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First record of acari Arrenurus Dugès, 1834 as a parasite of Odonata species in Brazil

Abstracts

Water mites are common and widespread parasites of some aquatic insects in freshwater habitats. This is the first record of acari Arrenurus Dugès, 1834, as a parasite of Odonata in Brazil. Water mites were sampled from Miathyria marcella (Selys, 1857) and Ischnura fluviatilis (Selys, 1876).

dragonfly; parasitism; water mites


Ácaros aquáticos são parasitas comuns de alguns insetos aquáticos em habitats de água doce. Este é o primeiro registro do ácaro Arrenurus Dugès, 1834, como parasita de Odonata no Brasil. Ácaros aquáticos foram coletados em Miathyria marcella (Selys, 1857) e Ischnura fluviatilis (Selys, 1876).

libélulas; parasitismo; ácaros aquáticos


Introduction

Water mites are common and widespread parasites of some aquatic insects in freshwater habitats (Milne et al. 2009MILNE, M.A., TOWNSEND, V.J., SMELSER, P., FELGENHAUER, B.E., MOORE, M.K. & SMYTH, F.J. 2009. Larval aquatic and terrestrial mites infesting a temperate assemblage of mosquitoes. Exp. Appl. Acarol. 47(1):19-33. PMid:18807202. http://dx.doi.org/10.1007/s10493-008-9194-2
http://dx.doi.org/10.1007/s10493-008-919...
, Rolff 2000ROLFF, J. 2000. Water mite parasitism in damselflies during emergence: two hosts, one pattern. Ecography 23(3):273-282. http://dx.doi.org/10.1111/j.1600-0587.2000.tb00282.x
http://dx.doi.org/10.1111/j.1600-0587.20...
). Mites establish a brief phoretic association, they use one animal by another for transportation, finding food, finding more favorable environmentals conditions and expanding the species' range (Lajeunesse 2007LAJEUNESSE, M.J. 2007. Ectoparasitism of Damselflies by Water Mites in Central Florida. Florida Entomologist. 90(4): 643-649. http://dx.doi.org/10.1653/0015-4040(2007)90[643:EODBWM]2.0.CO;2
http://dx.doi.org/10.1653/0015-4040(2007...
, MuMcuoglu & BraverMan 2010MUMCUOGLU, K.Y. & BRAVERMAN, Y. 2010. Parasitic and phoretic mites of Diptera in Israel and the Sinai Peninsula, Egypt. Israel J. Entomol. 40(1):195-203.). Their hosts during a very vulnerable stage: the larvae's transition from its aquatic habitat to the terrestrial habitat of the adult (Andrés & Cordero 1998ANDRÉS, J.A. & CORDERO, A. 1998. Effects of water mites on the damselfly Ceriagrion tenellum. Ecol. Entomol. 23(2):103-109., Forbes et al. 1999FORBES, M.R., MUMA, K.E. & SMITH, B.P. 1999. Parasitism of Sympetrum dragonflies by Arrenurus planus mites: maintenance of resistance particular to one species. Int. J. Parasitol. 29(1):991-999., Rolff et al. 2001ROLFF, J., VOGEL, C. & POETHKE, H.J. 2001. Co-evolution between ectoparasites and their insect hosts: a simulation study of a damselfly-water mite interaction. Ecol. Entmol. 26(6):638-645.). Hydrachnidia (Hydracarina) is the most diversified and abundant group of Acari in freshwaters (Sabatino et al. 2000SABATINO, A., GERECKE, R. & MARTIN, P. 2000. The biology and ecology of lotic water mites (Hydrachnidia). Freshwater Biol. 44(1):47-62. http://dx.doi.org/10.1046/j.1365-2427.2000.00591.x
http://dx.doi.org/10.1046/j.1365-2427.20...
). According to Andrew et al. 2012ANDREW, R.J., THAOKAR, N. & VERMA, P. 2012. Ectoparasitism of anisopteran dragonflies (Insecta:Odonata) by water mite larvae of Arrenurus spp. (Arachnida:Hydrachnida:Arrenuridae) in Central India. Acarina 20(2):194:198., water mites that use odonates as hosts are predominantly Arrenurus and at least 55 species have been described as ectoparasites of Odonata. Studies indicate that mite parasitism can affect longevity, the flight, the fecundity impeding the copulation or by blocking sperm transference to the male's secondary genitalia (Bonn et al. 1996BONN, A., GASSE, M., ROLFF, J., & MARTENS, A. 1996. Increase fluctuation asymmetry (FA) in the damselfly Coenagrion puella correlated with ectoparasite water mites: implication for fluctuation asymmetry theory. Oecologia. 108:596-598. http://dx.doi.org/10.1007/BF00329031
http://dx.doi.org/10.1007/BF00329031...
, Forbes 1991FORBES, M.R. 1991. Ectoparasites and mating success of male Enallagma ebrium damselfly (Odonata: Coenagrionidae). Oikos. 60(3):36-42. http://dx.doi.org/10.2307/3545076
http://dx.doi.org/10.2307/3545076...
, Forbes & Baker 1991FORBES, M.R.L. & BAKER, R.L. 1991. Condition and fecundity of the damselfly, Enallagma ebrium (Hagen): the importance of ectoparasites. Oecologia. 86(3):35-41. http://dx.doi.org/10.1007/BF00317598
http://dx.doi.org/10.1007/BF00317598...
).

The genus Arrenurus, contains 800 species (Smit 2010SMIT, H. 2010. Two new species of the genus Arrenurus from Pohnpei, Federal States of Micronesia (Acari: Hydrachnidia: Arrenuridae). Zootaxa 2006:50-54.), is the largest within the Arrenuridae and 161 of these species occur in South America (Rosso-de-Ferradás & Fernández 2005ROSSO-DE-FERRADÁS, B. & FERNÁNDEZ, H.R. 2005. Elenco y Biogeografía de los ácaros acuáticos (Acari, Parasitengona, Hydrachnidia) de Sudamérica. Graellsia 61(2):181-224. http://dx.doi.org/10.3989/graellsia.2005.v61.i2.19
http://dx.doi.org/10.3989/graellsia.2005...
, Rosso-de-Ferradás 2006ROSSO-DE-FERRADÁS, B. 2006. Arrenúridos de la cuenca del Río Paraná, Argentina (Acari: Parasitengona: Hydrachnidia). Revista Entomol. 65(4):23-34.). The basic life cycle of Arrenurus consists of seven stages: egg, inactive prelarvae, larvae, protonymph, deutonymph, tritonymph, and adult (Smith 1988SMITH, B.P. 1988. Host-parasite interaction and impacto of larval water mites on insects. Annu. Rev. Entomol. 33(1): 487-507. http://dx.doi.org/10.1146/annurev.en.33.010188.002415
http://dx.doi.org/10.1146/annurev.en.33....
). The larval stage is the only parasitic phase. Arrenurus larvae are parasites of some species of Odonata, Diptera, and Coleoptera (Smith 1988SMITH, B.P. 1988. Host-parasite interaction and impacto of larval water mites on insects. Annu. Rev. Entomol. 33(1): 487-507. http://dx.doi.org/10.1146/annurev.en.33.010188.002415
http://dx.doi.org/10.1146/annurev.en.33....
, Zawal 2006ZAWAL, A. 2006. Phoresy and parasitism: water mite larvae of the genus Arrenurus (Acari: Hydrachnidia) on Odonata from Lake Binowskie (NW Poland). Biol. Letters 43(2):257-276.). For example, in Europe Arrenurus was recorded on the following species of Odonata: Ceriagrion tenellum (De Villers, 1789); Coenagrion puella (Linnaeus, 1758); C. hastulatum (Charpentier, 1825); C. pulchellum (Vander Linden, 1823), and Erythromma najas (Hansemann, 1823) (Andrés & Cordero 1998ANDRÉS, J.A. & CORDERO, A. 1998. Effects of water mites on the damselfly Ceriagrion tenellum. Ecol. Entomol. 23(2):103-109., Rolff 2000ROLFF, J. 2000. Water mite parasitism in damselflies during emergence: two hosts, one pattern. Ecography 23(3):273-282. http://dx.doi.org/10.1111/j.1600-0587.2000.tb00282.x
http://dx.doi.org/10.1111/j.1600-0587.20...
, Zawal 2006ZAWAL, A. 2006. Phoresy and parasitism: water mite larvae of the genus Arrenurus (Acari: Hydrachnidia) on Odonata from Lake Binowskie (NW Poland). Biol. Letters 43(2):257-276.). In North American, Lajeunesse (2007)LAJEUNESSE, M.J. 2007. Ectoparasitism of Damselflies by Water Mites in Central Florida. Florida Entomologist. 90(4): 643-649. http://dx.doi.org/10.1653/0015-4040(2007)90[643:EODBWM]2.0.CO;2
http://dx.doi.org/10.1653/0015-4040(2007...
, recorded Arrenurus in Argia fumipennis atra Gloyd, 1968; Ischnura hastata (Say, 1840); Ischnura ramburii (Selys, 1850), and Nehalennia gracilis Morse, 1895. Reports and records of the interactions between Odonata and mites have been explored very little (Smith 1988SMITH, B.P. 1988. Host-parasite interaction and impacto of larval water mites on insects. Annu. Rev. Entomol. 33(1): 487-507. http://dx.doi.org/10.1146/annurev.en.33.010188.002415
http://dx.doi.org/10.1146/annurev.en.33....
), mainly in the Neotropical Region. In Brazil water mite parasitism (Acari: Hydrachnida) within and among odonate species is scarce, many species could only be identified as morphospecies of particular genera (Rosso-de-Ferradás 2006ROSSO-DE-FERRADÁS, B. 2006. Arrenúridos de la cuenca del Río Paraná, Argentina (Acari: Parasitengona: Hydrachnidia). Revista Entomol. 65(4):23-34.).

Our study is the first record of Arrenurus parasitism on Miathyria marcella (Selys, 1857) and Ischnura fluviatilis Selys, 1876 in the Neotropical region. Miathyria Kirby, 1889 is a Neotropical genus that comprises two species, M. marcella and M. simplex (Rambur, 1842), both of which occur in Brazil (Garrison et al. 2006GARRISON, R.W., VON ELLENRIEDER, N. & LOUTON, J.A. 2006. Dragonfly genera of the New World: An illustrated and annotated key to the Anisoptera. Johns Hopkins University Press, Baltimore.). Ischnura Charpentier, 1840 is cosmopolitan genus, with three described species in Brazil: I. capreolus (Hagen, 1861) I. ramburii (Selys, 1850) and I. fluviatilis (Selys 1876) (Lencioni 2006LENCIONI, F.A.A. 2006. Damselflies of Brazil: An illustrated identification guide - 2- Coenagrionidae families. All Print Editora, São Paulo., Garrison et al. 2010GARRISON, R.W., VON ELLENRIEDER, N. & LOUTON, J.A. 2010. Damselfly Genera of the New World: An illustrated and annotated key to the Zygoptera. Johns Hopkins University Press, Baltimore.).

Material and Methods

The specimens of Odonata were captured with an entomological net and examined under a stereoscopic microscope, the species was identified following the work of Heckman (2006)HECKMAN, C.W. 2006. Encyclopedia of South American Aquatic Insects: Odonata - Anisoptera. Illustrated Keys to Known Families, Genera, and Species in South America. Springer, Washington. and Lencioni (2006)LENCIONI, F.A.A. 2006. Damselflies of Brazil: An illustrated identification guide - 2- Coenagrionidae families. All Print Editora, São Paulo.. Only three specimes M. marcella and one I. fluviatilis were found with dust mites attached to the body. Two males of Miathyria marcella, were collected in Porto Murtinho (22°9′41.55″S and 57°32′2.68″W) and one in Bodoquena (20°42′15.38″S and 56°50′58.99″W), in the state of Mato Grosso do Sul, Brazil. The specimen of I. fluviatilis was captured in the Estação Ecológica Águas Emendadas (15°34′48.36″S and 47°41′26.22″W) in Brasília, Distrito Federal, Brazil. Both the species were in inhabit slow lotic waters.

The mites removed from the odonates were put into lactophenol to make them transparent; semi-permanent slide mounts were made using Hoyer's mounting media as preservative and examined under optical light microscopy (40x, 100x, 400x), the species was identified according to the key of Krantz (1978). The species in question could not be determined since the most important subgenera from the genus Arrenurus have been originally identified based on Palaeartic species. This has changed subsequently since their boundaries and definitions have become confusing and, in many cases, completely overlap (Rosso-de-Ferradás 2006ROSSO-DE-FERRADÁS, B. 2006. Arrenúridos de la cuenca del Río Paraná, Argentina (Acari: Parasitengona: Hydrachnidia). Revista Entomol. 65(4):23-34.). In addition, samples were not sufficient for an exhaustive comparison. The specimens of Odonata and water mites are deposited in the Setor de Entomologia Médica e Forense, Instituto Oswaldo Cruz, Fundação Oswaldo Cruz (IOC/FIOCRUZ).

Results and Discussion

Two of the three specimens of M. marcella were found with five to 10 aquatic mites attached to the ventral side of their thorax and some attached ventrally on the abdomen (Figure 1). Second Rolff (2000)ROLFF, J. 2000. Water mite parasitism in damselflies during emergence: two hosts, one pattern. Ecography 23(3):273-282. http://dx.doi.org/10.1111/j.1600-0587.2000.tb00282.x
http://dx.doi.org/10.1111/j.1600-0587.20...
the abundance of mites can ranged from 1 to 45 mites per host. Of the three specimens M. marcella had only one aquatic mite on the thorax. In I. fluviatilis, two aquatic mites were found on the thorax and abdomen of the specimen. Zawal (2006)ZAWAL, A. 2006. Phoresy and parasitism: water mite larvae of the genus Arrenurus (Acari: Hydrachnidia) on Odonata from Lake Binowskie (NW Poland). Biol. Letters 43(2):257-276. stated that mites show preference for the thorax and the middle segments of the abdomen. On the other hand, Mitchell (1959)MITCHELL, R. 1959. Life histories and larval behaviour of Arrenurid water-mites parasitizing Odonata. J. New York Entomol. S. 67(1):1-12. suggested that the selection of the attachment site on the hosts is directly related to the way Odonata females lay eggs above the water surface, but Rolff (2000)ROLFF, J. 2000. Water mite parasitism in damselflies during emergence: two hosts, one pattern. Ecography 23(3):273-282. http://dx.doi.org/10.1111/j.1600-0587.2000.tb00282.x
http://dx.doi.org/10.1111/j.1600-0587.20...
and Lajeunesse (2007)LAJEUNESSE, M.J. 2007. Ectoparasitism of Damselflies by Water Mites in Central Florida. Florida Entomologist. 90(4): 643-649. http://dx.doi.org/10.1653/0015-4040(2007)90[643:EODBWM]2.0.CO;2
http://dx.doi.org/10.1653/0015-4040(2007...
no found differences in parasite abundance due to host sex. However the behavior the oviposition from Odonata species can increase significantly the rate from infestation in hosts with submerged oviposition (Rolff 1997ROLFF, J. 1997. Better Hosts Dive: Detachment of Ectoparasitic Water Mites (Hydrachnellae: Arrenuridae) from Damselflies (Odonata: Coenagrionidae) J. Insect Behav. 10(6):819-827. http://dx.doi.org/10.1023/B:JOIR.0000010415.14483.e3
http://dx.doi.org/10.1023/B:JOIR.0000010...
). Specimens of Arrenurus were found on M. marcella during their larval phase, when they typically inhabit temporary or permanent lentic or slow lotic waters (Peckarsky et al. 1990PECKARSKY, B.L., FRAISSINET, P.R., PENTON, M.A. & CONKLIN, J.D. 1990. Freshwater Macroinvertebrates of Northeastern North America. Cornell University Press, New York.) and Lajeunesse (2007)LAJEUNESSE, M.J. 2007. Ectoparasitism of Damselflies by Water Mites in Central Florida. Florida Entomologist. 90(4): 643-649. http://dx.doi.org/10.1653/0015-4040(2007)90[643:EODBWM]2.0.CO;2
http://dx.doi.org/10.1653/0015-4040(2007...
reported for North American Arrenurus parasitizing I. hastata and I. ramburii also inhabit temporary or permanent lentic or slow lotic waters. Some studies indicate that the abundance of water mites can be synchronised with host's emergence patterns (Rolff 2000ROLFF, J. 2000. Water mite parasitism in damselflies during emergence: two hosts, one pattern. Ecography 23(3):273-282. http://dx.doi.org/10.1111/j.1600-0587.2000.tb00282.x
http://dx.doi.org/10.1111/j.1600-0587.20...
). Therefore basic information on the natural history of water mite parasitism is urgently needed to assess the host range and geographic distribution of these parasites (Bush et al. 2001BUSH, A.O., FERNANDEZ, J.C., ESCH, G.W. & SEED, J.R. 2001. Parasitism: the diversity and ecology of animal parasites. Univ. Press. Cambridge, Rolff 2001ROLFF, J. 2001. Evolutionary ecology of water mite-insect interactions: a critical appraisal. Arch. Hydrobiol. 152(1):353-368.).

Figure 1.
Aquatic mites Arrenurus on the thorax and abdomen of M. marcella. (Picture by Carlos Fernando S. Andrade).

We are grateful to Dra. Marina Vianna Braga, Dr. Fabio de Oliveira Roque and Raquel Taminato for their helpful reviewing of the manuscript. We would like to thank the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Fundação de Apoio ao Desenvolvimento do Ensino, Ciência e Tecnologia do Estado do Mato Grosso do Sul (FUNDECT), Programa Nacional de Cooperação Acadêmica (PROCAD) and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for grants and scholarships to the first author.

References

  • ANDRÉS, J.A. & CORDERO, A. 1998. Effects of water mites on the damselfly Ceriagrion tenellum. Ecol. Entomol. 23(2):103-109.
  • ANDREW, R.J., THAOKAR, N. & VERMA, P. 2012. Ectoparasitism of anisopteran dragonflies (Insecta:Odonata) by water mite larvae of Arrenurus spp. (Arachnida:Hydrachnida:Arrenuridae) in Central India. Acarina 20(2):194:198.
  • BONN, A., GASSE, M., ROLFF, J., & MARTENS, A. 1996. Increase fluctuation asymmetry (FA) in the damselfly Coenagrion puella correlated with ectoparasite water mites: implication for fluctuation asymmetry theory. Oecologia. 108:596-598. http://dx.doi.org/10.1007/BF00329031
    » http://dx.doi.org/10.1007/BF00329031
  • BUSH, A.O., FERNANDEZ, J.C., ESCH, G.W. & SEED, J.R. 2001. Parasitism: the diversity and ecology of animal parasites. Univ. Press. Cambridge
  • FORBES, M.R. 1991. Ectoparasites and mating success of male Enallagma ebrium damselfly (Odonata: Coenagrionidae). Oikos. 60(3):36-42. http://dx.doi.org/10.2307/3545076
    » http://dx.doi.org/10.2307/3545076
  • FORBES, M.R.L. & BAKER, R.L. 1991. Condition and fecundity of the damselfly, Enallagma ebrium (Hagen): the importance of ectoparasites. Oecologia. 86(3):35-41. http://dx.doi.org/10.1007/BF00317598
    » http://dx.doi.org/10.1007/BF00317598
  • FORBES, M.R., MUMA, K.E. & SMITH, B.P. 1999. Parasitism of Sympetrum dragonflies by Arrenurus planus mites: maintenance of resistance particular to one species. Int. J. Parasitol. 29(1):991-999.
  • GARRISON, R.W., VON ELLENRIEDER, N. & LOUTON, J.A. 2006. Dragonfly genera of the New World: An illustrated and annotated key to the Anisoptera. Johns Hopkins University Press, Baltimore.
  • GARRISON, R.W., VON ELLENRIEDER, N. & LOUTON, J.A. 2010. Damselfly Genera of the New World: An illustrated and annotated key to the Zygoptera. Johns Hopkins University Press, Baltimore.
  • HECKMAN, C.W. 2006. Encyclopedia of South American Aquatic Insects: Odonata - Anisoptera. Illustrated Keys to Known Families, Genera, and Species in South America. Springer, Washington.
  • KRANTZ, G.W 1978. A manual of acarology. 2nd ed. Oregur state Univ. Book.
  • LAJEUNESSE, M.J. 2007. Ectoparasitism of Damselflies by Water Mites in Central Florida. Florida Entomologist. 90(4): 643-649. http://dx.doi.org/10.1653/0015-4040(2007)90[643:EODBWM]2.0.CO;2
    » http://dx.doi.org/10.1653/0015-4040(2007)90
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  • MILNE, M.A., TOWNSEND, V.J., SMELSER, P., FELGENHAUER, B.E., MOORE, M.K. & SMYTH, F.J. 2009. Larval aquatic and terrestrial mites infesting a temperate assemblage of mosquitoes. Exp. Appl. Acarol. 47(1):19-33. PMid:18807202. http://dx.doi.org/10.1007/s10493-008-9194-2
    » http://dx.doi.org/10.1007/s10493-008-9194-2
  • MITCHELL, R. 1959. Life histories and larval behaviour of Arrenurid water-mites parasitizing Odonata. J. New York Entomol. S. 67(1):1-12.
  • MUMCUOGLU, K.Y. & BRAVERMAN, Y. 2010. Parasitic and phoretic mites of Diptera in Israel and the Sinai Peninsula, Egypt. Israel J. Entomol. 40(1):195-203.
  • PECKARSKY, B.L., FRAISSINET, P.R., PENTON, M.A. & CONKLIN, J.D. 1990. Freshwater Macroinvertebrates of Northeastern North America. Cornell University Press, New York.
  • ROLFF, J. 2001. Evolutionary ecology of water mite-insect interactions: a critical appraisal. Arch. Hydrobiol. 152(1):353-368.
  • ROLFF, J. 2000. Water mite parasitism in damselflies during emergence: two hosts, one pattern. Ecography 23(3):273-282. http://dx.doi.org/10.1111/j.1600-0587.2000.tb00282.x
    » http://dx.doi.org/10.1111/j.1600-0587.2000.tb00282.x
  • ROLFF, J. 1997. Better Hosts Dive: Detachment of Ectoparasitic Water Mites (Hydrachnellae: Arrenuridae) from Damselflies (Odonata: Coenagrionidae) J. Insect Behav. 10(6):819-827. http://dx.doi.org/10.1023/B:JOIR.0000010415.14483.e3
    » http://dx.doi.org/10.1023/B:JOIR.0000010415.14483.e3
  • ROLFF, J., VOGEL, C. & POETHKE, H.J. 2001. Co-evolution between ectoparasites and their insect hosts: a simulation study of a damselfly-water mite interaction. Ecol. Entmol. 26(6):638-645.
  • ROSSO-DE-FERRADÁS, B. & FERNÁNDEZ, H.R. 2005. Elenco y Biogeografía de los ácaros acuáticos (Acari, Parasitengona, Hydrachnidia) de Sudamérica. Graellsia 61(2):181-224. http://dx.doi.org/10.3989/graellsia.2005.v61.i2.19
    » http://dx.doi.org/10.3989/graellsia.2005.v61.i2.19
  • ROSSO-DE-FERRADÁS, B. 2006. Arrenúridos de la cuenca del Río Paraná, Argentina (Acari: Parasitengona: Hydrachnidia). Revista Entomol. 65(4):23-34.
  • SABATINO, A., GERECKE, R. & MARTIN, P. 2000. The biology and ecology of lotic water mites (Hydrachnidia). Freshwater Biol. 44(1):47-62. http://dx.doi.org/10.1046/j.1365-2427.2000.00591.x
    » http://dx.doi.org/10.1046/j.1365-2427.2000.00591.x
  • SMIT, H. 2010. Two new species of the genus Arrenurus from Pohnpei, Federal States of Micronesia (Acari: Hydrachnidia: Arrenuridae). Zootaxa 2006:50-54.
  • SMITH, B.P. 1988. Host-parasite interaction and impacto of larval water mites on insects. Annu. Rev. Entomol. 33(1): 487-507. http://dx.doi.org/10.1146/annurev.en.33.010188.002415
    » http://dx.doi.org/10.1146/annurev.en.33.010188.002415
  • ZAWAL, A. 2006. Phoresy and parasitism: water mite larvae of the genus Arrenurus (Acari: Hydrachnidia) on Odonata from Lake Binowskie (NW Poland). Biol. Letters 43(2):257-276.

Publication Dates

  • Publication in this collection
    Dec 2013

History

  • Received
    3 June 2013
  • Reviewed
    29 Aug 2013
  • Accepted
    7 Oct 2013
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