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Leg loss decreases endurance and increases oxygen consumption during locomotion in harvestmen

Abstract

Animal movements are highly constrained by morphology and energetics. In addition, predictable bodily damage can constrain locomotion even further. For example, for animals moving on land, losing legs may impose additional costs. We tested if losing legs affects the distance travelled over time (endurance) and the metabolic costs of locomotion (oxygen consumption) in Nelima paessleri harvestmen. These arachnids voluntary releases legs (i.e., autotomy) in response to predation attempts. We used flow-through respirometry as animals moved on a treadmill inside a sealed chamber. We found that endurance decreased gradually with an increasing number of legs lost. Interestingly, oxygen consumption increased only for harvestmen that lost three legs, but not for individuals that lost only a single leg. These results have different ecological and evolutionary implications. Reduced endurance may impair an animal’s ability to continue moving away from potential predators, while increased oxygen consumption makes movement costlier. Our findings suggest that individuals have a threshold number of legs that can be lost before experiencing measurable energetic consequences. Overall, our findings illustrate how animals respond to morphological modifications (i.e., damage) that affect the physiology of locomotion.

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Data availability

The complete dataset is available on Dryad (https://doi.org/10.5061/dryad.76hdr7ssv). All individuals were deposited as voucher specimens at the Essig Museum of Entomology, University of California—Berkeley.

Code availability

Code is available upon request to the corresponding author.

References

  1. Allen BJ, Levinton JS (2007) Costs of bearing a sexually selected ornamental weapon in a fiddler crab. Funct Ecol 21:154–161

    Google Scholar 

  2. Anderson JF (1993) Respiratory energetics of two Florida harvestmen. Comp Biochem Physiol Part A Physiol 105:67–72

    Google Scholar 

  3. Bartholomew GA, Vleck D, Vleck CM (1981) Instantaneous measurements of oxygen consumption during pre-flight warm-up and post-flight cooling in Sphingid and Saturniid moths. J Exp Biol 90:17–32

    Google Scholar 

  4. Biro PA, Stamps JA (2010) Do consistent individual differences in metabolic rate promote consistent individual differences in behavior? Trends Ecol Evol 25:653–659

    PubMed  Google Scholar 

  5. Chapple DG, Swain R (2002) Effect of caudal autotomy on locomotor performance in a viviparous skink, Niveoscincus metallicus. Funct Ecol 16:817–825

    Google Scholar 

  6. Chelini MC, Machado G (2014) Multiple lines of egg defense in a neotropical arachnid with temporary brood desertion. Ethology 120:1147–1154

    Google Scholar 

  7. Cokendolpher JC, Mitov PG (2007) Natural enemies. In: Pinto-da-Rocha R, Machado G, Giribet G (eds) Harvestmen: the biology of Opiliones. Harvard University Press, Cambridge, pp 339–373

    Google Scholar 

  8. Domínguez M, Escalante I, Carrasco-Rueda F, Figuerola-Hernández C, Ayup MM, Umaña MN, Ramos D, González-Zamora A, Brizuela C, Delgado W, Pacheco-Esquivel J (2016) Losing legs and walking hard: effects of autotomy and different substrates in the locomotion of harvestmen in the genus Prionostemma. J Arachnol 44:76–82

    Google Scholar 

  9. Emberts Z, Escalante I, Bateman PW (2019) The ecology and evolution of autotomy. Biol Rev 94:1881–1896

    PubMed  Google Scholar 

  10. Escalante I, Albín A, Aisenberg A (2013) Lacking sensory (rather than locomotive) legs affects locomotion but not food detection in the harvestman Holmbergiana weyenberghi. Can J Zool 91:726–731

    Google Scholar 

  11. Escalante I, Badger MA, Elias DO (2019) Variation in movement: multiple locomotor gaits in Neotropical harvestmen. Biol J Linn Soc 127:493–507

    Google Scholar 

  12. Escalante I, Badger MA, Elias DO (2020) Rapid recovery of locomotor performance after leg loss in harvestmen. Sci Rep 10:1–13

    Google Scholar 

  13. Fleming PA, Bateman PW (2007) Just drop it and run: the effect of limb autotomy on running distance and locomotion energetics of field crickets (Gryllus bimaculatus). J Exp Biol 210:1446–1454

    Google Scholar 

  14. Fleming PA, Muller D, Bateman PW (2007) Leave it all behind: a taxonomic perspective of autotomy in invertebrates. Biol Rev 82:481–510

    PubMed  Google Scholar 

  15. Fleming PA, Verburgt L, Scantlebury M, Medger K, Bateman PW (2009) Jettisoning ballast or fuel? Caudal autotomy and locomotory energetics of the Cape Dwarf Gecko Lygodactylus capensis (Gekkonidae). Physiol Biochem Zool 82:756–765

    PubMed  Google Scholar 

  16. Full RJ (1987) Locomotion energetics of the ghost crab: I. Metabolic cost and endurance. J Exp Biol 130:137–153

    Google Scholar 

  17. Full RJ (1991) The concepts of efficiency and economy in land locomotion. In: Blake RW, Blake RW (eds) Efficiency and economy in animal physiology. Cambridge University Press, Cambridge, pp 97–132

    Google Scholar 

  18. Full RJ, Tu MS (1991) Mechanics of a rapid running insect: two-, four- and six-legged locomotion. J Exp Biol 156:215–231

    CAS  PubMed  Google Scholar 

  19. Full RJ, Tullis A (1990) Capacity for sustained terrestrial locomotion in an insect: energetics, thermal dependence, and kinematics. J Comp Physiol B 160:573–581

    Google Scholar 

  20. Gast K, Kram R, Riemer R (2019) Preferred walking speed on rough terrain: is it all about energetics? J Exp Biol 222:jeb185447

    PubMed  Google Scholar 

  21. Grether GF, Donaldson ZR (2007) Communal roost site selection in a neotropical harvestman: Habitat limitation vs. tradition. Ethology 113:290–300

    Google Scholar 

  22. Grether GF, Aller TL, Grucky NK, Levi A, Antaky CC, Townsend VR (2014) Species differences and geographic variation in the communal roosting behavior of Prionostemma harvestmen in Central American rainforests. J Arachnol 42:257–267

    Google Scholar 

  23. Grossi B, Solis R, Veloso C, Canals M (2016) Consequences of sexual size dimorphism on energetics and locomotor performance of Grammostola rosea (Araneae; Teraphosidae). Physiol Entomol 41:281–288

    Google Scholar 

  24. Halsey LG, White CR (2019) Terrestrial locomotion energy costs vary considerably between species: no evidence that this is explained by rate of leg force production or ecology. Sci Rep 9:656

    PubMed  PubMed Central  Google Scholar 

  25. Hao X, Ma W, Liu C, Li Y, Qian Z, Ren L (2019) Analysis of spiders’ joint kinematics and driving modes under different ground conditions. Appl Bionics Biomech 2019:4617212

    PubMed  PubMed Central  Google Scholar 

  26. Herreid CF, Full RJ (1986) Energetics of hermit crabs during locomotion: the cost of carrying a shell. J Exp Biol 120:297–308

    Google Scholar 

  27. Herreid CF, Full RJ, Prawel DA (1981a) Energetics of cockroach locomotion. J Exp Biol 94:189–202

    Google Scholar 

  28. Herreid CF, Prawler DA, Full RJ (1981b) Energetics of running cockroaches. Science 212:331–333

    PubMed  Google Scholar 

  29. Höfer AM, Perry SF, Schmitz A (2000) Respiratory system of arachnids II: morphology of the tracheal system of Leiobunum rotundum and Nemastoma lugubre (Arachnida, Opiliones). Arthropod Struct Dev 29:13–21

    PubMed  Google Scholar 

  30. Hsieh ST (2016) Tail loss and narrow surfaces decrease locomotor stability in the arboreal green anole lizard (Anolis carolinensis). J Exp Biol 219:364–373

    PubMed  Google Scholar 

  31. Jindrich DI, Full RJ (1999) Many-legged maneuverability: dynamics of turning in hexapods. J Exp Biol 202:1603–1623

    PubMed  Google Scholar 

  32. Joseph PN, Emberts Z, Sasson DA, Miller CW (2018) Males that drop a sexually selected weapon grow larger testes. Evolution 72:113–122

    CAS  PubMed  Google Scholar 

  33. Kram R, Wong B, Full RJ (1997) Three-dimensional kinematics and limb kinetic energy of running cockroaches. J Exp Biol 200:1919–1929

    CAS  PubMed  Google Scholar 

  34. Lardies MA, Naya DE, Berrios P, Bozinovic F (2008) The cost of living slowly: metabolism, Q10 and repeatability in a South American harvestman. Physiol Entomol 33:193–199

    CAS  Google Scholar 

  35. Lighton JRB (2002) Lack of discontinuous gas exchange in a tracheate arthropod, Leiobunum townsendi (Arachnida, Opiliones). Physiol Entomol 27:170–174

    Google Scholar 

  36. Lu HL, Ding GH, Ding P, Ji X (2010) Tail autotomy plays no important role in influencing locomotor performance and anti-predator behavior in a cursorial gecko. Ethology 116:627–634

    Google Scholar 

  37. Machado G, Pomini AM (2008) Chemical and behavioral defenses of the neotropical harvestman Camarana flavipalpi (Arachnida: Opiliones). Biochem Syst Ecol 36:369–376

    CAS  Google Scholar 

  38. Maginnis TL (2006) The costs of autotomy and regeneration in animals: a review and framework for future research. Behav Ecol 17:857–872

    Google Scholar 

  39. Martin J, Avery RA (1998) Effect of tail loss on the movement patterns of the lizard, Psammodrones algirus. Funct Ecol 12:794–802

    Google Scholar 

  40. Mcgaw IJ (2006) Cardiovascular and respiratory responses associated with limb autotomy in the blue crab, Callinectes sapidus. Mar Freshw Behav Physiol 39:131–141

    Google Scholar 

  41. Mountcastle AM, Alexander TM, Switzer CM, Combes SA (2016) Wing wear reduces bumblebee flight performance in a dynamic obstacle course. Biol Lett 12:20160294

    PubMed  PubMed Central  Google Scholar 

  42. Naya DE, Veloso C, Muñoz JLP, Bozinovic F (2007) Some vaguely explored (but not trivial) costs of tail autotomy in lizards. Comp Biochem Physiol Mol Integr Physiol 146:189–193

    Google Scholar 

  43. O’Brien DM, Boisseau RP, Duell M, McCullough E, Powell E, Somjee U, Solie S, Painting C, Emlem DJ (2019) Muscle mass drives cost in sexually selected arthropod weapons. Proc R Soc B 286:20191063

    PubMed  Google Scholar 

  44. Phillipson J (1963) The use of respiratory data in estimating annual respiratory metabolism, with particular reference to Leiobunum rotundum (Latr.) (Phalangiida). Oikos 14:212–223

    Google Scholar 

  45. Pomini AM, Machado G, Pinto-da-Rocha R, Macías-Ordoñez R, Marsaioli AJ (2010) Lines of defense in the harvestman Hoplobunus mexicanus (Arachnida: Opiliones): Aposematism, stridulation, thanatosis, and irritant chemicals. Biochem Syst Ecol 38:300–308

    CAS  Google Scholar 

  46. Powell EC (2020) The evolution and ecology of weapon polymorphic New Zealand harvestmen (Arachnida, Opiliones, Neopilionidae). The University of Auckland, Auckland

    Google Scholar 

  47. Proud DN, Felgenhauer BE, Townsend VR, Osula DO, Gilmore WO, Napier ZL, Van Zandt VA (2012) Diversity and habitat use of Neotropical harvestmen (Arachnida: Opiliones) in a Costa Rican rainforest. ISRN Zool 2012:1–16

    Google Scholar 

  48. R Core Team (2019) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/

  49. Reinhardt L, Blickhan R (2014) Level locomotion in wood ants: evidence for grounded running. J Exp Biol 217:2358–2370

    PubMed  Google Scholar 

  50. Schmitz A (2005) Metabolic rates in harvestmen (Arachnida, Opiliones): the influence of running activity. Physiol Entomol 30:75–81

    Google Scholar 

  51. Schmitz A, Perry SF (2002) Morphometric analysis of the tracheal walls of the harvestmen Nemastoma lugubre (Arachnida, Opiliones, Nemastomatidae). Arthropod Struct Dev 30:229–241

    PubMed  Google Scholar 

  52. Sensenig AT, Shultz JW (2003) Mechanics of cuticular elastic energy storage in leg joints lacking extensor muscles in arachnids. J Exp Biol 206:771–784

    PubMed  Google Scholar 

  53. Sensenig AT, Shultz JW (2006) Mechanical energy oscillations during locomotion in the harvestman Leiobunum vittatum (Opiliones). J Arachnol 34:627–633

    Google Scholar 

  54. Shultz J (2000) Skeletomuscular anatomy of the harvestman Leiobunum aldrichi (Weed, 1893) (Arachnida: Opiliones: Palpatores) and its evolutionary significance. Zool J Linn Soc 128:401–438

    Google Scholar 

  55. Shultz JW, Pinto-da-Rocha R (2007) Morphology and functional anatomy. In: Pinto-da-Rocha R, Machado G, Giribet G (eds) Harvestmen: the biology of opiliones. Harvard University Press, Cambridge, pp 14–61

    Google Scholar 

  56. Somjee U, Woods HA, Duell M, Miller CW (2018) The hidden cost of sexually selected traits : the metabolic expense of maintaining a sexually selected weapon. Proc R Soc B Biol Sci 1:10–12

    Google Scholar 

  57. Starostová Z, Gvoždík L, Kratochvíl L (2017) An energetic perspective on tissue regeneration: the costs of tail autotomy in growing geckos. Comp Biochem Physiol Part A Mol Integr Physiol 206:82–86

    Google Scholar 

  58. Vogel S (2013) Comparative biomechanics: life’s physical world. Princeton University Press, Princeton

    Google Scholar 

  59. Wade RR, Loaiza-Phillips EM, Townsend VR, Proud DN (2011) Activity patterns of two species of neotropical harvestmen (Arachnida: Opiliones) From Costa Rica. Ann Entomol Soc Am 104:1360–1366

    Google Scholar 

  60. Weihmann T (2013) Crawling at high speeds: steady level locomotion in the spider Cupiennius salei-global kinematics and implications for centre of mass dynamics. PLoS ONE 8:e65788

    CAS  PubMed  PubMed Central  Google Scholar 

  61. Weihmann T, Günther M, Blickhan R (2012) Hydraulic leg extension is not necessarily the main drive in large spiders. J Exp Biol 215:578–583

    Google Scholar 

  62. Weinstein RB, Full RJ (1999) Intermittent locomotion increases endurance in a gecko. Physiol Biochem Zool 72:732–739

    CAS  PubMed  Google Scholar 

  63. Willemart RH, Farine JP, Gnaspini P (2009) Sensory biology of Phalangida harvestmen (Arachnida, Opiliones): a review, with new morphological data on 18 species. Acta Zool 90:209–227

    Google Scholar 

  64. Wilshin S, Shamble PS, Hovey KJ, Harris R, Spence AJ, Hsieh ST (2018) Limping following limb loss increases locomotor stability. J Exp Biol 221:174268

    Google Scholar 

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Acknowledgements

We are grateful to T. Daluro for collecting some of the field data, and her support during lab work. We are grateful with R.J. Full for his input on the design of this project, as well as for access to the open-flow respirometry at the Center for Integrative Biomechanics in Education and Research (CiBER) at UC Berkeley. T. Libby wrote the custom MATLAB script use to measure oxygen concentration. A. Saintsing provided extensive support for lab work. Finally, we are grateful to E. Lacey, R. Gillespie, A. Kamath, M. Raboin, members of the Elias Lab, and two anonymous reviewers for their feedback and input on previous versions of this manuscript. This research was done in compliance with institutional animal care protocols.

Funding

Funding for the project was provided by the 2018 program Student Mentoring and Research Teams (SMART) from UC Berkeley’s Graduate Division to I.E. and V.E., the Margaret C. Walker Fund for teaching and research in systematic entomology from the Essig Museum of Entomology at UC Berkeley to I.E, and a grant from the National Science Foundation for D.O.E. (IOS-1556421).

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IE and DOE designed the study. IE and VRE conducted the trials and analyzed the data. IE, VRE, and DOE wrote the manuscript. All authors read and approved the final manuscript.

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Correspondence to Ignacio Escalante.

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Escalante, I., Ellis, V.R. & Elias, D.O. Leg loss decreases endurance and increases oxygen consumption during locomotion in harvestmen. J Comp Physiol A 207, 257–268 (2021). https://doi.org/10.1007/s00359-020-01455-1

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Keywords

  • Autotomy
  • Locomotion energetics
  • Opiliones
  • Respirometry