# Monogenean fauna of alien tilapias (Cichlidae) in south China

Shuai Zhang, Tingting Zhi, Xiangli Xu, Yingying Zheng, Charles Félix Bilong

Bilong, Antoine Pariselle, Tingbao Yang

► To cite this version:

Shuai Zhang, Tingting Zhi, Xiangli Xu, Yingying Zheng, Charles Félix Bilong Bilong, et al., Monogenean fauna of alien tilapias (Cichlidae) in south China. Parasite, 2019, 26, pp.4. 10.1051/parasite/2019003. hal-03136238

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https://hal.umontpellier.fr/hal-03136238

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# Monogenean fauna of alien tilapias (Cichlidae) in south China

Shuai Zhang<fnref n="1" />, Tingting Zhi<fnref n="1" />, Xiangli Xu<fnref n="1" />, Yingying Zheng<fnref n="1" />, Charles Félix Bilong Bilong<fnref n="2" />, Antoine Pariselle<fnref n="3" />,*,
and Tingbao Yang<fnref n="1" />,*

Received 27 July 2018, Accepted 11 January 2019, Published online 4 February 2019

**Abstract** – Tilapias are important aquaculture fishes that have been introduced widely all over the world, often carrying their monogenean parasites with them. An extensive investigation on monogeneans of invasive tilapias was conducted in 19 natural water sources in south China between July 2015 and December 2017. We found nine known species of monogeneans, i.e., *Enterogyrus coronatus*, *E. malmbergi*, *Cichlidogyrus cirratus*, *C. halli*, *C. sclerosus*, *C. thurstonae*, *C. tilapiae*, *Scutogyrus longicornis*, *Gyrodactylus cichlidarum*, and one unknown *Gyrodactylus* species. In addition to reporting ten new hosts and four new geographical records, we observed new morphological characteristics of these species. Observation on living specimens of *Enterogyrus* spp. demonstrated that these two species have characteristic opisthaptoral retraction capacities, while the opisthaptor glands were not observed in our specimens of *E. coronatus* and *E. malmbergi*. The morphological differences of the accessory piece of the male copulatory complex between *C. cirratus* and *C. mbirizei* (character for species differentiation) could result from the observation at different perspectives, which indicates that *C. mbirizei* is likely a synonym of *C. cirratus*. A more detailed structure of the sclerotized parts of *Cichlidogyrus* spp. and *S. longicornis* were revealed by scanning electron microscopy. As was the case for the monogeneans found on alien tilapias from other geographic regions, the present study confirmed the high potential of these monogeneans to establish populations in new habitats.

**Key words:** Tilapias, *Enterogyrus*, *Cichlidogyrus*, *Scutogyrus*, *Gyrodactylus*, China.

**Résumé** – La faune des Monogènes des tilapias (Cichlidae) introduits en Chine du Sud. Les tilapias sont des poissons importants pour l'aquaculture dans le monde entier, où ils ont été largement introduits, souvent accompagnés de leurs Monogènes parasites. Suite à une étude extensive menée de juillet 2015 à décembre 2017 dans le Sud de la Chine, nous avons retrouvé 9 espèces déjà connues de ces parasites, à savoir *Enterogyrus coronatus*, *E. malmbergi*, *Cichlidogyrus cirratus*, *C. halli*, *C. sclerosus*, *C. thurstonae*, *C. tilapiae*, *Scutogyrus longicornis*, *Gyrodactylus cichlidarum*, plus un *Gyrodactylus* inconnu. En plus de dix nouveaux hôtes et de quatre nouvelles localités signalés pour ces espèces, nos résultats montrent quelques différences morphologiques avec les descriptions originnelles des espèces. Sur les spécimens vivants d'*Enterogyrus* l'opisthapteur montre des capacités de rétraction variables, ce qui n'a jamais été décrit chez *E. coronatus* et *E. malmbergi* ; ces hapteurs ne présentent pas de glandes. La différence principale entre *C. cirratus* et *C. mbirizei* (la forme de l'extrémité de la pièce accessoire de l'organe copulateur) pourrait n'être que le résultat de l'angle avec lequel on l'observe, ce qui pourrait indiquer une synonymie entre ces deux espèces. Des images en microscopie électronique à balayage montrent de nouveaux détails des pièces sclérifiées des espèces de *Cichlidogyrus* sp. et de *S. longicornis*. Comme cela a été le cas pour les Monogènes trouvés sur des tilapias introduits dans d'autres régions du monde, la présente étude confirme leur fort potentiel à établir des populations dans de nouveaux habitats.

<footnote n="1">¹ State Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory for Improved Variety Reproduction of Aquatic Economic Animals, and Research Center for Parasitic Organisms, School of Life Sciences, Sun Yat-sen University, Guangzhou 510275, China</footnote>

<footnote n="2">² Laboratory of Parasitology and Ecology, University of Yaoundé I, PO Box 812, Yaoundé, Cameroon</footnote>

<footnote n="3">³ ISEM, Univ Montpellier, CNRS, IRD, Montpellier, France</footnote>

<footnote>*Corresponding author: lssytb@mail.sysu.edu.cn;
antoine.pariselle@ird.fr</footnote>
## Introduction

Tilapias/Tilapia is the general name of fishes belonging to *Oreochromis* Günther, 1889, *Sarotherodon* Rüppell, 1852, *Tilapia* Smith, 1840 and *Coptodon* Gervais, 1848, all members of the Cichlidae. They are important aquaculture fishes in the world and have been introduced to at least 140 countries and have turned into worldwide invasive fishes [10]. As an important component of parasite fauna of tilapias, monogenean species reported from indigenous tilapias are very abundant, especially *Cichlidogyrus* species [26, 49]. In the course of tilapias introduction, monogenean species have unintentionally been brought to non-native countries, including the United States [40], Australia [57], Brazil [22, 56], China [28, 37, 58, 59], Colombia [25], Cuba [36], Iraq [1], Japan [33], Malaysia [29], Mexico [23, 46], Philippines [2], South Africa [26, 30], Thailand [27] and the UK [20], although there was a report of the whole gill parasite community loss [17].

As the country with the highest tilapias aquaculture production [16], China initially introduced Mozambique tilapia (*O. mossambicus* Peters, 1852) from Vietnam in 1956; other tilapias were then also introduced for culture or breed improvement [9, 60]. In the course of tilapias culture, the escapees gradually established wild populations in many natural waters of south China [21], which has become a great concern because they will not only damage the aquatic community, but also act as a refuge for aquaculture pathogens. In addition, they could acquire native parasites ([8, 23], and our unpublished data) and may spillback the parasites acquired to the endemic hosts [24]. However, extensive investigation of monogeneans of tilapias was lacking, although several sporadic reports indicated the existence of the alien gill parasites on tilapias in China [28, 37, 58, 59]. To fill this gap, an extensive investigation on the monogenean fauna of feral tilapias was carried out in south China between July 2015 and December 2017. The results presented in this paper include the monogenean fauna of tilapias and a supplementary description of new morphological features for three species.

## Material and methods

### Ethics

All the experimental handling was carried out in compliance with animal safety and ethics rule issued by the School of Life Sciences, Sun Yat-sen University.

### Host and parasite collection

Investigation of wild tilapias and their monogenean fauna was conducted in 19 natural waters sources in south China. These sampling locations were selected based on field study and reports [21, 37, 59] to cover the distribution of wild tilapias in south China (Fig. 1, Table 1). Year-round investigations were implemented monthly in three reservoirs from April 2016 to August 2017: Nanshui reservoir (24°44′N, 113°10′E), Gaozhou reservoir (22°08′N, 111°05′E) and Songtao reservoir (19°24′N, 109°33′E) to cover the seasonality of infection (data about seasonality of infection unpublished). Fishes

were identified by morphological features according to Fish-Base (www.fishbase.org). Nile tilapia *Oreochromis niloticus* and its hybrids were accepted as *O. niloticus* due to their indistinguishable morphologies. *Oreochromis niloticus* samples in Guangzhou, Guangdong Province were purchased from a local fish farm or caught from a small pond in the south campus of Sun Yat-sen University. These fishes were kept in the laboratory for observation of live parasite specimens.

Fish samples caught in the wild were individually killed and examined for parasites in the gills, stomach and urinary bladder. The parasite examination for the fish samples kept in the laboratory included the body surface. For identification, live monogeneans were detached with a dissecting needle, pipetted out, and mounted in a drop of ammonium picrate glycerin (GAP) on a slide under a coverslip, which was sealed using nail polish. After identification, target slides were rinsed in distilled water for 12–24 h until the nail polish could be easily removed, and the detached specimens were stored in vessels for further studies.

### Light microscopy and scanning electron microscopy

For SEM studies, worms were processed for scanning electron microscopy (SEM) according to Mo and Appleby [38] or Fannes et al. [15], sputter coated with gold and finally examined under Quanta 400 (FEI, Netherlands) in the Instrumental Analysis & Research Center, Sun Yat-sen University. For light microscopy studies, identified worms were digested following the protocol depicted by Fannes et al. [15], and later remounted in GAP on slides. Or alternatively, specimens were rinsed several times with water before being stained in Modified Gomori's Trichrome, dehydrated in an ethanol gradient, cleared in clove oil, and finally mounted in neutral Canada balsam. For *Gyrodactylus* species, GAP preserved specimens were digested *in situ*: proteinase K solution was dripped on one side of the coverslip, while a piece of filter paper was placed on the opposite side until the GAP solution was entirely replaced by proteinase K solution; later the same method was used to replace the digestive fluid by GAP solution.

### Morphological analyses

The numbering of the sclerotized parts of the species in genera *Scutogyrus*, *Cichlidogyrus* and *Enterogyrus* was adopted from ICOPA IV [14] and the terminology followed Pariselle and Euzet [49]. For *Gyrodactylus* species, the measurements of sclerotized parts and terminology followed Shinn et al. [54]. The terminology was employed as follows: anchor instead of gripus or hamulus; hooks rather than marginal hook, uncinulus or hooklet, and ventral bar instead of ventral transverse bar. Additionally, the ventral bar length represents the length of one branch rather than the whole length (with that of *Gyrodactylus* as an exception). The metrics are shown in Figure 2.

Photographs and measurements of the sclerotized parts were taken under an Olympus DX41 microscope equipped a DP73 Olympus camera (Olympus, Japan), and processed by the software cellSens Standard 1.7.1. Illustrations were drawn
<figure><img src="image_3.png" /><figcaption>**Figure 1.** Map of investigation sites of tilapias in south China. AM natural preservation zone, Macau; BN Lancang River, Xishuangbanna, Yunnan Province; BS Boai River, Baise, Guangxi Province; CJ Shilu reservoir, Changjiang, Hainan Province; CM Jiatan reservoir, Chengmai, Hainan Province; CZ Han River, Chaozhou, Guangdong Province; DZ Songtao reservoir, Danzhou, Hainan Province; FZ Min River, Fuzhou, Fujian Province; GM Nongba reservoir, Lincang, Yunnan Province; GZ fish farm and pond in Sun Yat-sen University, Guangzhou, Guangdong Province; HK Nandu River, Haikou, Hainan Province; HL fish market, Hualien, Taiwan; HY Xinfengjiang reservoir, Heyuan, Guangdong Province; LZ Liu River, Liuzhou, Guangxi Province; MM Gaozhou reservoir, Maoming, Guangdong Province; NN Bachi River, Nanning, Guangxi Province; QN Lancang River, Lincang, Yunnan Province; QZ Jin River, Quanzhou, Fujian Province; SG Nanshui reservoir, Shaoguan, Guangdong Province; XM Xixi River, Xiamen, Fujian Province.</figcaption></figure>

freehand with the aid of an Olympus U-DA drawing attachment and then digitized and processed using Adobe Illustrator CS6 (Adobe, USA). All measurements were taken in micrometers and presented in the following order: mean ± standard deviation (minimum – maximum, number of measurements). Voucher specimens were stored in the Research Center for Parasitic Organisms, School of Life Sciences, Sun Yat-sen University (SYSU) and a set of whole-mount specimens was also deposited in the Muséum National d'Histoire Naturelle, France (MNHN).

## Results

A total of 3,426 feral tilapias (including 1,789 *Coptodon zillii*, 113 *Sarotherodon galilaeus*, 1,477 *O. niloticus* and 47 *O. mossambicus*) and more than 50 cultured *O. niloticus* from south China were examined for monogenean parasites (see Table 1). The ten species of monogeneans collected belong to two families:

- Ancyrocephalidae Bychowsky & Nagibina, 1968 with three genera *Enterogyrus* Paperna, 1963, *Cichlidogyrus* Paperna, 1960 and *Scutogyrus* Pariselle & Euzet, 1995.

* From the stomach of the fish:

* *Enterogyrus coronatus* Pariselle, Lambert & Euzet, 1991 and *E. malmbergi* Bilong Bilong, 1988.

* From gills of the fish:

* *Cichlidogyrus cirratus* Paperna, 1964; *C. halli* Price & Kirk, 1967; *C. sclerosus* Paperna & Thurston, 1969; *C. thurstonae* Ergens, 1981 and *C. tilapiae* Paperna, 1960.

* *Scutogyrus longicornis* Paperna & Thurston, 1969.

- Gyrodactylidae Cobbold, 1864 with the genus *Gyrodactylus* von Nordmann, 1832 and the species *G. cichlidarum* Paperna, 1968 and *Gyrodactylus* sp1.

The urinary bladders did not host monogenean species.

## Family Ancyrocephalidae Bychowsky & Nagibina, 1968

### Genus *Enterogyrus* Paperna, 1963

#### *Enterogyrus coronatus* Pariselle, Lambert & Euzet, 1991

Type host: *Coptodon guineensis* (Perciformes: Cichlidae).

Hosts: *Oreochromis niloticus* and *Coptodon zillii*.

Site of infection: Stomach.

Type locality: Ebrié lagoon, Cote d'Ivoire.

Localities: Nanshui reservoir, Shaoguan, Guangdong province; Gaozhou reservoir, Maoming, Guangdong province; Xinfengjiang reservoir, Heyuan, Guangdong Province; River Liu, Liuzhou, Guangxi province; Boai River, Baise, Guangxi Province; Bachi River, Nanning, Guangxi Province; Jin River, Quanzhou, Fujian Province; Lancang River, Lincang, Yunnan Province; Lancang River, Xishuangbanna, Yunnan Province.

Number of voucher specimens observed: 31 (SYSUECO1-30; MNHN HEL906).

Description (Figs. 3, 4a-c, 10j): Four eyespots well developed without lenses. Tegument thick and transversally striated. Opisthaptor shape variable (tongue- or cup-shaped). Adults 421 ± 76.2 (292-574, 30) long and 149 ± 26.7 (101-205, 30) wide. Pharynx globular 32 ± 6.9 (22-56, 30) in diameter. Dorsal anchor with shaft longer than blade: *a* = 10 ± 2 (8-20, 29), *b* = 14 ± 2.6 (10-27, 29), *c* = 18 ± 3 (13-30, 29), *d* = 7 ± 1.2 (5-13, 29), *e* = 5 ± 1.3 (3-9, 29). Ventral
<table><caption>**Table 1.** Monogeneans of invasive tilapias with mean abundance in south China.</caption><thead><tr><th>Sites</th><th>Abbr.</th><th>Waters</th><th>Host species</th><th>No.</th><th>Cci</th><th>Cha</th><th>Csc</th><th>Cth</th><th>Cti</th><th>Slo</th><th>Eco</th><th>Ema</th></tr></thead><tbody><tr><td rowspan="3">Baise</td><td rowspan="3">BS</td><td rowspan="3">River</td><td>C. zillii</td><td>30</td><td>0.3</td><td>0.1</td><td>×</td><td>×</td><td>0.8</td><td>×</td><td>0.3</td><td>×</td></tr><tr><td>S. galilaeus</td><td>30</td><td>×</td><td>&lt;0.1</td><td>0.6</td><td>×</td><td>11.4</td><td>×</td><td>×</td><td>×</td></tr><tr><td>O. niloticus</td><td>30</td><td>2</td><td>6.6</td><td>6.1</td><td>1.6</td><td>12.9</td><td>3.4</td><td>×</td><td>0.1</td></tr><tr><td rowspan="2">Changjiang</td><td rowspan="2">CJ</td><td rowspan="2">Reservoir</td><td>C. zillii</td><td>20</td><td>0.9</td><td>0.1</td><td>×</td><td>×</td><td>3.4</td><td>1.3</td><td>×</td><td>×</td></tr><tr><td>O. niloticus</td><td>22</td><td>1.5</td><td>2.3</td><td>0.1</td><td>1.4</td><td>42.7</td><td>0.9</td><td>×</td><td>×</td></tr><tr><td rowspan="2">Chengmai</td><td rowspan="2">CM</td><td rowspan="2">Reservoir</td><td>C. zillii</td><td>128</td><td>0.9</td><td>0.2</td><td>×</td><td>&lt;0.1</td><td>5.1</td><td>&lt;0.1</td><td>×</td><td>×</td></tr><tr><td>O. niloticus</td><td>39</td><td>0.1</td><td>3.5</td><td>2.5</td><td>3</td><td>9.8</td><td>6.1</td><td>×</td><td>&lt;0.1</td></tr><tr><td rowspan="3">Chaozhou</td><td rowspan="3">CZ</td><td rowspan="3">River</td><td>C. zillii</td><td>108</td><td>0.1</td><td>×</td><td>&lt;0.1</td><td>×</td><td>0.4</td><td>&lt;0.1</td><td>×</td><td>×</td></tr><tr><td>S. galilaeus</td><td>13</td><td>×</td><td>×</td><td>0.4</td><td>×</td><td>6.5</td><td>×</td><td>×</td><td>0.2</td></tr><tr><td>O. niloticus</td><td>26</td><td>0.3</td><td>×</td><td>1.2</td><td>×</td><td>7.1</td><td>1.3</td><td>×</td><td>0.1</td></tr><tr><td rowspan="3">Danzhou</td><td rowspan="3">DZ</td><td rowspan="3">Reservoir</td><td>C. zillii</td><td>23</td><td>×</td><td>×</td><td>×</td><td>×</td><td>0.4</td><td>×</td><td>×</td><td>×</td></tr><tr><td>O. mossambicus</td><td>15</td><td>0.3</td><td>0.1</td><td>8.9</td><td>0.4</td><td>5.5</td><td>1.3</td><td>×</td><td>1.6</td></tr><tr><td>O. niloticus</td><td>492</td><td>5.2</td><td>7.7</td><td>3.7</td><td>7.5</td><td>11.9</td><td>6.9</td><td>×</td><td>1.6</td></tr><tr><td rowspan="3">Fuzhou</td><td rowspan="3">FZ</td><td rowspan="3">River</td><td>C. zillii</td><td>25</td><td>×</td><td>×</td><td>×</td><td>×</td><td>1</td><td>×</td><td>×</td><td>×</td></tr><tr><td>S. galilaeus</td><td>13</td><td>×</td><td>×</td><td>0.2</td><td>×</td><td>1.5</td><td>×</td><td>×</td><td>×</td></tr><tr><td>O. niloticus</td><td>17</td><td>×</td><td>×</td><td>0.1</td><td>×</td><td>0.6</td><td>×</td><td>×</td><td>×</td></tr><tr><td>Gengma</td><td>GM</td><td>Reservoir</td><td>O. niloticus</td><td>31</td><td>0.6</td><td>×</td><td>1.3</td><td>×</td><td>5.9</td><td>2.9</td><td>×</td><td>×</td></tr><tr><td>Guangzhou</td><td>GZ</td><td>Captivity</td><td>O. niloticus</td><td>&gt;50</td><td>×</td><td>×</td><td>√</td><td>√</td><td>√</td><td>√</td><td>×</td><td>√</td></tr><tr><td rowspan="3">Haikou</td><td rowspan="3">HK</td><td rowspan="3">Estuary</td><td>C. zillii</td><td>10</td><td>×</td><td>×</td><td>×</td><td>×</td><td>4.8</td><td>×</td><td>×</td><td>×</td></tr><tr><td>O. mossambicus</td><td>32</td><td>×</td><td>×</td><td>×</td><td>×</td><td>×</td><td>×</td><td>×</td><td>×</td></tr><tr><td>O. niloticus</td><td>32</td><td>×</td><td>×</td><td>×</td><td>×</td><td>1</td><td>×</td><td>×</td><td>×</td></tr><tr><td rowspan="3">Heyuan</td><td rowspan="3">HY</td><td rowspan="3">Reservoir</td><td>C. zillii</td><td>29</td><td>&lt;0.1</td><td>×</td><td>×</td><td>×</td><td>3.7</td><td>×</td><td>0.2</td><td>×</td></tr><tr><td>S. galilaeus</td><td>6</td><td>×</td><td>×</td><td>×</td><td>×</td><td>6.3</td><td>×</td><td>×</td><td>×</td></tr><tr><td>O. niloticus</td><td>7</td><td>2</td><td>3.4</td><td>0.7</td><td>0.3</td><td>26.9</td><td>2.1</td><td>×</td><td>×</td></tr><tr><td>Hualien</td><td>HL</td><td>Captivity</td><td>O. niloticus</td><td>1</td><td>1</td><td>×</td><td>×</td><td>1</td><td>1</td><td>×</td><td>×</td></tr><tr><td rowspan="2">Liuzhou</td><td rowspan="2">LZ</td><td rowspan="2">River</td><td>C. zillii</td><td>40</td><td>×</td><td>×</td><td>×</td><td>×</td><td>0.3</td><td>×</td><td>1.8</td><td>×</td></tr><tr><td>O. niloticus</td><td>13</td><td>×</td><td>0.3</td><td>1.4</td><td>×</td><td>4.1</td><td>1.2</td><td>0.4</td><td>0.5</td></tr><tr><td rowspan="2">Macau</td><td rowspan="2">AM</td><td rowspan="2">Estuary</td><td>C. zillii</td><td>6</td><td>×</td><td>×</td><td>×</td><td>×</td><td>×</td><td>×</td><td>×</td><td>×</td></tr><tr><td>O. niloticus</td><td>6</td><td>×</td><td>×</td><td>×</td><td>×</td><td>×</td><td>×</td><td>×</td><td>×</td></tr><tr><td rowspan="2">Maoming</td><td rowspan="2">MM</td><td rowspan="2">Reservoir</td><td>C. zillii</td><td>553</td><td>0.6</td><td>0.3</td><td>&lt;0.1</td><td>0.1</td><td>4</td><td>0.1</td><td>0.8</td><td>&lt;0.1</td></tr><tr><td>O. niloticus</td><td>599</td><td>2.5</td><td>5</td><td>1</td><td>4.6</td><td>15.6</td><td>5</td><td>×</td><td>0.3</td></tr><tr><td rowspan="3">Nanning</td><td rowspan="3">NN</td><td rowspan="3">River</td><td>C. zillii</td><td>30</td><td>&lt;0.1</td><td>0.1</td><td>×</td><td>×</td><td>5.1</td><td>×</td><td>0.1</td><td>×</td></tr><tr><td>S. galilaeus</td><td>6</td><td>×</td><td>×</td><td>0.3</td><td>×</td><td>14.2</td><td>×</td><td>×</td><td>×</td></tr><tr><td>O. niloticus</td><td>32</td><td>0.4</td><td>6</td><td>4.4</td><td>4.1</td><td>19.6</td><td>10.4</td><td>×</td><td>0.1</td></tr><tr><td rowspan="2">Quannei</td><td rowspan="2">QN</td><td rowspan="2">River</td><td>C. zillii</td><td>34</td><td>0.7</td><td>×</td><td>×</td><td>×</td><td>3.8</td><td>0.1</td><td>3</td><td>×</td></tr><tr><td>O. niloticus</td><td>30</td><td>2.2</td><td>×</td><td>1.2</td><td>0.8</td><td>9.5</td><td>3.8</td><td>×</td><td>1</td></tr><tr><td rowspan="3">Quanzhou</td><td rowspan="3">QZ</td><td rowspan="3">River</td><td>C. zillii</td><td>42</td><td>×</td><td>×</td><td>&lt;0.1</td><td>×</td><td>0.3</td><td>×</td><td>&lt;0.1</td><td>×</td></tr><tr><td>S. galilaeus</td><td>26</td><td>×</td><td>×</td><td>0.7</td><td>×</td><td>7.1</td><td>×</td><td>×</td><td>×</td></tr><tr><td>O. niloticus</td><td>31</td><td>0.1</td><td>×</td><td>2.7</td><td>0.3</td><td>4.5</td><td>1.1</td><td>×</td><td>0.2</td></tr><tr><td>Shaoguan</td><td>SG</td><td>Reservoir</td><td>C. zillii</td><td>683</td><td>&lt;0.1</td><td>×</td><td>×</td><td>&lt;0.1</td><td>1</td><td>×</td><td>1.8</td><td>×</td></tr><tr><td rowspan="3">Xiamen</td><td rowspan="3">XM</td><td rowspan="3">River</td><td>C. zillii</td><td>5</td><td>×</td><td>×</td><td>×</td><td>×</td><td>2</td><td>×</td><td>×</td><td>×</td></tr><tr><td>S. galilaeus</td><td>19</td><td>×</td><td>×</td><td>0.1</td><td>×</td><td>0.6</td><td>×</td><td>×</td><td>×</td></tr><tr><td>O. niloticus</td><td>28</td><td>×</td><td>×</td><td>1.5</td><td>0.6</td><td>5</td><td>1.2</td><td>×</td><td>×</td></tr><tr><td rowspan="2">Xishuangbanna</td><td rowspan="2">BN</td><td rowspan="2">River</td><td>C. zillii</td><td>23</td><td>×</td><td>×</td><td>×</td><td>×</td><td>0.2</td><td>&lt;0.1</td><td>1</td><td>×</td></tr><tr><td>O. niloticus</td><td>42</td><td>0.1</td><td>5.6</td><td>3.5</td><td>1.7</td><td>2</td><td>1.5</td><td>×</td><td>0.1</td></tr></tbody></table>

Abbr., abbreviation of sites; No., sampling number; Cti, *Cichlidogyrus tilapiæ*; Cci, *C. cirratus*; Cth, *C. thurstonae*; Csc, *C. sclerosus*; Cha, *C. halli*; Slo, *Scutogyrus longicornis*; Eco, *E. coronatus*; Ema, *E. malmbergi*. √, sampled, but data not recorded; ×, not sampled; –, not examined. There were twelve *G. cichlidarum* sampled, including two *G. cichlidarum* collected from Gaozhou reservoir, Maoming (MM) and Songtao reservoir, Danzhou (DZ), respectively, and eight collected from laboratory reared *O. niloticus* in Guangzhou (GZ). Only one *Gyrodactylus* sp1. collected from Songtao reservoir, Danzhou.

anchor smaller than dorsal one: *a* = 14 ± 2 (9–23, 29), *b* = 12 ± 1.6 (9–20, 29), *c* = 5 ± 1 (4–10, 29), *d* = 5 ± 1.1 (3–9, 29), *e* = 4 ± 0.9 (2–7, 28). Thin and weak V-shaped ventral bar: *x* = 9 ± 2.3 (7–16, 23), *w* = 1 ± 0.2 (0–1, 23). Hooks (marginal hooks) robust except first and second pairs (thinner): *I* = 12 ± 0.9 (11–13.7, 25), *II* = 12 ± 0.8 (10–13.1, 25), *III* = 13 ± 0.9 (10–13.8, 23), *IV* = 13 ± 0.9 (10–14.3, 27), *V* = 14 ± 0.9 (11–15.7, 28), *VI* = 14 ± 0.7 (12–14.7, 27),

VII = 13 ± 0.7 (12–14.8, 27). Penis spiral pattern: 4–2–3, 52 ± 13.5 (46–123, 30) long and 6 ± 1.7 (3–13, 30) wide at the base. Eggs oval, length 72 (*n* = 1) and width 66 (*n* = 1).

Remarks: According to the measurements and descriptions of the sclerotized parts, the present specimens resemble *E. coronatus* Pariselle et al. [50]. The hooks were almost identical in length but pairs I and II are discernibly slenderer than others [30]. The parasite can stretch out its retractable
<figure><img src="image_4.png" /><figcaption>**Figure 2.** (A–B) Measurements studied. (A) Measurements used to study *Cichlidogyrus* spp. and *Scutogyrus* spp. DB dorsal bar: *h*, length of dorsal bar auricle; *w*, dorsal bar maximum width; *x*, dorsal bar total length; *y*, distance between auricles; *z*, dorsal bar base end length. A anchor: *a*, anchor total length; *b*, anchor blade length; *c*, anchor shaft length; *d*, anchor guard length; *e*, anchor point length. Vg vagina: *x*, vagina total length, *w*, vagina maximum width. MCC male copulatory complex: *Ap*, accessory piece straight length; *St*, stalk length; *He*, heel straight length; *Pe*, penis: *x*, penis total curved length; *w*, penis maximum width. Pl auxiliary plate: *x*, auxiliary plate total length; *w*, auxiliary plate maximum width. H hook straight length. VB ventral bar: *w*, ventral bar maximum width; *x*, length of one ventral bar branch. (B) Measurements used to study *Enterogyrus* spp. VB ventral bar: *x*, length of one ventral bar branch; *w*, ventral bar maximum width. A anchor: *a*, anchor total length; *b*, anchor blade length; *c*, anchor shaft length; *d*, anchor guard length; *e*, anchor point length. Pe penis: *x*, penis total curved length; *w*, penis base maximum width.</figcaption></figure>

opisthaptor to anchor the stomach wall and withdraw it to relo-
cate to a new site during movement (based on the observations
*in situ* and GAP preserved specimens). As a result, *E. coronatus*
can present two body shapes depending on the different status
of opisthaptor: cup- or tongue-shaped (Fig. 4). No opisthaptor
glands were observed in the stained specimens, which was
different from the description of *E. cichlidarum* by Paperna
[42].

In the eight locations (Baise, Heyuan, Liuzhou, Maoming,
Nanning, Quannei, Quanzhou and Xishuangbanna) where
*E. coronatus* coexisted with the hosts *O. niloticus* and *C. zillii*,
*C. zillii* was always found with *E. coronatus* infection, while
*O. niloticus* was only found to be infected in Liuzhou (see
Table 1). Especially in Maoming, where both *O. niloticus*
and *C. zillii* were monthly sampled for year-round, *E. coronatus*
was exclusively collected from *C. zillii* (prevalence: 32.2%;
mean intensity: 2.1). In the whole investigation, *E. coronatus*
was not collected from *S. galilaeus* and *O. mossambicus*. This
species had previously been reported from *Tilapia guineensis*
(*Coptodon guineensis*) [50], *Tilapia dageti* (*Coptodon dageti*)
[34], and *Pseudocrenilabrus philander philander* [30]. In a
word, *E. coronatus* shows host preference to *C. zillii* in China
and it possesses the potential to infect other cichlids. The

occurrence of this species in the stomach of *O. niloticus* and
*C. zillii* from China provides new localities and new host
records.

*Enterogyrus malmbergi Bilong Bilong, 1988*

Type host: *Oreochromis niloticus*.

Hosts: *Sarotherodon galilaeus*, *Oreochromis mossambicus*, *Oreochromis niloticus* and *Coptodon zillii*.

Site of infection: Stomach.

Type locality: Sanaga River, Cameroon.

Localities: A pond in Sun Yat-sen University and a fish farm in Guangzhou, Guangdong province; Gaozhou reservoir, Maoming, Guangdong province; Han River, Chaozhou, Guangdong Province; Boai River, Baise, Guangxi Province; Bachi River, Nanning, Guangxi Province; Liu River, Liuzhou, Guangxi Province; Songtao reservoir, Danzhou, Hainan province; Jiatan reservoir, Chengmai, Hainan Province; Jin River, Quanzhou, Fujian Province; Lancang River, Xishuangbanna, Yunnan Province; Lancang River, Lincang, Yunnan Province.

Voucher specimens observed and deposited: 32 (SYSUEMA1-31; MNHN HEL907).

Description (Figs. 5, 6a-c, 10i): Four eyespots well devel-
oped without lenses. Tegument thick and striated transversally.
<figure><img src="image_5.png" /><figcaption>**Figure 3.** Drawings of sclerotized parts of *E. coronatus* Pariselle, Lambert & Euzet, 1991. DA, dorsal anchor; VA, ventral anchor; VB, ventral bar; Pe, penis; I–VII, hooks.</figcaption></figure>

Opisthaptor slightly retractable, body cup-shaped. Adults 721 ± 94.2 (481–854, 31) long and 284 ± 43.3 (218–361, 31) wide. Pharynx globular 56 ± 10.3 (38–77, 31) in diameter. Dorsal anchor with shaft shorter than blade: *a* = 26 ± 1.3 (23–29, 31), *b* = 36 ± 1.1 (33–38, 31), *c* = 26 ± 1.4 (22–29, 31), *d* = 16 ± 1.1 (13–18, 31), *e* = 7 ± 0.7 (5–8, 31). Ventral anchor smaller than dorsal one: *a* = 20 ± 1 (18–22, 31), *b* = 15 ± 0.6 (14–16, 31), *c* = 10 ± 0.9 (7–12, 31), *d* = 10 ± 0.8 (7–11, 31), *e* = 5 ± 0.7 (4–7, 31). Straight-shaped robust ventral bar: *x* = 25 ± 1.5 (21–28, 31), *w* = 3 ± 0.4 (2–4, 31). Hooks short, robust and basically identical: *I* = 15 ± 1.1 (13–18, 29), *II* = 14 ± 1 (12–17, 29), *III* = 14 ± 0.7 (13–15, 29), *IV* = 15 ± 1.2 (12–17, 29), *V* = 15 ± 1 (13–17, 29), *VI* = 15 ± 1.1 (12–17, 29), *VII* = 15 ± 0.8 (14–17, 30). Penis spiral pattern: 3–2–1/3–1–2, 49 ± 3.9 (43–58, 31) long and 6 ± 0.8 (5–8, 31) wide at the base. Eggs oval, length 91 ± 2.8 (86–93, 5) and width 77 ± 2.7 (72–79, 5).

Remarks: The morphologies and measurements of the sclerotized parts of our specimens basically agree with the previous description of *E. malmbergi*, but are slightly larger [7], probably influenced by environmental conditions [11]. The *in situ* observation of *E. malmbergi* found that the wound in the stomach of hosts was larger than those caused by *E. coronatus* [31] and the persistence of infection will enlarge the wound. No opisthaptor glands were observed in this species, which was consistent with descriptions of other *Enterogyrus* species [3, 5–7, 30, 50] except *E. cichlidarum* which was ever described with opisthaptor

glands [42]. In addition, *E. malmbergi* has a much less retractable opisthaptor (only cup-shaped) than *E. coronatus* (Figs. 4, 6).

In the ten sampling sites (Baise, Chengmai, Chaozhou, Danzhou, Liuzhou, Maoming, Nanning, Quannei, Quanzhou and Xishuangbanna), where *E. malmbergi* coexisted with the hosts *O. niloticus* and *C. zillii*, this parasite was always collected from *O. niloticus*, but not from *C. zillii* except in Maoming where both *O. niloticus* and *C. zillii* were found to be infected (see Table 1). Even in Maoming, year-round investigations revealed that *E. malmbergi* had much higher infection levels in *O. niloticus* (prevalence: 16.4%; mean intensity: 1.4) than in *C. zillii* (prevalence: 1.4%; mean intensity: 1.1). In addition, *E. malmbergi* was also sampled from *S. galilaeus* and *O. mossambicus* in the present study, and had previously been reported from *Cichlasoma callolepis* [23]. These results indicate that *E. malmbergi* presents host preference to *O. niloticus* in China, but has the potential to infect other cichlids. It is the first record of *E. malmbergi* in China, and with *C. zillii*, *S. galilaeus* and *O. mossambicus* as new host records.

## Genus *Cichlidogyrus* Paperna, 1960

### *Cichlidogyrus cirratus* Paperna, 1964

Type host: *Sarotherodon galilaeus*.

Hosts: *Oreochromis mossambicus*, *Oreochromis niloticus* and *Coptodon zillii*.

Site of infection: Gills.
<figure><img src="image_6.png" /><figcaption>**Figure 4.** Different body shape of *E. coronatus* Pariselle, Lambert & Euzet, 1991 under coverslip and the motion of opisthaptoral sclerotized parts depicted in drawings. (a) Cup-shaped body (retracted); (b) interim body shape; (c) tongue-shaped body (relaxed).</figcaption></figure>

Type locality: Tiberias Lake, Israel.

Localities: Nanshui reservoir, Shaoguan, Guangdong province; Gaozhou reservoir, Maoming, Guangdong province; Xinfengjiang reservoir, Heyuan, Guangdong Province; Han River, Chaozhou, Guangdong Province; Boai River, Baise, Guangxi Province; Bachi River, Nanning, Guangxi Province; Songtao reservoir, Danzhou, Hainan province; Shilu reservoir, Changjiang, Hainan Province; Jiatan reservoir, Chengmai, Hainan Province; Jin River, Quanzhou, Fujian Province; Lancang River, Xishuangbanna, Yunnan Province; Nongba reservoir, Lincang, Yunnan Province; Lancang River, Lincang, Yunnan Province.

Voucher specimens observed and deposited: 31 (SYSUCCI1–30; MNHN HEL902).

Description (Figs. 7, 8a, b, 10a, b): Adults 809 ± 199 (362–1088, 30) long and 129 ± 21.2 (89–180, 30) wide at level of ovary. Pharynx globular 31 ± 5 (21–39, 27) in diameter. Dorsal anchor with short shaft and regularly curved blade: *a* = 46 ± 1.9 (42–50, 30), *b* = 39 ± 1.4 (36–41, 30), *c* = 3 ± 1.2 (1–6, 30), *d* = 12 ± 2.4 (7–17, 30), *e* = 14 ± 1.4 (11–17, 30). Arched dorsal bar: *h* = 16 ± 1.3 (14–19, 29), *w* = 9 ± 1.4 (5–13, 30), *x* = 41 ± 2.4 (36–45, 30), *y* = 14 ± 1.5 (11–18, 28). Ventral anchor with undeveloped shaft: *a* = 49 ± 2.1 (44–52, 30), *b* = 45 ± 2.3 (40–48, 30), *c* = 1 ± 0.9 (0–3, 30), *d* = 9 ± 1.5

(6–12, 30), *e* = 17 ± 0.8 (15–18, 30). V-shaped ventral bar: *x* = 37 ± 2 (32–41, 30), *w* = 6 ± 0.6 (5–7, 30). Hooks short: *I* = 15 ± 0.6 (14–17, 29), *II* = 13 ± 0.9 (11–15, 24), *III* = 16 ± 1.2 (14–20, 26), *IV* = 22 ± 1.3 (19–24, 29), *V* = 24 ± 1.3 (21–27, 28), *VI* = 22 ± 1.8 (15–23, 28), *VII* = 18 ± 1 (15–20, 27). Very long and thin coiled penis, starting in a bulb with marked heel. Accessory piece, connected with the penis bulb by a rod, coated by a large, oval and thin membrane extended to the bifurcate ends: *Pe* = 210 ± 20.9 (165–240, 26), *He* = 12 ± 3.4 (8–25, 30), *Ap* = 41 ± 3.3 (35–49, 30). Penis end double sharped, not blunt. Very long and thin spirally coiled vagina, no valuable length could be taken.

Remarks: *Cichlidogyrus cirratus* was first described by Paperna [43] from the gills of *Tilapia galilaea* (*Sarotherodon galilaeus*) in Lake Tiberias, Israel, and redescribed by Ergens [13] from the gills of *Tilapia nilotica* (*Oreochromis niloticus*) in River Nile, Egypt. In the present study, *C. cirratus* was collected from *O. mossambicus* (new host), *O. niloticus* and *Coptodon zillii*, but was not found in its type host (*S. galilaeus*).

The long winding penis and the short first pair of hooks differentiates *C. cirratus* from all other congeneric species from cichlid hosts, except *C. mbirizei* Muterezi Bukinga et al., 2012 [39, 49]. The measurements of *C. cirratus* were consistent with those of *C. mbirizei*, and the latter was distinguished from
<figure><img src="image_7.png" /><figcaption>**Figure 5.** Drawings of sclerotized parts of *E. malmbergi* Bilong Bilong, 1988. DA, dorsal anchor; VA, ventral anchor; VB, ventral bar; Pe, penis; I-VII, hooks.</figcaption></figure>

*C. cirratus* in the original description by the shape of the accessory piece of the male copulatory complex (*C. mbirizei* without long expansion at mid-length and with two ends of rounded outgrowth *versus C. cirratus* with long expansion and hooked ends) and the vagina (double pitch in *C. mbirizei* versus sinuous in *C. cirratus*). However, the thin, long and transparent expansion in the middle of the accessory piece of *C. cirratus* was variable due to the different perspectives (Fig. 8). Moreover, two types of accessory piece extremity (hooked versus rounded outgrowth) could transform in digested specimens, when the accessory piece turns over (Fig. 8). These morphological features suggest that *C. mbirizei* and *C. cirratus* are likely synonymous. Pending genetic study, these two species are kept valid in the present study.

*Cichlidogyrus cirratus* (or *C. mbirizei*) was also recorded from non-native tilapias in Malaysia and Thailand [27, 29]. In addition, *Cichlidogyrus* sp. (named as *C. bananensis* by Xiao [59]) found in Lancang River in China was likely a misidentified *C. cirratus* as it shows close morphological and morphometric similarities to the latter, which was also collected from the same locality in the present study.

**Cichlidogyrus halli** Price & Kirk, 1967

Type host: *Oreochromis shiranus*.

Hosts: *Sarotherodon galilaeus*, *Oreochromis mossambicus*, *Oreochromis niloticus* and *Coptodon zillii*.

Site of infection: Gills.

Type locality: Upper Shire River, Malawi.

Localities: Gaozhou reservoir, Maoming, Guangdong province; Xinfengjiang reservoir, Heyuan, Guangdong Province; Boai River, Baise, Guangxi Province; Bachi River, Nanning, Guangxi Province; Liu River, Liuzhou, Guangxi Province; Songtao reservoir, Danzhou, Hainan province; Jiatan reservoir, Chengmai, Hainan Province; Shilu reservoir, Changjiang, Hainan Province; Lancang River, Xishuangbanna, Yunnan Province; Hualien, Taiwan.

Voucher specimens observed and deposited: 31 (SYSU-CHA1-30; MNHN HEL901).

Remarks: The morphologies and measurements of the voucher specimens in the present study agree with the previous ones from *C. halli* [12]. This species was also described from non-native tilapias in Brazil [22], South Africa [32], Thailand [27], Malaysia [29], Japan [33] and China [37, 59]. It is the first record of *C. halli* in *Coptodon zillii* and *O. mossambicus*.

**Cichlidogyrus sclerosus** Paperna & Thurston, 1969

Type host: *Oreochromis mossambicus*.

Hosts: *Sarotherodon galilaeus*, *Oreochromis mossambicus*, *Oreochromis niloticus* and *Coptodon zillii*.

Site of infection: Gills.

Type locality: Kajansi, Uganda.
<figure><img src="image_8.png" /><figcaption>**Figure 6.** Different body shape of *E. malmbergi* Bilong Bilong, 1988 under coverslip and the motion of opisthoptoral sclerotized parts depicted in drawings. (a) Cup-shaped body (retracted); (b) interim body shape; (c) cup-shaped body (relaxed).</figcaption></figure>

**Localities:** A pond in Sun Yat-sen University and a fish farm in Guangzhou, Guangdong province; Gaozhou reservoir, Maoming, Guangdong province; Xinfengjiang reservoir, Heyuan, Guangdong Province; Han River, Chaozhou, Guangdong Province; Boai River, Baise, Guangxi Province; Bachi River, Nanning, Guangxi Province; Liu River, Liuzhou, Guangxi Province; Songtao reservoir, Danzhou, Hainan province; Shilu reservoir, Changjiang, Hainan Province; Jiatan reservoir, Chengmai, Hainan Province; Xixi River, Xiamen, Fujian Province; Jin River, Quanzhou, Fujian Province; Min River, Fuzhou, Fujian Province; Lancang River, Xishuangbanna, Yunnan Province; Nongba reservoir, Lincang, Yunnan Province; Lancang River, Lincang, Yunnan Province.

Voucher specimens observed and deposited: 31 (SYSUCSC1-30; MNHN HEL903).

**Remarks:** The morphologies and measurements of specimens in the present study agree with the previous ones of *C. sclerosus* [12, 45]. This species has been reported from non-native tilapias in Iraq [1], Mexico [23, 46], Colombia [25], Thailand [27], Malaysia [29], South Africa [32], Brazil

[22], Japan [33] and China [28, 37, 58, 59]. *Sarotherodon galilaeus* represents a new host record of this parasite.

**Cichlidogyrus thurstonae Ergens, 1981**

**Type host:** *Oreochromis niloticus*.

**Hosts:** *Sarotherodon galilaeus*, *Oreochromis mossambicus*, *Oreochromis niloticus* and *Coptodon zillii*.

**Site of infection:** Gills.

**Type locality:** Nile River, Egypt.

**Localities:** A pond in Sun Yat-sen University and a fish farm in Guangzhou, Guangdong province; Nanshui reservoir, Shaoguan, Guangdong province; Gaozhou reservoir, Maoming, Guangdong province; Xinfengjiang reservoir, Heyuan, Guangdong Province; Boai River, Baise, Guangxi Province; Bachi River, Nanning, Guangxi Province; Songtao reservoir, Danzhou, Hainan province; Shilu reservoir, Changjiang, Hainan Province; Jiatan reservoir, Chengmai, Hainan Province; Xixi River, Xiamen, Fujian Province; Jin River, Quanzhou, Fujian Province; Lancang River, Xishuangbanna, Yunnan Province; Lancang River, Lincang, Yunnan Province; Lancang River, Lincang, Yunnan Province.
<figure><img src="image_9.png" /><figcaption>**Figure 7.** Opisthaptoral and genital sclerotized parts of *Cichlidogyrus cirratus* Paperna, 1964. Ap, accessory piece; DB, dorsal bar; DA, dorsal anchor; He, heel; Pe, penis; VA, ventral anchor; VB, ventral bar; Vg, vagina; I–VII, hooks.</figcaption></figure>

<figure><img src="image_10.png" /><figcaption>**Figure 8.** Morphology of the male copulatory complex of the same specimen of *Cichlidogyrus cirratus* observed in different angles. (a) undigested *C. cirratus*, (b) digested *C. cirratus*.</figcaption></figure>

Voucher specimens observed and deposited: 32 (SYSUCTH1–31; MNHN HEL904).

Remarks: The morphologies and measurements agree with the previous ones of *C. thurstonae* [13, 47]. This species has been reported from non-native tilapias in Thailand [27], Malaysia [29], Brazil [22] and China [28, 37]. This is the first record of *C. thurstonae* from *Coptodon zillii*.

*Cichlidogyrus tilapiae* Paperna, 1960

Type host: *Sarotherodon galilaeus*.

Hosts: *Sarotherodon galilaeus*, *Oreochromis mossambicus*, *Oreochromis niloticus* and *Coptodon zillii*.

Site of infection: Gills.

Type locality: Jordan and coastal system, Israel.

Localities: A pond in Sun Yat-sen University and a fish farm in Guangzhou, Guangdong Province; Xinfengjiang reservoir, Heyuan, Guangdong Province; Han River, Chaozhou,

Guangdong Province; Gaozhou reservoir, Maoming, Guangdong Province; Nanshui reservoir, Shaoguan, Guangdong Province; Boai River, Baise, Guangxi Province; Liu River, Liuzhou, Guangxi Province; Bachi River, Nanning, Guangxi Province; Shilu reservoir, Changjiang, Hainan Province; Jiatan reservoir, Chengmai, Hainan Province; Songtao reservoir, Danzhou, Hainan Province; Nandu River, Haikou, Hainan Province; Min River, Fuzhou, Fujian Province; Jin River, Quanzhou, Fujian Province; Xixi River, Xiamen, Fujian Province; Lancang River, Xishuangbanna, Yunnan Province; Nongba reservoir, Lincang, Yunnan Province; Lancang River, Lincang, Yunnan Province; Hualien, Taiwan.

Voucher specimens observed and deposited: 33 (SYSUCTI1–32; MNHN HEL905).

Remarks: The morphologies and measurements of the present specimens agree with the previous ones of *C. tilapiae* [12, 13, 41], which has been reported from non-native tilapias
<figure><img src="image_11.png" /><figcaption>**Figure 9.** Scanning electron micrographs of genital sclerotized parts of species of *Cichlidogyrus*, *Scutogyrus* and *Enterogyrus*. (a) Male copulatory complex of *C. cirratus*; (b) penis end of male copulatory complex of *C. cirratus*; (c) male copulatory complex of *C. sclerosus*; (d) male copulatory complex of *C. thurstonae*; (e) male copulatory complex of *S. longicornis*; (f) penis basement of *S. longicornis*; (g) vagina of *S. longicornis*; (h) male copulatory complex of *C. halli*; (i) penis of *E. malmbergi*; (j) penis of *E. coronatus*.</figcaption></figure>

in Iraq [1], Mexico [23], Colombia [25], Thailand [27], Malaysia [29], Japan [33], South Africa [32], Australia [57] and Brazil [22, 56]. *Cichlidogyrus haplochromii* Paperna & Thurston, 1969 found in Lancang River and Guangzhou in China by Li et al. [28], Meng [37] and Xiao [59], was obviously a misidentification of *C. tilapiae* due to their high degree of similarities in both measurements and morphologies.

**Genus Scutogyrus Pariselle & Euzet, 1995**

**Scutogyrus longicornis Paperna & Thurston, 1969**

Type host: *Sarotherodon galilaeus*.

Hosts: *Sarotherodon galilaeus*, *Oreochromis mossambicus*, *Oreochromis niloticus* and *Coptodon zillii*.

Site of infection: Gills.

Type locality: Lakes Georges and Albert, Uganda.

Localities: A pond in Sun Yat-sen University and a fish farm in Guangzhou, Guangdong province; Gaozhou reservoir, Maoming, Guangdong province; Han River, Chaozhou, Guangdong Province; Xinfengjiang reservoir, Heyuan, Guangdong Province; Bachi River, Nanning, Guangxi Province; Boai River, Baise, Guangxi Province; Liu River, Liuzhou, Guangxi Province; Songtao reservoir, Danzhou, Hainan province; Shilu reservoir, Changjiang, Hainan Province; Jiatan reservoir, Chengmai, Hainan Province; Xixi River, Xiamen, Fujian Province; Jin River, Quanzhou, Fujian Province; Lancang River, Xishuangbanna, Yunnan Province; Nongba reservoir, Lincang, Yunnan Province; Lancang River, Lincang, Yunnan Province; Hualien, Taiwan.

Voucher specimens observed and deposited: 31 (SYSUSLO1-30; MNHN HEL908).
<figure><img src="image_12.png" /><figcaption>**Figure 10.** Opisthaptoral sclerotized parts of *Gyrodactylus* sp1. (a) Central hook complex; (b) ventral bar; (c) hook; (d) hook sickle; (e) dorsal bar.</figcaption></figure>

**Remarks:** The description of specimens in the present study generally agrees with the previous ones of *S. longicornis* in morphologies and measurements [12, 45], except that a single large and numerous very small holes were seen on the basal portion of the male copulatory organ (see Fig. 9f) which were not previously described. This species had been reported from non-native tilapias in the Philippines [2], Mexico [23], Thailand [27], Malaysia [29], South Africa [32], Brazil [22] and China [28, 37, 58, 59].

**Family Gyrodactylidae Cobbold, 1864**

**Genus *Gyrodactylus* von Nordmann, 1832**

**Gyrodactylus cichlidarum Paperna, 1968**

Type host: *Sarotherodon galilaeus*.

Hosts: *Oreochromis niloticus*.

Site of infection: Skin, fins and rarely gills.

Type locality: Accra plain, Ghana.

**Localities:** A pond in Sun Yat-sen University and a fish farm in Guangzhou, Guangdong province; Gaozhou reservoir, Maoming, Guangdong province; Songtao reservoir, Danzhou, Hainan province.

Voucher specimens observed and deposited: 13 (SYSUGCH1-13).

**Remarks:** The morphologies and measurements of voucher specimens in the present study agree with the previous descriptions of *G. cichlidarum* which was firstly described by Paperna [44] in Ghana and redescribed by García-Vásquez et al. [20]. This species had also been reported from non-native tilapias in the Philippines [2] (*G. niloticus* was synonymized with *G. cichlidarum* [20]) and Mexico [46].

**Gyrodactylus sp1.**

Hosts: *Oreochromis niloticus*.

Site of infection: Gills.

**Localities:** Songtao reservoir, Danzhou, Hainan province.

Voucher specimens observed and deposited: 1 (SYSUSP1-1).

**Description (Fig. 10):** Only one GAP mounted specimen was measured under coverslip pressure. Body 373 long, 77 wide at level of uterus. Haptor, pharynx bulb and penis not measurable. Total length of anchor (hamulus) 50, shaft 32 long, point 22 long, root 22 long, aperture distance 16, proximal shaft width 7, distal shaft width 3, inner curve length 3. Anchor aperture angle 38°, anchor point curve angle 10° and inner anchor aperture angle 43°. Dorsal bar with two protuberances, 1.4 wide, 14 long. Ventral bar with two big rounded auricular processes, 19 wide, 35 long, ventral bar processes 9 long, mid-length of ventral bar processes 12 long, median portion 5 wide, ventral bar membrane 18 long. Hooks total length 23, shaft length 18, filament loop length 11, hook aperture length 3, sickle length 4, sickle proximal width 3, sickle distal width 3, instep height 0.4 and toe length 1.2.

**Remarks:** Although only one specimen has been collected, its characteristics of dorsal bar (with two protuberances) and ventral bar (with two large rounded auricular processes) made it resemble *Gyrodactylus yacatli* García-Vásquez et al., 2011 [19], which was first described from the gills and fins of *O. niloticus* cultured in Mexico and also from the fins of *O. niloticus* and *Pseudocrenilabrus philander* in Zimbabwe [61]. The marginal hook sickles of the present specimen are different from former descriptions (i.e., with a larger angle) [19, 61]. However, the drawings of dorsal bar in these descriptions were not consistent; the former had a straight dorsal bar but the latter possessed a dorsal bar with two protuberances. Our specimen was more like the description of Zahradníčková et al. [61], but could not be definitively identified.

**Discussion**

**Morphological characteristics of relevant monogenean species**

To date, there are eight valid African species of *Enterogyrus*, namely *E. cichlidarum* Paperna, 1963; *E. malmbergi*; *E. melenensis* Bilong Bilong, Birgi & Lambert, 1989;
*E. barombiensis* Bilong Bilong, Birgi & Euzet, 1991; *E. foratus* Pariselle, Lambert & Euzet, 1991; *E. coronatus*; *E. amieti* Bilong Bilong, Euzet & Birgi, 1996, and *E. crassus* Bilong Bilong, Birgi & Euzet, 1996 [3, 5-7, 49]. These species were initially described with two different opisthaptor features (cup- or tongue-shaped), which were used for the division of *Enterogyrus* into two groups [6, 30, 50]. However, the results in the present study, based on the observation of live worms of *E. coronatus* and *E. malmbergi* in situ, did not support this hypothesis. *Enterogyrus coronatus* presented a variable opisthaptoral shape during anchoring on the stomach wall (opisthaptor tongue-shaped) and shifting from one location to another (opisthaptor cup-shaped). The opisthaptor of *E. coronatus* was more variable than that of *E. malmbergi* which could only present a cup-shaped opisthaptor. In addition, the opisthaptoral sclerotized parts (posterior hooks (pairs I and II), ventral anchors and ventral bar) of *E. coronatus* were discernibly slenderer than those of *E. malmbergi*. This might facilitate the extension of the opisthaptor and its penetration into the stomach wall. Pathologically, *E. malmbergi* caused larger wounds than *E. coronatus* [31] in the stomach of the host, which might be ascribed to the larger body size and less extensible opisthaptor. This inference needs further confirmation by comparing the pathologies of other *Enterogyrus* species with slenderer opisthaptor sclerotized parts (*E. cichlidarum*, *E. melenensis*, *E. barombiensis*, *E. foratus* and *E. amieti*), and that of *E. crassus* which possesses larger opisthaptoral sclerotized parts.

The identification of *Cichlidogyrus* species was primarily based on the two-dimensional morphologies of the sclerotized parts in the whole-mount specimens, e.g., GAP preserved specimens. Based on the three-dimensional morphologies of the accessory piece terminal of the male copulatory complex of *C. cirratus*, considerable change was detected as a result of different view angle in the present study. This hints that three-dimensional morphologies of isolated sclerotized parts by modern technical methods such as laser scanning confocal fluorescence microscopy can provide more comprehensive information for taxonomic studies [18, 53].

## Monogenean fauna of exotic tilapias

Gill monogeneans from introduced tilapias have been studied widely around the world [1, 2, 22, 23, 25-29, 32, 46, 52, 56, 58], whereas few reports are available about stomach [2, 23, 30, 40], skin or fins parasites [20, 46]. However, there are no reports about urinary bladder monogeneans in invasive tilapias, though *Tilapia* sp. can be infected by *Urogyrus cichlidarum* Bilong Bilong, Birgi & Euzet, 1994 in Cameroon [4].

The introduction and spread of non-indigenous tilapias could be associated with the introduction and spread of their parasites, but the parasite species richness often decreased in comparison with that in their native range [55]. For example, it was reported that the monogenean species of *O. niloticus* numbered 18 in its native range [26, 48], while in the introduced areas they numbered between 1 and 7 although the species presented were similar [1, 2, 21, 22, 26-28, 32, 44, 50, 54, 56]. The similar monogenean species composition might be related to the similarity of tilapia strains cultured in different areas, e.g., genetically improved farmed tilapia

(GIFT), which was widely introduced and cultured around the world. It was ever reported once that the monogenean species were completely lost as a result of tilapia introduction [17]. In the present study, the monogenean fauna of tilapias also shows different species loss in the different locations (see Table 1), e.g., only *C. tilapiae* was found in two sites (Haikou and Gengma) and even no parasites in Macau.

This study reported ten new host records of several monogeneans on tilapias (*E. coronatus* from *Coptodon zillii* and *O. niloticus*; *E. malmbergi* from *Coptodon zillii*, *S. gali-laeus* and *O. mossambicus*; *C. halli* from *Coptodon zillii* and *O. mossambicus*; *C. thurstonae* from *Coptodon zillii*; *C. cirratus* from *O. mossambicus*; *C. sclerosus* from *S. gali-laeus*), which demonstrated their lower host specificity. However, the host specificities of these species were basically consistent with previous reports [35, 51]. In addition, the distinct host preference of *Enterogyrus* species (*E. malmbergi* prefers to infect *O. niloticus*; *E. coronatus* prefers to infect *Coptodon zillii*), together with the preferences of *Cichlidogyrus* and *Scutogyrus* species to *O. niloticus* in the present study, could be ascribed to the considerable intergeneric and parental care behavior differences of hosts [35].

In China, *Cichlidogyrus levequei* Pariselle & Euzet, 1996 was previously reported from *O. niloticus* [28], but it was not collected in the present study. However, the existence of this species in China is really doubtful because authors could not provide specimens and the description was too simple to judge the species [28]. In addition, *C. levequei* was recorded to be specific to the host *Coptodon coffea* which is endemic in West Africa [48].

## Conflict of interest

The authors declare no conflicts of interest.

*Acknowledgements.* This work was supported financially by the National Science Foundation grants (31472284 and 31872603) and Guangzhou science and technology plan project (2014J4100243) to Tingbao Yang in Sun Yat-sen University. The authors would also like to thank the two reviewers and the Editor-in-Chief for their great assistance to improve the manuscript.

## References

1. Abdul-Ameer KN, Atwan FK. 2016. First record of two species of the genus *Cichlidogyrus* Paperna, 1960 (Monogenea, Ancyrocephalidae) in Iraq on gills of two cichlid fishes. American Journal of Biology and Life Sciences, 4(3), 12-15.

2. Arthur JR, Lumanlan-Mayo S. 1997. Checklist of the parasites of fishes of the Philippines: FAO Fisheries Technical Paper. No. 369. FAO: Rome. p. 102.

3. Bilong Bilong CF, Birgi E, Euzet L. 1991. *Enterogyrus barombiensis* n. sp. (Monogenea, Ancyrocephalidae) parasite stomacal de trois Cichlidae endémiques du lac de cratère Barombi Mbo (Cameroun). Annales de Parasitologie humaine et comparée, 66, 105-108.

4. Bilong Bilong CF, Birgi E, Euzet L. 1994. *Urogyrus cichlidarum* gen. nov., sp. nov., Urogyridae fam. nov., monogène parasite de la vesse urinaire de poissons cichlidés au Cameroun. Canadian Journal of Zoology, 72, 561-566.
5. Bilong Bilong CF, Birgi E, Lambert A. 1989. *Enterogyrus melenensis* n. sp. (Monogenea, Ancyrocephalidae), parasite stomacal de *Hemichromis fasciatus* Peters, 1857 (Téléostéen, Cichlidae) du Sud-Cameroun. Revue de Zoologie Africaine, 103, 99-105.

6. Bilong Bilong CF, Euzet L, Birgi E. 1996. Monogenean stomach parasites of cichlid fishes from Cameroon: Two new species of the genus *Enterogyrus* Paperna, 1963 (Ancyrocephalidae). Systematic Parasitology, 34, 37-42.

7. Bilong Bilong CF. 1988. *Enterogyrus malmbergi* n. sp. (Monogenea-Ancyrocephalidae) parasite de l'estomac du Cichlidae *Tilapia nilotica* Linné, 1757 au Sud-Cameroun. Annales de la Faculté des Sciences de Yaoundé, Biologie-Biochimie, 5, 51-58.

8. Bittencourt LS, Pinheiro DA, Cárdenas MQ, Fernandes BM, Tavares-Dias M. 2014. Parasites of native Cichlidae populations and invasive *Oreochromis niloticus* (Linnaeus, 1758) in tributary of Amazonas River (Brazil). Revista Brasileira de Parasitologia Veterinária, 23, 44-54.

9. Chen SZ, Ye W. 1994. Preliminary study of the introduced tilapia species of China. Chinese Journal of Zoology, 29(3), 18-23. [in Chinese].

10. Deines AM, Wittmann ME, Deines JM, Lodge DM. 2016. Tradeoffs among ecosystem services associated with global tilapia introductions. Reviews in Fisheries Science & Aquaculture, 24(2), 178-191.

11. Dmitrieva E, Dimitrov G. 2002. Variability in the taxonomic characters of Black Sea gyrodactylids (Monogenea). Systematic Parasitology, 51, 199-206.

12. Douëllou L. 1993. Monogeneans of the genus *Cichlidogyrus* Paperna, 1960 (Dactylogyridae: Ancyrocephalinae) from cichlid fishes of Lake Kariba (Zimbabwe) with descriptions of five new species. Systematic Parasitology, 25, 159-186.

13. Ergens R. 1981. Nine species of the genus *Cichlidogyrus* Paperna, 1960 (Monogenea: Ancyrocephalinae) from Egyptian fishes. Folia Parasitologica, 28, 205-214.

14. Euzet L, Prost M. 1981. Report of the meeting on Monogenea: Problems of systematics, biology and ecology, in Review of advances in parasitology. Slusarski W, Editor. P.W.N Polish Scientific: Warsaw. p. 1003-1004.

15. Fannes W, Vanhove MPM, Huyse T, Paladini G. 2015. A scanning electron microscope technique for studying the sclerites of *Cichlidogyrus*. Parasitology Research, 114(5), 2031-2034.

16. FAO. 2018. Fishery and Aquaculture Statistics. Global aquaculture production 1950-2016 (FishstatJ), in FAO Fisheries and Aquaculture Department [online]. Rome. Updated 2018. www.fao.org/fishery/statistics/software/fishstatj/en. Accessed 20/06/2018.

17. Firmat C, Alibert P, Mutin G, Losseau M, Pariselle A, Sasal P. 2016. A case of complete loss of gill parasites in the invasive cichlid *Oreochromis mossambicus*. Parasitology Research, 115, 3657-3661.

18. Galli P, Strona G, Villa AM, Benzoni F, Fabrizio S, Doglia SM, Kritsky DC. 2006. Three-dimensional imaging of monogenoidean sclerites by laser scanning confocal fluorescence microscopy. Journal of Parasitology, 92(2), 395-399.

19. García-Vásquez A, Hansen H, Christison KW, Bron JE, Shinn AP. 2011. Description of three new species of *Gyrodactylus* von Nordmann, 1832 (Monogenea) parasitising *Oreochromis niloticus niloticus* (L.) and *O. mossambicus* (Peters) (Cichlidae). Acta Parasitologica, 56(1), 20-33.

20. García-Vásquez A, Hansen H, Shinn AP. 2007. A revised description of *Gyrodactylus cichlidarum* Paperna, 1968 (Gyrodactylidae) from the Nile tilapia, *Oreochromis niloticus niloticus* (Cichlidae), and its synonymy with *G. niloticus* Cone, Arthur et Bondad-Reantaso, 1995. Folia Parasitologica, 54, 129-140.

21. Gu DE, Mu XD, Xu M, Luo D, Wei H, Li YY, Zhu YJ, Luo JR, Hu YC. 2016. Identification of wild tilapia species in the main rivers of south China using mitochondrial control region sequence and morphology. Biochemical Systematics and Ecology, 65, 100-107.

22. Jerônimo GT, Speck GM, Cechinel MM, Gonçalves ELT, Martins ML. 2011. Seasonal variation on the ectoparasitic communities of Nile tilapia cultured in three regions in southern Brazil. Brazilian Journal of Biology, 71, 1-9.

23. Jiménez-García MI, Vidal-Martínez VM, López-Jiménez S. 2001. Monogeneans in introduced and native cichlids in México: Evidence for transfer. Journal of Parasitology, 87(4), 907-909.

24. Kelly DW, Paterson RA, Townsend CR, Poulin R, Tompkins DM. 2009. Parasite spillback: A neglected concept in invasion ecology? Ecology, 90, 2047-2056.

25. Kritsky DC, Thatcher VE. 1974. Monogenetic trematodes (Monopisthocotylea: Dactylogyridae) from freshwater fishes of Colombia, South America. Journal of Helminthology, 48, 59-66.

26. Le Roux LE, Avenant-Oldewage A. 2010. Checklist of the fish parasitic genus *Cichlidogyrus* (Monogenea), including its cosmopolitan distribution and host species. African Journal of Aquatic Science, 35(1), 21-36.

27. Lersuttichiewal T, Maneepitaksanti W, Purivirojkul W. 2015. Gill monogeneans of potentially cultured tilapias and first record of *Cichlidogyrus mbirizei* Bukinga et al., 2012, in Thailand. Walailak Journal of Science and Technology, 13(7), 543-553.

28. Li HY, Chen WT, Man GB, Yi ZS. 2009. Research on alien fish's Monogenea in Pearl River water system (part one): four species of Ancyrocephalidae parasiting in the gills of *Tilapia niloticus* (including three new records). Journal of Guangzhou University (Natural Science Edition), 8(3), 54-57. [in Chinese].

29. Lim SY, Ooi AL, Wong WL. 2016. Gill monogeneans of Nile tilapia (*Oreochromis niloticus*) and red hybrid tilapia (*Oreochromis* spp.) from the wild and fish farms in Perak, Malaysia: Infection dynamics and spatial distribution. SpringerPlus, 5(1), 1609.

30. Madanire-Moyo GN, Avenant-Oldewage A. 2014. A new locality and host record for *Enterogyrus coronatus* (Pariselle Lambert & Euzet (1991) in South Africa and a review of the morphology and distribution of *Enterogyrus* (Ancyrocephalidae) species. Helminthologia, 51(1), 13-22.

31. Madanire-Moyo GN, Avenant-Oldewage A. 2015. The histopathology of *Enterogyrus coronatus* Pariselle, Lambert & Euzet, 1991 (Monogeneoidea) in the stomach of the southern mouthbrooder *Pseudocrenilabrus philander* (Weber, 1897) (Cichlidae). African Zoology, 50(2), 175-180.

32. Madanire-Moyo GN, Matla MM, Olivier PAS, Luus-Powell WJ. 2011. Population dynamics and spatial distribution of monogeneans on the gills of *Oreochromis mossambicus* (Peters, 1852) from two lakes of the Limpopo River System, South Africa. Journal of Helminthology, 85(2), 146-152.

33. Maneepitaksanti W, Nagasawa K. 2012. Monogeneans of *Cichlidogyrus* Paperna, 1960 (Dactylogyridae), gill parasites of tilapias, from Okinawa Prefecture, Japan. Biogeography, 14, 111-119.

34. Mendlová M, Desdevises Y, Civáňová K, Pariselle A, Šimková A. 2012. Monogeneans of west African cichlid fish: Evolution and cophylogenetic interactions. PLoS One, 7(5), e37268.

35. Mendlová M, Šimková A. 2014. Evolution of host specificity in monogeneans parasitizing African cichlid fish. Parasites & Vectors, 7, 69.
36. Mendoza-Franco EF, Vidal-Martínez VM, Cruz-Quintana Y, Prats León FL. 2006. Monogeneans on native and introduced freshwater fishes from Cuba with the description of a new species of *Salsuginus* Beverley-Burton, 1984 from *Limia vittata* (Poeciliidae). Systematic Parasitology, 64, 181–190.

37. Meng FY. 2016. Morphological taxonomy of monogeneans and molecular identification of Diplozoidae and Ancyrocephalidae parasitizing 10 host fishes from Lancang River, Jinghong. Master thesis. Yunnan Normal University. [in Chinese].

38. Mo TA, Appleby C. 1990. A special technique for studying haptoral sclerites of monogeneans. Systematic Parasitology, 17, 103–108.

39. Muterezi Bukinga F, Vanhove MPM, Van Steenberge M, Pariselle A. 2012. Ancyrocephalidae (Monogenea) of Lake Tanganyika: III: *Cichlidogyrus* infecting the world's biggest cichlid and the non-endemic tribes Haplochromini, Oreochromini and Tylochromini (Teleostei, Cichlidae). Parasitology Research, 111(5), 2049–2061.

40. Noga EJ, Flowers JR. 1995. Invasion of *Tilapia mossambica* (Cichlidae) viscera by the monogenean *Enterogyrus cichlidarum*. Journal of Parasitology, 81(5), 815–817.

41. Paperna I. 1960. Studies of monogenetic trematodes in Israel. 2 monogenetic trematodes of cichlids. Bamidgeh Bulletin of Fish Culture in Israel, 12, 20–33.

42. Paperna I. 1963. *Enterogyrus cichlidarum* n. gen. n. sp., a monogenetic trematode parasitic in the intestine of fish. Bulletin of the Research Council of Israel, 11B, 183–187.

43. Paperna I. 1964. Parasitic helminths of inland-water fishes in Israel. Israel Journal of Zoology, 13(1), 1–26.

44. Paperna I. 1968. Monogenetic trematodes collected from fresh water fish in Ghana. Second report. Bamidgeh Bulletin of Fish Culture in Israel, 20, 80–100.

45. Paperna I, Thurston JP. 1969. Monogenetic trematodes collected from cichlid fish in Uganda; including the description of five new species of *Cichlidogyrus*. Revue de Zoologie et de Botanique Africaines, 79, 15–33.

46. Paredes-Trujillo A, Velazquez-Abunader I, Torres-Irineo E, Romero D, Vidal-Martinez VM. 2016. Geographical distribution of protozoan and metazoan parasites of farmed Nile tilapia *Oreochromis niloticus* (L.) (Perciformes: Cichlidae) in Yucatan, México. Parasites & Vectors, 9, 66.

47. Pariselle A, Bilong Bilong CF, Euzet L. 2003. Four new species of *Cichlidogyrus* Paperna, 1960 (Monogenea, Ancyrocephalidae), all gill parasites from African mouthbreeder tilapias of the genera *Sarotherodon* and *Oreochromis* (Pisces, Cichlidae), with a redescription of *C. thurstonae* Ergens, 1981. Systematic Parasitology, 56, 201–210.

48. Pariselle A, Euzet L. 1996. *Cichlidogyrus* Paperna, 1960 (Monogenea, Ancyrocephalidae): Gill parasites from West African Cichlidae of the subgenus *Coptodon* Regan, 1920 (Pisces), with descriptions of six new species. Systematic Parasitology, 34, 109–124.

49. Pariselle A, Euzet L. 2009. Systematic revision of dactylogyridean parasites (Monogenea) from cichlid fishes in Africa, the Levant and Madagascar. Zoosystema, 31(4), 849–898.

50. Pariselle A, Lambert A, Euzet L. 1991. A new type of haptor in mesoparasitic monogeneans of the genus *Enterogyrus* Paperna, 1963, with a description of *Enterogyrus foratus* n. sp. and *E. coronatus* n. sp, stomach parasites of cichlids in West Africa. Systematic Parasitology, 20, 211–220.

51. Pouyaud L, Desmarais E, Deveney M, Pariselle A. 2006. Phylogenetic relationships among monogenean gill parasites (Dactylogyridea, Ancyrocephalidae) infesting tilapiine hosts (Cichlidae): Systematic and evolutionary implications. Molecular Phylogenetics and Evolution, 38, 241–249.

52. Rindoria NM, Mungai LK, Yasindi AW, Otachi EO. 2016. Gill monogeneans of *Oreochromis niloticus* (Linnaeus, 1758) and *Oreochromis leucostictus* (Trewavas, 1933) in Lake Naivasha, Kenya. Parasitology Research, 115(4), 1501–1508.

53. Rossin MA, De Francesco PN, Timi JT. 2017. Three-dimensional morphology of rigid structures as a tool for taxonomic studies of Dactylogyridae (Monogenea). Parasitology Research, 116(10), 2813–2819.

54. Shinn AP, Hansen H, Olstad K, Bachmann L, Bakke TA. 2004. The use of morphometric characters to discriminate specimens of laboratory-reared and wild populations of *Gyrodactylus salaris* and *G. thymalli* (Monogenea). Folia Parasitologica, 51, 239–252.

55. Torchin ME, Mitchell CE. 2004. Parasites, pathogens and invasions by plants and animals. Frontiers in Ecology and the Environment, 2(4), 183–190.

56. Wanderson Pantoja MF, Neves LR, Dias MKR, Marinho RGB, Montagner D, Tavares-Dias M. 2012. Protozoan and metazoan parasites of Nile tilapia *Oreochromis niloticus* cultured in Brazil. Revista MVZ Córdoba, 17, 2812–2819.

57. Webb AC. 2003. The ecology of invasions of non-indigenous freshwater fish in north Queensland. PhD thesis. James Cook University.

58. Wu XY, Xie MQ, Li AX. 2006. Two new Chinese record genera — *Cichlidogyrus* Paperna, 1960 and *Scutogyrus* Pariselle & Euzet, 1995 (Monogenea, Ancyrocephalidae). Acta Zootaxonomica Sinica, 31(3), 536–540. [in Chinese].

59. Xiao JF. 2015. The morphology and host-specificity of Dactylogyridae and Ancyrocephalidae parasitizing 11 species of host fishes from Lancang River. Master thesis. Yunnan Normal University. [in Chinese].

60. Xiong W, Sui X, Liang SH, Chen Y. 2015. Non-native freshwater fish species in China. Reviews in Fish Biology and Fisheries, 25(4), 651–687.

61. Zahradníčková P, Barson M, Luus-Powell WJ, Přikrylová I. 2016. Species of *Gyrodactylus* von Nordmann, 1832 (Platyhelminthes: Monogenea) from cichlids from Zambezi and Limpopo river basins in Zimbabwe and South Africa: Evidence for unexplored species richness. Systematic Parasitology, 93(7), 679–700.

**Cite this article as:** Zhang S, Zhi T, Xu X, Zheng Y, Bilong Bilong CF, Pariselle A & Yang T. 2019. Monogenean fauna of alien tilapias (Cichlidae) in south China. *Parasite* **26**, 4.
<figure><img src="image_13.png" /></figure>

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