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Culicidae y Ceratopogonidae (Diptera: Nematocera) que habitan en fitotelmata en el Parque Nacional Iguazu, provincia de Misiones, Argentina subtropical.

Culicidae and Ceratopogonidae (Diptera: Nematocera) inhabiting phytotelmata in Iguazu National Park, Misiones Province, subtropical Argentina

INTRODUCTION

Phytotelmata are aquatic microenvironments formed by accumulation of water in any part of the body of plants such as leaves, flowers, stems or trunks (Frank & Lounibos, 1983). The communities of organisms that live in them are composed mainly of insects, immature stages of Diptera being dominant (Fish, 1983). The fact that phytotelmata are easy to handle small pools of water which allow to design experiments in natural conditions could account for the various studies carried out on them. Furthermore, some phytotelmata are important habitats that produce mosquito vectors of human diseases (Frank et al., 1988; O'Meara et al., 1995). The phytotelmata of Argentina have not been explored in depth, and only a few studies related to the invertebrate community living therein have been published. The first one was conducted in the subtropical region of Corrientes province, regarding the Bromeliaceae Aechmea distichantha Lemaire (Torales et al., 1972); it described the physical and chemical characteristics of water, provided an inventory of invertebrates, and highlighted the presence of immature stages of four species of mosquitoes, three of Culex L. and one of Phoniomyia Theobald (nowadays a subgenus of Wyeomyia Theobald). The remaining studies were conducted in temperate areas of Buenos Aires Province: Vucetich & Rossi (1980) described the chemical characteristics of water in the axils of Eryngium pandanifolium Cham & Schltdl. (Apiaceae) and presented a list of the micro-organisms collected. Balseiro (1983) made observations on the selectivity of plants as oviposition sites of Culex castroi Casal & Garcia. Marti et al. (2007) studied the seasonality of the immature stages of the culicid Isostomyia paranensis Brethes living in the axils of the Cyperaceae Scyrpus giganteus Kunth. Campos & Lounibos (1999) studied the host-plant specificity, seasonality and population dynamics of Culex castroi, Culex hepperi Casal & Garcia, and Culex renatoi Lane & Ramalho. In a recent study, Campos (2010) analyzed the macro invertebrate community and food chains of four species of Eryngium L. phytotelmata. Finally, Montero et al. (2010) studied whether there are differences in species richness, species composition and feeding guild structure between environments (sun and shade) and micro habitats (among or on foliage) of bromeliads. Moreover, they studied whether these differences are similar between seasons.

The knowledge of Ceratopogonidae breeding in phytotelmata in Argentina is scarce, and is mostly limited to isolated citations or descriptions of preimaginal stages that were found in these habitats. Within the haematophagous genus Culicoides Latreille, Ronderos & Spinelli (1990) recorded adults of C. nigrigenus Wirth & Blanton collected in A. distichantha in Salta province, and Ronderos & Spinelli (2000) described the immatures of C. bambusicola Lutz from internodes of the bamboo Guadua trinii (Nees) Ness ex Ruprecht in northern Corrientes and Misiones provinces, Ronderos et al. (2008) of C. charruus Spinelli & Martinez from Eryngium pandanifolium in Buenos Aires province, and Ronderos et al. (2010) of C. debilipalpis Lutz from treeholes in Entre Rios province. Spinelli & Rodriguez (1999) described Dasyhelea necrophila on the basis of material collected from flower vases plant-holding containers in La Plata cemetery; the species was found several times in other artificial containers, and likely breeds in phytotelmata in nature. Nothing is known about phytotelmatic ceratopogonids in Iguazu National Park.

Studies in Argentina are quite limited with regard to regions and types of phytotelmata. In this study, we present a list of phytotelmata of Iguazu National Park, located in the subtropical area of Argentina, and its culicid and ceratopogonid inhabitants.

MATERIAL AND METHODS

A field study was conducted from 2005 through 2007 in Iguazu National Park (25[degrees] 39' S, 54[degrees] 18' W), a subtropical area of Argentina. The park, in the Paranense forest ecoregion (Dinerstein et al., 1995), is located in the northern extreme of Misiones Province, separated from Brazil by the Iguazu River. The topography and drainage pattern of this ecoregion are the typical ones of a basaltic plateau, reaching altitudes of 700m. The annual rainfall varies between 1,500 and 2,000 mm, the dry season takes place in winter and the rainy season in summer. The mean temperature varies between 16[degrees]C in winter and 22[degrees]C in summer, and the dominant vegetation is the typical subtropical forest (APN, 2009).

All phytotelmata except bamboos were sampled by extracting the fluid contents with a pipette attached to a lift pump. After the first extraction, plants were flushed twice with clean tap water, and the aquatic contents extracted with a pipette after each wash. Samples from bamboo were taken by making a hole with a drill in the middle of the internodes, and extracting the content with a tube connected to a lift pump. After the extraction of the sample, the internodes were washed twice with clean water. Stumps (internodes opened after the falling of a bamboo) and broken bamboos were sampled with the same tube and lift pump used for internodes. All insects were killed in the field with 70% commercial ethyl alcohol, and preserved in 80% ethyl alcohol, except some immature dipterans which were carried alive to the laboratory to be reared individually and identified. Culicidae were classified and identified following Lane (1953 a, b), Darsie (1985), and Harbach (2007), and Ceratopogonidae following several publications containing keys and original descriptions of immatures which may be found in Borkent & Spinelli (2007).

RESULTS

Phytotelmata. Fourteen types of phytotelmata were identified in the park. Twelve are native and two introduced, as follows: bamboo Guadua trinii; Guadua chacoensis (Rojas) Londono & Peterson; Merostachys clausseni Munro (Poaceae); bromeliads Aechmea distichantha Lemaire; Aechmea recurvata (Klotzsch), L. B. Sm.; Billbergia nutans Wendl. ex Regel; Pseudananas sagenarius (Arruda) Camargo; Vriesea friburgensis Mez. (Bromeliaceae), False Caraguata Eryngium sp. (Apiaceae), elephant ear Alocasia odora (Lindl.) Hoch; Philodendron bipinnatifidum Schott ex Endl. (Araceae); brave nettles Urera baccifera (L.) Gaudich. Ex Wedd. (Urticaceae); Maranta sp. (Marantaceae), and the palmettos Euterpe edulis Mart. (Arecaceae) of which P. sagenarius and A. odora are introduced.

Only nine classes of phytotelmata host immatures of Culicidae and Ceratopogonidae (Tables I and II). Bamboos, treeholes and floral bracts of Euterpe edulis are woody phytotelmata. E. edulis produces phytotelmata when the bracts fall to the ground. The remaining phytotelmata are herbaceous and belong to Apiaceae, Araceae and Bromeliaceae.

No culicids or ceratopogonids were collected from the introduced plants (P. sagenarius and A. odora), or from A. recurvata, Maranta sp., and U. baccifera. Of these plants, four other than U. baccifera hold water in their leaf axils. Urera baccifera is the least known as phytotelmata. It is a shrub with spiny and hairy stems usually 1 to 2 m high (maximum 5m), and a cavity capable of containing water is formed in the stems when they break. The hole is small (about 1-2cm in diameter) but because the stems are hollow, the depth can be equal to the length of the branch.

Culicidae (Table I). Immatures were collected from 9 native phytotelmata. Twenty six species grouped into 10 genera were collected. Five species belong to Toxorhynchitinae, 21 to Culicinae, and no species of Anophelinae were recorded. Culicinae was represented by 14 species of Sabethini, five of Culicini and two of Aedini, all of them native except Aedes aegypti L.

The highest species richness (n = 10) was recorded from G. chacoensis, followed by G. trinii and A. distichantha (n = 6); M. clausseni and E. edulis (n = 4); and P. bipinnatifidum, V friburguensis, Eryngium sp. and treeholes (n = 2).

All species living in the fallen bracts of E. edulis, belonging to Limatus Theobald, Trichoprosopon Theobald, Wyeomyia, and Culex were found exclusively in that phytotelm. This makes E. edulis the phytotelm with the highest number of exclusive species. On the other hand, all species that inhabit Eryngium spp. belong to a single subgenus, Culex (Phytotelmatomyia) Rossi & Harbach.

The low number of species found in treeholes (n = 1) could be attributed to the fact that this habitat was scarcely explored in the present study (n = 1), in comparison to the other phytotelmata.

Wyeomyia was the best represented genus in the phytotelmata of Iguazu. Of the 11 collected species of this genus (Table I), four were not identified. Two of them were collected in abundance (n > 60) from the internodes of both Guadua bamboo, but adults were not obtained from the reared immatures. Although the other two species, collected from the axils of P. bipinnatifidum and internodes of M. clausseni, were reared and adults were obtained, they could not be identified as any known species from the region.

Ceratopogonidae (Table II). Immatures of Ceratopogonidae were collected from seven native phytotelmata, represented by nine species grouped in six genera. Three species belong to Forcipomyiinae, five to Ceratopogoninae and one to Dasyheleinae.

The highest species richness (n = 5) was recorded from treeholes, following by G. chacoensis, (n = 3); A. distichantha (n = 2) and E. pandanifolium, V friburgensis, G. trinii and M. clausseni (n = 1). The community of ceratopogonids that live in treeholes exhibits not only the greatest richness in species, but also in genera (n = 4).

Culicoides bambusicola Lutz was the most ubiquitous species, being present in treeholes, bamboo, and bromeliads, contrasting with its congener C. paranensis (Goeldi), collected only from treeholes.

DISCUSSION

Culicidae. The community of mosquitoes that inhabits phytotelmata of the subtropical region of Argentina is mainly dominated by species of Sabethini, contrasting with the temperate region where Culicini species are predominant (Campos & Lounibos, 1999; Campos, 2010). This difference could be attributed to the high diversity of phytotelmata of the subtropics in contrast to the temperate region.

It is worth pointing out the close association between species of the subgenus Culex (Phytotelmatomyia) with Eryngium species, and the fact that they have not been found inhabiting other phytotelmata. On the other hand, it is also remarkable that Eryngium is not attractive for species of other genera of mosquitoes. The strong association between mosquitoes of the subgenus C. (Phytotelmatomyia) and Eryngium plants is reaffirmed by our observations in Iguazu Park, where Eryngium spp. co-inhabit with bromeliads, and E. edulis houses species of Culex that belong to other subgenera.

On the basis of the finding of immatures of Toxorhynchites guadalupensis (Dyar & Knab) in internodes of Guadua bamboo during this study, the geographical distribution and host plants of this species is extended. It was previously reported from the northwestern Provinces of Catamarca, Jujuy, Salta and Tucuman (Mitchell & Darsie, 1985) from axils of A. distichantha (Augier et al., 2003). It is also herein extended the range of host plants of Wyeomyia muhlensis (Petrocchi) and Microculex imitator Theobald, which had been cited previously only from A. distichantha (Torales et al., 1972), and Culex chaguanco Casal, Garcia & Fernandez, that were collected previously from treeholes (Casal et al., 1968). In this study, we collected immature stages of W. muhlensis and C. chaguanco from bracts of E. edulis, and M. imitator from axils of V friburguensis.

Only two invasive species of Aedini are known in Argentina, both residents of phytotelmata, A. aegypti and Aedes albopictus (Skuse). Aedes aegypti was found breeding in axils of P bipinnatifidum as well as in artificial containers in Iguazu National Park. Aedes albopictus was not encountered during this study, although this species has been found in the nearby city of Iguazu, breeding in axils of Bromeliaceae (Rossi et al., 1999). Aedes albopictus inhabits bromeliads, as well as treeholes in Florida, USA (Hawley, 1988; O'Meara et al., 1995), and Brazil (Cunha et al., 2002), and its invasion in Argentina forests needs extreme caution and further monitoring.

Ceratopogonidae. Several species of ceratopogonids of Culicoides, Dasyhelea Kieffer, Forcipomyia Meigen, and other genera are known to develop in phytotelmata in the Neotropical region (e.g.: Roger, 1964; Yanoviak, 1999; Spinelli et al., 2007), but only Culicoides spp. and Dasyhelea spp. were reported from such habitats in Argentina (e.g.: Ronderos & Spinelli, 1990; Spinelli & Rodriguez, 1999). Most of the ceratopogonid larvae from the Neotropical region were collected from bromeliads and treeholes (e.g.: Yanoviak, 1999, Ospina-Bautista et al., 2004), and a few from other less known phytotelmata (e.g.: Fish & Soria, 1978; Vitale, 1977; Campos, 2010).

A study carried out in Panama (Vitale, 1977) showed that bromeliads, treeholes and water-containing bamboo internodes are the phytotelmata where the species of Culicoides occur more frequently other than in Heliconia L. (Musaceae) Xanthosoma Schott (Araceae) leaf axils, and Costus L. (Costaceae) inflorescences as well as in a water holding palm frond. In accordance with Vitale (1977), during this study the species of Culicoides were mainly collected from treeholes and bamboo internodes, and to a lesser extent from other phytotelmata. Vitale (1977) also collected larvae of the predaceous midges genera Bezzia Kieffer and Palpomyia Meigen from bromeliads, whereas during this study species of both genera were collected from treeholes. Moreover, Palpomyia guarani Lane was collected from bamboo internodes.

Observations made by other authors (Vitale, 1977; Fish & Soria, 1978; Ronderos & Spinelli, 2000; Ronderos et al., 2010), as well as during this study, show that the species of Stilobezzia whose larvae inhabit phytotelmata have a tendency to select woody plants (dendrotelmata) as their breeding site. Species of Dasyhelea and Atrichopogon Kieffer, meanwhile, prefer herbaceous plants, while species of Bezzia, Culiciodes, Forcipomyia and Palpomyia live in woody and herbaceous plants. More intensive research is needed in order to confirm specificity between species of midges and their host plants.

ACKNOWLEDGEMENTS

We acknowledge the authorities of Administracion de Parques Nacionales, Delegacion Regional Noreste (APN), and Centro de Investigaciones Ecologicas Subtropicales (CIES), for logistic help and granting of permissions. This study is dedicated to the memory of Monica Camposano, who gave us her warm hospitality during our stay at the CIES. We also thank Eduardo Lestani for providing collected Ceratopogonidae, Patricio Ramirez Llorens for leading us through the labyrinthine paths of the forest, Justo Herrera for his help in plants identification and Monica Caviglia for English review. This research was supported by an International Cooperation Project D 1369 from Consejo Nacional de Investigaciones Cientificas y Tecnicas (CONICET), Argentina, and Researcher Exchange Program, Japan Society for the Promotion of Science (JSPS), Japan. This is a contribution of the Instituto de Limnologia Journal Series No 900.

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CAMPOS Raul E. * ****, Gustavo SPINELLI** **** and Motoyoshi MOGI***

* Instituto de Limnologia "Dr. Raul A. Ringuelet", Universidad Nacional de La Plata CONICET, CC 712 (1900) La Plata, Buenos Aires, Argentina; e-mail: rcampos@ilpla.edu.ar

** Division de Entomologia, Museo de Ciencias Naturales de La Plata. Paseo del Bosque s/no. (1900) La Plata, Buenos Aires Argentina; e-mail: spinelli@museo.fcnym.unlp.edu.ar

*** Division of Parasitology, Department of Pathology and Biodefence, Faculty of Medicine, Saga University, Nabeshima 5-1-1, Saga 849-8501, Japan; e-mail: motomogi@festa.ocn.ne.jp

**** Consejo Nacional de Investigaciones Cientificas y Tecnicas (CONICET)
Table I. Culicidae and host phytotelmata at Iguazu National Park,
Misiones Province, Argentina. a: leaf axil, b: fallen floral
bract, i: internode, s: stump.

Subfamily--Tribe   Species                        Phytotelmata

Toxorhynchitinae   Toxorhynchites (Lynchiella)    A. distichantha (a)
                    bambusicolus (Lutz & Neiva)   G. chacoensis (i)
                   Toxorhynchites (Lynchiella)    G. chacoensis (i)
                     guadalupensis (Dyar &
                     Knab)
                   Toxorhynchites (Lynchiella)    A. distichantha (a)
                     solstitialis (Lutz)          V. friburgensis (a)
                   Toxorhynchites (Lynchiella)    M. clausseni (i)
                     theobaldi (Dyar & Knab)
                   Toxorhynchites sp.             A. distichantha (a)
Culicinae
  Sabethini        Limatus durhamii Theobald      E. edulis (b)
                   Runchomyia reversa             G. chacoensis (i)
                     (Lane & Cerqueira)           G. trinii (s)
                   Sabethes (Sabethes)            Treehole
                     albiprivus Theobald
                   Sabethes (Sabethinus)          M. clausseni (i)
                     aurescens (Lutz)             G. chacoensis (i)
                   Sabethes (Sabethinus)          G. chacoensis (i)
                     identicus Dyar & Knab
                   Trichoprosopon                 E. edulis (b)
                     (Trichoprosopon)
                     compressum Lutz
                   Trichoprosopon                 G. trinii (s)
                     (Trichoprosopon)             M. clausseni (s)
                     pallidiventer (Lutz)         A. distichantha (a)
                   Wyeomyia (Dendromyia)          P. bipinnatifidum (a)
                     belkini Casal & Garcia
                   Wyeomyia (Phoniomyia)          E. edulis (b)
                     muhlensis (Petrocchi)
                   Wyeomyia (Phoniomyia)          A. distichantha (a)
                     quasilongirostri Theobald.
                   Wyeomyia (Wyeomyia)            G. chacoensis (i)
                     codiocampa Dyar & Knab       G. trinii (i)
                   Wyeomyia (Wyeomyia)            A. distichantha (a)
                     limai Lane & Cerqueira       M. clausseni (i)
                   Wyeomyia (Wyeomyia) sabethea   G. chacoensis (i)
                     Lane & Cerqueira             G. trinii (i)
                                                  M. clausseni (i)
                   Wyeomyia (Wyeomyia)            G. chacoensis (i)
                     serrata Lutz
                   Wyeomyia sp. 1                 G. chacoensis (i)
                                                  G. trinii (i)
                   Wyeomyia sp. 2                 G. chacoensis (i)
                                                  G. trinii (i)
                   Wyeomyia sp. 3                 P. bipinnatifidum (a)
                   Wyeomyia sp. 4                 M. clausseni (i)
  Culicini         Culex (Phytotelmatomyia)       Eryngium sp.
                     castroi Casal & Garcia
                   Culex (Phytotelmatomyia) sp.   Eryngium sp.
                   Culex (Anoedioporpa)           E. edulis (b).
                     chaguanco Casal,
                     Garcia & Fernandez
                   Microculex imitator Theobald   A. distichantha (a)
                                                  V. friburgensis (a)
  Aedini           Aedes (Stegomyia) aegypti L.   P. bipinnatifidum (a)
                   Haemagogus (Conopostgeus)      Treeholes
                     leococelaenus (Dyar &
                     Shannon)

Table II. Ceratopogonidae and host phytotelmata at Iguazu
National Park, Misiones Province, Argentina. a: leaf axil,
i: internode; s: stump.

Subfamily--Tribe   Species                         Phytotelmata

Forcipomyiinae     Atrichopogon sp.                A. distichantha (a)
                   Forcipomyia (Euprojoannsia)     Treehole
                     sp.
                   Forcipomyia (Warmkea) sp.       E. pandanifolium (a)
Dasyheleinae       Dasyhelea sp.                   A. distichantha (a)
Ceratopogoninae                                    G. chacoensis (i)
  Culicoidini      Culicoides bambusicola Lutz     G. trinii (i)
                                                   M. clausseni (i,s)
                                                   V. friburgensis (a)
                                                   Treehole
                   Culicoides paraensis (Goeldi)   Treehole
  Ceratopogonini   Stilobezzia n. sp.              G. chacoensis (i,s)
  Palpomyiini      Bezzia snowi Lane               Treehole
                   Palpomyia guarani Lane          G. chacoensis (i)
                                                   Treehole
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Author:Campos, Raul E.; Spinelli, Gustavo; Mogi, Motoyoshi
Publication:Revista de la Sociedad Entomologica Argentina
Date:Jan 1, 2011
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