Зоологический журнал, 2022, T. 101, № 2, стр. 145-152

MATERIALS AND METHODS

RESULTS

Among 694 individuals of Monomia haanii examined, including 428 males and 266 females, 366 crabs (52.7%) were infested by epibiotic pedunculate barnacles. These barnacles belong to 4 species: Octolasmis angulata, O. neptuni, O. warwicki and Dianajonesia tridens (Fig. 1).

Fig. 1.

The epibiotic pedunculate barnacle infested portunid crab Momomia haanii: A – Octolasmis angulata on gill, B – O. neptuni on gill, C – O. warwicki on carapace, D – Dianajonesia tridens on maxilliped. Scale bars: 3 mm.

Each host was infested by 1 to 4 epibiont species. There is a clear negative correlation between the number of barnacle species infesting the crabs and the percentage of such crabs among infested crabs. The percentage of crabs hosting only 1 barnacle species was the highest (58.2% of infested crabs), while the percentage of crabs hosting all 4 barnacle species reached only 3.6% (Fig. 2).

Fig. 2.

Percentage of host infested by one to four epibiont barnacle species.

The prevalence of infestation by O. angulata on M. haanii was 49.6%, which was markedly higher than this of other barnacles. O. angulata and O. warwicki had the highest level of infestation intensity, 6 (1–97) and 6 (1–186) barnacles per host, respectively (Table 1).

Comparison of infestation state showed that the prevalence of infestation by each barnacle species was not significantly different between male and female crabs. Similarly, host sex had no impact on the median intensities of infestation by O. angulata and O. warwicki. On another hand, the median intensities of infestation by O. neptuni and D. tridens were determined by the host sex (Table 1).

Examined sample of female crabs included 74 ovigerous and 192 non-ovigerous individuals (Table 2). Prevalences of infestation by each of barnacle species of non-ovigerous crabs seemed to be higher than these of ovigerous crabs, but statistical analyses did not confirm these differences. Similarly, the median intensities of infestation did not differ significantly between these two host groups.

The impact of the crab size on the infestation state is presented in Table 3. Crabs of less than 40 mm carapace width were not infested. The smallest M. haanii bearing stalked barnacles was the male with the carapace width of 41 mm. Crabs of the size group 40–49 mm were infested by 2 epibionts: O. angulata and O. warwicki. The smallest crabs infested by O. neptuni and D. tridens were found in the group 50–59 mm. Prevalence of infestation strongly positively correlated with crabs’ size (Table 4). Similarly, the positive correlations between carapace width of hosts and median intensities of infestation by distinct species were observed.

Two species, O. angulata and O. neptuni colonized inner host branchial chambers at 4 different positions including: gills, maxillipeds, dorsal and ventral surfaces of the branchial chamber. O. warwicki attached to the external integument of the crab in the areas of the external surface of carapace, swimming legs, walking legs, chelipeds and abdomen. D. tridens were found on gills, the surface of the branchial chambers under the gills, maxillipeds and the carapace margin (the boundary between the branchial chamber and the external integument) (Table 5).

O. angulata: 4135 individuals of O. angulata were found on studied crabs with the majority attached on the surface of gills (64.8% of total) and the dorsal surface of the branchial chamber (34.8% of total) (Table 5). The median intensity of infestation differed significantly between gills 1 to 8. Most of O. angulata were concentrated on the surface of gills 4, 5 and 6. Among them, gill 4 was the most preferred site for the attachment with the largest number (1050 barnacles), the highest prevalence (30.4%) and the highest median intensity (3 (1–41)) of infestation. The infestation state parameters by each barnacle species on different gills are presented in Table 6.

O. neptuni: Similarly to O. angulata, O. neptuni was found exclusively in the branchial chamber of the host, mostly on the gills (73.1% of the total, Table 5). Majority of these barnacles were found on the gills from 4 to 6 (82.8% of the total on gills, Table 6). The median intensities of infestation did not differ significantly between gills.

D. tridens: The surface of gills hosted 85.3% of the total number of D. tridens (58 individuals, Table 5). Only 3 individuals were found at the margin of the carapace of a single host. This species preferred to attach to gills from 3 to 7, gill 4 was found to bear up to 38 individuals of D. tridens (65.5% of the total on gills, Table 6). The statistical analysis did not show a significant difference in the intensity of infestation among gills.

O. warwicki: The vast majority of O. warwicki was recorded on the external surface of hosts’ carapaces (Table 5). The number of barnacles attached to swimming legs was higher than these on walking legs and chelipeds. A single large female crab was recorded bearing 3 individuals of this barnacle on its abdomen.

DISCUSSION

In the present study, the infestation of Monomia haanii crabs by epibiont pedunculate barnacles was reported for the first time. Three of these barnacles belong to genus Octolasmis, the remaining species is Dianajonesia tridens (previously treated as Temnaspis or Octolasmis tridens (Koçak, Kemal, 2008)). The studies on infestation by epibiotic barnacles conducted on 2 other common portunid crabs (Portunus pelagicus and P. sanguinolentus) in the same area showed that all 4 species infesting M. haanii infest these hosts as well (Oanh et al., 2018, 2018a). The wide distribution of O. angulata among hosts is acknowledged in other studies as well (Jeffries et al., 1982; Kumaravel et al., 2009; Li et al., 2014; Rasheed, Mustaquim, 2017). Also, in the study performed in the waters off Singapore the lack of host specialization was observed in O. warwicki and D. tridens, from 12 portunid crab species studied, they infested 10 and 7 species, respectively. However, only in Vietnamese waters all pedunculate barnacles infested all studied hosts without exception. Waters of Central Vietnam represent a region characterized by relatively low pedunculate barnacle species diversity, i.e. only 4 barnacle species were found settling on all 3 portunid crab hosts studied (Oanh et al., 2018, 2018a). In comparison, in the waters off Singapore 10 barnacle species infested portunid crabs (Jeffries et al., 1982), in Indian waters portunid crabs were observed hosting 6 species of barnacles (Kumaravel et al., 2009), in the waters off Karachi 5 barnacle species were infesting portunid crabs (Rasheed, Mustaquim, 2017). On another hand, prevalence of infestation in Vietnam, where it ranges from 50.8 to 84.5%, depending on the host is markedly higher than this parameter in Indian (11.1–35.3%) and Pakistan (2.9–10.8%) waters and is on par with the region off Singapore (12–100%, only the hosts where the studied sample size was more than 19 individuals were considered). Summing up, we tend to conclude that Vietnamese waters represent a region with a relatively low pedunculate species diversity, absence of host preference and a relatively high level of prevalence of infestation.

With the impact of the environmental conditions, the morphology or biology of the host itself could significantly influence on the barnacle infestation. In particular, in the waters adjacent to Singapore 56 decapod species were examined in order to assess the infestation by octolasmis barnacles (Jeffries et al., 1982). Twenty seven species (including 12 portunid crabs) of them were observed bearing barnacles. Infestation prevalence varied from 12 to 100% among these carbs. Similarly, in the waters off central Vietnam, prevalence of infestation of P. sanguinolentus (Oanh et al., 2018a) was quite high (84.5%), while this parameter reached 50.8% in P. pelagicus (Oanh et al., 2018) and 58.7% in M. haanii (present study). Thus, Monomia haanii falls into the group of crabs highly subjected for infestation but is still less infested than the most infested species such as P. sanguinolentus or Scylla serrata (Jeffries et al., 1982; Oanh et al., 2018a).

With the exception of O. neptuni and D. tridens, the infestation status expressed in both prevalence and intensity did not depend on the sex of M. haanii. The same pattern of host sex dependent distribution was observed in barnacles infesting P. sanguinolentus in the waters off Vietnam (Oanh et al., 2018a). On the contrary, study on P. pelagicus in the same area revealed that host’s sex impact the abundance of all pedunculate barnacles, except O. neptuni (Binh et al., 2018). This observation leads us to conclusion that impact of the host’s sex is random and does not impact the infestation by pedunculate barnacles by itself. Similarly, studies in other regions do not reveal any clear pattern in impact of the host’s sex on infestation. Some studies show that there is no connection between these parameters (Santos, Bueno, 2002; Li et al., 2014), while in other prevalence, intensity or both parameters were significantly different between male and female hosts, even if the same species of the host or barnacle were studied (Rasheed and Mustaquim, 2017; Machado et al., 2013; Sheilds, 1992).

Infestation by stalked barnacles strongly positively correlated with the carapace width of the host. The similar relationship was reported before on some other host species such as O. angulata on Scylla serrata (Jeffries et al., 1992), O. lowei on Callinectes ornatus (Santos, Bueno, 2002), O. bullata on Portunus sanguinolentus (Li et al., 2014), O. angulata and D. tridens on P. sanguinolentus (Oanh et al., 2018a). The previous studies demonstrated that the larger crabs have the longer duration of the intermolt phrase (Jeffries et al., 1992; Josileen, Menon, 2005). This explains the correlation between infestation state and size of host crab because the longer interval between two ecdyses of host allows a greater amount of epibionts to settle.

Epibiotic barnacles did not distribute on the host’s body randomly. O. angulata and O. neptuni were observed only in branchial chambers, O. warwicki was the only species which settled on the external integument of M. haanii, while D. tridens occurred both in the branchial chambers and at the host carapace’s margin. These records are consistent with previous reports on distribution sites of these barnacles infesting other hosts, such as P. pelagicus (Oanh et al., 2018), P. sanguinolentus (Oanh et al., 2018a), Scylla serrata and Thalamita danae (Jeffries et al., 2005). Voris and Jeffries (1997) hypothesized that the barnacles living inside the branchial chambers of decapods, where they covered and protected by host stabilized carapace (such as O. bullata, O. angulata, O. neptuni, O. lowei…) possess small, delicate capitular plates. Others with strong, large capitular plates tend to attach themselves to the external surface of the host (Voris, Jeffries, 1997). Our results generally match with these hypotheses, in particular, O. warwicki and D. tridens having the largest capitular plates among studied species tend to settle on the external integument of the crab or the carapace margin, while O. angulata and O. neptuni, which have small capitular plates, settle exclusively in the branchial chambers. However, this general trend is broken in D. tridens, which tends to settle on the gills. According to Voris and Jeffries (1997) this observation may be explained by the tendency of this barnacle to settle in the areas where they are more exposed to the pressure of respiratory currents, but our observation does not support this hypothesis. The explanation for the concentration of barnacles in the branchial chambers was given in the articles published earlier (Jeffries, Voris, 1983; Gannon, Wheatly, 1992; Voris et al., 2000; Li et al., 2014). In particular, the host’s respiratory currents, supplying food and oxygen for permanently fixed epibionts, may determine their settlement positions. Our findings completely correspond to this theory, in particular, gills were the most occupied part of the branchial chamber (Table 5). In turn, gill 4, which is exposed to the strongest respiratory currents (Arudpragasam, Naylor, 1964) was the most preferred attachment site.

CONCLUSIONS

The present study confirms some trends observed in preceding research. Vietnamese waters appear to be a region characterised by relatively low diversity of pedunculate barnacles and relatively high intensity of infestation. None of the barnacle species inhabiting the area of research was host specific, which also can be considered the specific trait of this area.

Portunid crab Monomia haanii seems to be highly subjected to barnacle infestation, additionally the crab’s size has a significant impact on the prevalence of infestation. On another hand no relationship between crab’s sex and infestation state was observed.

Finally the distribution of the pedunculate barnacles on the host’s body generally followed the basic distributional patterns of this group of epibionts.