Abstract
Assessing information about prey before attacking is crucial for predators. Whip spiders (Arachnida, Amblypygi) are predatory arachnids that prey mainly on arthropods and whose first pair of legs concentrates many sensory structures. Nonetheless, these aspects of amblypygid biology have been mostly studied in a few species of Phrynidae and basic information about predatory behavior and sensory morphology remain scarce for other families. In this study, we described the sensory morphology of the antenniform leg and the predatory behavior of Charinus asturius Pinto-da-Rocha, Machado and Weygoldt, 2002, a representative of the family Charinidae. We report the presence of most sensilla types described in the better studied Phrynidae and highlight novel aspects such as the morphology of the tarsal organ and the reduced number of rod sensilla. Our behavioral results underscore the importance of antenniform legs in the predatory behavior of C. asturius. Finally, we suggest new avenues to advance the knowledge about the importance of antenniform legs for capturing living prey.
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References
Anjum F, Turni H, Mulder PG, van der Burg J, Brecht M (2006) Tactile guidance of prey capture in Etruscan shrews. PNAS 103:16544–16549. https://doi.org/10.1073/pnas.0605573103
Anton S, Tichy H (1994) Hygro- and thermoreceptors in tip-pore sensilla of the tarsal organ of the spider Cupiennius salei: innervation and central projection. Cell Tissue Res 278:399–407. https://doi.org/10.1007/BF00414182
Beck L, Foelix R, Gödeke E, Kaiser R (1974) Über die Haarsensillen der Geißelspinne Admetus pumilio (Arach., Amblypygi). Naturwissenschaften 61:327–328. https://doi.org/10.1007/BF00599566
Beck L, Foelix R, Gödeke E, Kaiser R (1977) Morphology, larval development, and hair sensilla of the antenniform legs of the whip spider Heterophrynus longicornis Butler (Arach., Amblypygi). Zoomorphologie 88:259–276. https://doi.org/10.1007/BF00995476
Bingman VP, Graving JM, Hebets EA, Wiegmann DD (2017) Importance of the antenniform legs, but not vision, for homing by the neotropical whip spider Paraphrynus laevifrons. J Exp Biol 220:885–890. https://doi.org/10.1242/jeb.149823
Casto P, Gosser J, Wiegmann DD, Hebets EA, Bingman VP (2019) Self-derived chemical cues support home refuge recognition in the whip spider Phrynus marginemaculatus (Amblypygi: Phrynidae). J Arachnol 47:290–292. https://doi.org/10.1636/JoA-S-18-067
Chapin KJ, Hebets EA (2016) The behavioral ecology of amblypygids. J Arachnol 44:1–15. https://doi.org/10.1636/V15-62.1
Cunningham SJ, Castro I, Potter MA (2009) The relative importance of olfaction and remote touch in prey detection by North Island brown kiwis. Anim Behav 78:899–905. https://doi.org/10.1016/j.anbehav.2009.07.015
Dawkins R, Krebs JR (1979) Arms races between and within species. P Roy Soc Lond B Bio 205:489–511. https://doi.org/10.1098/rspb.1979.0081
Delle Cave L (1975) On some sense organs on the first pair of legs of Damon diadema Simon, 1876 (Amblypygi Arachnida). Monitore Zool Ital 9:203–211. https://doi.org/10.1080/00269786.1975.10736253
Dumpert K (1978) Spider odor receptor: electrophysiological proof. Experientia 34:754–756. https://doi.org/10.1007/BF01947305
Ehn R, Tichy H (1994) Hygro- and thermoreceptive tarsal organ in the spider Cupiennius salei. J Comp Physiol A 174:345–350. https://doi.org/10.1007/BF00240216
Fertin A, Casas J (2007) Orientation towards prey in antlions: efficient use of wave propagation in sand. J Exp Biol 210:3337–3343. https://doi.org/10.1242/jeb.004473
FitzGibbon CD (1989) A cost to individuals with reduced vigilance in groups of Thomson’s gazelles hunted by cheetahs. Anim Behav 37:508–510. https://doi.org/10.1016/0003-3472(89)90098-5
Foelix RF (1985) Mechano- and chemoreceptive sensilla. In: Neurobiology of arachnids, vol 67, 2nd edn. Springer, Berlin, Heidelberg, pp 118–137. https://doi.org/10.1007/978-3-642-70348-5_7
Foelix RF, Chu-Wang IW, Beck L (1975) Fine structure of tarsal sensory organs in the whip spider Admetus pumilio (Amblypygi, Arachnida). Tissue Cell 7:331–346. https://doi.org/10.1016/0040-8166(75)90009-9
Forster RR (1980). Evolution of the tarsal organ, the respiratory system and the female genitalia in spiders. In: VIII International Arachnol. Kongr, Vienna
Fowler-Finn KD, Hebets EA (2006) An examination of agonistic interactions in the whip spider Phrynus marginemaculatus (Arachnida, Amblypygi). J Arachnol 34:62–76. https://doi.org/10.1636/S04-104.1
Gainett G, Michalik P, Müller CHG, Giribet G, Talarico G, Willemart RH (2017) Putative thermo-/hygroreceptive tarsal sensilla on the sensory legs of an armored harvestman (Arachnida, Opiliones). Zool Anz 270:81–97. https://doi.org/10.1016/j.jcz.2017.10.004
Gainett G, Sharma PP, Fernandes N, Pinto-da-Rocha R, Giribet G, Willemart RH (2019) Evolution of a sensory cluster on the legs of Opiliones (Arachnida) informs multi-level phylogenetic relationships. Zool J Linn Soc 187:143–165. https://doi.org/10.1093/zoolinnean/zlz016
Garwood RJ, Dunlop JA, Knecht BJ, Hegna TA (2017) The phylogeny of fossil whip spiders. BMC Evol Biol 17:105. https://doi.org/10.1186/s12862-017-0931-1
Hebets EA, Chapman RF (2000) Electrophysiological studies of olfaction in the whip spider Phrynus parvulus (Arachnida, Amblypygi). J Insect Physiol 46:1441–1448. https://doi.org/10.1016/S0022-1910(00)00068-8
Hebets EA, Aceves-Aparicio A, Aguilar-Argüello S, Bingman VP, Escalante I, Gering EJ, Nelsen DR, Rivera J, Sánchez-Ruiz JA, Segura-Hernández L, Settepani V, Wiegmanni DD, Stafstrom JA (2014) Multimodal sensory reliance in the nocturnal homing of the amblypygid Phrynus pseudoparvulus (Class Arachnida, Order Amblypygi)? Behav process 108:123–130. https://doi.org/10.1016/j.beproc.2014.09.014
Hoy JL, Yavorska I, Wehr M, Niell CM (2016) Vision drives accurate approach behavior during prey capture in laboratory mice. Curr Biol 26:3046–3052. https://doi.org/10.1016/j.cub.2016.09.009
Igelmund P (1987) Morphology, sense organs, and regeneration of the forelegs (whips) of the whip spider Heterophrynus elaphus (Arachnida, Amblypygi). J Morphol 193:75–89. https://doi.org/10.1002/jmor.1051930108
Kalko EK (1995) Insect pursuit, prey capture and echolocation in pipestirelle bats (Microchiroptera). Anim Behav 50:861–880. https://doi.org/10.1016/0003-3472(95)80090-5
Klopsch C, Kuhlmann HC, Barth FG (2013) Airflow elicits a spider's jump towards airborne prey II Flow characteristics guiding behaviour. J Roy Soc Interface 10:20120820. https://doi.org/10.1098/rsif.2012.0820
Krause J, Godin JGJ (1995) Predator preferences for attacking particular prey group sizes: consequences for predator hunting success and prey predation risk. Anim Behav 50:465–473. https://doi.org/10.1006/anbe.1995.0260
Ladle RJ, Velander K (2003) Fishing behavior in a giant whip spider. J Arachnol 31:154–156. https://doi.org/10.1636/0161-8202(2003)031[0154:FBIAGW]2.0.CO;2
Mayntz D, Raubenheimer D, Salomon M, Toft S, Simpson SJ (2005) Nutrient-specific foraging in invertebrate predators. Science 307:111–113. https://doi.org/10.1126/science.1105493
Milledge GA (2011) A revision of Storenosoma Hogg and description of a new genus, Oztira (Araneae: Amaurobiidae). Rec Aus Mus 63:1–32. https://doi.org/10.3853/j.0067-1975.63.2011.1579
Mineo MF, Del Claro K (2006) Mechanoreceptive function of pectines in the Brazilian yellow scorpion Tityus serrulatus: perception of substrate-borne vibrations and prey detection. Acta Ethol 9:79–85. https://doi.org/10.1007/s10211-006-0021-7
Miranda GS, Aharon S, Gavish-Regev E, Giupponi APL, Wizen G (2016a) A new species of Charinus Simon, 1892 (Arachnida: Amblypygi: Charinidae) from Israel and new records of C. ioanniticus (Kritscher, 1959). Eur J Taxon 234:1–18. https://doi.org/10.5852/ejt.2016.234
Miranda GS, Milleri-Pinto M, Gonçalves-Souza T, Giupponi APL, Scharff N (2016b) A new species of Charinus Simon 1892 from Brazil, with notes on behavior (Amblypygi, Charinidae). ZooKeys 621:15–36. https://doi.org/10.3897/zookeys.621.9980
Olberg RM (2012) Visual control of prey-capture flight in dragonflies. Curr Opin Neurobiol 22:267–271. https://doi.org/10.1016/j.conb.2011.11.015
Pinto-da-Rocha R, Machado G, Weygoldt P (2002) Two new species of Charinus Simon, 1892 from Brazil with biological notes (Arachnida; Amblypygi; Charinidae). J Nat Hist 36:107–118. https://doi.org/10.3897/zookeys.621.9980
Platnick NI, Abrahim N, Alvarez-Padilla F, Andriamalala D, Baehr BC, Baert L et al (2012) Tarsal Organ Morphology and the Phylogeny of Goblin Spiders (Araneae, Oonopidae), with Notes on Basal Genera. Am Mus Novit 3736:1–52. https://doi.org/10.1206/3736.2
Raven RJ, Stumkat K, Gray MR (2001) Revisions of Australian ground-hunting spiders: I. Amauropelma gen. nov. (Araneomorphae: Ctenidae). Rec West Aust Mus Suppl 64:187. https://doi.org/10.18195/issn.0313-122x.64.2001.187-227
Rhebergen F, Taylor RC, Ryan MJ, Page RA, Halfwerk W (2015) Multimodal cues improve prey localization under complex environmental conditions. Proc Roy Soc Lond B Bio 282:20151403. https://doi.org/10.1098/rspb.2015.1403
Riggins JJ, Hoback WW (2005) Diurnal tiger beetles (Coleoptera: Cicindelidae) capture prey without sight. J insect Behav 18:305–312. https://doi.org/10.1007/s10905-005-3691-5
Santer RD, Hebets EA (2007) Agonistic signals received by an arthropod filiform hair allude to the prevalence of near-field sound communication. Proc Roy Soc B-Bioll Sci 275:363–368. https://doi.org/10.1098/rspb.2007.1466
Santer RD, Hebets EA (2009) Prey capture by the whip spider Phrynus marginemaculatus CL Koch. J Arachnol 37:109–112. https://doi.org/10.1636/st07-139.1
Santer RD, Hebets EA (2011a) The sensory and behavioural biology of whip spiders (Arachnida, Amblypygi). In: Spider physiology and behaviour, 1st edn, vol 41. Elsevier, pp 1–64. https://doi.org/10.1016/B978-0-12-415919-8.00001-X
Santer RD, Hebets EA (2011b) Evidence for air movement signals in the agonistic behaviour of a nocturnal arachnid (order Amblypygi). PLoS ONE 6:e22473. https://doi.org/10.1371/journal.pone.0022473
Segovia JMG, Del-Claro WR (2015) Delicate fangs smart killing. Anim Behav 101:169–177. https://doi.org/10.1016/j.anbehav.2014.12.025
Segovia JMG, Neco L, Willemart R (2018) On the habitat use of the Neotropical whip spider Charinus asturius (Arachnida: Amblypygi). Zoologia 35:e12874. https://doi.org/10.3897/zoologia.35.e12874
Seiter M, Lemell P, Gredler R, Wolff JO (2019) Strike kinematics in the whip spider Charon sp. (Amblypygi: Charontidae). J Arachnol 47:260–265. https://doi.org/10.1636/JoA-S-18-089
Souza ES, Willemart RH (2011) Harvest-ironman: heavy armature, and not its defensive secretions, protects a harvestman against a spider. Anim Behav 81:127–133. https://doi.org/10.1016/j.anbehav.2010.09.023
Tagliatela J, Gallão JE, Bichuette ME (2019) Repertório comportamental de Charinus mysticus Giupponi & Kury 2002. Speleo tema 29:57–63
Talarico G, Palacios-Vargas JG, Silva MF, Alberti G (2005) First ultrastructural observations on the tarsal pore organ of Pseudocellus pearsei and P. boneti (Arachnida, Ricinulei). J Arachnol 33:604–612. https://doi.org/10.1636/04-110.1
Talarico G, Palacios-Vargas JG, Fuentes Silva M, Alberti G (2006) Ultrastructure of tarsal sensilla and other integument structures of two Pseudocellus species (Ricinulei, Arachnida). J Morphol 267:441–463. https://doi.org/10.1002/jmor.10415
Toft S (1999) Prey choice and spider fitness. J Arachnol 27:301–307
Walsh RE, Rayor LS (2008) Kin discrimination in the amblypygid, Damon diadema. J Arachnol 36:336–343. https://doi.org/10.1636/CSt07-138.1
Weygoldt P (1995) A whip spider that ate rolled oats, with observations on prey-capture behaviour in whip spiders. Newsl Br Arachnol Soc 74:6–8. https://doi.org/10.1636/ST07-139.1
Weygoldt P (1996) Evolutionary morphology of whip spiders: towards a phylogenetic system (Chelicerata: Arachnida: Amblypygi). J Zool Syst Evol Res 34:185–202. https://doi.org/10.1111/j.1439-0469.1996.tb00825.x
Weygoldt P (2000) Whip spiders (Chelicerata, Amblypygi). Apollo Books
Weygoldt P (2002a) Fighting, courtship, and spermatophore morphology of the whip spider Musicodamon atlanteus Fage, 1939 (Phrynichidae) (Chelicerata, Amblypygi). Zool Anz 241:245–254. https://doi.org/10.1078/0044-5231-00072
Weygoldt P (2002) Reproductive biology of Phrynichus dhofarensis Weygoldt, Pohl & Polak, 2002 (Chelicerata, amblypygi, phrynichidae). Zool Anz 241:305–315. https://doi.org/10.1078/0044-5231-00074
Weygoldt P (2003) Reproductive biology of two species of Phrynichus, P. exophthalmus Whittick, 1940 and P. deflersi arabicus nov. ssp. (Chelicerata: Amblypygi). Zool Anz 242:193–208. https://doi.org/10.1078/0044-5231-00097
Weygoldt P (2008) Spermatophores, female genitalia, and courtship behaviour of two whip spider species, Charinus africanus and Damon tibialis (Chelicerata: Amblypygi). Zool Anz 247:223–232. https://doi.org/10.1016/j.jcz.2007.12.002
Wignall AE, Taylor PW (2009) Alternative predatory tactics of an araneophagic assassin bug (Stenolemus bituberus). Acta Ethol 12:23–27. https://doi.org/10.1007/s10211-008-0049-y
Acknowledgements
We thank Thaiany Costa for her assistance with preparing the material for SEM. The technicians Phillip Lenktaitis and Sheila Carmo helped us photographing the specimens. G. Murayama, J. Fadil and the staff of the Parque Estadual de Ilhabela: Agnaldo, Betinho, Bicudo, Ivomar, Marcos, Pernambuco and Esmérida helped us during the field work. We are very grateful to Alex Damico for providing us lodging during the field trip and Gustavo Miranda for reading an early draft of this manuscript. We also thank two anonymous reviewers for providing comments that helped us to improve this manuscript.
Funding
This study was financially supported by CAPES and Fundação de Amparo à Pesquisa do Estado de São Paulo (São Paulo Research Foundation, FAPESP): Proc. 2014/19191-3 to JMGS and 2015/01815-9 to RH.W, CNPq 302879/2016-1 to RHW.
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Segovia, J.M.G., Gainett, G. & Willemart, R.H. Predatory behavior and sensory morphology of the whip spider Charinus asturius (Arachnida: Amblypygi). J Ethol 38, 273–280 (2020). https://doi.org/10.1007/s10164-020-00648-0
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DOI: https://doi.org/10.1007/s10164-020-00648-0