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Effects of Autotomy and Different Substrates in the Locomotion of Harvestmen in the Genus Prionost

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Effects of Autotomy and Different Substrates in the Locomotion of Harvestmen in the Genus Prionost Losing legs and walking hard: effects of autotomy and different substrates in the locomotion of harvestmen in the genus Prionostemma Author(s): Marisol Domínguez, Ignacio Escalante, Farah Carrasco-Rueda, Cielo E. Figuerola-Hernández, María Marta Ayup, María Natalia Umaña, Daniel Ramos, Arturo González-Zamora, Carolina Brizuela, Willy Delgado and Jessica Pacheco-Esquivel Source: Journal of Arachnology, 44(1):76-82. Published By: American Arachnological Society DOI: http://dx.doi.org/10.1636/J15-08.1 URL: http://www.bioone.org/doi/full/10.1636/J15-08.1 BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder. BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. 2016. Journal of Arachnology 44:76–82 Losing legs and walking hard: effects of autotomy and different substrates in the locomotion of harvestmen in the genus Prionostemma Marisol Domínguez1, Ignacio Escalante2,12, Farah Carrasco-Rueda3,13, Cielo E. Figuerola-Hernández4, María Marta Ayup5, María Natalia Umaña6, Daniel Ramos7, Arturo González-Zamora8,14, Carolina Brizuela9, Willy Delgado10 and Jessica Pacheco-Esquivel11: 1Departamento de Ecología, Genética y Evolución & IEGEBA-CONICET, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina. E-mail: [email protected]; 2Escuela de Biología, Universidad de Costa Rica; 3Center for Conservation, Education and Sustainability, Smithsonian Conservation Biology Institute, National Zoological Park, Washington DC, USA; 4Biology Department, University of Puerto Rico at Río Piedras, San Juan, Puerto Rico; 5Instituto de Ecología Regional, Universidad Nacional de Tucumán, Tucumán, Argentina; 6Department of Plant Biology, Michigan State University, East Lansing, Michigan, USA; 7Universidad Laica Eloy Alfaro de Manabí-Manta. Manta, Ecuador; 8Instituto de Ecología A.C., Xalapa, Veracruz, México; 9Escuela de Ciencias Biológicas, Universidad Nacional, Costa Rica; 10Museo de Historia Natural de la Universidad Nacional de San Agustín de Arequipa, Perú; 11Pontificia Universidad Católica del Ecuador. Pichincha, Ecuador; 12Current address: Department of Environmental Science, Policy, and Management. University of California, Berkeley, USA; 13Current address: School of Natural Resources and Environment, University of Florida, Gainesville, Florida, USA. 14Current address: Instituto de Investigaciones Biológicas, Universidad Veracruzana, Xalapa, Veracruz, Mexico Abstract. Autotomy, the strategy of voluntarily releasing a leg during an encounter with a potential predator or in agonistic interactions between conspecifics, is common in animals. The potential costs of this behavior have been scarcely studied. In addition, locomotion and substrate-dependent performance might be affected by autotomy. We did a comparative and observational study to investigate whether losing legs affects the escape speed and trajectory of harvestmen in the genus Prionostemma Pocock, 1903 (Eupnoi: Sclerosomatidae) on different substrates: soil (the least roughened), smooth bark and mossy bark (the most roughened) in a tropical premontane forest in Costa Rica. We observed that 71% of the individuals found were missing at least one leg. Harvestmen, regardless of leg condition, walked faster and made fewer turns in their trajectory in the soil. While climbing, they were faster on smooth bark than in moss. On all substrates, autotomized individuals were slower and had a more erratic trajectory than intact ones. The type of missing legs (sensory or locomotor) had no influence on the speed or trajectory. We experimentally induced autotomy and found that walking speed on soil decreases if individuals lose a leg. Our findings confirm that losing legs affects locomotion, and we provide novel insights on how locomotion in these harvestmen depends on surface roughness. Our data suggest that moss could be a type of substrate that requires more elaborate skills in balance, orientation and texture recognition than smooth bark. Keywords: Costa Rica, Eupnoi, Opiliones, Sclerosomatidae A wide variety of animals display defense mechanisms in L. vittatum Say, 1821) showed reduction in walking and climb- which a body part or limb is voluntarily released. For instance, ing speed, as well as in foraging ability, after losing up to three geckos (Congdon et al. 1974), lizards (Bellairs & Bryant 1985), legs (Guffey 1999; Houghton et al. 2011). In Holmbergiana scorpions (Mattoni et al. 2015) and sea snails (Lewin 1970) self- weyenberghi Holmberg, 1876 from Uruguay, individuals miss- amputate their tail when they feel threatened; while some crick- ing one sensory leg walked and climbed a log slower than indi- ets (Bateman & Fleming 2005) and spiders (Eisner & Camazine viduals lacking locomotor legs or individuals with all of their 1983) release a leg, a strategy known as autotomy. Autotomy legs (Escalante et al. 2013). These findings suggest that lacking enhances survival because the detached member can distract a sensory legs may confer greater costs in orientation, balance predator allowing the animal to escape (Maginnis 2006). How- and substrate recognition. ever, it may have direct costs in locomotion and the biomecha- Based on the different biophysical properties of the environ- nical performance of animals. ment in which animals are found (Spagna et al. 2007), a sub- Current information about the effect of autotomy on the strate-dependent change in performance is expected. Substrate locomotion of animals suggests long-term costs in locomotion roughness can affect the locomotor performance or walking (Bateman & Fleming 2005; Maginnis 2006; Combes et al. speed of cursorial animals (Spagna et al. 2007; Spence et al. 2010). For example, tail loss in European wall lizards (Podarcis 2010). Spagna et al. (2007) experimentally tested how differ- muralis) increased running speed and distance traveled but ences in a two-dimensional terrain surface affected the decreased their arboreal performance (Brown et al. 1995). running speed and locomotor performance in spiders (Hololena Wrinn & Uetz (2008) studied the effect of autotomy in the adnexa Chamberlin & Gertsch, 1929), crabs (Ocypode quadrata North American wolf spiders Schizocosa ocreata (Hentz, Fabricius, 1787) and cockroaches (Periplaneta americana 1844) and found a reduction in prey capture rates. Harvestmen Linnaeus, 1758). The authors found that animals could attain or “daddy long-legs” (Arachnida: Opiliones) of two Leiobunum high speed even when a substantial percentage of the terrain species from North America (L. nigripes Weed, 1887 and was experimentally removed (they removed up to 90% of the 76 DOMINGUEZ ET AL.—LOCOMOTION: EFFECT OF AUTOTOMY & SUBSTRATE 77 surface contact area in wire mesh), altering the probability of METHODS support and consequently, the stability and speed. All these Study site.—We performed trials in Las Cruces Biological arthropods did this by changing the orientation of their legs Station, San Vito de Coto Brus, Puntarenas province, Costa and using leg spines to improve contact with the surface Rica (8u 479 N, 82u 579 W), between 20–22 January 2012; and (Spagna et al. 2007). In addition, a recent study showed that between 19–21 January 2013. The site is a 300 ha pre-montane a species of beetle (Dendroctonus ponderosae Hopkins, 1902) wet forest reserve (elevation 1200 m; air temperature 13–26 uC; presented better grip walking on smooth bark than on rough 4000 mm annual rainfall). bark of pine trees (Ferrenberg & Mitton 2014). Therefore, com- Field observations and experimental design.—We captured plex, intricate and three-dimensional substrates are expected to advanced juveniles and adult Prionostemma spp. harvestmen impose greater locomotor costs. However, this hypothesis by hand along the Río Java, Melissa and Jungle trails. We remains untested. In our study, we investigated the effects of did not determine the sex of individuals because this could substrate complexity in natural conditions on locomotor per- have stressed them and affected their behavior. A total of 218 formance of harvestmen that either had or had not suffered individuals were located mostly on tree trunks at 1 – 2 m height. an autotomy event. Substrate complexity will ultimately have Manipulation and observations were made during the day important consequences for biomechanical performance and (0900 – 1500 hrs). We placed individuals in plastic cubic fitness. containers (30 x 15 x 15 cm) with wetted cotton, leaves and To achieve this, we tested three substrates commonly used by branches for a minimum of 20 min before trials to acclimate. these harvestmen: soil, smooth bark and mossy bark. These We recorded the number and type of missing legs prior to substrates could be
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