First record of the invasive tapeworm, Schyzocotyle acheilognathi (Pseudophyllidea; Bothriocephalidae) in native freshwater fish, Brazil

Schyzocotyle acheilognathi is a tapeworm cestode commonly found in native freshwater fishes from Asia. This cestode has low host specificity and for that reason it has been registered parasitizing more than 200 cultured and wild fish species, besides amphibians, reptiles and birds from different regions of the world. With a high pathogenic potential, S. acheilognathi may cause mortalities in highly infected fish. In South America, Schyzocotyle was reported in Cyprinus carpio from a Brazilian fish farm at the municipality of Cornélio Procópio, northern Paraná State and from the natural environment in C. carpio from Neuquen River, Patagonia, Argentina. So far, there has been no report of this parasite in South American native fishes. Herein we report the first occurrence of the invasive tapeworm S. acheilognathi in Rineloricaria pentamaculata (Siluriformes, Loricariidae), a native armored freshwater catfish from southern Brazil.


INTRODUCTION
Invasive species is a major cause of biological diversity loss (Baillie et al. 2004). The fish escape from fish farms is crucial on the dispersion of exotic species worldwide in aquatic environments (Agostinho et al. 2006). This escape is often associated to the diffusion of new pathogens carried by them (Agostinho et al. 2006).

INVASIVE TAPEWORM
The tapeworm Schyzocotyle acheilognathi (Yamaguti, 1934) Brabec, Waeschenbach, Scholz, Littlewood and Kuchta, 2015(syn. Bothriocephalus acheilognathi Yamaguti, 1934) is a cestode commonly found in native freshwater fishes from Asia. This cestode has low host specificity (Salgado-Maldonado et al. 2015) and for that reason it has been registered parasitizing more than 200 cultured and wild fish species, besides amphibians, reptiles and birds from different regions of the world (Scholz et al. 2012, Yera et al. 2013. In fishes, the tapeworm life cycle starts with the host being infected by ingestion of copepod crustaceans (Cyclopoida) contaminated with coracid larvae (Liao and Shih 1956).
Exotic in the Neotropical region, S. acheilognathi occurrence has been substantially related to carp fish farming, usually from places with high occurrence of this parasite (Salgado-Maldonado andPineda-López 2003, Salgado-Maldonado et al. 2015). Eventually, the parasite reaches the natural environment and its ichthyofauna through contaminated fish-farming escapes, causing serious injuries to native fishes such as perforation of the gastrointestinal tract, anemia, reduction of growth and reproduction capacity, muscle fatigue, weakened swimming capacity and secondary bacterial infections. With a high pathogenic potential, S. acheilognathi may cause mortalities in highly infected fish (Salgado-Maldonado and Pineda-López 2003).
This cestode is widely distributed throughout the Americas. In North America, many authors recorded S. acheilognathi in several localities in the United States (Cole and Choudhury 2016). Salgado-Maldonado and Rubio-Godoy (2014) updated the distribution of this tapeworm in Mexico, where the species peaks its invasive host record in America (50 freshwater fish species from seven families). In Central America, this parasite has been recorded from Puerto Rico ( Fishes were collected monthly in Lajeadão River (Figure 1d), tributary of Ivaí River, located in municipality of Borrazópolis, Northern Paraná State, Brazil (24º01'32.85''S; 51º36'46.98''W). Collection permit was granted by Sisbio to FCJ (#42829-1) and Ethical Use of Animals Commission of Universidade Estadual de Londrina (CEUA/UEL 11110.2015.14). Fish specimens were captured with sieves (85 cm diameter / 0.2 mm mesh) and a Kicknet that consists of a net (2 mm mesh) with two wooden rods on the edges. Hosts were euthanized with Eugenol overdosage 3.000 mg/L (Lucena et al. 2013); mass and length were taken before necropsy. Vouchers were cataloged and deposited at the Museu de Zoologia da Universidade Estadual de Londrina. Fish intestine was placed on petri dish and analyzed under stereomicroscopy for parasites. Collected cestode was fixed with slight compression between lamina and glass slide using AFA, stained with cloridric carmine, dehydrated in alcoholic series, and diaphanizad with Eugenol in temporary mounts (Eiras et al. 2006). Furthermore, we used taxonomic descriptions and others reports, such as Yamaguti (1934), Pool (1987 and Scholz (1997) to identification. The specimen was deposited in the Coleção Helmintológica do Instituto Oswaldo Cruz (CHIOC), Rio de Janeiro, under accession number CHIOC 38570.
Fifteen specimens of R. pentamaculata were collected, and only a single specimen presented one cestode parasitizing the small intestine. The cestode was identified as S. acheilognathi by the following combination of characters (in micrometers): body length (about 2550 long); a wide scolex heartshaped (581.3 long x 723.4 width) with narrow, deep dorsally and lateral bothrias short and very deep; neck absent and first proglottid imediatelly posterior to scolex; imature proglottids much narrower 2001). As a bottom dweller fish, it is mostly found among foliage or on muddy or sandy bottom (FCJ, personal observation), feeding on small organisms on the substrate (Rapp Py-Daniel 1997). This habit must have facilitated the ingestion of infected cyclopoid and consequently S. acheilognathi. The stretch of stream where R. pentamaculata were collected is under strong anthropic influence and presents agriculture along its banks and a narrow band of riparian vegetation. Likely, S. acheilognathi could have been introduced into this stream by parasitized carps that accidentally have escaped from fish farm near to sampled site.
Schyzocotyle acheilognathi presents high capacity of adaptation to several environments (Pérez-Ponce de León et al. 2009). Due to wide distribution around the world mostly achieved by invasion of new habitats, this cestode is considered to be the most successful known freshwater helminth (Dove and Fletcher 2000), being recorded in several fish species and other vertebrate groups due to its great rate of adaptation to phylogenetically distant hosts. According Salgado-Maldonado and Pineda-López (2003), the high adaptive capacity of this cestode in Mexico is related to a combination of factors: its low intermediate and definite hosts specificity; the high abundance of cyclopoid copepods in Mexican freshwater habitats (which are intermediate host of this helminth); the amount of open niche availability, the existence of several dispersion windows throughout the year; the stable appropriate temperature for larval development all year round (16 -25° C); the presence of birds as eggs carriers; and the accentuated anthropogenic introduction of carps which are usual hosts to S. acheilognathi. Alarmingly, the same conditions are commonly observed in freshwater habitat throughout Brazil, therefore must be considered a country with elevated potential for fast diffusion of S. acheilognathi.
The presence of this parasite in a Brazilian native freshwater fish is a new record of introduction than scolex (196.7 long x 203.97 width); mature proglottids 224.2 long and 534.1 width, gravid proglottids 316.7 long and 769.5 width; imature, mature and gravid segments with rounded edges; cirrus sac 77 long and 70 width; medullary testes; lobed ovary 365.5 long and 179 width near posterior margin of proglottids; eggs 47 -59 long and 31 -37 width (10 eggs measured) (Figure 1a-c).
Rinelocaria pentamaculata lives in a widely variety of habitats, from streams to great lakes (Langeani and Araújo 1994, Reis and Cardoso of exotic species, marking the importance of parasite fauna investigation and inventory, as well as the study of introduced fishes in natural environments. Besides predation and competition for resources, non-native fishes directly affect habitat integrity by dissemination of exotic parasite species that accidentally infect native species, culminating in irreversible reduction of local diversity. The introduction of exotic organism and habitat destruction are among the main threats to conservation of endemic and extinction-susceptible species (Agostinho et al. 2005).