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First host record of Epipompilus (Hymenoptera: Pompilidae) from Brazil and discussion of prey carriage mechanism

ABSTRACT

We register for first time the occurrence of Epipompilus tucumanus Evans, 1967 in Brazil, and record the spider Ariadna boliviana Simon, 1907 as its host. The observations were made in the National Park of Chapada dos Guimarães, Mato Grosso, Brazil. The prey carriage mechanism is described for first time for this genus, and we provide a video showing this behavior.

Keywords
Behavior; Brazilian Cerrado; Host association; Segestriidae; Spider wasp

The spider wasp genus Epipompilus Kohl, 1884 comprises 51 species, 17 of which occur in the Neotropical Region and 34 in the Australian Region (Evans, 1953Evans, H.E., 1953. Comparative ethology and the systematics of spider wasps. Syst Zool 2, 155-172.; Elliot, 2007Elliot, M.G., 2007. Annotated catalogue of the Pompilidae (Hymenoptera) of Australia. Zootaxa 1428, 1-83.). The biology of this genus is poorly known, and prey has been reported for only two species: E. insularis Kohl, 1884 (Pollard, 1982Pollard, S.D., 1982. Epipompilus insularis (Hymenoptera: Pompilidae), a parasitoid of hunting spiders. New Zeal J Zool 9, 37-39.; Harris, 1987Harris, A.C., 1987. Pompilidae (Insecta: Hymenoptera). Fauna of New Zealand 12, 1-154.) and E. platensis (Roig-Alsina and Barneche, 2017Roig-Alsina, A., Barneche, J., 2017. The genus Epipompilus in Argentina (Hymenoptera: Pompilidae). Rev Soc Entomol 76, 33-38.). Six spider families have been reported up to now as Epipompilus host: Clubionidae, Desidae, Heteropodidae, Salticidae, Sparassidae and Segestriidae (Evans, 1972Evans, H.E., 1972. Revision of the Australian and New Guinean species of Epipompilus (Hymenoptera: Pompilidae). Pac Insects 14, 101-131.; Pollard, 1982Pollard, S.D., 1982. Epipompilus insularis (Hymenoptera: Pompilidae), a parasitoid of hunting spiders. New Zeal J Zool 9, 37-39.; Harris, 1987Harris, A.C., 1987. Pompilidae (Insecta: Hymenoptera). Fauna of New Zealand 12, 1-154.; Shimizu, 1994Shimizu, A., 1994. Phylogeny and classification of the family Pompilidae. Tokyo Metropolitan University Bulletin of Natural History 2, 1-142.; Roig-Alsina and Barneche, 2017Roig-Alsina, A., Barneche, J., 2017. The genus Epipompilus in Argentina (Hymenoptera: Pompilidae). Rev Soc Entomol 76, 33-38.).

Evans (1967)Evans, H.E., 1967. Studies on neotropical Pompilidae (Hymenoptera) III. Additional notes on Epipompilus Kohl. Breviora 273, 1-15, Available from: http://biostor.org/reference/4267.
http://biostor.org/reference/4267...
describes Epipompilus tucumanus from Tucuman and Jujuy (Argentina) in Chacoan biogeographical province, and also from San Esteban, Venezuela, at the Venezuelan biogeographical province. Evans (1976)Evans, H.E., 1976. Studies on Neotropical Pompilidae (Hymenoptera). X. Supplementary notes. Psyche 83, 263-270. added another locality from Buena Vista in Santa Cruz, Bolivia, at Rondonian biogeographical province.

On March 28, 2016, around 11 AM, at the National Park of Chapada dos Guimarães, MT, Brazil (-15.4069° -55.8239°, 610m asl.) (Fig. 1), two of us (B.M.T. and V.M.L.) observed a female of E. tucumanus (Fig. 2) carrying a cursorial spider on a trail inside the Cerrado sensu stricto. According to Morrone (2014)Morrone, J.J., 2014. Biogeographical regionalisation of the Neotropical region. Zootaxa 3782, 001-110. this site is located in the Cerrado biogeographical province, Chacoan sub-region, and Chacoan dominion. The climate of this region is classified by Köppen into Tropical with dry winter (Aw) (Alvares et al., 2013Alvares, C.A., Stape, J.L., Sentelhas, P.C., Gonçalves, J.L.M., Sparovek, G., 2013. Köppen's climate classification map for Brazil. Meteorol Z 22, 711-728.). The wasp was collected and deposited in the Hymenoptera collection of the Museu de Biodiversidade (MuBio), Universidade Federal da Grande Dourados (UFGD), Mato Grosso do Sul State, Brazil (voucher number Hym-00191-P). The spider was determined by Dr. Antônio D. Brescovit, and deposited in the arachnid's collection of the Instituto Butantan, São Paulo State, Brazil (voucher number IBSP-211845).

Fig. 1
Collecting localities of Epipompilus tucumanus Evans, 1967 in South America, with biogeographic provinces (Morrone, 2014Morrone, J.J., 2014. Biogeographical regionalisation of the Neotropical region. Zootaxa 3782, 001-110.), including the type locality and Evans (1976)Evans, H.E., 1976. Studies on Neotropical Pompilidae (Hymenoptera). X. Supplementary notes. Psyche 83, 263-270. record. Highlighting the Chapada dos Guimarães National Park limits, with our collecting point (red star).

Fig. 2
E. tucumanus ♀ lateral habitus.

We sent pictures of the specimen collected in Chapada dos Guimarães to Dr. Arturo Roig-Alsina for identification, and we compared it with the images of the holotype available at https://mczbase.mcz.harvard.edu/guid/MCZ:Ent:31320. We agree that the specimen is a variation of E. tucumanusEvans (1967)Evans, H.E., 1967. Studies on neotropical Pompilidae (Hymenoptera) III. Additional notes on Epipompilus Kohl. Breviora 273, 1-15, Available from: http://biostor.org/reference/4267.
http://biostor.org/reference/4267...
. It differs from Evans's description by the followings characters: 1- the ivory-white spot is present only on the scape (Fig. 3), Evans (1967)Evans, H.E., 1967. Studies on neotropical Pompilidae (Hymenoptera) III. Additional notes on Epipompilus Kohl. Breviora 273, 1-15, Available from: http://biostor.org/reference/4267.
http://biostor.org/reference/4267...
comments that such spots are present on the first three antennal segments; 2- the mesoscutum is wholly black, without ferruginous midline posteriorly (Fig. 4); 3- the whitish band on the posterior margin of the pronotum has no rufous border (Figs. 3 and 4); 4- the first gastral segment and the basal ⅔ of tergum II are ferruginous, with the remainder black (Fig. 5); 5- the whitish markings on meso- and hindtibiae are reduced on the outer and the inner surface (Fig. 6); 6- the clypeus is 2.0× as wide as its median length (Fig. 7); 7- the middle interocular distance equals 0.51× width of the head (Fig. 7); 8- the lower interocular distance is equal to 0.9× of the upper one (Fig. 7); 9- unlike the holotype, our specimen has oval white spots between the antennal lobes and eyes (Fig. 8). In view of these differences possibly the specimen represents an undescribed species.

Fig. 3
E. tucumanus ♀ dorsal view of head and thorax.

Fig. 4
E. tucumanus ♀ thorax in lateral view.

Fig. 5
E. tucumanus ♀ metasoma in dorsolateral view.

Fig. 6
E. tucumanus ♀ hind tibia.

Fig. 7
E. tucumanus ♀ frontal view of head.

Fig. 8
E. tucumanus ♀ front ventral view of head.

The spider captured by E. tucumanus is an adult female of Ariadna boliviana Simon, 1907 (Araneae: Segestriidae) (Figs. 9 and 10), and this is the first prey record for E. tucumanus. The genus Ariadna (Segestriidae) was recently registered as host of Epipompilus platensis from Argentina (Roig-Alsina and Barneche, 2017Roig-Alsina, A., Barneche, J., 2017. The genus Epipompilus in Argentina (Hymenoptera: Pompilidae). Rev Soc Entomol 76, 33-38.). This spider is nocturnal, sedentary and usually lives in silk tubes constructed in trunk or rock holes (Capocasale, 1998Capocasale, R.M., 1998. Arañas del Uruguay, VIII. Contribución al conocimiento de Segestria ruficeps Guérin (Araneae, Segestriidae). Comunicaciones Zoológicas del Museo de Historia Natural de Montevideo 190, 1-12.; Grismado, 2008Grismado, C.J., 2008. A taxonomic revision of the spider genus Ariadna Audouin, 1826 in Argentina and Chile, with the description of five new species (Arachnida, Araneae, Segestriidae). Zoosystema 30, 333-360.). Ariadna Audouin, 1826 occurs on all continents except Antarctica, and A. boliviana is known from Brazil, Bolivia, Suriname and Paraguay (Giroti, 2013Giroti, A.M., (Ph.D. thesis) 2013. Revisão taxonômica das aranhas neotropicais do gênero Ariadna Audouin, 1826 (Araneae Segestriidae), Universidade de São Paulo, São Paulo, Brasil, 146pp.).

Fig. 9
Ariadna boliviana dorsal view.

Fig. 10
Ariadna boliviana ventral view.

Epipompilus tucumanus, as other spider wasps, uses the mandibles for prey carrying. The wasp drags the spider walking sideways and sometimes backwards, mostly keeping it by the spinnerets, but also can hold the prey by the legs or chelicera to overcome obstacles in the leaf litter like twigs and stones (Videos 1 and 2).

The prey carriage mechanism is similar in Dipogon Fox, 1897 (Pompilidae), in which prey carriage occurs backwards and sideways, also the way these wasps hold their prey (Evans and Yoshimoto, 1962Evans, H.E., Yoshimoto, C.M., 1962. The ecology and nesting behaviour of the Pompilidae of the Northeastern United States. Misc Publ Ent Soc Amer 3, 67-119.; Kurczewski et al., 2017Kurczewski, F.E., Edwards, G.B., Pitts, J.P., 2017. Hosts, nesting behavior, and ecology of some North American spider wasps (Hymenoptera: Pompilidae), II. Southeast Nat 16, 1-82.). Evans (1962)Evans, H.E., 1962. The evolution of prey-carrying mechanism in wasps. Evolution 16, 468-483. classifies this behavior as a variation of Mandibular Mechanism type One (M1): simply grasp the host with their mandibles on any convenient part of the body and drag it backwards into a hole. Genise (1980)Genise, J.F., 1980. Evolución de mecanismos de transporte de presas en avispas. Reclasificación de los tipos mandibulares y esquema evolutivo general. Rev Soc Entomol Arg 39, 19-36. comments that this variant hardly is a transition between different kinds of prey carriage mechanisms, and that carriage behavior is related to the prey size and weight, proposing an exclusive variant for mandibular carriage mechanism type (Variant 5).

The maternal behavior varies significantly in Epipompilus. Pollard (1982)Pollard, S.D., 1982. Epipompilus insularis (Hymenoptera: Pompilidae), a parasitoid of hunting spiders. New Zeal J Zool 9, 37-39. and Harris (1987)Harris, A.C., 1987. Pompilidae (Insecta: Hymenoptera). Fauna of New Zealand 12, 1-154. observed in New Zealand that E. insularis oviposit on the spider's body immediately after having paralyzed it (the paralysis is very light and short); no transportation to a nest was observed. After laying the egg the wasp moves away and the spider retakes its normal activities until the wasp larva kills it. Evans (1953)Evans, H.E., 1953. Comparative ethology and the systematics of spider wasps. Syst Zool 2, 155-172. expressed the sequence of behavior stated for E. insularis by the formula VPO (Venari = to hunt; Pungere = to sting the prey; Ovum parere = to lay the egg) or VO, and expressed the opinion that such ethological sequences represents primitive conditions within Aculeata. In contrast, E. tucumanus showed a more complex ethological sequence that should be described as VPTOC (Venari; Pungere; Transferre = to carry the prey; Ovum parere; Claudere = to close the cell); this last formula applies to every species of Pompilidae that carries its host to a nest and enclosures it in a cell. Evans (op. cit.) thought that VPTOC is the most primitive behavioral sequence within Pompilidae, and that VPO could be derived from VPTOC.

Acknowledgments

We sincerely thanks Dr. Arturo Roig-Alsina for species identification; Dr. Antônio D. Brescovit for spider identification, and Dr. Wojciech Pulawski for review the manuscript; the researchers Isabelli L. T. de Jesus, Larissa T. da Silva and Vander Carbonari for their field assistance; ICMBio's staff from Parque Nacional da Chapada dos Guimarães, for the holding in the field. Collect license number: ICMBio 51296-1. B.M.T. is supported by CAPES, process number: PDSE 88881.131920/2016-01.

Appendix A Supplementary data

Supplementary data associated with this article can be found, in the online version, at doi: 10.1016/j.rbe.2018.08.003.

References

  • Alvares, C.A., Stape, J.L., Sentelhas, P.C., Gonçalves, J.L.M., Sparovek, G., 2013. Köppen's climate classification map for Brazil. Meteorol Z 22, 711-728.
  • Capocasale, R.M., 1998. Arañas del Uruguay, VIII. Contribución al conocimiento de Segestria ruficeps Guérin (Araneae, Segestriidae). Comunicaciones Zoológicas del Museo de Historia Natural de Montevideo 190, 1-12.
  • Elliot, M.G., 2007. Annotated catalogue of the Pompilidae (Hymenoptera) of Australia. Zootaxa 1428, 1-83.
  • Evans, H.E., 1953. Comparative ethology and the systematics of spider wasps. Syst Zool 2, 155-172.
  • Evans, H.E., 1962. The evolution of prey-carrying mechanism in wasps. Evolution 16, 468-483.
  • Evans, H.E., 1967. Studies on neotropical Pompilidae (Hymenoptera) III. Additional notes on Epipompilus Kohl. Breviora 273, 1-15, Available from: http://biostor.org/reference/4267
    » http://biostor.org/reference/4267
  • Evans, H.E., 1972. Revision of the Australian and New Guinean species of Epipompilus (Hymenoptera: Pompilidae). Pac Insects 14, 101-131.
  • Evans, H.E., 1976. Studies on Neotropical Pompilidae (Hymenoptera). X. Supplementary notes. Psyche 83, 263-270.
  • Evans, H.E., Yoshimoto, C.M., 1962. The ecology and nesting behaviour of the Pompilidae of the Northeastern United States. Misc Publ Ent Soc Amer 3, 67-119.
  • Genise, J.F., 1980. Evolución de mecanismos de transporte de presas en avispas. Reclasificación de los tipos mandibulares y esquema evolutivo general. Rev Soc Entomol Arg 39, 19-36.
  • Giroti, A.M., (Ph.D. thesis) 2013. Revisão taxonômica das aranhas neotropicais do gênero Ariadna Audouin, 1826 (Araneae Segestriidae), Universidade de São Paulo, São Paulo, Brasil, 146pp.
  • Grismado, C.J., 2008. A taxonomic revision of the spider genus Ariadna Audouin, 1826 in Argentina and Chile, with the description of five new species (Arachnida, Araneae, Segestriidae). Zoosystema 30, 333-360.
  • Harris, A.C., 1987. Pompilidae (Insecta: Hymenoptera). Fauna of New Zealand 12, 1-154.
  • Kurczewski, F.E., Edwards, G.B., Pitts, J.P., 2017. Hosts, nesting behavior, and ecology of some North American spider wasps (Hymenoptera: Pompilidae), II. Southeast Nat 16, 1-82.
  • Morrone, J.J., 2014. Biogeographical regionalisation of the Neotropical region. Zootaxa 3782, 001-110.
  • Pollard, S.D., 1982. Epipompilus insularis (Hymenoptera: Pompilidae), a parasitoid of hunting spiders. New Zeal J Zool 9, 37-39.
  • Roig-Alsina, A., Barneche, J., 2017. The genus Epipompilus in Argentina (Hymenoptera: Pompilidae). Rev Soc Entomol 76, 33-38.
  • Shimizu, A., 1994. Phylogeny and classification of the family Pompilidae. Tokyo Metropolitan University Bulletin of Natural History 2, 1-142.

Edited by

Associate Editor: James Carpenter

Publication Dates

  • Publication in this collection
    Oct-Dec 2018

History

  • Received
    15 June 2018
  • Accepted
    20 Aug 2018
  • Published
    3 Sept 2018
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