constraints to make quantitative predictions about how an animal forages, can therefore be powerful tools to evaluate how the fitness of the host can be compromised by a parasitic disease that alters its foraging behaviour. Such changes in foraging, in addition to having indirect negative effects on host fitness, might also in turn affect parasite fitness by influencing their transmission dynamics.

Parasites and pathogens have been routinely linked to the recent decline in honeybee populations [3], but their negative role has generally been considered only from a direct, pathological viewpoint. Some studies have however shown parasitic infections, such as one with the microsporidian Nosema ceranae, have a negative impact on the foraging behaviour of honeybees [4–7], which could be related to a significant energetic stress in the infected individuals [8] and its influence on a variety of specific behaviours [9–11]. However, how these changes translate to individual- and colony-level effects in terms of nutritional budgets and life-history patterns are not well known. Central place foragers such as honeybeeswith a fixed lifetime flight cost budget are generally predicted tomaximize their efficiencyof energetic gain, (Gain2Cost)/Cost rather than their net rate of energetic gain, (Gain2Cost)/Time, during foraging as this allows them to maximize their foraging lifespan [12–14]. The goal of this study was therefore to determine whether a parasitic infection can influence the foraging behaviour in terms of what is predicted by these two alternative foraging currencies. & 2014 The Author(s) Published by the Royal Society. All rights reserved.Infected honeybee foragers incur a higher loss in efficiency than in the rate of energetic gain

Dhruba Naug

Department of Biology, Colorado State University, Fort Collins, CO 80523, USA

Parasites, by altering the nutritional and energetic state of their hosts, can significantly alter their foraging behaviour. In honeybees, an infection with Nosema ceranae has been shown to lower the energetic state of individual bees, bringing about changes in behaviours associated with foraging.

Comparing the foraging trip times, hive times in between trips, and the crop contents of uninfected and infected foragers as they depart on foraging trips and return from them, this study examined how any differences in these variables influence alternative foraging currencies. The results show that infected bees take longer foraging trips, spend shorter time in the hive between successive trips and bring back less sugar from each trip.

These changes have a stronger adverse effect on their efficiency of energetic gain as compared with their rate of energetic gain, which has important implications for individual and colony life history. 1. Introduction 116

N = du ra -trips h 20 the hi filled b rsbl.royalsocietypublishing.org

Biol.Lett.10:20140731 2 on November 6, 2014http://rsbl.royalsocietypublishing.org/Downloaded from 2. Material and methods

An observation hive was assembled with adult bees and brood from a source colony, which was also used to supply the observation hive with 500 one-day-old bees every other week. Capped brood was extracted 1–2 days before they were due to hatch and kept in an incubator maintained at 328C. Newly emerged bees were tagged with unique number tags and individually fed, half of them with 30 ml of sucrose solution and the other half with 30 ml of sucrose solution containing N. ceranae spores at a concentration of 1  106 ml21, before being introduced into the observation hive.

Behavioural observations were conducted on the observation hive for 4 h, alternating between morning and afternoon sessions, 4 days a week, in those weeks in which new bees were not introduced into the hive. Behavioural sampling consisted of watching the entrance of a hive and recording the departure and arrival times of tagged foragers. Once a tagged forager had a record of successive departure and arrival times from which at least five trip times and between-trips hive times could be calculated, she was opportunistically captured while she was either departing on a foraging flight or returning from one. The captured bees were euthanized and the crop content of each bee was collected on a coverslip by squeezing the thorax. The volume of the contents was measured with a graduated microcapillary tube and the sucrose concentration was determined with a hand-held refractometer [15]. The bee was 0 trip time between 5 10 15