Isolated Helminth Parasites
Cestodes (tapeworms) are a diverse group of exclusively parasitic flatworms with a unique morphology and complex life cycles [15, 56]. This includes the order Caryophyllidea, a small group of monozoic, non-segmented cestodes parasitizing freshwater teleost fishes. In Indomalayan region, 59 species of Caryophyllidea belonging to 15 genera and 3 families (Capingentidae, Caryophyllaeidae, and Lytocestidae) have been reported infecting the walking catfish, C. batrachus [8]. In this study, the isolated cestode from C. batrachus and C. gariepinus was B. serialis from the family Lytocestidae. This genus is widely distributed in the Philippines, India, Bangladesh, and Malaysia [8]. In the Philippines, B. serialis is well known for infecting the intestines of C. batrachus which were first recorded by Velasquez [69] and Lopez [46–47] in Luzon. It is believed that the said parasite was introduced into the country through the importation of C. batrachus for aquaculture [43]. On the other hand, no records of B. serialis were found infecting C. gariepinus in the country making this a new host record (Table 2). B. serialis is distinguished from other cestodes through the following morphological characteristics: (1) segmentation and proglottidization are absent on its body, (2) scolex exhibits no variation, has no specialized attachment organs, and has its widest part in the middle portion and is wider than the neck, (3) vitelline follicles having two lateral rows which reaches posteriorly to the cirrus sac from the tip of the scolex and within reach to the anterior arms of the ovary, and (4) a prominent H-shaped ovary located at the posterior end of the cestode (Fig. 3) [49].
Nematodes of the family Camallanidae are divided into three subfamilies: Camallaninae, Procamallaninae, and Paracamallaninae, and are mainly blood-sucking parasites found in the gastrointestinal tract of marine, brackish-water, and freshwater fishes, as well as several aquatic reptiles and amphibians [66]. In the Philippines, representatives of the genus Camallanus have been regularly documented in fishes belonging to family Channidae [4]. However, records suggest that no C. sonaiensis has been recorded in the country, making this the first study to document the said taxa infecting C. striata. C. sonaiensis is a new species of nematode that was first recorded in Assam, India infecting the intestines of Heteropneustes fossilis [44]. With 16.66% prevalence, 4.5 mean intensity, 0.44 abundance, and 1.5 index of infection, the said parasite was found to infect more female hosts than male ones. Males had a prevalence of 11.11%, abundance of 0.44, mean intensity of 4, and index of infection at 0.44. Furthermore, overall rates of prevalence (14.28%), mean intensity (4.3), abundance (0.62), and index of infection (1.86) were recorded in C. sonaiensis [44]. This nematode parasite is identifiable by the following characters: (1) large orange-brown buccal capsule with highly transversely striated cuticle, (2) internally, the buccal capsule has 9–10 beaded longitudinal ridges (lateral view), as well as 1–2 incomplete dorsal and ventral ridges, (3) a dorsal and ventral tridents, each with three posteriorly pointed prongs extending beyond the base of the buccal capsule. The central prong of the trident is wider and longer than the dorsal and ventral prongs making them unequal (4) a slender single spicule with a rounded and wider anterior end and pointed posterior end and (5) a tiny tail tapering to bifid spiny ends (dorsal and ventral) with 10–11 pairs of pedunculated caudal papillae (Fig. 4) [44].
On the other hand, the genus Contracaecum is the sole member of the Anisakidae family to have the potential to infect both terrestrial and aquatic hosts, along with a wide variety of vertebrates and invertebrates. With more than 100 species, the aforementioned genus is the most abundant and diverse group within the Anisakidae family [64]. Contracaecum nematodes go through a complex life cycle which involves the release of their egg into the water via the feces of a bird (the parasite's definitive host), which develops into a second-stage larvae (L2) before infecting aquatic arthropods such cyclopoid copepods (intermediate host). The L2 larvae subsequently become third-stage larvae (L3) after the infected copepod were consumed by a fish (another intermediate host). Thereafter, when the L3 larvae were eventually consumed by their definitive host, it develops into sexually mature adults and penetrates their intestinal wall and muscles, completing the life cycle [32]. In fishes, Contracaecum larval and adult forms may affect host health which can cause economic losses in fisheries [24]. On the other hand, humans serves as an accidental host of the aforementioned parasite through the unintentional consumption of its L3 larvae by eating an infected raw fish. This could lead in life-threatening anisakidosis, which is manifested by a variety of gastrointestinal symptoms [63]. In Africa, Contracaecum sp. has been recorded to be the most prevalent parasite of South African fishes [10]. It is found to be highly prevalent in C. gariepinus, infecting nearly all examined fishes, having an infection intensity of up to 700 to 2000 larvae [52]. In the Philippines, Hanviriyapant [30] first recorded the Contracaecum sp. larva isolated from the walls of pyloric caeca and intestine of Clarias macrocephalus in Luzon. C. macrocephalus is a native species in the Philippines, which may indicate that native hosts in the country has been infected by the said parasite long before C. garieinus has been introduced in the Philippines and parasite transmission may have been from native to invasive host, this however requires further investigation. Consequently, this study includes the first instance of the said parasite infecting the stomach of C. gariepinus. Species-level identification of the said parasite which occurs in fish as L3, is not possible due to the absence of its reproductive organs [11] and hence can be identified up to the genus level only through the following morphological characteristics: (1) presence of intestinal cecum and ventricular appendix and (2) an excretory pore located at the anterior end, near the boring tooth (Fig. 5) [41].
Trematodes from the family Cephalogonimidae are spinose digenean parasite, which are commonly found in the gastrointestinal tract of reptiles, fishes and amphibians [34]. The family is composed of five genera: Cephalogonimus, Paracephalogonimus, Cephalogonimoides, Emoleptalea, and Masenia. The latter is among the most significant digenean trematode parasites due to its wide geographic distribution worldwide [19]. Masenia has been recorded parasitizing the intestines of marine and freshwater ray-finned fishes (Actinoptrygii) in Africa and Asia [50]. Moreover, the definitive hosts of the said genus are known for their remarkable host specificity which are often fishes in the order Siluriformes which includes C. batrachus, Clarias anguillaris, Clarias senegalensis, Clarias fuscus, Heteropneustes fossilis, Mystus vittatus, and Rita rita in Asia and C. gariepinus, Clarias ngamensis, Clarias anguillaris, Synodontis victoriae, and Heterobranchus longifilis in Africa [22]. Similarly, records shows that C. gariepinus are commonly infected by two Masenia species namely M. bangweulensis [9] and Masenia nkomatiensis [26]. In this study, M. cf. bangweulensis were isolated from the intestine of C. gariepinus which is the first record in the Philippines. The main features of this digenetic trematode include (1) having two rows of alternating circumoral spines around the oral sucker, (2) an oval body that is widest at the level of the ovary and testis, (3) a funnel-shaped oral sucker and a spherical pharynx behind it, (4) an elongated and curved cirrus sac, (5) a spherical ventral sucker located one third of its body's length, (6) a circular ovary located behind the ventral sucker on the left side, and (7) a vitelline glands next to the testis (Fig. 6) [9, 10]. The identification of the said parasite can be confirmed by employing scanning electron microscopy (SEM) to examine the number of its circumoral spines which usually ranges from 44–48 and differs in every Masenia species [12].
Parasite and Host Fish Community in Marikina River
Albeit no significant difference due to a low number of representative samples, the high prevalence of parasites in C. batrachus and C. gariepinus could be attributed to the host’s ecology which is widely regarded as a significant factor influencing parasite burden than the host phylogeny [38]. In particular, Combes [21–22] introduced the term “Filters” which is the mechanism responsible for parasite-host co-existence that influence parasite burden. There are two types of filters: the encounter and the compatibility filter. The former is the probability that the host will have a contact with a certain parasite which can be influenced by host behavior, feeding habits, size and age among others. While, the latter is the probability that a parasite and a potential host can live together which can be influenced by the host’s and the parasite’s physiology and biology. Then, if the two aforementioned filters matches together it results to a successful parasite-host co-existence. For instance, host's diet has a significant role in the abundance and richness of parasites in fishes [40]. Omnivorous and carnivorous fishes such as those from the family Clariidae and Channidae respectively are more prone to infection because they consume mainly invertebrates and fishes which are commonly an intermediate host of some infective larval stage parasite [48, 58]. While, herbivorous fishes such as those from the family Loricaridae are less prone to infection because they mainly eat algae and plants [40].
Moreover, host body size is widely considered to be a factor in determining the richness of parasite species [60]. In the study of Mgbemena et al. [53], C. gariepinus of greater lengths and weight were found to have higher infection than their shorter counterparts. This could be rationally explained by the changes in their feeding behavior and food uptake capacity that arise with age, wherein older fish eat more and are hence more prone to ingest parasites [63]. Consequently, change of food preference as fish matures from macrophytes to zooplankton and macroinvertebrates which are commonly an intermediate host of some infective larval stage parasite coupled with the host's omnivorous feeding habits, can increase the likelihood that the host will ingest an infected prey and become infected [48].
On the other hand, the newly recorded parasite genera and species in the Philippines may play a key role in the impacts that IAFS hosts may pose in the alteration of disease dynamics in Marikina River [44]. This includes the "spillback" of parasites, in which parasite transmission from native hosts to alien hosts leads to an increase in infection in native hosts as alien hosts amplify its transmission [37], while in other circumstances a "dilution" occurs if alien hosts reduces the transmission [57].Additionally, new parasite species introduced to their non-native range may spread to native hosts, resulting in the emergence of new diseases in native fishes causing parasite "spillover" or "pathogen pollution" [72].