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First evidence of parasitation of a Bosmina (Cladocera) by a water mite larva in a karst sinkhole, in Quintana Roo (Yucatán Peninsula, México)

Montes-Ortiz, Lucia1 ; Goldschmidt, Tom 2 and Elías-Gutiérrez, Manuel3

1✉ El Colegio de la Frontera Sur, Avenida Centenario km 5.5, Chetumal 77014, Quintana Roo, México.
2Zoologische Staatssammlung, Münchhausenstraβe 21, D-81247 München, Germany.
3El Colegio de la Frontera Sur, Avenida Centenario km 5.5, Chetumal 77014, Quintana Roo, México.

2019 - Volume: 59 Issue: 1 pages: 111-114

https://doi.org/10.24349/acarologia/20194315

Short note

Keywords

water mites parasitism Cladocera behavior SEM

Abstract

For the first time a parasitic relationship between a water mite larva and a Cladocera is found and documented by scanning electron microscope (SEM) imaging. A Unionicolidae larva (cf. Unionicola) has been found attached to a Bosmina tubicen (Cladocera) collected in a karst sinkhole (cenote) in the southeast of the Yucatán Peninsula (México).


Introduction

Water mites have a complex life cycle compose by three active stages: larva, deutonymph and adult and three resting stages: prelarva, protonymph and tritonymph plus the egg (Smith, 1988; Smith et al., 2010). The majority of water mite larvae parasitize adult insects, whereas the free living deutonymphs and adults – with few exceptions – are predators feeding on insect larvae and microcrustacea (Smith and Oliver, 1986; Proctor et al., 2015; Martin, 2005). In general, the hexapod larvae actively seek an appropriate host and become an ectoparasite, which is passively transported while feeding on host fluids. The parasitic / phoretic phase has great importance not only for nutrition, but as well for dispersal of the water mite larvae (Smith and Oliver, 1986; Martin, 2005; Proctor et al., 2015). A host-specific association has been well documented between many water mite larvae and nearly all major groups of aquatic insects as Diptera (mainly Chironomidae), Odonata, Plecoptera, Hemiptera, Coleoptera and Trichoptera (Smith and Oliver, 1986; Martin, 2004). So far, no parasitic relationship with Cladocera has been documented, though deutonymphs and adults of several water mite groups (including the Unionicolidae) can be considered as predators of cladocerans (Proctor and Pritchard, 1989; Proctor et al., 2015). However larva and host range of many taxa is still unknown and a lot of undescribed species (and behavioral patterns) can still be expected – especially, but not only in the tropics (Proctor et al. 2015).

The observations we present, and document by SEM-images, will certainly contribute to increase the knowledge of larval water mite behavior.

Material and methods

During a faunistic survey of zooplankton composition (Montes-Ortiz and Elías-Gutiérrez, 2018) in the karst sinkhole Cenote Azul (Quintana Roo, México), we found a water mite larva attached to a cladoceran. The specimens were fixed in 96% ethanol and dehydrated subsequently in an ethanol series of 30%, 40%, 50%, 60%, 70%, 80%, 90% and 100% for 15 minutes. The dehydrated sample were critical point dried and gold-coated to be observed under a Scanning Electron Microscope (JEOL-JSM6010) at 10kV (Elías-Gutiérrez et al., 2008).

Results and Discussion

The water mite larva was tentatively identified as Unionicola sp. (Unionicolidae) (Prasad and Cook, 1972; Smith et al. 2010; pers. comm. M. Vidrine); the Cladocera could be identified as Bosmina tubicen Brehm, 1953 previously found in the area by Elías-Gutiérrez et al. (2008). The SEM pictures clearly show, that the water mite larva is attached to the lateral side of the valve of the cladoceran (most probably parasitizing) (Figs. 1 and 2) – a behavior never reported for water mite larvae so far.

Figure 1. Water mite larva (Unionicola sp.) attached to a water flea (Bosmina tubicen). The scale bar indicates 50 μm.

The observation is especially remarkable, as so far, the larvae of Unionicolidae are known to parasitize the adult stages of Diptera (Chironomidae) and Trichoptera, and in most cases investigated up to now a defined host specificity has been found (Proctor et al. 2015). Although, recently, the exceptional case of a trichopteran larva as host of Unionicola larvae has been reported by Martin and Tempelman (2014). Rare similar findings have so far been interpreted as accidental or pure phoretic ("pre-parasitic") associations. However, the authors emphasize that the association they found has to be interpreted as truly parasitic, as the water mite larvae were typically engorged, and suggests evidence for an alternative life cycle of the respective water mite species (Martin and Templemann, 2014). Additionally, Buczyńska et al., (2015) reported the finding of water mite larvae (Tiphys torris) attached to a Trichoptera pupa. As well in this case the authors pointed out that the water mite larvae were truly parasitic as they were enlarged. However, in this case the authors interpreted their findings as rather accidental caused by an extended lack of access to a proper host (Buczyńska et al., 2015).

Proctor et al. (2015) indicate that the opportunities to contact a host occur irregularly in space and time. In this sense, Collins (1975) reported that 75% of Wandesia thermalis Viets, 1938 larvae fail to locate a host in a system where the distribution of it is clustered and unpredictable.

Consequently, a possible explanation for the unusual association reported here is that the larva did not find an appropriate host and therefore attached to the Cladocera. Though Chironomidae (a registered host for Unionicola) are an abundant and diverse group in the system (Montes-Ortiz y Elías-Gutiérrez, 2018). Another explanation for the documented finding could be that the larva has attacked the cladocera in order to feed on it for a short time before the continuation of its search for a proper host – a behavior as well never documented. Even though the larva is not enlarged, clear traces of the attack are visible (Fig. 2A).

Figure 2. A – Lateral view of the Unionicola larva, frontal view on the Bosmina. B – Close up of perforations made by pedipalps and chelicerae of the water mite in the valve of the water flea. Scale bars indicate 50 μm.

In both possible cases the discovery reported here provides an important contribution to the extension of the existing concept and knowledge on water mite life cycles and their interaction with other members of the invertebrate fauna. Furthermore it has to be emphasized, that the knowledge and understanding of water mite life cycles is still fragmentary and even more limited in the tropics.

Acknowledgments

This finding was made as part of the Doctoral studies of the first author at El Colegio de la Frontera Sur, supported by the fellowship 2018-000012-01NACF-07816 from the National Council of Science and Technology (CONACYT). This is a contribution financed by the Mexican Network of barcodes of life (MEXBOL – grant 271108). The SEM images presented here were obtain in the Barcoding Laboratory Chetumal Node of MEXBOL in El Colegio de la Frontera Sur. Malcome Vidrine (USA), Reinhard Gerecke (Germany) and Peter Martin (Germany) contributed valuable information on the water mite larva.

References

Buczyńska E., Buczyński P., Zawal A., Michoński G., Szlauer-Łukaszewska A. 2015. First record of parasitism of water mite larva (Acari:Hydrachnidia) on the pupa of Trichoptera. Acta Parasitol.60(2): 196-199. doi:10.1515/ap-2015-0028

Collins N.C. 1975. Tactics of host explotation by a thermophilic water mite. Misc. Publ. Entomol. Soc. Am. 9: 359-370.

Elías-Gutiérrez M., Suárez-Morales E., Gutiérrez-Aguirre M., Silva-Briano M., Granado-Ramírez J., Garfias-Espejo T. 2008. Cladócera y Copépoda de las aguas continentales. CONABIO, UNAM, Mexico: 322 pp.

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Martin P., Tempelman D. 2014. An unusual association between water mite larvae (Hydrachnidia, Acari) and a larval caddis fly host (Trichoptera). Lauterbornia 77: 15-21.

Montes-Ortiz L., Elías-Gutiérrez M. 2018. Faunistic survey of the zooplankton community in an oligotrophic sinkhole, Cenote Azul (Quintana Roo, Mexico), using different sampling methods, and documented with DNA barcodes. J. Limnol. 77 (3). doi:10.4081/jlimnol.2018.1746

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Proctor H.C., Smith I.M., Cook D.R., Smith B.P. 2015. Subphylum Chelicerata, Class Arachnida. In: Thorp, J., Rogers, D.C. (Eds.), Ecology and General Biology: Thorp and Covich´s Freshwater Invertebrates, Academic Press, 599- 660.

Smith B.P. 1988. Host-parasite interaction and impact of larval water mites on insects. Ann. Rev. Entomol. 33: 487-507. doi:10.1146/annurev.en.33.010188.002415

Smith I.M., Oliver D.R. 1986. Review of parasitic associations of larval water mites (Acari: Parasitengona: Hydrachnida) with insect host. Can. Entomol. 118: 407- 472. doi:10.4039/Ent118407-5

Smith I.M., Cook D.R., Smith B.P. 2010. Water mites (Hydrachnidiae) and other arachnids. In: Thorp, J.H., Covich, A.P. (Eds), Ecology and Classification of North American Freshwater Invertebrates. Third ed. Academic Press (Elsevier), .485-586.



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Article editorial history
Date received:
2018-10-08
Date accepted:
2019-01-29
Date published:
2019-02-08

Edited by:
Auger, Philippe

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License
2019 Montes-Ortiz, Lucia; Goldschmidt, Tom and Elías-Gutiérrez, Manuel
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