論文
Temporal Change in Infection of Philometroides seriolae (Nematoda: Philometridae) in the Definitive Host, Seriola quinqueradiata
2025 年 60 巻 4 号 p. 185-190
詳細
2025 年 60 巻 4 号 p. 185-190
Philometroides seriolae infection was monitored monthly over a 16-mo period in a single population of wild Japanese amberjack Seriola quinqueradiata, estimated to be 2–5 years old that maintained in a sea cage where no new infection could occur. The overall prevalence and mean intensity of infection was 65.0% (78/120) and 6.2 ± 5.5 worms per infected fish (1–26), respectively. Female nematodes, ranging from 2.0 to 41.3 cm in body length, were unevenly distributed within the skeletal muscle, with a higher proportion located in the dorsal (62.7%) and posterior (45.4%) regions. Some mature worms exited the host, while others remained in the muscle. Parasite remnants including dead worms, scars and empty cavities where nematode had resided, were observed in most of the fish examined. Live nematodes collected in July and August 2020 consisted of two size classes. In the following months, the larger worms disappeared, while smaller ones continued to grow, reaching lengths of up to 30 cm by June of the following year. These findings suggest that P. seriolae remains in Japanese amberjack for at least 1.5 year and that infection likely occurs through ingestion of small paratenic fish hosts.
Five species of parasites are known to infect the skeletal muscle of Japanese amberjack Seriola quinqueradiata, one of the most important fishery resources in Japan (Ogawa, 2023). Among them, the microsporidian, Microsporidium seriolae is the most serious parasite affecting cultured Japanese amberjack, as the infection is widespread among juveniles, and heavily infected individuals exhibit poor growth accompanied by increased mortality (Kawakami et al., 2021; Yanagi et al., 2021). In contrast, in wild Japanese amberjack, the large philometrid nematode Philometroides seriolae, which can reach up to 51 cm in length (Ishii, 1931), is the most significant and conspicuous parasite. All of these large worms are females, which grow to such remarkable sizes and typically inhabit a cavity within the host musculature, where their bodies are folded in a zigzag pattern (Ogawa, 2023). Although the infection is usually not fatal, marketable fish harboring these large worms lose their commercial value due to unaesthetic appearances of the parasite, resulting in serious economic losses.
Despite the industrial importance of this nematode, little is known about its infection patterns in wild populations of Japanese amberjack. Although the life cycle of P. seriolae was recently demonstrated experimentally using a surrogate copepod as the intermediate host (Ogawa et al., 2023), the natural intermediate hosts remain unidentified. Furthermore, knowledge of the parasite’s general biology, including its natural life cycle, development within the host and longevity, remains very limited. This study aimed to clarify the temporal dynamics of P. seriolae infection in the definitive host. For this purpose, we conducted a 16-month monitoring study on a single population of naturally infected Japanese amberjack, maintained in a sea cage where no new infections could occur, enabling assessment of seasonal changes in infection status and parasite development within the host.
Philometroides seriolae was sampled from a total of 120 individuals of Japanese amberjack with a mean fork length of 75.2 ± 5.7 cm and mean body weight of 5.6 ± 1.7 kg. These fish were caught in Nagasaki Prefecture, Japan in April 2020 and were estimated to be 2–5 years old at the time of capture, based on Watari et al. (2019). To prevent new infections, the amberjack were maintained in a net cage at Nagasaki Prefectural Institute of Fisheries, Nagasaki Prefecture, Japan, where no P. seriolae infection had been confirmed. The fish were initially fed a diet of defrosted fish and moist pellets, followed by dry pellets five days a week until satiated.
Sampling was conducted approximately once per month from April 2020 to August 2021 (a total of 16 occasions) with 3–10 fish examined at each sampling (Table 1). Each fish was filleted and sectioned into 1 cm slices to allow visually inspect for the presence of nematodes. When nematodes or their remnants were found, their numbers and locations on the fish body (right/left; ventral/dorsal; anterior/middle/posterior) were recorded (Fig. 1). Prevalence and intensity were recorded for both live nematodes and parasite remnants, including dead worms, scars and empty cavities where nematodes had previously resided (Fig. 2).
| Sampling date | Water temperature | No. examined | Body length (cm) | Fork length (cm) | Body weight (kg) | Infection prevalence (count) | Mean intensity (range) |
|---|---|---|---|---|---|---|---|
| 2020/4/21 | 16.9°C | 5 | 68.3 ± 5.6 | 76.7 ± 5.8 | 5.3 ± 1.2 | 80% (4/5) | 4.8 ± 3.1 (2–9) |
| 5/20 | 19.8°C | 5 | 70.7 ± 3.9 | 78.8 ± 4.1 | 5.3 ± 1.0 | 80% (4/5) | 1.8 ± 1.0 (1–3) |
| 6/17 | 23.9°C | 10 | 64.6 ± 4.4 | 72.3 ± 5.1 | 4.8 ± 1.0 | 40% (4/10) | 11.3 ± 10.5 (1–23) |
| 7/15 | 24.4°C | 10 | 63.2 ± 3.2 | 71.1 ± 3.6 | 4.3 ± 0.7 | 90% (9/10) | 10.7 ± 7.8 (3–26) |
| 8/12 | 28.6°C | 10 | 65.5 ± 4.3 | 73.2 ± 4.6 | 4.7± 1.1 | 100% (10/10) | 8.4 ± 5.0 (2–16) |
| 9/10 | 26.8°C | 10 | 66.2 ± 4.0 | 74.4 ± 4.4 | 4.6 ± 0.6 | 80% (8/10) | 7.6 ± 6.0 (1–18) |
| 10/8 | 23.9°C | 10 | 66.2 ± 3.9 | 74.1 ± 4.4 | 4.8 ± 0.4 | 50% (5/10) | 4.0 ± 2.4 (1–7) |
| 11/5 | 21.4°C | 10 | 64.5 ± 3.0 | 72.0 ± 3.2 | 4.7 ± 0.5 | 50% (5/10) | 3.4 ± 2.6 (1–7) |
| 12/8 | 17.8°C | 10 | 63.9 ± 4.4 | 71.5 ± 4.8 | 4.9 ± 0.9 | 80% (8/10) | 5.6 ± 4.1 (1–11) |
| 2021/1/12 | 14.3°C | 10 | 69.7 ± 4.1 | 77.9 ± 5.1 | 6.9 ± 1.3 | 60% (6/10) | 6.8 ± 8.8 (1–24) |
| 2/9 | 14.5°C | 10 | 71.1 ± 5.5 | 79.1 ± 6.0 | 7.7 ± 1.6 | 60% (6/10) | 2.7 ± 1.9 (1–6) |
| 3/9 | 14.7°C | 5 | 72.5 ± 4.9 | 80.6 ± 5.3 | 8.0 ± 1.3 | 40% (2/5) | 3.5 ± 2.1 (2–5) |
| 4/8 | 17.1°C | 5 | 75.6 ± 2.9 | 83.7 ± 3.5 | 8.6 ± 1.0 | 40% (2/5) | 4.0 ± 4.2 (1–7) |
| 5/18 | 20.2°C | 3 | 72.9 ± 4.8 | 81.0 ± 5.2 | 7.6 ± 1.2 | 67% (2/3) | 4.0 ± 2.8 (2–6) |
| 6/15 | 23.4°C | 3 | 72.6 ± 1.1 | 80.8 ± 1.4 | 7.1 ± 0.7 | 67% (2/3) | 3.0 ± 2.8 (1–5) |
| 8/6 | 30.1°C | 4 | 68.5 ± 3.1 | 76.3 ± 3.5 | 5.7 ± 0.9 | 25% (1/4) | 5.0 ± 0 (5) |
Recovered live nematodes were either fixed in 70% ethanol or frozen for later analysis. All intact specimens (n = 103) were individually photographed for body measurements using ImageJ software. Each worm was then dissected, and the contents in the uterus were collected into microtubes. The contents were thoroughly vortexed, and subsamples were photographed under a digital microscope. The number of eggs and larvae in each subsample image was counted, and the maturity status of each female nematode was categorized into three stages: 1) undeveloped (no eggs or larvae present), 2) ovigerous (eggs only), or 3) gravid (both eggs and hatched larvae present).
Temporal changes in the prevalence and intensity of infection, body size of female nematodes, and their reproductive development were analyzed to estimate the growth, maturation, and longevity of P. seriolae within Japanese amberjack.
Statistical analysisDifference in parasite abundance among the body regions (right/left; ventral/dorsal; anterior/middle/posterior) were analyzed using the chi-square test. Statistical analyses were performed using JMP ver. 17.2 (SAS Institute Japan), with the significance level set at p < 0.05.
Throughout the study period, a total of 485 live female parasites were collected. The overall prevalence and mean intensity of infection were 65.0% (78/120) and 6.2 ± 5.5 worms/infected fish (range: 1–26), respectively. There was no significant difference in parasite abundance between the left and right sides of the fish body. However, when both sides were combined, 62.7% of the worms were located on the dorsal side, compared to 37.3% on the ventral side, with a statistically significant difference (chi-square test, p < 0.0001) (Fig. 1). Similarly, the highest proportion of worms was found in the posterior region (45.4%), followed by the middle (37.3%) and anterior regions (17.3%), with statistically significant differences among these regions (p < 0.0001) (Fig. 1). Overall, 28.5% of worms were found in the dorso-posterior region.
Monthly prevalence and mean intensity of infection fluctuated between 25.0% and 100%, and between 1.8 and 11.3 worms/infected fish, respectively (Table 1, Fig. 3). In addition to live worms, parasite remnants were frequently observed (Fig. 2). Dead parasites, parasite scars, and empty cavity were present in 60–100%, with one exception of 25% (1/4) in August 2021, of the fish examined throughout the study period (Table 1, Fig. 4).
The body length of retrieved female nematodes ranged from 2.0 cm to 41.3 cm, with a mean (±SD) length of 17.4 ± 8.7 cm. Maturity of the nematodes generally progressed with body growth. Among the three maturity stages defined in Materials and Methods, 75% (39/52) of the undeveloped nematodes were less than 15 cm in body length, while 92% (33/36) of ovigerous ones were over 15 cm in body length and over 93% (14/15) of gravid ones reached more than 20 cm in length (Fig. 5).
Seasonal patterns were observed in parasite development: younger nematodes were more frequently detected from summer to autumn, while gravid worms increased from spring to early summer (Fig. 5). In July and August 2020, two distinct size groups were present: large, gravid worms exceeding 35 cm in body length (36.0–41.3 cm; n=5) and small ones mostly under 20 cm (2.0–21.4 cm; n=29), including one gravid individual, one ovigerous, and 27 without eggs or larvae in the uterus (Fig. 5). In the subsequent months, the large worms disappeared, while smaller ones continued to grow, reaching gravid, approximately 30 cm in length by June of the following year. The proportion of gravid nematodes gradually increased from January to June.
The two distinct size classes of P. seriolae females coexisted in July and August 2020, suggesting seasonality in parasite maturation. In our previous experimental study (Ogawa et al., 2023), two young adults of P. seriolae, one measuring 23.5 cm in body length and the other unmeasurable, were recovered from the skeletal muscle of Japanese amberjack 11 mo after the fish had ingested the copepod Tigriopus japonicus harboring infective larvae in their hemocoels. These worms were identified as ovigerous adults, as their uteri contained only eggs. Based on these experimental data, it is assumed that the large, fully gravid females in July and August in the present study had infected the fish at least one year earlier. Furthermore, the smaller nematodes detected during the same period became gravid by the following summer, indicating that maturation and development of P. seriolae females in the definitive host require more than one year. Combining the previous experimental findings with the present results, it is estimated that female P. seriolae remains within the definitive host for at least 1.5 years.
No large gravid females, which appeared in July and August 2020, were recovered in the following months. Besides, dead worms, their scars and empty cavities in the muscle tissues seem to increase from spring to summer months. These suggest that gravid females exited the host after completing development in summer months, likely to release hatched larvae into the environment, as previously reported by Nakajima et al. (1970), while concurrently some females succumbed in the host tissue. The reason why some gravid worms exited the host while others succumbed in the musculature remains unclear and warrants further investigation.
Japanese amberjack up to 10 cm in total length feed primarily on zooplankton, while those larger than 13 cm feed exclusively on fish (Anraku and Azeta, 1965). Under culture conditions, amberjack reach approximately 13 cm in body length at around 100 days of age (Yamazaki, 2006; Yamazaki et al., 2002). This suggests that the window during which Japanese amberjack can acquire P. seriolae infection by ingesting infected copepods is quite narrow. In other words, it is highly probable that the amberjack in this study, estimated to be 2–5 years old in April 2020, had acquired infection through ingestion of small fish acting as a paratenic hosts.
To date, Philometra obturans, which infects the piscivorous pike Esox lucius, is the only philometrid species known to utilize fish paratenic hosts as the primary route of infection (Moravec, 2004). Although the paratenic host(s) of P. seriolae has not yet been specified, the present findings represent a second case in which the involvement of paratenic fish host(s) is suggested in the life cycles of philometrid nematodes.
Philometroides seriolae infection rarely occurs in cultured Japanese amberjack. This is likely because small wild juveniles, known as “mojako”, which aggregate around drifting algae in early spring, are commonly used as seedlings for aquaculture. There have been no records of nematode infection in these wild-caught mojako. However, P. seriolae infection has occasionally been observed in cultured amberjack when larger-sized wild juveniles, up to one-year old, were used when mojako availability was insufficient (Ogawa, 2023). To avoid P. seriolae infection in aquaculture, it is strongly recommended that large-sized wild-caught fish, which have likely already become piscivorous, not be used as culture seeds.
The female nematodes were unevenly distributed within the host’s skeletal musculature, with higher proportion located in the dorsal side compared to the ventral side, and in the posterior region compared to the anterior and middle regions. The reason for the frequent occurrence of worms in the dorso-posterior region remains unclear, particularly given that this area is smaller than the anterior and middle body regions. Since P. seriolae infection may result in rejection of fish at market due to the presence of large, unaesthetic worms, particular attention should be given to careful inspection of the dorso-posterior region when assessing fish for the presence of this parasite.
We thank Jirou Miyahara, Takanobu Wakasugi, Yoshiyuki Ishii, Yasunori Masuyama, Hironori Okuda, Yasuko Oshita, Kumiko Furutani, Miwa Hamaguchi, Miha Ueno, Manami Sakamoto, Yumiko Okawa, Nagasaki Prefectural Institute of Fisheries, for their assistance in monthly inspections of Japanese amberjack for P. seriolae infection. We also express our gratitude to the members of Fish Disease Lab, Aquaculture Research Institute of Kindai University, for their assistance in data collection and organization. Part of this study was presented at the annual meetings of Japanese Society of Fish Pathology in Tokyo on March 17, 2025. This study was partially supported by a Grant-in-Aid for Scientific Research (C) (no. 21K05735) from the Japan Society for the Promotion of Science.
