Association between Ichthyocladius (Diptera: Chironomidae) and armored catfishes in the Guareí River basin, São Paulo State, Brazil

Abstract

Ichthyocladius is a genus of chironomid (Diptera, Insecta) whose immature forms live attached to the bodies of some species of freshwater fishes. Here we investigate the association between Ichthyocladius spp. and armored catfish in streams of the Guareí River basin, Paraná River system, Brazil. We provide the first record of I. lilianae associated with fish in the São Paulo State and the Paraná River basin. In addition, this is the first report of Ichthyocladius associated with the armored catfishes Hypostomus iheringii and H. tietensis. Lastly, we record two undescribed species of Chironomidae (i.e., Ichthyocladius sp. 1 and Ichthyocladius sp. 2) associated with fishes.

Key words
fish fins; insects; larvae; Loricariidae; pupae; Upper Paraná River basin

INTRODUCTION

Different organisms can associate with fishes, either as parasites, commensals or mutualists. Freshwater fishes are hosts to many forms of life, including protozoa (e.g., Eiras et al. 2012, Martins et al. 2012), immature insects (e.g., Roque et al. 2004, Sydow et al. 2008), annelids (e.g., Ranzani-Paiva & Silva-Souza 2004), crustaceans (e.g., Neves & Tavares-Dias 2019) and other fishes (e.g., Zuanon & Sazima 2004, 2005). Among the insects, immature stages (i.e., larvae and pupae) of some Chironomidae (Diptera) may live attached to the bodies of aquatic animals (Tokeshi 1993, Roque et al. 2004, Sydow et al. 2008, Henriques-Oliveira & Nessimian 2009). Larva and pupae of the genus Ichthyocladius Fittkau, 1974, in particular, have been reported to live attached to fishes (e.g., Mendes et al. 2004, Roque et al. 2004).

Currently, Ichthyocladius is represented by three species, Ichthyocladius neotropicus Fittkau, 1974, the type species of the genus, I. kronichticola Mendes, Andersen & Sæther, 2004, and I. lilianae Mendes, Andersen & Sæther, 2004 (Mendes et al. 2004), as well as several additional species awaiting formal description. Individuals of I. kronichticola and I. lilianae have been reported to live in association with armored catfish (Mendes et al. 2004, Roque et al. 2004). Ichthyocladius lilianae has been recorded in waterbodies of three Brazilian States: Rio Grande do Sul (Sydow et al. 2008, Dala-Corte & Melo 2018), Minas Gerais (Mendes et al. 2004), and Rio de Janeiro (Henriques-Oliveira & Nessimian 2009).

In a recent study, Azevedo-Santos et al. (2020) investigated the fish fauna of the Guareí River basin (Upper Paraná River basin), São Paulo, Brazil. When examining the material collected, we noted the presence of species of Ichthyocladius living on armored catfishes. In this short paper, we investigate the association between these insects with fishes. In particular, we report for the first time the association of I. lilianae and two other undescribed species of Chironomidae with armored catfish (Loricariidae) in the Paraná River basin, São Paulo State, Brazil.

MATERIALS AND METHODS

Fish specimens were collected in the Guareí River basin, located in the upper reaches of the Paranapanema River (Paraná River system), São Paulo, Brazil. Armored catfishes were sampled in two tributaries of the right bank of the Guareí River during June and August 2017. Fish sampling is described in Azevedo-Santos et al. (2020). Sampling sites were designated as R1 (-23.434932°S -48.388695°W) and R2 (-23.460077°S -48.414122°W) (Figure 1).

Figure 1
Sampling reaches (R1 and R2) in the Guareí River system - map modified from Azevedo-Santos et al. (2020).

We searched for chironomids on the exterior surfaces of captured loricariids. All larvae and prepupae were removed and mounted on slides with Euparal®. Chironomidae species were identified according to Fittkau (1974) and Mendes et al. (2004) and by comparison with type specimens deposited at the Museu de Zoologia da Universidade de São Paulo (hereafter MZ), São Paulo, Brazil. Immature individuals (at least one for each species of Ichthyocladius) were deposited as vouchers at the MZ. Standard Length (SL) of all hosts was measured with a digital caliper (in millimeters - mm). Classification of the catfishes (see Table SI) followed Fricke et al. (2019a, b).

RESULTS

We examined nine armored catfishes, of which six served as hosts for Ichthyocladius. We recorded 13 larvae and one prepupa of the genus Ichthyocladius, including I. lilianae and two taxa identified at the morphospecies level (Ichthyocladius sp. 1 and Ichthyocladius sp. 2). This is the first record of I. lilianae for the Paraná River basin and for the State of São Paulo. The catfish hosts were individuals of Hypostomus iheringii (Regan, 1908) and H. tietensis (Ihering, 1905) (28.6 - 95.2 mm of SL). We found larvae attached to different regions of the body — including the eyes and fins (Table I; and examples in Figure 2a-d). Virtually all fish with associated chironomids had Ichthyocladius in the adipose fin region.

Figure 2
The association between chironomids and armored catfishes: (a) red arrow indicates Ichthyocladius lilianae in the adipose fin of Hypostomus tietensis; (b) red arrow indicates Ichthyocladius sp. 1 in the right eye of H. tietensis; (c) red arrow indicates the head of I. lilianae; (d) red arrow indicates I. lilianae on the adipose fin of H. iheringii.

Table I
Chironomids associated with armored catfishes from the Guareí River basin, São Paulo, Brazil. Classifications and voucher numbers can be found in Table SI.

Reach	Hosts	Associated species (local in the fish)
R1	One Hypostomus iheringii (Regan, 1908)	Three larvae of Ichthyocladius lilianae (right eye; left eye; lateral of the adipose fin)
R1	One Hypostomus tietensis (Ihering, 1905)	One larvae of Ichthyocladius sp.1 (right eye); and one larvae of I. lilianae (lateral of the adipose fin)
R2	One Hypostomus iheringii (Regan, 1908)	One larvae of I. lilianae (lateral of the adipose fin)
R2	One Hypostomus iheringii (Regan, 1908)	Two larvae of I. lilianae (pectoral fin; lateral of the adipose fin)
R2	One Hypostomus iheringii (Regan, 1908)	One larvae of I. lilianae (lateral of adipose fin)
R2	One Hypostomus iheringi (Regan, 1908)	Two larvae of Ichthyocladius sp. 2 (both on the lateral of the adipose fin); two larvae of I. lilianae (near to the adipose fin and other between the adipose fin and caudal fin); and one prepupa of I. lilianae (near to the adipose fin basin).

DISCUSSION

Ichthyocladius lilianae was described by Mendes et al. (2004) based on specimens collected in the São Francisco basin, Minas Gerais State. These authors reported its association with two loricariid fishes, Harttia sp. and Hypostomus cf. garmani (Regan, 1904). This species of chironomid has since been recorded in four Brazilian states and in different hydrographic basins, including São Francisco and Paraíba do Sul (Sydow et al. 2008, Mendes et al. 2004, Dala-Corte & Melo 2018, Henriques-Oliveira & Nessimian 2009; see details in Table II). Our work expanded its recorded range to include São Paulo State and the Paraná River basin.

Table II
Fish species with records of Ichthyocladius lilianae on their body.

Host (fish)	Hydrographic basins	Brazilian State	Reference
SILURIFORMES
Loricariidae
Ancistrus cf. multispinis (Regan, 1912)	Maquiné River	Rio Grande do Sul	Sydow et al. (2008)
Harttia sp.	São Francisco River	Minas Gerais	Mendes et al. (2004)
Hypostomus cf. garmani (Regan, 1904)	São Francisco River	Minas Gerais	Mendes et al. (2004)
Hypostomus iheringii (Regan, 1908)	Guareí River	São Paulo	This work
Hypostomus tietensis (Ihering, 1905)	Guareí River	São Paulo	This work
Pareiorhaphis hypselurus (Pereira & Reis, 2002)	Maquiné River	Rio Grande do Sul	Sydow et al. (2008), Dala-Corte & Melo (2018)
Pareiorhaphis nudula (Reis & Pereira, 1999)	Maquiné River	Rio Grande do Sul	Sydow et al. (2008)
Pareiorhina rudolphi (Miranda Ribeiro, 1911)	Preto River	Rio de Janeiro	Henriques-Oliveira & Nessimian (2009)
Trichomycteridae
Trichomycterus mirissumba Costa, 1992	Preto River	Rio de Janeiro	Henriques-Oliveira & Nessimian (2009)

We recorded two undescribed Chironomidae species (e.g., Ichthyocladius sp. 1 and Ichthyocladius sp. 2) associated with catfishes in the Guareí River system. Ichthyocladius sp. 1 is the only one without anal seta among the known species. The procersus is also absent in this species. Ichthyocladius sp. 2 differs from other species of Ichthyocladius by presenting the mentum with more than 24 median teeth and the premandible with pale teeth. In addition to these two, three additional species of the genus await formal description, being one from Ecuador (Fittkau 1974), other from Marauiá River, and the last from Argentina (Mendes et al. 2004). Therefore, the diversity of Chironomidae associated with catfishes is certainly underestimated.

Only two previous studies have reported an association between Ichthyocladius and Hypostomus Lacepède, 1803. Mendes et al. (2004) mentioned the presence of Ichthyocladius on H. cf. garmani while Roque et al. (2004) reported the interaction with Hypostomus species. Our work is the first to report Ichthyocladius on H. iheringii and H. tietensis. All hosts had at least one chironomid in the region close to the adipose fin. In the studied streams, the hosts were captured in rocky streambeds with moderate water flow, or with some turbulence. It is likely that the adipose fin, because of its particular position, is less disturbed by water turbulence, providing greater opportunities for adherence by Ichthyocladius. Individuals were also found in the eye, sometimes within the orbit (e.g., Figure 2b), possibly because it provides a more stable environment.

We finalize by emphasizing the need for more studies on the taxonomy, biogeography and ecology of Ichthyocladius — including field surveys and laboratory investigations. These organisms and their ecological interactions are poorly understood, and their possible effects on fish ecology and behavior remain largely unknown.

ACKNOWLEDGMENTS

We are grateful to Hamilton A. Rodrigues (UNESP), who helped with the fieldwork. Three reviewers provided important corrections and suggestions. We wish thanks to Claudio G. Froehlich and James A. Nienow for corrections on this manuscript. Authors were supported by: Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (scholarship to VMAS - FC-001); Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP; fellowship to EMS - process number 2018/11068-9), and Conselho Nacional de Desenvolvimento Científico e Tecnológico (grants to FMP).

SUPPLEMENTARY MATERIAL

Table SI. Classification of chironomids and armored catfishes (sensuFricke et al. 2019a, b) from the Guareí River Basin, São Paulo, Brazil.

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Publication Dates

• Publication in this collection
  25 Nov 2022
• Date of issue
  2022

History

• Received
  23 Nov 2020
• Accepted
  8 Mar 2021