What causes wing wear in foraging bumble bees?

SUMMARY Flying is an ecologically important behaviour in many insects, but it often results in permanent wing damage. Although wing wear in insects is often used as a method to determine insect age, and is associated with an increased risk of mortality, the causes of wing wear are unresolved. In this paper, we examine whether wing use while foraging explains wing wear in bumble bees (Bombus spp.). Wing wear may result from three distinct flight characteristics during foraging: time spent in flight, flight frequency and frequency of wing collisions with vegetation. To test these hypotheses for causes of wing wear, we recorded digital video of individually marked bumble bees foraging in nature on 12 different plant species that result in variation in these flight characteristics, and recaptured these individuals to photograph their wings over time. Bumble bees with a higher frequency of wing collisions showed an increased loss of wing area, which became more severe over time. Neither time in flight nor flight frequency was uniquely and significantly associated with wing wear. Therefore, the collision frequency hypothesis best explained wing wear in bumble bees. We conclude that wing use during foraging in bumble bees results in wing wear. Wing wear reflects behaviour, not simply age. Because wing wear has elsewhere been shown to increase mortality, this study provides an important mechanism linking foraging behaviour with lifespan.

[1]  R. Allsopp Wing fray in Glossina morsitans centralis Machado (Diptera: Glossinidae) , 1985 .

[2]  G. Robinson,et al.  Lipid stores, ovary development, and brain gene expression in Polistes metricus females , 2009, Insectes Sociaux.

[3]  R. Moritz,et al.  Foraging distance in Bombus terrestris L. (Hymenoptera: Apidae) , 2008, Apidologie.

[4]  W. M. Whitten,et al.  Fragrance Collection, Storage, and Accumulation by Individual Male Orchid Bees , 2004, Journal of Chemical Ecology.

[5]  A. Bourke,et al.  Conservation genetics, foraging distance and nest density of the scarce Great Yellow Bumblebee (Bombus distinguendus) , 2010, Molecular ecology.

[6]  Steven N. Austad,et al.  Animal Behaviour , 44 , 6 Longevity , Senescence , and the Genome , 2017 .

[7]  M. Mangel,et al.  Seasonal effects on superparasitism by Rhagoletis completa , 1994 .

[8]  S. W. Batra Anthophora pilipes villosula Sm. (Hymenoptera: Anthophoridae), a manageable Japanese bee that visits blueberries and apples during cool, rainy, spring weather , 1994 .

[9]  M. López-Uribe,et al.  Nectar-foraging behavior of Euglossine bees (Hymenoptera: Apidae) in urban areas , 2008, Apidologie.

[10]  B. Heinrich,et al.  Metabolic rates related to muscle activity in bumblebees. , 1974, The Journal of experimental biology.

[11]  R. Fell,et al.  Adult longevity of workers of the bumble bees Bombus fervidus (F.) and Bombus pennsylvanicus (De Geer) (Hymenoptera: Apidae) , 1987 .

[12]  R. Dudley The Biomechanics of Insect Flight: Form, Function, Evolution , 1999 .

[13]  R. Cartar,et al.  Morphological senescence and longevity : an experiment relating wing wear and life span in foraging wild bumble bees , 1992 .

[14]  A. D. Brian Division of Labour and Foraging in Bombus Agrorum Fabricius , 1952 .

[15]  U. Mueller,et al.  A method for estimating the age of bees: Age-dependent wing wear and coloration in the Wool-Carder beeAnthidium manicatum (hymenoptera: Megachilidae) , 1993, Journal of Insect Behavior.

[16]  Robert E. Page,et al.  Division of labor during honey bee colony defense , 1990, Behavioral Ecology and Sociobiology.

[17]  J. Alcock Male size and survival: the effects of male combat and bird predation in Dawson’s burrowing bees, Amegilladawsoni , 1996 .

[18]  S A Combes,et al.  Dynamics of animal movement in an ecological context: dragonfly wing damage reduces flight performance and predation success , 2010, Biology Letters.

[19]  Sean O'Donnell,et al.  Thresholds of Response in Nest Thermoregulation by Worker Bumble Bees, Bombus bifarius nearcticus (Hymenoptera: Apidae) , 2001 .

[20]  A. D. Higginson,et al.  Accumulating wing damage affects foraging decisions in honeybees (Apis mellifera L.) , 2004 .

[21]  W. Blanckenhorn,et al.  Using age grading by wing injuries to estimate size‐dependent adult survivorship in the field: a case study of the yellow dung fly Scathophaga stercoraria , 2002 .

[22]  P. Smeets,et al.  Longevity of Bombus terrestris workers (Hymenoptera: Apidae) in relation to pollen availability, in the absence of foraging , 2003 .

[23]  W. W. Benson,et al.  Body Mass and not Wing Length Predicts Territorial Success in a Tropical Satyrine Butterfly , 2008 .

[24]  F. H. Rodd,et al.  Mortality rates of adult bumble bee workers (Hymenoptera: Apidae) , 1980 .

[25]  D. Kemp Contest behavior in territorial male butterflies: does size matter? , 2000 .

[26]  R. Dukas,et al.  Mortality rates of honey bees in the wild , 2008, Insectes Sociaux.

[27]  A. D. Higginson,et al.  Paying for nectar with wingbeats: a new model of honeybee foraging , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[28]  J. Kingsolver EXPERIMENTAL ANALYSES OF WING SIZE, FLIGHT, AND SURVIVAL IN THE WESTERN WHITE BUTTERFLY , 1999, Evolution; international journal of organic evolution.

[29]  R. Wootton FUNCTIONAL MORPHOLOGY OF INSECT WINGS , 1992 .

[30]  O. Rueppell,et al.  Biodemographic analysis of male honey bee mortality , 2005, Aging cell.

[31]  R. Robbins The "False Head" Hypothesis: Predation and Wing Pattern Variation of Lycaenid Butterflies , 1981, The American Naturalist.

[32]  T. Casey,et al.  Wingstroke frequency of foraging and hovering bumblebees in relation to morphology and temperature , 1991 .

[33]  R. Cartar,et al.  Wing wear affects wing use and choice of floral density in foraging bumble bees , 2011 .

[34]  Anders Hedenström,et al.  Wing wear, aerodynamics and flight energetics in bumblebees (Bombus terrestris): an experimental study , 2001 .

[35]  M. Inoue,et al.  Spatiotemporal distribution and resource use of scoliid wasps (Hymenoptera) in coastal sand dunes , 2006 .

[36]  W. Kutsch,et al.  Relationships between body mass, motor output and flight variables during free flight of juvenile and mature adult locusts, Schistocerca gregaria. , 2000, The Journal of experimental biology.

[37]  Benjamin Jantzen,et al.  Hindwings are unnecessary for flight but essential for execution of normal evasive flight in Lepidoptera , 2008, Proceedings of the National Academy of Sciences.

[38]  J. Spaethe,et al.  Bigger is better: implications of body size for flight ability under different light conditions and the evolution of alloethism in bumblebees , 2007 .

[39]  R. S. Sohal,et al.  Mating behavior, physical activity and aging in the housefly, Musca domestica. , 1973, Experimental gerontology.

[40]  Bernd Heinrich,et al.  "Majoring" and "Minoring" by Foraging Bumblebees, Bombus Vagans: An Experimental Analysis , 1979 .

[41]  M. Schwarz,et al.  Sociality in the Australian Allodapine Bee Brevineura elongata: Small Colony Sizes Despite Large Benefits to Group Living , 2006, Journal of Insect Behavior.

[42]  J. Hargrove,et al.  The flight performance of tsetse flies. , 1975, Journal of insect physiology.

[43]  Andrew P. Martin,et al.  Bumblebee flight distances in relation to the forage landscape. , 2008, The Journal of animal ecology.

[44]  J. Cresswell How and why do nectar-foraging bumblebees initiate movements between inflorescences of wild bergamot Monarda fistulosa (Lamiaceae)? , 1990, Oecologia.

[45]  John B. Free,et al.  Bumblebee economics , 1979, Nature.

[46]  C. A. Garófalo Bionomics of Bombus (Fervidobombus) Morio 2. Body Size and Length of Life of Workers , 1978 .

[47]  M. Richards Variable worker behaviour in the weakly eusocial sweat bee, Halictus sexcinctus Fabricius , 2003, Insectes Sociaux.

[48]  R. Cartar,et al.  Robust flight performance of bumble bees with artificially induced wing wear , 2008 .

[49]  G. Kastberger,et al.  Aggressive and Docile Colony Defence Patterns in Apis mellifera. A Retreater–Releaser Concept , 2008, Journal of Insect Behavior.

[50]  T. Tscharntke,et al.  Bumblebees experience landscapes at different spatial scales: possible implications for coexistence , 2006, Oecologia.

[51]  R. Wall,et al.  Age‐grading adult insects: a review of techniques , 1999 .