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Resting Metabolic Rates of Two Orbweb Spiders: a first Approach to Evolutionary Success of Ecribellate Spiders

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Resting Metabolic Rates of Two Orbweb Spiders: a first Approach to Evolutionary Success of Ecribellate Spiders Journal of Insect Physiology 57 (2011) 427–432 Contents lists available at ScienceDirect Journal of Insect Physiology journal homepage: www.elsevier.com/locate/jinsphys Resting metabolic rates of two orbweb spiders: A first approach to evolutionary success of ecribellate spiders Tatiana Hideko Kawamoto a,b,*, Fabio de A. Machado c,1, Gustavo E. Kaneto d,2, Hilton F. Japyassu ´ e a Laborato ´rio de Artro ´podes do Instituto Butantan, Av. Vital Brazil, 1500, Butantan, Sa ˜o Paulo, SP 05503-000, Brazil b Programa de Po ´s-graduac¸a˜o em Psicologia Experimental, Instituto de Psicologia da Universidade de Sa ˜o Paulo, Sa ˜o Paulo, SP, Brazil c Laborato ´rio de Herpetologia/Morfometria, Museu de Zoologia da USP, Av. Nazare ´, 481, Ipiranga, Sa ˜o Paulo, SP 04263-000, Brazil d Laborato ´rio de Ecofisiologia e Fisiologia Evolutiva, Departamento de Fisiologia, Instituto de Biocie ˆncias da USP, Rua do Mata ˜o, 321 – Travessa 14, Cidade Universita ´ria, Sa ˜o Paulo, SP 05508-900, Brazil e Instituto de Biologia/UFBA, NuEVo – Nu ´cleo de Etologia e Evoluc¸a˜o, Rua Bara ˜o de Geremoabo, s/n, Campus Universita ´rio de Ondina, Salvador, BA 40170-115, Brazil ARTICLE INFO ABSTRACT Article history: Spiders are considered conservative with regard to their resting metabolic rate, presenting the same Received 11 September 2010 allometric relation with body mass as the majority of land-arthropods. Nevertheless, web-building is Received in revised form 4 January 2011 thought to have a great impact on the energetic metabolism, and any modification that affects this Accepted 4 January 2011 complex behavior is expected to have an impact over the daily energetic budget. We analyzed the Available online 6 January 2011 possibility of the presence of the cribellum having an effect on the allometric relation between resting metabolic rate and body mass for an ecribellate species ( Zosis geniculata ) and a cribellate one ( Metazygia Keywords: rogenhoferi ), and employed a model selection approach to test if these species had the same allometric Araneidae relationship as other land-arthropods. Our results show that M. rogenhoferi has a higher resting Energetics Likelihood metabolic rate, while Z. geniculata fitted the allometric prediction for land arthropods. This indicates that Metabolism the absence of the cribellum is associated with a higher resting metabolic rate, thus explaining the higher Uloboridae promptness to activity found for the ecribellate species. If our result proves to be a general rule among spiders, the radiation of Araneoidea could be connected to a more energy-consuming life style. Thus, we briefly outline an alternative model of diversification of Araneoidea that accounts for this possibility. ß 2011 Elsevier Ltd. All rights reserved. 1. Introduction Spiders are typically sit-and-wait foragers remaining motion- less most of the time, a condition which stresses the importance of All living organisms use many energy-consuming processes to the resting metabolic rate in their life cycle. Food availability limits stay alive and reproduce. On the one hand, metabolic rates vary and shapes the ecology and behavior of spiders ( Wise, 1993 ), with changes of environmental and physiological conditions; on affecting several life history traits such as reproduction ( Eberhard, the other hand, metabolic rates pose limits to physiological 1979 ), web building ( Pasquet et al., 1994; Sandoval, 1994 ), changes and environmental interactions. In this way, metabolic sociality ( Rypstra, 1985; Kim, 2000 ) and growth ( Vollrath, rates have important ecological and evolutionary consequences 1985 ). Spiders may have evolved adaptations to unpredictable (Garland and Carter, 1994; Chown, 2001 ), and have often been and low prey availability ( Greenstone and Bennett, 1980 ), a evoked in discussions about physiological ecology and evolution- condition that would perfectly match their alleged low resting ary physiology ( Reinhold, 1999 ). metabolic rates ( Anderson, 1970 ). However, Lighton et al. (2001) argued that spiders actually have a metabolism that is very similar to that of other land-arthropods. Overall, it was shown that the arthropod resting metabolic rate could be considered extremely * Corresponding author. Present address: Laborato ´ rio Ecofisiologia e Fisiologia Evolutiva, Departamento de Fisiologia, Instituto de Biocieˆncias da USP, Rua do conservative, and that a general allometric rule between body Mata˜o, 321 – Travessa 14, Cidade Universita ´ria, Sa˜o Paulo, SP 05508-900, Brazil. mass and resting metabolic rate could be modeled for all land Tel.: +55 11 30917609/37267222; fax: +55 11 30918095. arthropods, except for tarantulas ( Shillington, 2005 ), scorpions and E-mail addresses: [email protected] (T.H. Kawamoto), ticks ( Lighton et al., 2001 ). [email protected] , [email protected] (F.d.A. Machado), [email protected] One important source of effects on energetic metabolism is the (G.E. Kaneto), [email protected] (H.F. Japyassu ´ ). 1 Tel.: +55 11 20658130; fax: +55 11 82631029. execution of energetically costly behaviors ( Reinhold, 1999 ), an 2 Tel.: +55 11 3091 7609. aspect particularly neglected in the study of spider physiology. 0022-1910/$ – see front matter ß 2011 Elsevier Ltd. All rights reserved. doi: 10.1016/j.jinsphys.2011.01.001 428 T.H. Kawamoto et al. / Journal of Insect Physiology 57 (2011) 427–432 Despite the fact that spiders are sit-and-wait foragers, a typical metabolism and body mass of a cribellate and an ecribellate economic foraging strategy as mentioned above, they are able to species, and employed a model selection approach to explore the exhibit some behaviors with important impacts in their daily allometric relation between these variables compared to the energetic budget ( Watson and Lighton, 1994 ). Among web prediction for land arthropods ( Lighton et al., 2001 ). Finally, we weavers, the web building behavior is the main energetic briefly discuss the relevance of our findings to the understanding of expenditure, thus any modification that affects the cost of web diversity within the clade of orbweavers. Ecribellate orbweavers building should be expected to have metabolic impact on the (Araneoidea) comprise 27.8% of the total number of spider species organism, probably influencing the energetic budget and other (Platnick, 2010 , catalog version 10.5), and all attempted explana- significant aspects of the spiders’ life, such as reproduction and tions to this huge diversity ( Lubin, 1986; Eberhard, 1989; Craig survival rate ( Angilletta et al., 2003 ). The loss of the cribellate silk is et al., 1994; Ko¨hler and Vollrath, 1995; Opell et al., 2006 ) have been probably one of these modifications. contentious in one way or another ( Lubin, 1986; Craig and The cribellum is a modification of the anterior median Freeman, 1991; Craig and Ebert, 1994; Opell, 1996, 1998; spinnerets into one or two small flat plates densely covered with Watanabe, 1999; Zschokke, 2002; Li et al., 2004; Bruce et al., tiny spigots which, together with the calamistrum, a row of strong 2005 ). Based on our findings, we present a new model that could bristles on the metatarsus of leg IV, produce the cribellate silk explain the radiation of orbweb spiders. (Foelix, 1996 ). Even though the cribellate spiders were originally considered a separate group which followed an evolutionary path 2. Methods parallel to ecribellate spiders, resulting in numerous convergences (Shear, 1986 ), recent phylogenetic studies have shown that the 2.1. Species cribellum is, in fact, plesiomorphic for all extant spiders and most groups exhibit a secondary loss of this character ( Lehtinen, 1967; We chose Zosis geniculata (Olivier, 1789; Uloboridae) and Coddington and Levi, 1991; Griswold et al., 1999 ). The production Metazygia rogenhoferi (Keyserling, 1878; Araneidae) as represen- of the cribellate orbweb is more expensive than the production of tatives of the cribellate and ecribellate orb weavers, respectively. an ecribellate orbweb: while ecribellate webs are adhesive due to The choice was based on several criteria that enhance compara- an aqueous, diluted glue, the cribellate silk is constituted of bility between these species. For example, they have a similar adult numerous tiny proteic fibrils that need to be repeatedly ‘‘combed’’ body size and overall shape, they spin similar-sized orb webs in order to produce the capture spiral ( Peters, 1987 ). Cribellate (Fig. 1 ), both species do not show univoltine life cycle and their spiders also reingest their webs less frequently than ecribellate orb families are at the base of the sister clades Deinopoidea (cribellate) weavers. Indeed, it was shown that there is a significant difference and Araneoidea (ecribellate), thus minimizing the effects of these in energy economy of web building and maintenance of viscid characteristics on the variables being analyzed. Furthermore, in orbwebs when compared to cribellate orbwebs (e.g. Opell, 1996, order to control for sexual dimorphism and ontogeny we analyzed 1998 ). Finally, cribellate spiders seem to be more reluctant to only adult females. abandon their webs than ecribellate spiders, even when submitted We analyzed ten individuals of M. rogenhoferi and twenty to low prey availability, suggesting that the energetic and individuals of Z. geniculata . Specimens from both species were behavioral commitment to web building is greater in cribellate collected in the city of Sa˜o Paulo. Adult females were brought to the animals ( Kawamoto, 2007; Kawamoto and Japyassu ´ , 2007 ). lab and kept inside individual acrylic boxes (31 cm  31 cm  In the present work we investigate the possibility that the 12 cm) in a room with a 12:12 light cycle and small temperature behavioral and physiological differences associated with the (24–26 8C) and humidity (76–81% UR) variation. Many M. presence or absence of the cribellum have an effect on the resting rogenhoferi specimens died in the first week at the laboratory [()TD$FIG]metabolic rate of spiders. In order to do that we measured resting due to nematoid or fungus parasitism. After this first week Fig. 1. Zosis geniculata (a) and Metazygia rogenhoferi (b), scale 3 mm. Drawings based on photographs of webs of Z. geniculata (c) and M.
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