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. 2021 Aug 2;46(1):1–7. doi: 10.1007/s12639-021-01430-w

Neobenedenia melleni from reef ornamental fish species in a retailer of Southeastern Brazil and its possible role as a mechanical vector of bacterial infection

Pedro H M Cardoso 1,✉, Rachel S Relvas 1, Simone de C Balian 1, Andre P Poor 1, Andrea M Moreno 1, Luísa Z Moreno 1, Mikaela R F Barbosa 3, Maria I Z Sato 3, William E Furtado 2,4, Maurício L Martins 2
PMCID: PMC8901895  PMID: 35299920

Abstract

Annually, more than 2500 ornamental fish species are traded worldwide. Forty percent of these are from marine water. Some 98% of marine species are wild-caught from their natural habitat, and the majority subsequently exported. Wild fish frequently carry pathogens, which could induce diseases after the stress of capture. Neobenedenia melleni is a platyhelminth that mainly attaches to the skin and eyes of the host. It provokes dermal inflammation, epidermal loss, skin depigmentation, reduction in the number of mucous cells, and, consequently, decreased mucus protection, and declining immunological barriers. This makes fish susceptible to secondary infections. A total of 47 wild reef fish from a retailer were examined, suspected to be infected with ectoparasites. The morphological identification revealed N. melleni as a monogenean agent. One monogenean specimen was collected from the eye of each of the 40 fish analyzed to evaluate possible bacterial secondary infections using the matrix-assisted laser desorption ionization–time-of-flight mass spectrometry (MALDI-TOF MS) technique. The MALDI-TOF MS identified that 59% of monogenean collected from the eyes had bacteria, including some pathogenic to fish. This led us to believe that the ectoparasite can be a possible mechanical vector of pathogenic bacteria for fish culture and maintenance. The use of praziquantel as an antiparasitic agent is also discussed.

Keywords: Marine reef fish, Monogenea, Capsalidae, Mechanical vector, Secondary infection

Introduction

Annually, more than 2500 ornamental fish species are traded worldwide. Forty percent are from marine water and 60% from freshwater. Although most freshwater fish originate from aquaculture, 98% of marine species are captured from their natural habitat and the majority subsequently exported (Dey 2016). Wild fish frequently carry pathogens, which could induce disease after the stress of capture. Thus, marine ornamental fish imports could lead to the introduction of new diseases in a country (Whittington and Chong 2007; Kristiansen et al. 2020).

Neobenedenia melleni (MacCallum, 1927) is a platyhelminth that belongs to the Capsalidae family of the Monogenea class (Whittington 2004). Most monogeneans have a narrow host spectrum, with high host specificity. However, Neobenedenia melleni does not follow this pattern. The parasite infects more than 100 marine teleost species of following families, such as Acanthuridae, Balistidae, Chaetodontidae, Diodontidae, Labridae, Ostraciidae and Pomacanthidae families (Cardoso et al. 2019). Geographically, N. melleni is distributed in tropical and subtropical areas of North America, Australia, and Southeast Asia (Deveney et al. 2001; Whittington 2004).

Stressful environments (such as high stocking density, poor sanitary conditions, low water quality, biofouling, transport, and thermal stress) can lead to animal immunosuppression. This can act as a predisposing factor for secondary infections (Kerber et al. 2011; Kristiansen et al. 2020). Besides, high temperatures (24–30 °C) accelerate the life cycle of N. melleni (Valles-Vega et al. 2019). The parasite has a direct life cycle and is an oviparous hermaphrodite that can reproduce by self-fertilization. In other words, a single N. melleni can lay eggs and then disseminate the parasite to other fish (Hoai and Hutson 2014).

Neobenedenia melleni mainly attaches to the skin and eyes of the host, although it may also appear on the gills and nostrils (Trujillo-González et al. 2015; Cardoso et al. 2019). This decreases the immunological barriers like lost mucus caused by the irritation of haptor that make fish susceptible to secondary infections caused by bacteria that monogeneans can transport. The parasite participates as a mechanical vector (Buchmann and Bresciani 2006; Reed et al. 2019; Trujillo-González et al. 2015). Despite few papers on the subject of mechanical vectors transmitting diseases for aquatic animals, this is a relatively recurrent theme in other areas of knowledge. Several scientific studies report insects as mechanical vectors of disease, noting the insects can carry pathogenic and often multiresistant bacteria to hospital environments or transmit diseases to livestock (Dawit et al. 2012; Garcia and Lise 2013; Shahi et al. 2017; Do Nascimento et al. 2020).

Moreover, high infections can promote lethargy, corneal opacity, blindness, ulcers, and skin hemorrhage caused by monogenean parasite infection that can also affect locomotion (erratic swimming), sensory perception, and thermal and ion regulation, and provoke mortality (Noga 2010; Kerber et al. 2011; Silva et al. 2014; Trujillo-González et al. 2015). The size of the parasite varies from 2 to 6 mm in length and 1.5 to 3 mm in width, which allows it to be seen by the naked eye (Carvalho and Luque 2009; Kerber et al. 2011). Diagnosis consists of the identification of the parasite by observation under a microscope and morphologic characterization following the procedures described by Whittington and Horton (1996).

In Brazil, there are reports of N. melleni infecting both captured ornamental fish and cultured fish (Carvalho and Luque 2009; Kerber et al. 2011; Silva et al. 2014; Cardoso et al. 2019). In this study, we report the occurrence of N. melleni on the eye, fin, and skin of wild reef ornamental fish in a retailer in São Paulo, Brazil, the occurrence of bacteria in the integument of the parasite, and the possible role of the infected fish as a mechanical vector.

Materials and methods

Animals

The ornamental reef fish of Acanthuridae (Paracanthurus hepatus n = 4, Zebrasoma flavens n = 6, Zebrasoma scopas n = 4, Acanthurus sohal n = 2), Balistidae (Balistoides conspillum n = 1), Chaetodontidae (Chelmon rostratus n = 2, Chaetodon auriga n = 2, Chaetodon kleinii n = 1), Gobiidae (Cryptocentrus leptocephalus n = 2), Labridae (Macropharyngodon meleagris n = 2), Pomacanthidae (Pomacanthus imperator n = 3, Pomacanthus semicirculatus n = 2, Pomacanthus navarchus n = 1, Pomacanthus sextriatus n = 2, Pomacanthus asfur n = 2, Centropyge bispinosa n = 3, Centropyge bicolor n = 2, Centropyge vrolikii n = 2), Pomacentridae (Amphiprion ocellaris n = 2), and Serranidae (Cromileptes altivelis n = 2) families were analyzed. The animals belonged to a retailer in São Paulo, Southeastern Brazil that reported an increase in the mortality of marine fish. All marine fish had been previously imported for a wholesaler accredited by the Ministry of Agriculture, Livestock, and Supply. Fish were quarantined for eight days before being purchased and marketed (Fig. 1).

Fig. 1.

Fig. 1

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The white arrow of N. melleni in the eye, fin, and skin of ornamental reef fish (a) and b P. sextriatus; c P. imperator; d P. semicirculatus; e P. asfur; f C. altivelis; g P. hepatus; h Z. flavens from a retailer in São Paulo, Southeastern Brazil

In the retailer company, all marine fish bought were wild marine fish and maintained in an individual system of 1 m3 with 10 interconnected aquariums. Water quality parameters were measured daily and maintained at a temperature of 26 °C, salinity 29 ppt, dissolved oxygen 5 mg L−1, pH 8.2, total ammonia < 0.1 mg L−1, and nitrite < 0.05 mg L−1. The fish were fed three times a day ad libitum with a mixed commercial diet (Aquarium Munster® Dr. Bassleer Biofish food Professional Care and Chlorella granules).

The retailer reported that 10 days post-arrival, all fish presented behavioral alterations such as flashing, skin depigmentation, fin lesions, eye opacity, and chronic mortality. The fish were examined by a veterinarian as part of a disease investigation. Suspected of ectoparasites, all fish were submitted to a skin scraping and then subjected separately to a freshwater bath at the same water temperature for 3–5 min.

The fish were allocated in the same system as before their freshwater bath and treated with three doses of praziquantel (2 mg L−1) with an interval of 7 and 14 days from the first day of treatment. One day (15th day), after the third treatment with praziquantel, the fish were bathed in fresh water to verify the parasite presence on the skin and eye.

Morphological identification of the ectoparasite

After the freshwater bath, one fallen parasite from each fish was collected with surgical forceps, bathed in the heated water at 56 °C for laxness, and fixed in 70% alcohol for identification. In the laboratory, they were washed in distilled water in a Petri dish, mounted in Hoyer’s following routine procedures (Kritsky et al. 1995) for observation of sclerotized structures. Photomicrographs were obtained in a differential interference contrast (DIC) microscope (ZEISS Axio Imager A2) and the structures were compared to those described by Whittington and Horton (1996). Parasitological indexes such as prevalence, mean intensity and mean abundance followed the calculation proposed by Bush et al. (1997).

Bacterial isolation from the monogenean

One ectoparasite settled in the opaque eye of 40 fish was collected with surgical forceps and washed in 70% alcohol for 3 s to disinfect for possible water contaminants. Then, the specimens were stored in Eppendorf tubes with 500 µL of saline solution and vortexed for 1 min to release possible bacteria from the ectoparasite's integument. Then, 10 µL of the suspension was plated in culture T.C.B.S Cholera medium (Oxoid Ltd, Basingstoke, Hampshire, United Kingdom) and 5% sheep blood agar (Difco-BBL, Sparks, MD, USA). The agar plates were incubated under aerobic conditions at 37 °C for 24–48 h.

Selected colonies were identified by the matrix-assisted laser desorption ionization–time-of-flight mass spectrometry (MALDI-TOF MS) technique. MALDI-TOF MS sample preparation and processing were executed as previously described by Hijazin et al. (2012). For the MALDI-TOF MS identification, the spectra were loaded into MALDI BioTyper™ 3.0 and compared with the manufacturer’s library. Standard Bruker interpretative criteria were applied. Scores ≥ 2.0 were accepted for species assignment and scores ≥ 1.7 but ≤ 2.0 for genus identification.

Results

The ectoparasite was identified as the monogenean N. melleni (MacCallum, 1927) Yamaguti, 1963 (Capsalidae). They were present on the body surface and eyes and fell off with a freshwater bath. The prevalence, mean intensity, and mean abundance of N. melleni in each species of fish with clinical signs are described in Table 1. The highest mean intensity and mean abundance occurred in P. asfur and P. navarchus. On the other hand, the lowest mean intensity and mean abundance occurred in C. rostratus and Z. scopas (Fig. 2).

Table 1.

Parasitological indices of reef ornamental fish species parasitized by Neobenedenia melleni from Southeastern Brazil

Common name Scientic name P MI VA MA
Palette surgeonfish Paracanthurus hepatus 1,00 3,75 (2–7) 3,75
Yellow tang Zebrasoma flavens 1,00 10,33 (7–16) 10,33
Twotone tang Zebrasoma scopas 0,75 2,00 (1–3) 1,50
Clown anemonefish Amphiprion ocellaris 1,00 5,33 (2–9) 5,33
Emperor angelfish Pomacanthus imperator 1,00 5,33 (4–7) 5,33
Semicircle angelfish Pomacanthus semicirculatus 1,00 6,00 (4–8) 6,00
Bluegirdled angelfish Pomacanthus navarchus 1,00 20,00 (20–20) 20,00
Sixbar angelfish Pomacanthus sextriatus 1,00 4,00 (2–6) 4,00
Sohal surgeonfish Acanthurus sohal 1,00 4,50 (3–6) 4,50
Blackspotted wrasse Macropharyngodon meleagris 1,00 3,50 (3–4) 3,50
Clown triggerfish Balistoides conspillum 1,00 9,00 (9–9) 9,00
Pink-speckled shrimpgoby Cryptocentrus leptocephalus 1,00 4,00 (4–4) 4,00
Twospined angelfish Centropyge bispinosa 1,00 5,67 (2–8) 5,67
Bicolor angelfish Centropyge bicolor 1,00 3,50 (3–4) 3,50
Pearlscale angelfish Centropyge vrolikii 1,00 2,50 (2–3) 2,50
Humpback grouper Cromileptes altivelis 1,00 3,00 (2–4) 3,00
Copperband butterflyfish Chelmon rostratus 1,00 2,00 (1–3) 2,00
Threadfin butterflyfish Chaetodon auriga 1,00 3,00 (2–4) 3,00
Sunburst butterflyfish Chaetodon kleinii 1,00 3,00 (3–3) 3,00
Arabian angelfish Pomacanthus asfur 1,00 19,50 (14–25) 19,50
All fishes 0,98 5,85 (1–25) 5,73
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PI parasitological indices, P% prevalence, MI mean intensity, In parentheses VA variation amplitude, MA mean abundance of N. melleni from each species analyzed in the study

Fig. 2.

Fig. 2

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Macroscopic photo of adult (a); and light photomicrographs of Neobenedenia melleni MacCallum, 1927 (Monogenea: Capsalidae), from marine ornamental fish collected in São Paulo, Brazil; b anterior part; c haptor

Bacteriological analysis of the monogeneans collected from the eyes of the fish showed that 59% (n = 24) tested positive for the presence of bacteria, of which 15% (n = 6) were identified as Acinetobacter johnsonii, 2% (n = 1) as Pseudomonas composti, 17% (n = 7) as P. oleovorans, 15% (n = 6) as P. putida, 2% (n = 1) as Vibrio pelagius and 7% (n = 3) as V. harveyi.

All treated fish in the aquarium system that presented behavior or clinical signs of disease recovered 15 days after the first treatment with praziquantel. Besides, they did not show parasites on the posterior after a freshwater bath. As a result, they were allowed to be commercialized.

Discussion

Neobenedenia melleni has low host specificity and has been found in several fish species, including reef fish (Bullard et al. 2003; Whittington and Horton 1996; Cardoso et al. 2019). In the retailer shop, the first clinical manifestations appeared in angelfish (Pomacanthidae family), many displaying eye and fin opacity signals. This situation was observed in P. navarchus and P. asfur, which presented opaque eyes and fins and a higher mean intensity value. Opacity is caused by damage and inflammation in the epidermis induced by the haptor (fixation structure) together with the parasite's overlap in the tissue and infection by opportunistic bacteria (Trujillo-González et al. 2015).

The bacteria A. johnsonii, P. putida, V. harveyi, and V. pelagius (isolated from the monogenean integument in our study) are reported in the scientific literature as pathogenic to marine fish and may have a high lethality rate (Villamil et al. 2003; Altinok et al. 2006; Hashem and El-Barbary 2013; Kozińska et al. 2014; Zhang et al. 2020). Acinetobacter johnsonii infection induces a congestive systemic disease, exophthalmia, scale loss, and hemorrhages in the skin, eyes, and gills (Kozińska et al. 2014; Pękala-Safińska 2018). Pseudomonas putida is a bacteria present in the microbiota (Pękala-Safińska 2018). However, it can lead to opportunistic ulcerative disease, provoking exophthalmia and ulceration of the dorsal fin, skin, musculature, and, in advanced cases, vertebrae (Altinok et al. 2006). In V. harveyi and V. pelagius, it can cause a systemic disease with congestion, hemorrhage, necrosis, and ulceration in several organs such as the intestine, kidney, stomach, and spleen (Villamil et al. 2003; Hashem and El-Barbary 2013; Zhang et al. 2020).

Mathematical models have also been created showing that mechanical vectors like flies transmit diseases from contaminated to healthy environments (Cousins et al. 2019). Some species of flies are known to carry pathogenic bacteria on their feet. The flies are thus mechanical vectors that transmit diseases to herds of healthy land animals (Oliveira et al. 2011). Taking this logic into account, N.melleni can serve as a mechanical vector, carry pathogenic bacteria in its haptor, and transmit diseases to healthy fish. In this study, the findings of bacteria in the parasite may be similar, but studies in this area are scarce.

Consequently, the presence of the parasite, together with bacterial infection, can lead to economic losses of high-value animals in the Brazilian market. Therefore, eliminating the monogeneans (which cause damage to the tegument of the animals) at the receipt of fish is a control action to prevent infection, dispersal, and losses due to opportunistic bacterial infections. Imported fish are often weakened and have a low immune system, which can lead to disease and death.

After the end of the system treatment, none of the fish showed any change in behavior or clinical signs of disease and no animal presented the attached parasite after freshwater bath. There are several options for the treatment of clinical signs of disease caused by this parasite. However, praziquantel bath and dip treatments showed high efficacy against adult forms with few side effects and a large safety margin (Morales-Serna et al. 2018; Bader et al. 2019). Our study demonstrated that the successful combination of freshwater baths and praziquantel treatments corroborates previous studies.

As previously discussed by Cardoso et al. (2019), the early diagnosis and adoption of control measures with a freshwater bath followed by treatment with praziquantel improve the prognosis of diseased fish. The prognosis success is even greater when the fish are maintained under adequate water quality conditions and fed a balanced diet. Under optimal conditions, tropical marine species should be kept at temperatures ranging from 22 to 27 °C, 30 ppt salinity (Noga 2010), recommended dissolved oxygen at 5.5 mg L−1 (never lower than 4.0 mg L−1), minimum pH 8.1, maximum total ammonia 0.37 mg L−1 (at 25 °C), maximum nitrite 0.125 mg/L, and maximum nitrate 100 mg L−1 (OATA 2008). During the study, the fish were maintained under the recommended water quality parameters, resulting in a good prognosis.

The investment in qualified professionals, capable of correctly diagnosing, handling, and treating fish contributes positively to the health of the animals and, consequently, to the wholesale company, which will have healthy fish for sale to retail consumers. This study showed that the monogenean integument constitutes possibly an important mechanical vector of opportunistic bacteria that could affect the health status of ornamental fish maintained.

Conclusion

Based on our results, we conclude that N. melleni infects different species of wild reef fish in the retailer. We believe that monogeneans can carry pathogenic bacteria to marine fish like A. johnsonii, P. putida, and V. harveyi, which can contribute to secondary bacterial infections due to injuries caused by the parasite's haptor and the role as a mechanical vector. These results emphasize the importance of quarantine, early diagnosis, and treatment to control and prevent diseases and death in aquatic animals. Future studies can be developed to correlate parasitism caused by monogeneans and bacterial infection in fish lesions. Molecular biology studies of the bacteria present in the parasite's fixation organs, with the bacteria present in the fish lesions, can confirm this hypothesis of the mechanical vector.

Acknowledgements

This study was financed in part by the Coordination of Improvement of Higher Education Personnel—Brazil (CAPES)—Finance Code 001. Fellowship grants to P.H.M.C. (CAPES 1808006) and L.Z.M. (CNPq 154900/2018-4). A.M.M. is CNPq research fellow (grant 310736/2018-8) and M.L.M (grant 306635/2018-6).

Authors contribution

Conceived and designed the study—PHMC; Sample processing: PHMC, LZM, MVR, STD; APP; Analyzed the data—PHMC, MLM, SCB, AMM; Writing (original draft preparation)—PHMC, RSR, WEF, MLM; Funding: PHMC, MLM, SCB, AMM. All authors read and approved the final manuscript.

Data availability

The data that support the findings of this study are available from the corresponding author upon reasonable request.

Declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable guidelines for the care and use of animals were followed by the authors.

Footnotes

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Availability Statement

The data that support the findings of this study are available from the corresponding author upon reasonable request.

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