First report of Epibiont ciliates (Ciliophora: Peritrichia) living on larvae of Leptophlebiidae (Ephemeroptera) from Brazil

Daniel Peroni Abrahão José Leonardo Mello Guilherme Gorni Juliano José Corbi About the authors

ABSTRACT

Epibiosis was understood as a commensalism relation between two or more organisms. However, some studies have shown that epibionts can cause deleterious effects to their host. Here, we reported the first report of epibiosis between protozoa Epibiont ciliates (Ciliophora: Peritrichia) living on larvae of Ephemeroptera from Brazil.

Key words:
epibiosis; Protozoa; Ephemeroptera

Epibiosis is a facultative association of two organisms: the epibiont and the basibiont. The word "epibiont" comprises organisms that, during the sessile stage of their life cycle, are attached to the surface of a living substratum, while the basibiont lodges and constitutes a support 11 - Dias RJP, Cabral AF, Stephan NNC, Martins RT, Silva-Neto ID, Alves RG, D´agosto MA. Record of Rhabdostyla chironomi Kahl, 1933 (Ciliophora, Peritrichia) Epibiont on Chironomidae larvae (Diptera, Chironomidae) in a lotic system in Brazil. Brazilian Journal of Biology. 2007; 67(4), p.783-785.,22 - Fernandez-Leborans G, Tato-Porto ML. A review of the species of Protozoan Epibionts on Crustaceans.I. Peritrichciliates. Crustaceana. 2000; 73(6), p. 643-683.,33 - Wahl M, Marine Epibiosis, I. Fouling and antifouling some basic aspects. Marine Ecology Progress Series. 1989; 58, p.175-189.. Numerous species of protozoa belonging to the group of peritrich Ciliophora can be found living in other aquatic organisms. As pointed to by 33 - Wahl M, Marine Epibiosis, I. Fouling and antifouling some basic aspects. Marine Ecology Progress Series. 1989; 58, p.175-189., because of epibiosis, the host and the epibiont have beneficial and negative aspects. The negative effects of epibiosis on the host may involve, for example, a decrease in survival capability and perturbation of movement 44 - Henebry MS, Ridgeway BT. Epizoic ciliated protozoa of planktonic Copepods and Cladocerans and their possible use as indicators of organic pollution. Transactions of the American Microscopical Society. 1979; 98(4), p. 495-508.. Epibiosis is beneficial for epibiont protozoa, which can be transported to regions richer in food or to much more oxygenated places, as pointed out by 55 - Regali-Seleghim MH, Godinho MJL. Peritrichepibiont protozoans in the zooplankton of a subtropical shallow aquatic ecosystem (Monjolinho Reservoir, São Carlos, Brazil). J. Plankton Res. 2004; 26(5), p.501-508.. As pointed by following works 66 - Liu X and Gong J. Revealing the Diversity and Quantity of Peritrich Ciliates in Environmental Samples Using Specific Primer-based PCR and Quantitative PCR. Microbes Environment. 2012; 27(4), p.497-503., peritrichs are a diverse, ecologically important ciliate group usually with a complex life cycle.

Several ciliate protozoans live as epibionts on animals and plants, using them as 11 - Dias RJP, Cabral AF, Stephan NNC, Martins RT, Silva-Neto ID, Alves RG, D´agosto MA. Record of Rhabdostyla chironomi Kahl, 1933 (Ciliophora, Peritrichia) Epibiont on Chironomidae larvae (Diptera, Chironomidae) in a lotic system in Brazil. Brazilian Journal of Biology. 2007; 67(4), p.783-785.. Most ciliates, for example, of the genus Rhabdostyla Kent, 1880 (Peritrichia, Epistylidae), live as epibionts of freshwater invertebrates, such as rotifers, crustaceans (Cladocerans, Copepods), insects from the orders Ephemeroptera and Diptera (Chironomidae), and annelids (Oligochaeta and Polychaeta) 11 - Dias RJP, Cabral AF, Stephan NNC, Martins RT, Silva-Neto ID, Alves RG, D´agosto MA. Record of Rhabdostyla chironomi Kahl, 1933 (Ciliophora, Peritrichia) Epibiont on Chironomidae larvae (Diptera, Chironomidae) in a lotic system in Brazil. Brazilian Journal of Biology. 2007; 67(4), p.783-785.. Along these lines 55 - Regali-Seleghim MH, Godinho MJL. Peritrichepibiont protozoans in the zooplankton of a subtropical shallow aquatic ecosystem (Monjolinho Reservoir, São Carlos, Brazil). J. Plankton Res. 2004; 26(5), p.501-508., found Rhabdostyla sp. and Scyphidia sp. living on copepods 22 - Fernandez-Leborans G, Tato-Porto ML. A review of the species of Protozoan Epibionts on Crustaceans.I. Peritrichciliates. Crustaceana. 2000; 73(6), p. 643-683., points to epibionts living on custraceans 11 - Dias RJP, Cabral AF, Stephan NNC, Martins RT, Silva-Neto ID, Alves RG, D´agosto MA. Record of Rhabdostyla chironomi Kahl, 1933 (Ciliophora, Peritrichia) Epibiont on Chironomidae larvae (Diptera, Chironomidae) in a lotic system in Brazil. Brazilian Journal of Biology. 2007; 67(4), p.783-785. found Rhabdostyla chironomi inhabiting the Chironomidae larvae ventral tubles 77 - Dias RJP, Cabral AF, Martins RT, Stephan NNC, Silva‐Neto ID, Alves RG and D'Agosto M. Occurrence of peritrich ciliates on the limnic oligochaete Limnodrilus hoffmeisteri (Oligochaeta, Tubificidae) in the neotropics. Journal of Natural History.2009; 43(1-2), p.1-15., that found the occurrence of peritrich ciliates on the limnic oligochaete Limnodrilus hoffmeisteri and 88 - Dias RJP, Silva - Neto ID and Costa JM. Sítio de localização de protistas ciliados peritríquios (Ciliophora: Peritrichia) epibiontes sobre ninfas de Kempnyia Klapálek, 1914 (Insecta: Plecoptera: Perlidae). 2009. Anais do IX Congresso de Ecologia do Brasil, 13 a 17 de setembro, São Lourenço - MG. that points the occurrence of Epistylis sp. (Ciliophora: Peritrichia) living on nymphs of Kempnyia (Plecoptera). It is also known that Ciliophora can cause problems in niloticus rearing (Oreochromis niloticus) 99 - Zanolo R, Yamamura, MH. Parasitas em tilápias-do-nilo criadas em sistema de tanques-rede. Semina: Ciências Agrárias. 2006; 27(2), p.281-288. and that these situations play an important ecological role in freshwater ecosystems, but much of the work described is morphological and taxonomic aspects 1010 -Dias RJP, D'ávila S, Wieloch AH, D'agosto M. Protozoan ciliate epibionts on the freshwater apple snail Pomaceafigulinain a urban stream of south-east. Brazil Journal of Natural History . 2008; 42, p. 1409-1420..Within the Ephemeroptera (Insecta), there is a description of nymphs parasitized by nematodes, where they can cause damage such as infertility and male larvae developing feminine appearance as pointed by reference 1111 -Pritchard G, Zloty J. Life histories of two Ameletus mayflies (Ephemeroptera) in two mountain streams: the influence of temperature, body size, and parasitism. Journal of the North American Benthological Society. 1994; p.557-568..

Here, we report a first record of epibiont ciliates (Ciliophora: Peritrichia) living on larvae of Leptophlebiidae (Ephemeroptera), from Brazil (see Figure 1). The organisms were collected in September 2015, from the Monjolinho Reservoir, using a "D" aquatic net (0,25mm of mesh size) by the kick sampling method, during a survey of benthic macroinvertebrates. Organisms were separated on illuminated tray and fixed in 70% alcohol. The Ephemeroptera were identified using the identification key 1212 -Hamada N, Nessimian JL, Querino RB. Insetos aquáticos na Amazônia brasileira: taxonomia, biologia e ecologia. Embrapa Meio-Norte-Livros cie. 2014.,1313 -Mugnai R, Nessimian JL, Baptista DF. Manual de identificação de macroinvertebrados aquáticos do estado do Rio de Janeiro. Technical Books Editora, Rio de Janeiro. 2010. and the epibionts ciliates were identified using 1414 -Foissner W, Berger H. 1996. A user-friendly guide to ciliates (Protozoa, Ciliophora) commonly used by hydrobiologists as bioindicators in rivers, lakes, and waste waters, with notes on their ecology. Freshwater Biol. 35:375-498.. The Monjolinho reservoir is located in the campus of the Federal University of São Carlos (São Paulo, Brazil) in a subtropical region (47°53'W and 22°01'S).

Figure 1
A. Leptophlebiidae (Ephemeroptera) with Epibiont ciliates (Protozoa: Ciliophora) (zoom 4x); B. Zoom in Epibiont ciliates (Ciliophora:Peritrichia) on the dorsal side Leptophlebiidae (Ephemeroptera) (zoom 10x); C. Epibiont ciliates (Ciliophora:Peritrichia) (zoom 10x); D. Epibiont ciliates (Ciliophora:Peritrichia) (zoom 40x).

The epibiont ciliates were found usually located on the head and on the pronotum and mesonotum (thorax) (see Figure 1). The presence of epibionts generally on the head and on the pronotum and mesonotum (thorax) of the Ephemeroptera can bring some feed difficulties for these aquatic organism. On the other hand, as pointed by work 44 - Henebry MS, Ridgeway BT. Epizoic ciliated protozoa of planktonic Copepods and Cladocerans and their possible use as indicators of organic pollution. Transactions of the American Microscopical Society. 1979; 98(4), p. 495-508. peritrichs primarily consume bacteria, their location on the body of the host is indifferent.

As pointed by 55 - Regali-Seleghim MH, Godinho MJL. Peritrichepibiont protozoans in the zooplankton of a subtropical shallow aquatic ecosystem (Monjolinho Reservoir, São Carlos, Brazil). J. Plankton Res. 2004; 26(5), p.501-508. consider that bigger organisms are easier targets for the epibionts than smaller ones. Consequently, our observations may be related to epibiont preference for these aquatic organisms or to the presence of a comparatively larger adhesion surface offered by each Odonata individual.

ACKNOWLEDGEMENTS

We would like to thank the LEAA laboratory team (USP) and the department of Hydraulic and Sanitation (SHS).

REFERENCES

  • 1
    - Dias RJP, Cabral AF, Stephan NNC, Martins RT, Silva-Neto ID, Alves RG, D´agosto MA. Record of Rhabdostyla chironomi Kahl, 1933 (Ciliophora, Peritrichia) Epibiont on Chironomidae larvae (Diptera, Chironomidae) in a lotic system in Brazil. Brazilian Journal of Biology. 2007; 67(4), p.783-785.
  • 2
    - Fernandez-Leborans G, Tato-Porto ML. A review of the species of Protozoan Epibionts on Crustaceans.I. Peritrichciliates. Crustaceana. 2000; 73(6), p. 643-683.
  • 3
    - Wahl M, Marine Epibiosis, I. Fouling and antifouling some basic aspects. Marine Ecology Progress Series. 1989; 58, p.175-189.
  • 4
    - Henebry MS, Ridgeway BT. Epizoic ciliated protozoa of planktonic Copepods and Cladocerans and their possible use as indicators of organic pollution. Transactions of the American Microscopical Society. 1979; 98(4), p. 495-508.
  • 5
    - Regali-Seleghim MH, Godinho MJL. Peritrichepibiont protozoans in the zooplankton of a subtropical shallow aquatic ecosystem (Monjolinho Reservoir, São Carlos, Brazil). J. Plankton Res. 2004; 26(5), p.501-508.
  • 6
    - Liu X and Gong J. Revealing the Diversity and Quantity of Peritrich Ciliates in Environmental Samples Using Specific Primer-based PCR and Quantitative PCR. Microbes Environment. 2012; 27(4), p.497-503.
  • 7
    - Dias RJP, Cabral AF, Martins RT, Stephan NNC, Silva‐Neto ID, Alves RG and D'Agosto M. Occurrence of peritrich ciliates on the limnic oligochaete Limnodrilus hoffmeisteri (Oligochaeta, Tubificidae) in the neotropics. Journal of Natural History.2009; 43(1-2), p.1-15.
  • 8
    - Dias RJP, Silva - Neto ID and Costa JM. Sítio de localização de protistas ciliados peritríquios (Ciliophora: Peritrichia) epibiontes sobre ninfas de Kempnyia Klapálek, 1914 (Insecta: Plecoptera: Perlidae). 2009. Anais do IX Congresso de Ecologia do Brasil, 13 a 17 de setembro, São Lourenço - MG.
  • 9
    - Zanolo R, Yamamura, MH. Parasitas em tilápias-do-nilo criadas em sistema de tanques-rede. Semina: Ciências Agrárias. 2006; 27(2), p.281-288.
  • 10
    -Dias RJP, D'ávila S, Wieloch AH, D'agosto M. Protozoan ciliate epibionts on the freshwater apple snail Pomaceafigulinain a urban stream of south-east. Brazil Journal of Natural History . 2008; 42, p. 1409-1420.
  • 11
    -Pritchard G, Zloty J. Life histories of two Ameletus mayflies (Ephemeroptera) in two mountain streams: the influence of temperature, body size, and parasitism. Journal of the North American Benthological Society. 1994; p.557-568.
  • 12
    -Hamada N, Nessimian JL, Querino RB. Insetos aquáticos na Amazônia brasileira: taxonomia, biologia e ecologia. Embrapa Meio-Norte-Livros cie. 2014.
  • 13
    -Mugnai R, Nessimian JL, Baptista DF. Manual de identificação de macroinvertebrados aquáticos do estado do Rio de Janeiro. Technical Books Editora, Rio de Janeiro. 2010.
  • 14
    -Foissner W, Berger H. 1996. A user-friendly guide to ciliates (Protozoa, Ciliophora) commonly used by hydrobiologists as bioindicators in rivers, lakes, and waste waters, with notes on their ecology. Freshwater Biol. 35:375-498.

Publication Dates

  • Publication in this collection
    2017

History

  • Received
    03 Feb 2016
  • Accepted
    14 July 2016
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