SHORT COMMUNICATION

Inverted roles: Spider predation upon Neotropical velvet worms

(Epiperipatus spp.; Onychophora: Peripatidae)

 

Rosmery Franco1 and Julián Monge-Nájera2

1. Departamento de Biología, Universidad de Pamplona, Pamplona, Norte de Santander, Colombia, rosmeryf402@gmail.com

2. Laboratorio de Ecología Urbana, Universidad Estatal a Distancia (UNED), 2050 San José, Costa Rica; julianmonge@gmail.com

Received 27-VI-2016 • Corrected 15-VII-2016 • Accepted 25-VII-2016

Abstract: Velvet worms are ancient predators with Cambrian origins that occasionally prey on Ctenid spiders. Here we report the opposite case: wolf spiders (Ctenus spp.) feeding on Epiperipatus spp. in Colombia and Costa Rica. Apparently the worms could not expel their defensive adhesive, and the efficacy of the spider venom suggests that onychophoran nerves and muscles are biochemically equivalent to those of insects.

 

Key words: Predatory behavior, Neotropical invertebrates, spider venom and onychophorans.

Velvet worms are ancient predators with a fossil record that extends 515 million years to the Cambrian (Monge Nájera & Ho, 1999; 2000). It is unknown how −and if− they hunted under water in tidal mudflats, but the adhesive net they currently use for defense and to hunt does not function in seawater (Monge-Nájera, Barrientos & Aguilar, 1993; Concha et al., 2015). They are eaten by birds and snakes and even fish during Amazon floods (Monge-Nájera, Barrientos & Aguilar, 1993), and in turn they prey on spiders (Read & Hughes, 1987; Dias & Lo-Man-Hung, 2009). Here we report two cases of the opposite interaction: Ctenid spiders feeding on onychophorans in Colombia and Costa Rica.

The observations were done in two reserves, Tamá and La Selva. Parque Nacional Natural Tamá, Colombia (7° 02’ - 7° 27’ N, 72° 02’ - 72° 28’ W) has an unknown biodiversity of onychophorans and is covered by tropical cloud forest, Andean forest and paramo (MAVDT, 2008). La Selva Biological Station, Costa Rica (10°25’19”N, 84°00’54” W) has onychophorans of the genus Epiperipatus and includes primary and secondary lowland rainforest (McGlynn & Kelley, 1999).

At 19:00 hours, January 27, 2011, the first author photographed a female wolf spider (Ctenus sp.) eating an immobilized velvet worm, Epiperipatus sp. (Peripatidae, Figure 1).

The spider held the worm against a leaf and was eating the rear end. The skin of that part had already been digested and a dark band, possibly the intestine, was partly visible. The worm’s body was twisted, so the rear end’s ventral side was upwards. In the front part there were some markings (perhaps wounds), a drop of urine in the fourth right leg and no signs of defensive glue expelling. The antennae were bent downwards, suggesting that the animal was dead (Figure 1).

The other case was observed by Joseph Warfel in La Selva, near May 2003 or 2004. The spider (Ctenus sp.) was feeding on a dead Epiperipatus sp., about 1.5 m above ground (Figure 2). Some external digestion is seen in the middle of the body.

Like spiders, velvet worms have external digestion, which has the evolutionary value of reducing body weight and functioning under water (Hernández-García, Martín & Castro, 2000). We do not know why the spiders started digestion of these prey in the middle of the body instead of the rear or head.

Why do onychophorans hunt dangerous predators such as Theraphosid and Ctenid spiders (Read & Hughes, 1987; Dias & Lo-Man-Hung, 2009) and are feared by Opiliones (Cook, Smith, Proud, Víquez, & Townsend, 2013)? Perhaps the amount of nutrition justifies the risk and these particular onychophorans, which hunt at night guided by olfaction and touch, were unlucky and attacked too large prey (see an informal report by Read, 1985). But the absence of expelled defensive adhesive in both cases suggests that the worms were attacked by surprise.

The chemical composition and action of Ctenus venoms are poorly known (Okamoto et al., 2009) but the efficacy of the spider’s venom suggests that the worm’s nerves and muscles are biochemically equivalent to those of insects, which are only distantly related to velvet worms.

Curiously, velvet worms have inspired an unexpected number of cartoons (Monge-Nájera, & Morera-Brenes, 2015) and there is one imagining a different outcome of a worm/spider encounter (http://goo.gl/gXTsw8). We hope this note inspires others to record any cases of predation related to these poorly known worms.

ACKNOWLEDGMENTS

We thank Carlos Víquez (INBio) for identifying the spiders, Joseph Warfel for the excellent photograph in Fig. 2; Lawrence Millman for his help and Bernal Morera for the worms’ identification and guidance.

REFERENCES

Concha, A., Mellado, P., Morera-Brenes, B., Costa, C. S., Mahadevan, L., & Monge-Nájera, J. (2015). Oscillation of the velvet worm slime jet by passive hydrodynamic instability. Nature communications, 6: 6292.

Cook, D. R., Smith, A. T., Proud, D. N., Víquez, C., & Townsend Jr, V. R. (2013). Defensive responses of Neotropical harvestmen (Arachnida, Opiliones) to generalist invertebrate predators. Caribbean Journal of Science, 47(2-3), 325-334.

Dias, Sidclay C., & N. F. Lo-Man-Hung. (2009): “First record of an onychophoran (Onychophora, Peripatidae) feeding on a theraphosid spider (Araneae, Theraphosidae).” Journal of Arachnology, 37 (1), 116-117.

Hernández-García, V., Martín, A. Y., & Castro, J. J. (2000). Evidence of external digestion of crustaceans in Octopus vulgaris paralarvae. Journal of the Marine Biological Association of the UK, 80(03), 559-560.

MAVDT. (2008). Parque Nacional Natural Tamá: Plan de Manejo 2006 – 2010. Bogotá: Ministerio de Ambiente, Vivienda y Desarrollo Territorial.

McGlynn, T. P., & Kelley, C. D. (1999). Distribution of a Costa Rican wet forest velvet worm (Onychophora: Peripatidae). Annals of the Entomological Society of America, 92(1), 53-55.

Monge-Nájera, J., Barrientos, Z., & Aguilar, F. (1993). Behavior of Epiperipatus biolleyi (Onychophora: Peripatidae) under laboratory conditions. Revista de Biología Tropical, 41(3 A), 689-696.

Monge-Nájera, J., & Hou, X. (1999). 500 Millones de años de evolución: onicóforos, los primeros animales que caminaron (Onychophora). Boletín SEA, 26, 171-178.

Monge-Nájera, J., & Hou, X. (2000). Disparity, decimation and the Cambrian” explosion”: comparison of early Cambrian and Present faunal communities with emphasis on velvet worms (Onychophora). Revista de Biología Tropical, 48(2-3), 333-351.

Monge-Nájera, J., & Morera-Brenes, B. (2015). Velvet Worms (Onychophora) in Folklore and Art: Geographic Pattern, Types of Cultural Reference and Public Perception. British Journal of Education, Society & Behavioural Science, 10(3), 1-9.

Okamoto, C. K., Queiroz, G. P., Gutierrez, V. P., de Almeida, D. M., Cury, Y., Bertani, R., Okamoto, C. K., Queiroz, G. P., Gutierez, V. P., de Almeida, D. M., Cury, Y., Bertani, R., & Tambourgi, D. V. (2009). Ctenus medius and Phoneutria nigriventer spiders venoms share noxious proinflammatory activities. Journal of Medical Entomology, 46(1), 58-66.

Read, M. (1985). Stalking the Collared Peripatus. Natural History, 94 (9), 56.

Read, VM St J. & R. N. Hughes. (1987): “Feeding behaviour and prey choice in Macroperipatus torquatus (Onychophora).” Proceedings of the Royal Society of London B: Biological Sciences, 230 (1261), 483-506.

Resumen: Papeles invertidos: arañas depredadoras de gusanos de terciopelo neotropicales (Epiperipatus spp.; Onychophora: Peripatidae). Los gusanos de terciopelo (Onychophora) son antiguos depredadores de origen cámbrico que ocasionalmente consumen arañas cténidas. Aquí informamos el caso contrario: arañas (Ctenus spp.) alimentándose de gusanos onicóforos (Epiperipatus spp.) en Colombia y Costa Rica. Aparentemente las presas no lograron expulsar su red defensiva y la eficacia del veneno de araña sugiere que los nervios y músculos de los onicóforos son bioquímicamente equivalentes a los de los insectos.

 

Palabras clave: Comportamiento depredador, invertebrados neotropicales, veneno de araña y onicóforos.