Norileca indica (Milne Edwards, 1840)

Kottarathil, Helna Ameri, Sahadevan, Amrutha Vani, Kattamballi, Rijin & Kappalli, Sudha, 2019, Fig. 3 in Fig. 1. Norileca indica and its protandrous hermaphroditic reproductive system. A in Chloeia incerta de Quatrefages 1866, Zoological Studies 58 (35), pp. 1-12 : 2-6

Occurrence of Norileca indica

Out of the 3752 individuals of Rastrelliger kanagurta surveyed, 1152 showed infection with the cymothoid N. indica ; the prevalence, intensity, and abundance were recorded as 30.70%, 1.71, and 0.52, respectively. A total of 1962 parasite specimens were recovered at different life cycle stages: 1062 females (54.12%), 810 males (41.28%), 76 transitionals (3.87%), and 10 juveniles (0.50%) ( Figs. 1 and 2 ; Table 1). In two instances, a pair of infective stage manca II was also recovered ( Fig. 2C ). A boxplot representation of the size (length) variation in recovered parasites at different life cycle stages is given in figure 3. There was a steep increase in the length of parasites in the sequential developmental stages from juvenile to male, transitional, and female stages.

In most instances (804/1962 recovered parasites), two N. indica individuals simultaneously parasitized one host. Among them, 89.17% (717/804) were male-female, 7.46% (60/804) were male-transitional, 0.37% (3/804) were female-juvenile, 0.62% (5/804) were juvenile-male, 0.12% (1/804) were male-male, 0.49% (4/804) were female-transitional, 0.12% (1/804) were juvenile-juvenile, and 1.61% (13/804) were female-female ( Fig. 4 ). Of the remaining fish individuals with a single parasite (17.83%; 350/1962), 312 were female (89.14%), 26 were male (7.42%), and 12 were transitional (3.42%) ( Table 1). Of these fish occupied by a single parasite, the vacant gill chamber showed a deep pit-like depression, indicating that a parasite had been there before. In total, 1062 females were recovered, 903 of which were further classified according to the condition of their brood pouch. 40% of females carried eggs (uncleaved or embryonic stage), 23% carried larvae in their marsupium, 19% had an empty brood pouch, and 18% had no brood pouch ( Fig. 5).

Monthly and seasonal variations in prevalence

The prevalence of N. indica in R. kanagurta exhibited monthly variation ranging from 11.6 to 51.6%; the maximum prevalence was recorded in March and minimum prevalence in September. From October, the prevalence of N. indica showed a steady increase from 19.66% and maximum prevalence was noticed in March (51.6%). During April and May, the prevalence of N. indica infection was high and stable (46.66% and 47%, respectively); prevalence then dropped over the subsequent months until September ( Fig. 6 ). In order to analyze the variation in prevalence across seasons, the months were categorized into winter (October-January), pre-summer/summer (February-May), and monsoon/ post-monsoon months (June-September). Norileca indica presence fluctuated significantly across seasons ( Fig. 7 ). The prevalence was significantly highest (p = 0.001) during the pre-summer/summer months, and declined significantly (p = 0.029) during the monsoon/ post-monsoon periods. However, the prevalence was not statistically significant (p = 0.098) between winter and monsoon/post-monsoon periods. According to the Bonferroni test, the rate of prevalence was significantly different between the following periods; pre-summer/ summer and winter, monsoon/post-monsoon and pre-summer/summer. There was no significant difference in the rate of prevalence between monsoon/post-monsoon and winter.

Correlations between host and parasite

Of the 88 marine fish species in the families surveyed ( Scombridae , Stromateidae , Carangidae , Teraponidae , Ambassidae , Engraulidae , Belonidae , Clupeidae , Dasyatidae , etc.), the cymothoid N. indica was recovered only from the Indian mackerel Rastrelliger kanagurta , suggesting that this is its only host in the Malabar Coast. In all instances, the brachial chamber of the host fish appeared to be the only site that N. indica infected ( Fig. 2 ). The parasite was found settled in the chamber with its dorsal side facing the brachial floor and abdomen facing the operculum. It used the pereopods to cling to the mucus membrane of the operculum; the cephalon was oriented towards the anterior end of the host fish ( Fig. 2A ). The shape of the female body was shown to have characteristic asymmetry depending on whether it occupied the right or left branchial chamber of the host—the body of those occupying the right brachial cavity was hunched to the left and that occupying the left cavity was hunched to the right.

Norileca indica was found to be significantly more prevalent in large host fish (total length: 16.1–24 cm) than small ones (total length: 12–16 cm) (p = 0.048). Larger fish harbored larger parasites, and most small fish harbored juvenile parasites. A positive correlation was observed between host fish and parasite size (R 2 = 0.16, r = 0.40; N = 46) ( Fig. 8).

The fecundity of N. indica ranged from 64–540, and parasite size ranged from 23.5–34.0 mm. A total of 18 female parasites were sampled for fecundity analysis. A positive correlation was observed between the size of female N. indica and their fecundity (R 2 = 0.61, r = 0.78; N = 18) ( Fig. 8).

The continuous lodging of parasites resulted in the formation of a large pit in the gill chamber. The physical forces exerted by the parasite on the gills might be the reason why the gill filaments often atrophied, especially those of the 1st and 2nd holobranchs. Its severity was found to be relatively high in gill chambers where largesized female N. indica settled ( Fig. 2D ). The mucus membrane of the operculum also showed severe damage with copious secretions of mucous, likely due to the clinging of the parasite.

Figures

Fig. 1. Life cycle stages of N. indica recovered from R. kanagurta. ES-1, ES-II, and ES-III: Eggs undergoing embryonic development; Manca-I and Manca-II: larval stages; male, transitional, and female: adult stages.

Fig. 2. Infection by N. indica – site of attachment, tissue damage, and adaptations for clinging to the host fish. A, Male-Female (ñ -ò) pair in the gill chamber (branchial cavity) of R. kanagurta; B, juvenile-ò pair; C, Manca-II (first infective stage); D and E. damaged gill chamber (arrow) and gills due to the infection of N. indica; F, gill of uninfected fish j- Juvenile, m-manca-I. G, male pereopods; H, female pereopods; I, mouthpart complex.

Fig. 4. Occurrence of N. indica in pairs with different life cycle stage combinations. M/F: male-female (89.17%; 717/804), male-transitional (7.46%; 60/804), female-juvenile (0.37%; 3/804), juvenile-male (0.62%; 5/804), male-male (0.12%; 1/804), female-transitional (0.49%; 4/804), juvenile-juvenile (0.12%; 1/804), and female-female (1.61%; 13/804).

Fig. 6. Monthly prevalence of N. indica along the Malabar Coast of Kerala during the study period.

Fig. 7. Seasonal variation in the prevalence of N. indica along the Malabar Coast of Kerala. Overall variations among the three seasons was statistically shown using one-way ANOVA (** p = 0.0011). Paired t-test of prevalence between monsoon/post-monsoon and winter seasons (ns-no significance; p = 0.0983) and paired t-test of prevalence at pre-summer/summer vs monsoon/post-monsoon were significantly different (p = 0.0293).