Take-off mechanisms in parasitoid wasps

ABSTRACT High-speed video analyses of the natural behaviour of parasitoid wasps revealed three strategies used to launch the insects into the air. Which strategy is the most energy efficient? In Pteromalus puparum, 92% of take-offs by were propelled entirely by movements of the middle and hind legs, which were depressed at their coxo-trochanteral and extended at their femoro-tibial joints. The front legs left the ground first, followed by the hind legs, so that the middle legs provided the final propulsion. Second, in other species of a similar mass, Cotesia glomerata and Leptopilina boulardi, all take-offs were propelled by a mean of 2.8 and 3.8 wingbeats, respectively, with little or no contribution from the legs. The first strategy resulted in take-off times that were four times shorter (5 versus 22.8 ms) and take-off velocities that were four times faster (0.8 versus 0.2 m s−1). Calculations from the kinematics indicate that propulsion by the legs was the most energy-efficient strategy, because more energy is put into propulsion of the body, whereas in take-off propelled by repetitive wing movements energy is lost to generating these movements and moving the air. In heavier species such as Netelia testacea and Amblyteles armatorius, take-off was propelled by the combined movements of the middle and hind legs and wingbeats. In A. armatorius, this resulted in the longest mean take-off time of 33.8 ms but an intermediate take-off velocity of 0.4 m s−1. In all three strategies the performance could be explained without invoking energy storage and power amplification mechanisms. Summary: Parasitoid wasps use three strategies to take off: propulsion by rapid leg movements, propulsion by flapping wing movements and a combination of the two. Leg movements provide the most energy-efficient mechanism.

[1]  M. Burrows,et al.  Jumping mechanisms and performance of snow fleas (Mecoptera, Boreidae) , 2011, Journal of Experimental Biology.

[2]  M. Burrows Jumping from the surface of water by the long-legged fly Hydrophorus (Diptera, Dolichopodidae) , 2013, Journal of Experimental Biology.

[3]  M. Burrows Energy storage and synchronisation of hind leg movements during jumping in planthopper insects (Hemiptera, Issidae) , 2010, Journal of Experimental Biology.

[4]  R. Dudley,et al.  Directed aerial descent in canopy ants , 2005, Nature.

[5]  Robert Dudley,et al.  Aerial manoeuvrability in wingless gliding ants (Cephalotes atratus) , 2010, Proceedings of the Royal Society B: Biological Sciences.

[6]  M. Burrows,et al.  Jumping mechanisms and strategies in moths (Lepidoptera) , 2015, The Journal of Experimental Biology.

[7]  D. Magdalena Sorger,et al.  Snap! Trap‐jaw ants in Borneo also jump using their legs , 2015 .

[8]  G. Gibson MESOTHORACIC SKELETOMUSCULATURE AND MECHANICS OF FLIGHT AND JUMPING IN EUPELMINAE (HYMENOPTERA, CHALCIDOIDEA: EUPELMIDAE) , 1986, The Canadian Entomologist.

[9]  S. Patek,et al.  Multifunctionality and mechanical origins: Ballistic jaw propulsion in trap-jaw ants , 2006, Proceedings of the National Academy of Sciences.

[10]  M. Burrows,et al.  Jumping performance of froghopper insects , 2006, Journal of Experimental Biology.

[11]  Sarah Hammond,et al.  Ontogeny of flight initiation in the fly Drosophila melanogaster: implications for the giant fibre system , 2007, Journal of Comparative Physiology A.

[12]  M. Burrows,et al.  Jumping and kicking in bush crickets , 2003, Journal of Experimental Biology.

[13]  M. Burrows,et al.  Jumping performance of flea hoppers and other mirid bugs (Hemiptera, Miridae) , 2017, Journal of Experimental Biology.

[14]  A. Suarez,et al.  Mandible-Powered Escape Jumps in Trap-Jaw Ants Increase Survival Rates during Predator-Prey Encounters , 2015, PloS one.

[15]  S. Sunada,et al.  PERFORMANCE OF A BUTTERFLY IN TAKE-OFF FLIGHT , 1993 .

[16]  Barbara J. Sharanowski,et al.  Utility of the DNA barcoding gene fragment for parasitic wasp phylogeny (Hymenoptera: Ichneumonoidea): data release and new measure of taxonomic congruence , 2012, Molecular ecology resources.

[17]  D. Gerling,et al.  Whiteflies stabilize their take-off with closed wings , 2016, Journal of Experimental Biology.

[18]  Jérôme Casas,et al.  Force balance in the take-off of a pierid butterfly: relative importance and timing of leg impulsion and aerodynamic forces , 2013, Journal of Experimental Biology.

[19]  M. Dickinson,et al.  Visually Mediated Motor Planning in the Escape Response of Drosophila , 2008, Current Biology.

[20]  J. Trimarchi,et al.  Flight initiations in Drosophila melanogaster are mediated by several distinct motor patterns , 1995, Journal of Comparative Physiology A.

[21]  M. Burrows,et al.  Mantises Exchange Angular Momentum between Three Rotating Body Parts to Jump Precisely to Targets , 2015, Current Biology.

[22]  R. Josephson Contraction dynamics and power output of skeletal muscle. , 1993, Annual review of physiology.

[23]  H. Bennet-Clark,et al.  The jump of the flea: a study of the energetics and a model of the mechanism. , 1967, The Journal of experimental biology.

[24]  M. Burrows,et al.  Jumping performance of planthoppers (Hemiptera, Issidae) , 2009, Journal of Experimental Biology.

[26]  M. Burrows,et al.  Jumping mechanisms of treehopper insects (Hemiptera, Auchenorrhyncha, Membracidae) , 2013, Journal of Experimental Biology.

[27]  H. Bennet-Clark,et al.  The energetics of the jump of the locust Schistocerca gregaria. , 1975, The Journal of experimental biology.

[28]  A. Leonardo,et al.  A spike-timing mechanism for action selection , 2014, Nature Neuroscience.

[29]  M. Burrows,et al.  Interacting Gears Synchronize Propulsive Leg Movements in a Jumping Insect , 2013, Science.

[30]  G. Boyan,et al.  A novel mechanism for jumping in the indian antHarpegnathos saltator (Jerdon) (Formicidae, Ponerinae) , 2005, Experientia.

[31]  The ants that jump: Different techniques to take off , 1994 .

[32]  Malcolm Burrows,et al.  Biomechanics: Froghopper insects leap to new heights , 2003, Nature.

[33]  M. Tuda,et al.  Costs and benefits of larval jumping behaviour of Bathyplectes anurus , 2015, The Science of Nature.

[34]  J. Trimarchi,et al.  Initiation of flight in the unrestrained fly, Drosophila melanogaster , 2009 .

[35]  C. Ellington Power and efficiency of insect flight muscle. , 1985, The Journal of experimental biology.

[36]  J. Billen,et al.  Multiple jumping behaviors in the antHarpegnathos saltator , 1992, Naturwissenschaften.

[37]  M. Burrows,et al.  Jumping mechanisms in adult caddis flies (Insecta, Trichoptera) , 2015, The Journal of Experimental Biology.

[38]  M. Burrows,et al.  Jumping mechanisms in lacewings (Neuroptera, Chrysopidae and Hemerobiidae) , 2014, Journal of Experimental Biology.

[39]  Graham N Askew,et al.  Muscle designed for maximum short-term power output: quail flight muscle. , 2002, The Journal of experimental biology.

[40]  Seán G. Brady,et al.  Phylogenomic Insights into the Evolution of Stinging Wasps and the Origins of Ants and Bees , 2017, Current Biology.