INTRODUCTION
Trematodes (Digenea) have complex life cycles usually involving two invertebrates as intermediate hosts, and one vertebrate (predominantly fish) as the final host. The transfer of these parasites often involves different predator-prey interactions between the hosts (Rohde, Reference Rohde1993; Marcogliese, Reference Marcogliese1995; Martorelli, Reference Martorelli2001).
It is well known that some species of digenean parasites on fish, such as Monascus filiformis (Rudolphi 1819) Looss, 1907, use medusae and chaetognaths as secondary hosts (Marcogliese, Reference Marcogliese1995; Martorelli, Reference Martorelli2001; Daponte et al., Reference Daponte, Gil de Pertierra, Palmieri and Ostrowski de Nuñez2006). In recent years knowledge about the intermediate medusa hosts of this parasite has increased (Martorelli, Reference Martorelli2001; Diaz Briz et al., Reference Diaz Briz, Martorelli, Genzano and Mianzan2012), however, little is known about their complete life cycle and only 11 fish species around the world have been reported to be final hosts (Køie, Reference Køie1979; Quintero-Alonso et al., Reference Quintero-Alonso, Martínez-Ubeira, Fernández and Sanmartín1988; Girola et al., Reference Girola, Martorelli and Sardella1992; Martorelli & Cremonte, Reference Martorelli and Cremonte1998; Sey et al., Reference Sey, Nahhas, Uch and Vang2003; MacKenzie et al., Reference MacKenzie, Campbell, Mattiucci, Ramos, Pereira and Abaunza2004; Oguz & Bray, Reference Oguz and Bray2006; Keser et al., Reference Keser, Bray, Oguz, Çelen, Erdoğan, Doğuturk, Aklanoğlu and Marti2007; Kohn et al., Reference Kohn, Fernandes and Cohen2007).
In the South-western Atlantic Ocean, most records of final fish hosts of Monascus filiformis correspond to tropical waters (Brazil) (Amato, Reference Amato1982; Wallet & Kohn, Reference Wallet and Kohn1987; Pereira et al., Reference Pereira, Fernandes and Robaldo2000). For temperate waters (Argentina), information about fish hosts is scarce, and only one complete life cycle has been described for this parasite, involving the bivalve Nucula obliqua Lamarck, 1819 as first intermediate host, the hydromedusa Liriope tetraphylla (Chamisso and Eysenhardt, 1821) and the chaetognath Saggita sp. as secondary hosts, and the fish Trachurus lathami Nichols, 1920 as final host (Girola et al., Reference Girola, Martorelli and Sardella1992; Martorelli & Cremonte, Reference Martorelli and Cremonte1998).
As part of a project studying the role of gelatinous plankton in food webs, the gut content of many specimens of fish Stromateus brasiliensis Fowler 1906, from cold temperate waters of Patagonia (45°–49° S) was analysed. This demersal-pelagic fish (commonly denominated pampanito) is exclusively a jellyfish consumer (see Mianzan et al., Reference Mianzan, Marí, Prenski and Sanchez1996; Cousseau & Perrota, Reference Cousseau and Perrota2000; Diaz Briz, Reference Diaz Briz2014). In this work, we report for the first time the occurrence of Monascus filiformis on Stromateus brasiliensis, expanding the knowledge about the final hosts of this parasite, as well as the role of medusae as intermediate hosts of this parasite. We infer which medusa species of the area may be involved in the life cycle of this digenean.
MATERIALS AND METHODS
The fish were collected on the Continental Shelf of Patagonia Argentina (45°–49°S 59°–63°W, see Figure 1) in the South-western Atlantic Ocean, by the cruise ‘Eduardo Holmberg’ of Instituto Nacional de Investigación y Desarrollo Pesquero (INIDEP) during February 2009, using demersal trawls. They were frozen on board. In the laboratory, all gut contents of pampanito were examined under stereomicroscope to determine the presence of digenean parasites and gelatinous organisms. Digenean parasites were removed with dissection needles, fixed in 10% formalin and stained with Gill's Haematoxylin, dehydrated in an ethanol series, cleared in clove oil and mounted in Canada balsam. All measurements of 10 mature parasite individuals were taken using an ocular micrometer. The morphological features and measurements of these parasites corresponded with those previously reported by Køie (Reference Køie1979), Cribb et al. (Reference Cribb, Anderson and Bray1999), Sey et al. (Reference Sey, Nahhas, Uch and Vang2003) and Kohn et al. (Reference Kohn, Fernandes and Cohen2007). The ecological terminology used to estimate the prevalence followed the criteria of Bush et al. (Reference Bush, Lafferty, Lotz and Shostak1997) and Rózsa et al. (Reference Rózsa, Reiczigel and Majoros2000). The digeneans were kept in the collection of the Mar del Plata University (UNMdP – Box PDM01) and in La Plata Museum Helminthological Collection under the numbers MLP-He 7019.
Fig. 1. The study area (Patagonia Argentina continental shelf) with detail of stations sampled. Black triangles represent stations with specimens of Stromateus brasiliensis parasitized by Monascus filiformis; White triangles represent stations with specimens without parasites. For each station sampled, N represents the total number of specimens analysed and the numbers of parasitized fish are given in parentheses.
Nematocysts (stinging organelles typical of cnidarians) found in the stomach contents of the parasitized fish were identified according to Mariscal (Reference Mariscal, Musatine and Lenhoff1974) and Östman (Reference Östman2000).
RESULTS
A total of 80 specimens of Stromateus brasiliensis were analysed (Figure 2A). Ten of these hosted adult stages of Monascus filiformis within their gut contents (total prevalence 12.5%) (Figure 1). A total of 68 parasites were found, with intensities ranging between 1 and 24 parasites per fish.
Fig. 2. (A) The new final host Stromateus brasiliensis; (B) microscopic view of adult Monascus filiformis found in this study; (C) drawing of adult M. filiformis. Scale bars: A, 12 cm; B–C, 1.5 mm.
The following description is based on 10 Monascus filiformis (fixed and mounted specimens): Body elongated, 1593–4288 µm (mean = 2603; SD = 965) length and 166–319 µm (mean = 209; SD = 45.5) maximum width. Oral sucker subterminal, sub-globular to slightly elongated with a longitudinal aperture and usually larger than the ventral sucker 165–248 µm (mean = 189.7; SD = 24.3) × 125–178 µm (mean = 151.1; SD = 15.6). Acetabulum anterior, 95–130 µm (mean = 117.6; SD = 14.02) × 106–120 µm (mean = 112.8; SD = 4.8) Muscular pharynx 67–107 µm (mean = 86.5; SD = 15.1) × 41–63 µm (mean = 51.3; SD = 8.3), oesophagus with a proximal portion lined with integument and distal portion coated by bulky epithelial cells. Intestine with a blind left small arm and a right arm that extends to the end of the body. Uroproct not present. Testes rounded in tandem located in the second body part. Cirrus pouch pre-acetabular containing bipartite seminal vesicle, prostate pars and ejaculatory duct. Genital pore located on the acetabular side of cirrus pouch. Ovary, lobed, in the middle third of the body. Uterine coils at the rear end of the body filled with operculated eggs 31–44 µm (mean = 37.6; SD = 5.3) × 17–24 µm (mean = 20.3; SD = 2.5) and vitelline follicles lateral, extending from near posterior level of acetabulum to mid-level between testes (Figure 2B, C).
The stomachs of parasitized fish presented completely digested contents with thick mucus appearance. Although no visible structures of jellyfish were observed, nematocysts were found in these stomach contents, and corresponded to the type of spherical and oval isorhizas (15–20 µm of length) (Figure 3A, B) and mastigophores (40–50 µm length) (Figure 3C). Other prey items were not found in these stomachs.
Fig. 3. Microscopic view of nematocysts found in stomach contents of parasitized Stromateus brasiliensis. (A) spherical isorhizas; (B) oval isorhizas; (C) mastigophores. Scale bar: 15 µm.
DISCUSSION
In this study, the occurrence of Monascus filiformis is reported for the first time in the gut contents of Stromateus brasiliensis from cold temperate waters (Patagonia Argentina) of the south-western Atlantic Ocean.
A limited number of fish species in the world are known to be final hosts of this parasite. Prior to this study, Monascus filiformis had been reported in only two unnamed species of Pampus (Stromateidae) from India (Sey et al., Reference Sey, Nahhas, Uch and Vang2003), on Cepola rubescens (Cepolidae) from Italy, on Selaroides leptolepis (Carangidae) from Kuwait, on Mugil ophuyseni (Mugilidae) from China (Sey et al., Reference Sey, Nahhas, Uch and Vang2003), on Trachurus trachurus (Carangidae) from Denmark, Iberian Peninsula, Norway and Turkey (Køie, Reference Køie1979; Lozano et al., Reference Lozano, Ubeda, De Rojas, Ariza and Guevara2001; MacKenzie et al., Reference MacKenzie, Campbell, Mattiucci, Ramos, Pereira and Abaunza2004; Oguz & Bray, Reference Oguz and Bray2006) and, on Trachurus lathami (Carangidae) from Venezuela (Nasir & Gómez, Reference Nasir and Gomez1977). In the South-western Atlantic Ocean, Monascus filiformis has been found only in five species of fish from subtropical waters of Brazil: Chloroscombrus chrysurus (Carangidae) and Trachurus lathami (Carangidae) (Amato, Reference Amato1982), Oligoplites saurus (Carangidae) (Travassos et al., Reference Travassos, Freitas and Bührnheim1965, Reference Travassos, Freitas and Bührnheim1967), Peprilus paru (Stromateidae) (Wallet & Khon, Reference Wallet and Kohn1987), Micropogonias furnieri (Sciaenidae) (Pereira et al., Reference Pereira, Fernandes and Robaldo2000); and from cold temperate waters of Argentina it was reported infesting only Trachurus lathami (Girola et al., Reference Girola, Martorelli and Sardella1992).
The pampanito, Stromateus brasiliensis, has been considered a consumer of ctenophores (Marí, Reference Marí1985; Mianzan et al., Reference Mianzan, Marí, Prenski and Sanchez1996; Perrota & Cousseau, Reference Cousseau and Perrota2000); but it also predates heavily on medusae in the study area (Mianzan et al., Reference Mianzan, Marí, Prenski and Sanchez1996; Diaz Briz, Reference Diaz Briz2014). Monascus filiformis was never found in ctenophores. This digenean has been reported only in chaetognaths (Martorelli & Cremonte, Reference Martorelli and Cremonte1998; Daponte et al., Reference Daponte, Gil de Pertierra, Palmieri and Ostrowski de Nuñez2006, Reference Daponte, Gil de Pertierra, Palmieri and Ostrowski de Nuñez2008) and medusae (Martorelli, Reference Martorelli2001; Diaz Briz et al., Reference Diaz Briz, Martorelli, Genzano and Mianzan2012) in the area; however, chaetognaths are not a known food source of pampanito (Marí, Reference Marí1985; Mianzan et al., Reference Mianzan, Marí, Prenski and Sanchez1996; Cousseau & Perrota, Reference Cousseau and Perrota2000; Diaz Briz, Reference Diaz Briz2014).
In this study different types of nematocysts (Figure 3) were found in the stomach contents of parasitized fish. This fact supports the idea that the transmission of Monascus filiformis occurs when parasitized medusae are eaten by pampanito. It is well known that medusae with high values of parasitism prevalence are considered important in the transmission of digenean to final fish hosts (Lauckner, Reference Lauckner and Kinne1980; Marcogliese, Reference Marcogliese2002; Diaz Briz et al., Reference Diaz Briz, Martorelli, Genzano and Mianzan2012). The high prevalences (from 27 to 70%) of Monascus filiformis reported by Diaz Briz et al. (Reference Diaz Briz, Martorelli, Genzano and Mianzan2012) in Proboscidactyla mutabilis, Aequorea spp. and Eucheilota ventricularis in Patagonian waters, suggest that these hydromedusa species may be involved in the life cycle of this parasite (Figure 4). These medusae species show an overlapping distribution with the examined Stromateus brasiliensis (Cousseau & Perrota, Reference Cousseau and Perrota2000; Genzano et al., Reference Genzano, Mianzan and Bouillon2008; Rodríguez, Reference Rodríguez2013). In addition, the morphological features (size and shape) of the nematocysts found in the stomachs of parasitized fish are consistent with some nematocysts that constitute the cnidae of these three medusa species (Diaz Briz, personal observation). Therefore, the presence of Monascus filiformis and nematocysts in gut contents of Stromateus brasiliensis would not be an occasional or isolated event but would be a consequence of their specific trophic habits.
Fig. 4. Life cycle of Monascus filiformis and the potential routes of transmission in the area.
This fish, unlike the other species belonging to suborder Stromateoidei, has anatomical adaptations in its digestive tract that facilitate the consumption of these gelatinous organisms. Among these adaptations are the specialized pharyngeal sacs covered with buds and conical horn-denticles that serve to crush the gelatinous prey and prevent regurgitation, a large stomach to store greater amounts of food and long digestive tracts (Haedrich, Reference Haedrich1967; Macpherson, Reference Macpherson1983; Harbison, Reference Harbison1993).
It is well known that parasites use predator–prey relationships among their hosts to facilitate their transmission (Marcogliese, Reference Marcogliese1995). Therefore, their presence within a host population provide information on the host's diet and on the predators of the host, as well as the trophic role of the host in the marine food web (see Marcogliese, Reference Marcogliese2004, Reference Marcogliese and Rohde2005).
Even though predation by fish on jellyfish has not yet been determined through parasitism (Arai, Reference Arai2005), a high prevalence of digenean parasites in medusae allows us to infer that jelly may have an important role in the transmission of parasites to their final fish hosts (Lauckner, Reference Lauckner and Kinne1980; Marcogliese, Reference Marcogliese2002; Diaz Briz et al., Reference Diaz Briz, Martorelli, Genzano and Mianzan2012). Therefore, we hypothesized that the medusa species with high prevalences above mentioned from the area could be important for the transmission of Monascus filiformis to pampanito. Hence, we propose that the final host, Stromateus brasiliensis, may acquire the parasite by eating these infected medusae in the area (see Figure 4).
Thus, our studies have expanded our knowledge of the final hosts of Monascus filiformis as well as the secondary medusa hosts that may be involved in its life cycle in the area. Future studies about the life cycles of these digeneans, seasonality in medusae hosts, and distribution of their first intermediate and final fish hosts will allow us to achieve a better understanding of the role that gelatinous plankton have in local pelagic food webs.
ACKNOWLEDGEMENTS
Thank are due to Laura Carlino for correcting grammar and style. We also thank the INIDEP (Instituto Nacional de Investigación y Desarrollo Pesquero) which provided the study material and infrastructure.
FINANCIAL SUPPORT
This work was partially supported by the Consejo Nacional de Investigaciones Científicas y Técnicas (grant number: PIP CONICET 0152) and Universidad Nacional de Mar del Plata (grant number: UNdMP – EXA 639/13).
