THE FIRST RECORD OF PARASITISM BY FORCIPOMYIA (DIPTERA: CERATOPOGONIDAE) IN CUBAN ODONATES

INTRODUCTION

Adult odonates are the dominant predators in small streams and ponds (Suhling et al., 2015), and a main component of freshwater ecosystems. They are prey of vertebrates, but surprisingly they have no parasitoids, except during the egg stage (e.g. Santolamazza et al., 2011). However, there is a subgenus of biting midge, Pterobosca, genus Forcipomyia, with worldwide distribution, which has 23 species (Borkent and Wirth, 1997; Borkent, 2012), many of them specialised in attacking adult dragonflies. Some other species placed in different subgenera of Forcipomyia are also found on wings of odonates (Borkent, 2012). In Europe, Forcipomyia paludis is known to attack more than 70 species of dragonflies (Martens et al., 2007; Vinko et al., 2017; Cordero-Rivera et al., 2019). In Asia, there are several species associated to odonates like F. latipes, F. fidens (Macfie, 1936a), F. aerobates (Macfie, 1936b), F. tokunagai (Naraoka, 1999) and F. debenhamae (Orr and Cranston, 1997), and a review of pictures of odonates from Cambodia revealed a high incidence of one unidentified species of Forcipomyia (Kosterin et al., 2012). Odonates from Yunnan (China) and from the Fiji islands, have been also observed with Forcipomyia in their wings (A. Cordero Rivera, per. obs). One species has been described from odonates from Aldabra Atoll in the Indian Ocean (Wirth and Ratanaworabhan, 1976). Apparently the subgenus Pterobosca is rare in Africa, with only one species described from Liberia in association with odonates (Macfie, 1926).

In America three species of the subgenus Pterobosca have been recorded, but only one, F. incubans, as a parasite of adult odonates, being common and widespread (Macfie, 1936a; Clastrier and Legrand, 1984, 1990; Marino and von Ellenrieder, 1999; Guillermo-Ferreira and Vilela, 2013). To our knowledge, this interaction between odonates and biting midges has never been recorded in the Antilles.

OBJECTIVES

- We describe the finding of Forcipomyia on the wings of odonates in Cuba.

MATERIALS AND METHODS

From 18-22 June 2017 and 10-13 January 2018, seven localities were visited within the Zapata Swamp in a general survey of Odonata for the region. Odonates were captured with entomological nets, identified in situ, and some voucher specimens were retained and preserved at the Museum Felipe Poey of the University of La Havana, Cuba.

We found that part of the individuals had small Diptera attached to the wings or body. Therefore, we collected a few of these specimens for further identification. The flies were studied at the Scanning Electron Microscopy facilities of Centro de Apoio Científico-Tecnolóxico á Investigación (CACTI, University of Vigo).

The identification of the Odonata species was made through the available specialized bibliography, including Alayo (1968), Needham et al. (2000), Trapero-Quintana and Naranjo López (2004) and Westfall and May (2006). The flies were found to belong to the genus Forcipomyia, which is a worldwide parasite of odonates (Wildermuth and Martens, 2007). We compared the specimens collected with the other species of Forcipomyia known to occur in odonates in America, following Clastrier and Legrand (1984, 1990).

RESULTS

In June 2017, we found a midge belonging to the genus Forcipomyia attached to the wings of libellulids at the Hondones locality, 22.232496 N -81.106734 W (datum WGS84), but not at the other localities sampled. Species parasitized at Hondones locality included Erythrodiplax simplicicollis, E. umbrata, Crocothemis servilia, and Perithemis domitia. All midges were found attached to the wings of the odonates (Fig. 1), but in P. domitia, a midge was found on the thorax (Fig. 1B), which is unusual. In January 2018, we found only one male of P. domitia with one midge, at Maneadero, 22.405980N -81.622298 W (datum WGS84), (Hondones was not sampled). We did not find parasitism on damselflies in both sampling periods. The specimens of Forcipomyia collected match the description of F. (Pterobosca) incubans by Clastrier and Legrand (1984), the most widespread species of this genus parasitizing odonates in the American continent.

DISCUSSION

We report here the first case of biting-midge parasitism on Cuban odonates. Forcipomyia (Pterobosca) incubans is the species commonly found in America associated with Odonata wings, and a predictive model based on habitat characteristics, includes Cuba as a highly probable area for the species (Guillermo-Ferreira and Vilela, 2013). Furthermore, the species reported as being parasitized by F. incubans commonly belong to the genera Erythrodiplax and Erythemis (Marino and von Ellenrieder, 1999; Guillermo-Ferreira and Vilela, 2013), the same that were parasitized in Cuba. However, in some regions, F. incubans may parasitize other libellulids, particularly of the genera Uracis and Orthemis, or even other families like Aeshnidae (Clastrier and Legrand, 1990).

Huerta (2006) reviewed the records of F. incubans on Odonata, and found only two records on a zygopteran, and the majority in Libellulidae. As far as we know, the finding of a midge attached to the thorax of an odonate has not been reported in America. However, this behaviour has been observed in Brazil (Cordero-Rivera, unpublished). Some species of Forcipomyia that parasitize odonates have been found on the thorax of damselflies in Borneo (Orr and Cranston, 1997), and also in Europe (Wildermuth and Martens, 2007). There is one observation of several biting midges attacking an emerging dragonfly in NW Spain, including feeding on the eye and the abdomen of the dragonfly (Cordero-Rivera et al., 2019). Therefore, biting midges may attack other parts of dragonflies and not only the wings, which is the usual behaviour. It remains a future challenge to demonstrate if this interaction has deleterious effects on the odonates, or if the midges are mainly phoretic, as some have suggested (Orr and Cranston, 1997). Detailed observations of the European F. paludis suggest that the midges drain a significant amount of haemolymph and therefore are true parasites (Wildermuth and Martens, 2007), a fact that was assumed by the first students of this interaction (Macfie, 1926).

ACKNOWLEDGMENTS

We thank Yoandis García Correa specialist of Biosphere Reserve Ciénaga de Zapata for guiding us in the reserve. Many thanks to Dennis Paulson for his suggestions to improve our English. Funding was provided by a grant from the Spanish Ministry of Economy and Competitiveness to ACR, which included FEDER funds (CGL2014-53140-P). S.F. was funded by the project PORBIOTA - Portuguese E-Infrastructure for Information and Research on Biodiversity (POCI-01-0145-FEDER-022127), supported by Operational Thematic Program for Competitiveness and Internationalization (POCI), under the PORTUGAL 2020 Partnership Agreement, through the European Regional Development Fund (FEDER). We thank the anonymous reviewers of the manuscript.

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[Recibido: 07 de enero, 2019. Aceptado para publicación: 25 de abril, 2019]