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Review

Epibiotic Communities of Common Crab Species in the Coastal Barents Sea: Biodiversity and Infestation Patterns

Murmansk Marine Biological Institute of the Russian Academy of Sciences (MMBI RAS), 183010 Murmansk, Russia
*
Author to whom correspondence should be addressed.
Diversity 2022, 14(1), 6; https://doi.org/10.3390/d14010006
Submission received: 13 December 2021 / Revised: 20 December 2021 / Accepted: 21 December 2021 / Published: 23 December 2021

Abstract

:
Crabs are important ecosystem engineers in marine habitats worldwide. Based on long-term data, we analyzed the species composition and infestation indices of epibionts and symbionts colonizing the great spider crab, Hyas araneus, and two lithodid crabs—the northern stone crab, Lithodes maja, and the red king crab, Paralithodes camtschaticus—in the coastal zone of the Barents Sea. The epibiotic communities found on great spider crabs were closer to northern stone crabs (33%) compared to red king crabs (25%). The prevalence of mobile symbionts (amphipods, Ischyrocerus, and polychaetes, Harmothoe) and common epibionts, such as barnacles and hydrozoans, was low on great spider crabs and high on the body and in the gills of lithodid crabs. Epiphytes were abundant on great spider crabs but not present on both species of lithodid crabs. Egg symbionts found on H. araneus and P. camtschaticus do not affect their local populations. Differences in the fouling communities found on the three crab species are associated with host size range, surface properties of their carapaces, and behavior patterns.

Graphical Abstract

1. Introduction

Only a few species of relatively large crustaceans occur in the coastal zone of the Barents Sea. Among them, the highest abundance and biomass are registered for one member of the family Oregonidae, the great spider crab, Hyas araneus (Linnaeus, 1758), and two members of the family Lithodidae, the red king crab, Paralithodes camtschaticus (Tilesius, 1815), and the northern stone crab, Lithodes maja (Linnaeus, 1758). Unlike to the true crab, Hyas araneus, which has the normal five pairs of legs, lithodid crabs are considered to be a crab-like species because their 5th pair of legs is reduced and hidden under the carapace where it is used to clean the crab gills. In the literature, however, L. maja and P. camtschaticus are also referred to as “crabs”. Great spider crabs and northern stone crabs are native inhabitants of the Barents Sea and both have no commercial value [1], while red king crabs were introduced into the Barents Sea from the North Pacific and are considered to be a highly valued delicacy on the international market [2,3] and a source for producing valuable biochemical substances [4]. Although, in the coastal Barents Sea, each species has specific ecological and ethological features [1,2,5,6,7], these crabs often occur at the same locations.
Epibiosis is a common phenomenon in aquatic systems, especially in marine environments where wave turbulence has caused many mobile and sessile organisms to evolve a system of settlement and attachment to hard, relatively stable surfaces provided by other organisms [8,9,10]. The calcified body surface of decapod crustaceans is known to be a suitable substrate for many species of marine animals and plants [8,11,12,13]. Investigations have focused on studying the nature of epibiosis. This is important because they can contribute to basic knowledge on important aspects of the hosts’ biology including molting and growth patterns, behavior, and migration activity [14]. In many cases, studies on the flora and fauna associated with living marine invertebrates can provide new information on the biology of epibionts and symbionts, and can clarify biodiversity data in the region [11]. Long-term studies of the advantages and disadvantages for hosts and epibionts, together with examinations of the hosts’ health, can help to evaluate or re-evaluate the nature of the relationships between the epibionts and their hosts [15,16,17,18].
As top predators, all of the crab species chosen for our study are considered to be key organisms and ecological engineers in the local benthic communities, i.e., they directly or indirectly modulate the availability of resources to other species by causing physical state changes in biotic or abiotic materials [19,20,21]. Particular importance is set to P. camtschaticus because this species is a subject of important fishery in the Barents Sea with annual landings of 9836 and 10,820 t in 2019 and 2020, respectively [22,23,24]. Many important biological aspects of great spider crabs, northern stone crabs, and red king crabs—including distribution and recruitment patterns, behavior, reproduction, growth, and physiology—have already been studied in the Barents Sea [1,2,7,25,26,27,28,29,30,31,32]. Fouling communities were also described [5,6,16,33,34,35,36,37,38,39,40,41], but no comparative studies have been undertaken in this field yet.
For this reason, the aim of our study was to compare the fouling communities of H. araneus, L. maja, and P. camtschaticus in relation to their biology. To obtain comparable results, we used data for adult crabs with old shells (age of exoskeleton > 1 year).

2. Infestation Patterns

2.1. Hyas araneus

A total of 41 taxa were registered on this crab species in the coastal Barents Sea (Table 1). Among them, the copepods, Harpacticus uniremis and Tisbe furcate (in the gills), the attached polychaetes, Placostegus tridentatus, Circeis armoricana, and Spirobranchus triqueter, as well as the red algae, Ptilota gunneri and Palmaria palmata, and the brown algae, Dictyosiphon foeniculaceus, were the most abundant [38]. The majority of harpacticoid copepods were found in the gills, while the polychaetes and algae prevailed on the carapace and limbs (Figure 1a,b). The mean carapace width (CW) of H. araneus was 60.1 ± 1.6 mm (mean ± SE), with a size range of 41.0–78.8 mm.

2.2. Lithodes maja

A total of 26 taxa were registered on the northern stone crabs (Table 1) with the highest prevalence found for typical epibionts [5,30,36]. Attached species were presented by the hydrozoans, Obelia, and the polychaetes, Placostegus tridentatus and Circeis armoricana (Figure 2a). Mobile species were presented by the symbiotic amphipods, Ischyrocerus commensalis, which predominantly colonized the mouthparts and gills, and by polynoid polychaetes, Harmothoe imbricata. The mean CW of L. maja was 91.9 ± 1.3, ranging from 77.0–101.0 mm.

2.3. Paralithodes camtschaticus

Among 25 taxa of associated species found on red king crabs in the coastal Barents Sea, the amphipods, Ischyrocerus commensalis (in the gills and on the mouthparts, Figure 2b,c) and Ischyrocerus anguipes (on the carapace and limbs), as well as the hydrozoan, Obelia longissima (on the carapace and limbs), had the highest frequency of occurrence (Table 1). Symbiotic amphipods were also registered on the female egg clutches, but these findings were rare (Figure 2d). The mean CW of P. camtschaticus was 154.9 ± 3.2, with a size range of 121.5–227.0 mm.

3. Comparison of Epibiotic Communities

3.1. General Patterns

The epibiont prevalence differs significantly among the three crab species [30]. The maximum similarity was seen in the case of congeneric species, L. maja and P. camtschaticus (Bray–Curtis similarity index 64%), and the minimum similarity was registered for P. camtschaticus and H. araneus (25%).
In the case of L. maja and H. araneus, this index was 33%. In the case of H. araneus and L. maja, the maximum contribution to the dissimilarity was registered for Ischyrocerus commensalis, Obelia longissima, Harmothoe imbricata, and Harpacticus uniremis. In the case of H. araneus and P. camtschaticus, the most important species were Ischyrocerus commensalis, Obelia longissima, Harpacticus uniremis, Placostegus tridentatus, and Ischyrocerus anguipes. Dissimilarity between fouling communities of L. maja and P. camtschaticus was attributed to nine species (each had a contribution of 5% or higher): Placostegus tridentatus, Obelia geniculata, Heteranomia scuamula, Harmothoe imbricata, Balanus balanus, Obelia longissima, Circeis armoricana, Callopora lineata, and Disporella hispida (Table 2). These results are also supported by Chi-square tests (Table S1).
The mean intensity of Ischyrocerus commensalis on great spider crabs is significantly lower than on lithodid crabs, while this index calculated for Ischyrocerus anguipes is similar on all three crab species [37,38,42]. The same results were found for the bivalve mollusks, Mytilus edulis and Heteranomia squamula, and the barnacle, Balanus crenatus (Table S2). The mean intensity of Circeis armoricana did not vary singnificantly between great spider crabs and northern stone crabs, but was significantly higher compared to red king crabs [5,30,36].

3.2. Factors: Ecology and Behavior of Hosts

The most diverse assemblage of fouling organisms was registered on great spider crabs. This result is linked to the presence of algae on their carapaces. In contrast to Hyas araneus, no algae species were found on red king crabs and northern stone crabs. It is most likely that this pattern is associated with the ecology of H. araneus in the coastal Barents Sea where these crabs usually occur at 5–25 m depths in laminarian kelps. At deeper sites, H. araneus is distributed on rocky or muddy bottoms [26]. In contrast to adult lithodid crabs, algae play an important role in the ration of great spider crabs [1,43]. This increases a chance to be fouled by algae for H. araneus.
In addition, some authors classify H. araneus as decorators, i.e., crabs which actively attach foreign matter to their bodies or external structures aiming to protect themselves against predators and/or abiotic forces [44,45]. In Hyas, this behavior pattern seems to take place at the early stages of ontogenesis (Figure 1c) because epibiotic algae were rarely seen on great spider crabs that reached a terminal molt, suggesting only passive settlement of algal zoospores on the carapace [38]. Similar behavior was registered for other spider crabs such as Maja squinado [46] and Maja crispata [47].
We registered a relatively high incidence of infestation of the turbellarian worm, Peraclistus oophagus, on H. araneus. This species is known to be an egg predator [48] and, therefore, it was found only on the female egg masses. However, negative effects for the host are negligible due to the high fecundity of H. araneus [48]. Peraclistus were not recorded on the egg clutches of northern stone crabs and red king crabs in contrast to the symbiotic amphipods, Ischyrocerus commensalis. The last species, however, is considered to be a scavenger rather than a true egg predator; its presence could have a positive effect because Ischyrocerus commensalis ingests dead eggs and, therefore, may be responsible for sanitary tasks [17].

3.3. Factors: Ecology and Behavior of Epibionts

Heavy fouling by epiphytes on the exoskeleton of great spider crabs leads to lower infestation levels of other attached species [38]. This explains the rare occurrence of hydrozoans on H. araneus. In older crabs, epibiotic algae are replaced by sedentary polychaete worms, which are also preventing other epibionts to settle on the host carapaces [38]. This fact partially explains the low infestation indices of symbiotic amphipods on the great spider crabs compared to red king crabs. However, the main reason is that the amphipods cannot find suitable food on great spider crabs; this is confirmed by the rare localization of these symbionts on the mouthparts of H. araneus. An opposite pattern is registered for lithodid crabs, especially for red king crabs. The ischyrocerid amphipods are known to feed on the crab food remnants and detritus concentrated on the mouthparts and limbs of their hosts [16,34,42]. Both inter- and intra-specific competition was reported for Ischyrocerus commensalis [49,50], confirming its adaptation to symbiotic lifestyle on king crabs [42]. Similar relationships were described for the amphipod, Caprella ungulina, on the subantarctic false king crab, Paralomis granulosa [51].
We found a less frequent occurrence of the symbiotic amphipods in the gills of great spider crabs but higher prevalences of small copepods compared to lithodid crabs. This result is explained by the fact that the carapace of H. araneus is more tightly attached to the body than in the case of lithodid crabs, preventing colonization of their respiration organs by large amphipods [1,25]. In contrast, small copepods may easily occupy great spider crabs as a result of being drawn into the gills during the host respiration activity; they can live here without competition with other symbionts, in contrast to the gill community of red king crabs, where large amphipod specimens can feed on harpacticoid copepods [35].

3.4. Factors: Host Size and Carapace Properties

Although the diversity of associated organisms is higher on great spider crabs, they have lower infestation indices than we registered on both species of lithodid crabs: the maximum prevalence of each epibiont is 50% on H. araneus, and 100% on L. maja and P. camtschaticus. Most likely, this pattern reflects the size differences observed among the crab species: the smallest CW is registered for great spider crabs and the largest size for red king crabs [52]. Smaller hosts have less surface area for settling, and a positive association between body size and infestation indices was reported for many decapod–crustacean–epibiotic associations across the world’s oceans [8,11,53,54,55,56].
The fouling community of the great spider crab is closer to that observed on another native species, the northern stone crab, rather than the red king crab. This result is associated with the higher prevalence of sedentary polychaetes on L. maja compared to P. camtschaticus. It is known that juvenile northern stone crabs have a great number of spines, most of which become reduced as the crabs mature [1]; hence, the carapace and limbs of northern stone crabs are rough in comparison to the smooth body surface of red king crabs (Figure 2e,f) [36]. Irregular rough surfaces have been shown to be a more favorable substrate for settlement of typical attached taxa [57,58] and, therefore, support the highest species richness, abundance, and diversity [59,60], explaining the higher proportions of tubular polychaetes, hydrozoans, and bryozoans on L. maja.
The chemical composition of the body surface also differs significantly between great spider crabs and lithodid crabs so that the green- and brown-green-colored carapaces of H. araneus consist of higher proportions of N and P than the red-colored carapaces of L. maja и P. camtschaticus [61]. Such surfaces are more favorable for algal zoospores because they have been shown to demonstrate positive chemotaxis to substrata rich in N and P [62].

4. Conclusions

Our comparative study has shown that great spider crabs harbored lower numbers of mobile symbionts (the corophioid amphipods, Ischyrocerus commensalis and Ischyrocerus anguipes, and the polynoid polychaetes, Harmothoe imbricata) than the crabs in the family Lithodidae. Typical attached taxa, such as barnacles and hydrozoans, were also less abundant on the great spider crabs. The main feature of the Hyas araneus fouling community is the presence of epiphytes, which were not found on the lithodid crabs analyzed. The main differences in the structure of epibiotic assemblages on the three crab species are linked with differences in their body size, surface properties of the carapace, and behavior patterns. Egg symbionts, such as the tubellarian worm, Peraclistus oophagus, on Hyas araneus and the amphipod, Ischyrocerus commensalis, on Paralithodes camtschaticus, seem to have no or a negligible impact on the host populations.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/d14010006/s1, Table S1: Differences among the prevalences of associated organisms on great spider crabs (Hyas araneus), northern stone crabs (Lithodes maja), and red king crabs (Paralithodes camtschaticus) as revealed by Chi-square tests; Table S2: Differences among mean intensities of common associated organisms on great spider crabs (Hyas araneus), northern stone crabs (Lithodes maja), and red king crabs (Paralithodes camtschaticus), as revealed by Kruskal–Wallis tests, followed by Bonferroni tests for medians.

Author Contributions

Conceptualization, A.G.D.; methodology, A.G.D.; validation, A.G.D. and V.G.D.; investigation, A.G.D. and V.G.D.; visualization V.G.D.; writing—original draft, A.G.D. All authors have read and agreed to the published version of the manuscript.

Funding

This study was funded by the Ministry of Science and Higher Education of the Russian Federation.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Kuznetsov, V.V. The Biology of Abundant and the Most Common Species of Crustaceans in the Barents and White Seas; Nauka: Moscow, Russia, 1964. (In Russian) [Google Scholar]
  2. Dvoretsky, A.G.; Dvoretsky, V.G. Red king crab (Paralithodes camtschaticus) fisheries in Russian waters: Historical review and present status. Rev. Fish Biol. Fish. 2018, 28, 331–353. [Google Scholar] [CrossRef]
  3. Dvoretsky, A.G.; Bichkaeva, F.A.; Baranova, N.F.; Dvoretsky, V.G. Fatty acid composition of the Barents Sea red king crab (Paralithodes camtschaticus) leg meat. J. Food Compos. Anal. 2021, 98, 103826. [Google Scholar] [CrossRef]
  4. Ponomareva, T.; Timchenko, M.; Filippov, M.; Lapaev, S.; Sogorin, E. Prospects of red king crab hepatopancreas processing: Fundamental and applied biochemistry. Recycling 2021, 6, 3. [Google Scholar] [CrossRef]
  5. Dvoretsky, A.G.; Dvoretsky, V.G. Epifauna associated with the northern stone crab Lithodes maia in the Barents Sea. Polar Biol. 2008, 31, 1149–1152. [Google Scholar] [CrossRef]
  6. Dvoretsky, A.G.; Dvoretsky, V.G. Limb autotomy patterns in Paralithodes camtschaticus (Tilesius, 1815), an invasive crab, in the coastal Barents Sea. J. Exp. Mar. Biol. Ecol. 2009, 377, 20–27. [Google Scholar] [CrossRef]
  7. Dvoretsky, A.G.; Dvoretsky, V.G. Population dynamics of the invasive lithodid crab, Paralithodes camtschaticus, in a typical bay of the Barents Sea. ICES J. Mar. Sci. 2013, 70, 1255–1262. [Google Scholar] [CrossRef]
  8. Fernandez-Leborans, G. Epibiosis in Crustacea: An overview. Crustaceana 2010, 83, 549–640. [Google Scholar] [CrossRef]
  9. Ramos-Rivera, B.S.; Castro-Mondragon, H.; Kuk-Dzul, J.G.; Flores-Rodríguez, P.; Flores-Garza, R. Diversity of epibionts associated with Lepidochelys olivacea (Eschscholtz 1829) sea turtles nesting in the Mexican South Pacific. Animals 2021, 11, 1734. [Google Scholar] [CrossRef]
  10. Frahm, J.L.; Brooks, W.R. The use of chemical cues by sargassum shrimps Latreutes fucorum and Leander tenuicornis in establishing and maintaining a symbiosis with the host sargassum algae. Diversity 2021, 13, 305. [Google Scholar] [CrossRef]
  11. Williams, J.D.; McDermott, J.J. Hermit crab biocoenoses; A worldwide review of the diversity and natural history of hermit crab associates. J. Exp. Mar. Biol. Ecol. 2004, 305, 1–128. [Google Scholar] [CrossRef]
  12. Bhaduri, R.N.; Valentich-Scott, P.; Hilgers, M.; Singh, R. New host record for the California mussel Mytilus californianus (Bivalvia, Mytilidae), epibiotic on the pacific sand crab Emerita analoga (Decapoda, Hippidae) from Monterey Bay, California (U.S.A.). Crustaceana 2017, 90, 69–75. [Google Scholar] [CrossRef]
  13. De Gier, W.; Becker, C.A. Review of the ecomorphology of pinnotherine pea crabs (Brachyura: Pinnotheridae), with an updated list of symbiont-host associations. Diversity 2020, 12, 431. [Google Scholar] [CrossRef]
  14. Lovrich, G.A.; Calcagno, J.A.; Smith, B.D. The barnacle Notobalanus flosculus as an indicator of the intermolt period of the male lithodid crab Paralomis granulosa. Mar. Biol. 2003, 143, 143–156. [Google Scholar] [CrossRef]
  15. Gannon, A.T.; Wheatly, M.G. Physiological effects of an ectocommensal gill barnacle, Octolasmis muelleri, on gas exchange in the blue crab Callinectes sapidus. J. Crustac. Biol. 1992, 12, 11–18. [Google Scholar] [CrossRef]
  16. Dvoretsky, A.G.; Dvoretsky, V.G. Distribution of amphipods Ischyrocerus on the red king crab, Paralithodes camtschaticus: Possible interactions with the host in the Barents Sea. Estuar. Coast. Shelf Sci. 2009, 82, 390–396. [Google Scholar] [CrossRef]
  17. Dvoretsky, A.G.; Dvoretsky, V.G. The amphipod Ischyrocerus commensalis on the eggs of the red king crab Paralithodes camtschaticus: Egg predator or scavenger? Aquaculture 2010, 298, 185–189. [Google Scholar] [CrossRef]
  18. Dvoretsky, A.G.; Dvoretsky, V.G. New echinoderm-crab epibiotic associations from the coastal Barents Sea. Animals 2021, 11, 917. [Google Scholar] [CrossRef] [PubMed]
  19. Wright, J.P.; Jones, C.G. The concept of organisms as ecosystem engineers ten years on: Progress, limitations, and challenges. BioScience 2006, 56, 203–209. [Google Scholar] [CrossRef] [Green Version]
  20. Berke, S.K. Functional groups of ecosystem engineers: A proposed classification with comments on current issues. Integr. Comp. Biol. 2010, 50, 147–157. [Google Scholar] [CrossRef] [Green Version]
  21. Pickering, T.R.; Poirier, L.A.; Barrett, T.J.; McKenna, S.; Davidson, J.; Quijón, P.A. Non-indigenous predators threaten ecosystem engineers: Interactive effects of green crab and oyster size on American oyster mortality. Mar. Environ. Res. 2017, 127, 24–31. [Google Scholar] [CrossRef]
  22. Dvoretsky, A.G.; Tipisova, E.V.; Elfimova, A.E.; Alikina, V.A.; Dvoretsky, V.G. Sex hormones in hemolymph of red king crabs from the Barents Sea. Animals 2021, 11, 2149. [Google Scholar] [CrossRef]
  23. Dvoretsky, A.G.; Dvoretsky, V.G. Cucumaria in Russian waters of the Barents Sea: Biological aspects and aquaculture potential. Front. Mar. Sci. 2021, 8, 613453. [Google Scholar] [CrossRef]
  24. Dvoretsky, A.G.; Dvoretsky, V.G. Renewal of the recreational red king crab fishery in Russian waters of the Barents Sea: Potential benefits and costs. Mar. Policy 2022, 136, 104916. [Google Scholar] [CrossRef]
  25. Kuzmin, S.A.; Gudimova, E.N. Introduction of the Kamchatka (Red King) Crab in the Barents Sea: Peculiarities of Biology, Perspectives of Fishery; KSC RAS Press: Apatity, Russia, 2002. (In Russian) [Google Scholar]
  26. Sokolov, V.I. Decapod Crustaceans of the Barents Sea. Tr. VNIRO 2003, 142, 25–76. (In Russian) [Google Scholar]
  27. Dvoretsky, A.G.; Dvoretsky, V.G. Commercial fish and shellfish in the Barents Sea: Have introduced crab species affected the population trajectories of commercial fish? Rev. Fish Biol. Fish. 2015, 25, 297–322. [Google Scholar] [CrossRef]
  28. Dvoretsky, A.G.; Dvoretsky, V.G. Size at maturity of female red king crab, Paralithodes camtschaticus, from the costal zone of Kola Peninsula (southern Barents Sea). Cah. Biol. Mar. 2015, 56, 49–54. [Google Scholar]
  29. Dvoretsky, A.G.; Dvoretsky, V.G. Inter-annual dynamics of the Barents Sea red king crab (Paralithodes camtschaticus) stock indices in relation to environmental factors. Polar Sci. 2016, 10, 541–552. [Google Scholar] [CrossRef]
  30. Dvoretsky, A.G.; Dvoretsky, V.G. Ecology of Red King Crab in the Coastal Barents Sea; SSC RAS Publishers: Rostov-on-Don, Russia, 2018. (In Russian) [Google Scholar]
  31. Dvoretsky, A.G.; Dvoretsky, V.G. Effects of environmental factors on the abundance, biomass, and individual weight of juvenile red king crabs in the Barents Sea. Front. Mar. Sci. 2020, 7, 726. [Google Scholar] [CrossRef]
  32. Deart, Y.V.; Antokhina, T.I.; Spiridonov, V.A.; Britayev, T.A. Seasonal distribution of red king crab in Zelenaya Inlet (Murmansk coast, Barents Sea). Tr. VNIRO 2018, 172, 149–159. (In Russian) [Google Scholar] [CrossRef]
  33. Dvoretsky, A.G.; Dvoretsky, V.G. Fouling community of the red king crab, Paralithodes camtschaticus (Tilesius 1815), in a subarctic fjord of the Barents Sea. Polar Biol. 2009, 32, 1047–1054. [Google Scholar] [CrossRef]
  34. Dvoretsky, A.G.; Dvoretsky, V.G. Some aspects of the biology of the amphipods Ischyrocerus anguipes associated with the red king crab, Paralithodes camtschaticus, in the Barents Sea. Polar Biol. 2009, 32, 463–469. [Google Scholar] [CrossRef]
  35. Dvoretsky, A.G.; Dvoretsky, V.G. Copepods associated with the red king crab Paralithodes camtschaticus (Tilesius, 1815) in the Barents Sea. Zool. Stud. 2013, 52, 17. [Google Scholar] [CrossRef] [Green Version]
  36. Dvoretsky, A.G.; Dvoretsky, V.G. Epibionts and commensals of the troll crab (Lithodes maja, Decapoda, Lithodidae) in the Barents Sea. Zool. Zhurnal 2019, 98, 365–370. (In Russian) [Google Scholar]
  37. Dvoretsky, A.G.; Dvoretsky, V.G. Epifauna associated with an introduced crab in the Barents Sea: A 5-year study. ICES J. Mar. Sci. 2010, 67, 204–214. [Google Scholar] [CrossRef] [Green Version]
  38. Dvoretsky, A.G. Epibionts of the great spider crab, Hyas araneus (Linnaeus, 1758), in the Barents Sea. Polar Biol. 2012, 35, 625–631. [Google Scholar] [CrossRef]
  39. Dvoretsky, A.G.; Dvoretsky, V.G. Structure of symbiotic assemblages on red king crabs in the coastal Barents Sea in 2012. Tr. VNIRO 2018, 172, 160–171, (In Russian with English Abstract). [Google Scholar] [CrossRef]
  40. Dvoretsky, A.G.; Dvoretsky, V.G. Symbionts and sessile microbiota of red king crab from eastern Murman (Dalnezelenetskaya Bay, Barents Sea) in July 2014. Bull. Kamchatka State Tech. Univ. 2020, 51, 66–72. (In Russian) [Google Scholar] [CrossRef]
  41. Dvoretsky, A.G. Red king crab in the coastal Barents Sea: A review of MMBI studies. Trans. Kola Sci. Centre 2020, 11, 134–149. (In Russian) [Google Scholar] [CrossRef]
  42. Dvoretsky, A.G.; Dvoretsky, V.G. Population biology of Ischyrocerus commensalis, a crab-associated amphipod, in the southern Barents Sea: A multi-annual summer study. Mar. Ecol. 2011, 32, 498–508. [Google Scholar] [CrossRef]
  43. Pavlova, L.V. Red king crab trophic relations and its influence on bottom biocenoses. In Biology and Physiology of the Red King Crab from the Coastal Zone of the Barents Sea; Matishov, G.G., Ed.; KSC RAS Press: Apatity, Russia, 2008; pp. 77–104. (In Russian) [Google Scholar]
  44. Berke, S.K.; Woodin, S.A. Energetic costs, ontogenetic shifts and sexual dimorphism in spider crab decoration. Funct. Ecol. 2008, 22, 1125–1133. [Google Scholar] [CrossRef]
  45. Tanduo, V.; Virgili, R.; Osca, D.; Crocetta, F. Hiding in fouling communities: A native spider crab decorating with a cryptogenic bryozoan in a Mediterranean marina. J. Mar. Sci. Eng. 2021, 9, 495. [Google Scholar] [CrossRef]
  46. Parapar, J.; Fernandez, L.; Gonzalez-Gurriaran, E.; Muino, R. Epibiosis and masking material in the spider crab Maja squinado (Decapoda: Majidae) in the Ria de Arousa (Galicia, NW Spain). Cah. Biol. Mar. 1997, 38, 221–234. [Google Scholar]
  47. Bedini, R.; Canali, M.G.; Bedini, A. Use of camouflaging materials in some brachyuran crabs of the Mediterranean infralittoral zone. Cah. Biol. Mar. 2003, 44, 375–383. [Google Scholar]
  48. Uspenskaya, A.V. Parasitic Fauna of the Benthic Crustaceans in the Barents Sea; AN SSSR Press: Moscow, Russia, 1963. (In Russian) [Google Scholar]
  49. Dvoretsky, A.G.; Dvoretsky, V.G. Interspecific relationships of symbiotic amphipods on the red king crab in the Barents Sea. Dokl. Biol. Sci. 2010, 433, 279–281. [Google Scholar] [CrossRef]
  50. Dvoretsky, A.G.; Dvoretsky, V.G. Interspecific competition of symbiotic and fouling species of red king crab in the Barents Sea. Dokl. Biol. Sci. 2011, 440, 300–302. [Google Scholar] [CrossRef]
  51. Medina, Á.; Figueroa, T.; Canete, J.I. Caprella ungulina Mayer, 1903 (Amphipoda: Caprellidae): Epizoan of Paralomis granulosa (Hombron & Jacquinot, 1846) (Decapoda: Lithodidae) in Magellan waters, Chile. Anal. Inst. Patagon. 2017, 45, 17–29. [Google Scholar]
  52. Dvoretsky, A.G.; Dvoretsky, V.G. Size-at-age of juvenile red king crab (Paralithodes camtschaticus) in the coastal Barents Sea. Cah. Biol. Mar. 2014, 55, 43–48. [Google Scholar]
  53. Savoie, L.; Miron, J.; Biron, M. Fouling community of the snow crab Chionoecetes opilio in Atlantic Canada. J. Crustac. Biol. 2007, 27, 30–36. [Google Scholar] [CrossRef] [Green Version]
  54. Firstater, F.N.; Hidalgo, F.G.; Lomovasky, B.G.; Gallegos, P.; Amero, P.; Iribarne, O.O. Effects of epibiotic Enteromorpha spp. on the mole crab Emerita analoga in the Peruvian central coast. J. Mar. Biol. Assoc. UK 2009, 89, 363–370. [Google Scholar]
  55. Di Camillo, C.; Bo, M.; Puce, S.; Tazioli, S.; Froglia, C.; Bavestrello, G. The epibiontic assemblage of Geryon longipes (Crustacea: Decapoda: Geryonidae) from the Southern Adriatic Sea. Ital. J. Zool. 2008, 75, 29–35. [Google Scholar] [CrossRef]
  56. Ibrahim, N.K. Epibiont communities of the two spider crabs Schizophrys aspera (H. Milne Edwards, 1834) and Hyastenus hilgendorfi (De Man, 1887) in Great Bitter Lakes, Suez Canal, Egypt. Egypt. J. Aquat. Biol. Fish. 2012, 16, 133–144. [Google Scholar] [CrossRef] [Green Version]
  57. Patil, J.S.; Anil, A.C. Epibiotic community of the horseshoe crab Tachypleus gigas. Mar. Biol. 2000, 136, 699–713. [Google Scholar] [CrossRef]
  58. Balazy, P.; Kuklinski, P. Arctic field experiment shows differences in epifaunal assemblages between natural and artificial substrates of different heterogeneity and origin. J. Exp. Mar. Biol. Ecol. 2017, 486, 178–187. [Google Scholar] [CrossRef]
  59. Balazy, P.; Kuklinski, P.; Wlodarska-Kowalczuk, M.; Gluchowska, M.; Barnes, D.K.A. Factors affecting biodiversity on hermit crab shells. Hydrobiologia 2016, 773, 207–224. [Google Scholar] [CrossRef] [Green Version]
  60. Gravina, M.F.; Pierri, C.; Mercurio, M.; Nonnis Marzano, C.; Giangrande, A. Polychaete diversity related to different mesophotic bioconstructions along the southeastern Italian coast. Diversity 2021, 13, 239. [Google Scholar] [CrossRef]
  61. Uryash, V.F.; Kokurina, N.Y.; Kashtanov, E.A.; Zagorskaya, D.S.; Kovacheva, N.P. Influence of species-specificity of crab families on physicochemical properties of crab shell chitin. Vestn. Lobachevsky Univ. Nizhny Novgorod 2012, 3, 83–86. (In Russian) [Google Scholar]
  62. Fukuhara, Y.; Mizuta, H.; Yasui, H. Swimming activities of zoospores of Laminaria japonica (Phaeophyceae). Fish. Sci. 2002, 68, 1173–1181. [Google Scholar] [CrossRef]
Figure 1. Hyas araneus. Adult great spider crabs colonized by the brown algae, Dictyosiphon foeniculaceus, (a) the polychaete, Spirobranchus triqueter (b), and a young crab decorated with epiphytes (c).
Figure 1. Hyas araneus. Adult great spider crabs colonized by the brown algae, Dictyosiphon foeniculaceus, (a) the polychaete, Spirobranchus triqueter (b), and a young crab decorated with epiphytes (c).
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Figure 2. Lithodes maja and Paralithodes camtschaticus. Typical epibiotic community of northern stone crabs (a). Symbiotic amphipods, Ischyrocerus commensalis, in the gills (b), on the mouthparts (c), and on the egg masses (d) of red king crabs. Carapaces of a recently molted northern stone crab (e) and red king crab (f).
Figure 2. Lithodes maja and Paralithodes camtschaticus. Typical epibiotic community of northern stone crabs (a). Symbiotic amphipods, Ischyrocerus commensalis, in the gills (b), on the mouthparts (c), and on the egg masses (d) of red king crabs. Carapaces of a recently molted northern stone crab (e) and red king crab (f).
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Table 1. List of taxa and infestation indices for associated organisms found on great spider crabs (Hyas araneus), northern stone crabs (Lithodes maja), and red king crabs (Paralithodes camtschaticus) in the coastal Barents Sea.
Table 1. List of taxa and infestation indices for associated organisms found on great spider crabs (Hyas araneus), northern stone crabs (Lithodes maja), and red king crabs (Paralithodes camtschaticus) in the coastal Barents Sea.
TaxaHyas araneusLithodes majaParalithodes camtschaticus
Pr
95%C.I.
IntPr
95%C.I.
IntPr
95%C.I.
Int
X ± SERangeX ± SERangeX ± SERange
Algae
Acrosiphonia sp.17.9
6–30
Alaria esculenta (Linnaeus) Greville, 18305.1
1–12
Chordaria flagelliformis (O.F.Müller) C.Agardh, 181725.6
12–39
Desmarestia aculeata (Linnaeus) J.V.Lamouroux, 181312.8
2–23
Dictyosiphon foeniculaceus (Hudson) Greville, 183023.1
10–36
Laminaria digitata (Hudson) J.V.Lamouroux, 18135.1
1–12
Palmaria palmata (Linnaeus) Weber and Mohr, 180528.2
14–42
Ptilota gunneri P.C.Silva, Maggs and M.Irvine, 199330.8
16–45
Saccharina latissima (Linnaeus) C.E.Lane, C.Mayes, Druehl and G.W.Saunders, 200610.3
1–20
Ulvaria obscura (Kützing) P.Gayral ex C.Bliding, 196923.1
10–36
Hydrozoa
Coryne hincksi Bonnevie, 18982.6
0–8
Halecium beanii (Johnston, 1838)2.6
0–8
2.4
0–7
Obelia geniculata (Linnaeus, 1758)10.3
1–20
48.6
33–65
4.8
1–11
Obelia longissima (Pallas, 1766)17.9
6–30
94.6
87–100
66.7
52–81
Turbellaria
Peraclistus oophagus (Friedmann, 1924)23.1
10–36
Nemettini
Nemertini g. sp.10.3
1–20
15.8 ± 10.14–4610.8
1–21
4.3 ± 2.61–122.4
0–7
1.0 ± 0.01–1
Polychaeta
Bushiella (Jugaria) similis (Bush, 1905)2.7
0–8
2.0 ± 0.02–2
Circeis armoricana Saint–Joseph, 189438.5
23–54
23.9 ± 6.53–9359.5
44–75
89.4 ± 32.54–34533.3
19–48
5.3 ± 2.31–33
Eumida sanguinea (Oersted, 1843)5.4
0–13
1.5 ± 0.51–22.4
0–7
1.0 ± 0.01–1
Harmothoe imbricata (Linnaeus, 1767)70.3
56–85
1.3 ± 0.21–333.3
19–48
1.4 ± 0.21–3
Lepidonotus squamatus (Linnaeus, 1758)2.7
0–8
1.0 ± 0.01–1
Placostegus tridentatus (Fabricius, 1779)43.6
28–59
64.9
49–80
Protula tubularia (Montagu, 1803)7.7
1–16
1.3 ± 0.61–2
Spirobranchus triqueter (Linnaeus, 1758)20.5
8–33
1.9 ± 0.51–58.1
1–17
Hirudinea
Crangonobdella fabricii (Malm, 1863)2.4
0–7
2.0 ± 0.02–2
Johanssonia arctica (Johansson, 1898)2.7
0–8
3.0 ± 0.03–311.9
2–22
1.4 ± 0.21–2
Platibdella olriki (Malm, 1863)2.6
0–8
1.0 ± 0.01–1
Bivalvia
Heteranomia squamula (Linnaeus, 1758)7.7
1–16
3 ± 1.51–648.6
33–65
13.9 ± 9.41–799.5
1–18
2 ± 0.71–4
Hiatella arctica (Linnaeus, 1767)13.5
2–25
4.4 ± 2.41–54.8
1–11
1.5 ± 0.51–2
Mytilus edulis Linnaeus, 175810.3
1–20
1.3 ± 0.31–232.4
17–48
1.4 ± 0.21–326.2
13–39
2.1 ± 0.61–8
Gastropoda
Margarites sp.5.1
1–12
4.5 ± 3.51–8
Copepoda
Calanus finmarchicus (Gunner, 1765)2.6
0–8
1.0 ± 0.01–1
Ectinosoma neglectum Sars G.O., 190425.6
12–39
44.5 ± 25.51–2692.7
0–8
2.0 ± 0.02–2
Harpacticus uniremis Krøyer, 184246.2
31–62
10.8 ± 5.61–1012.4
0–7
1.0 ± 0.01–1
Tisbe furcata (Baird, 1837)30.8
16–45
79.3 ± 18.37–2358.1
1–17
2.0 ± 0.61–32.4
0–7
17.0 ± 0.017–17
Zaus abbreviatus Sars G.O., 19042.6
0–8
1.0 ± 0.01–1
Amphipoda
Ampelisca sp.2.4
0–7
1.0 ± 0.01–1
Gammarellus homari (Fabricius, 1779)10.3
1–20
1.0 ± 0.01–15.4
0–13
2.0 ± 1.01–32.4
0–7
1.0 ± 0.01–1
Hippomedon propinqvus G.O. Sars, 18905.1
1–12
2.5 ± 1.51–4
Ischyrocerus anguipes Krøyer, 183812.8
2–23
5.8 ± 4.11–2248.6
33–65
9.1 ± 1.21–2352.4
37–67
9.4 ± 3.41–70
Ischyrocerus commensalis Chevreux, 19005.1
1–12
5.5 ± 1.54–794.6
87–100
26.5 ± 3.58–109100.0
100–100
79.8 ± 11.65–492
Cirripedia
Balanus balanus (Linnaeus, 1758)2.6
0–8
9.0 ± 0.09–935.1
20–51
1.7 ± 0.21–34.8
1–11
1.5 ± 0.51–2
Balanus crenatus Brugiere 178932.4
17–48
3.2 ± 0.61–826.2
13–39
2.9 ± 0.81–9
Verruca stroemia (O.F. Muller, 1776)2.6
0–8
3.0 ± 0.03–3
Bryozoa
Bugula harmsworth Waters, 19005.1
1–12
Callopora lineata (Linnaeus, 1767)7.7
1–16
29.7
15–44
4.8
1–11
Crisia denticulata (Lamarck, 1816)10.8
1–21
Disporella hispida (Fleming, 1828)7.7
1–16
27.0
13–41
4.8
1–11
Patinella verrucaria (Linnaeus, 1758)15.4
4–27
13.5
2–25
2.4
0–7
Porella smitti Kluge, 19072.6
0–8
Tricellaria arctica Busk, 185510.3
1–20
18.9
6–32
4.8
1–11
Note: Pr—prevalence of infestation (% of infested crabs, above the line), 95%C.I.—95% confidence interval (below the line), Int—intensity of infestation (individuals per infested crab), X—mean, SE—standard error.
Table 2. Results of the SIMPER analysis on infestation indices: contributions of main taxa (%) to dissimilarities within different crab species in the coastal Barents Sea.
Table 2. Results of the SIMPER analysis on infestation indices: contributions of main taxa (%) to dissimilarities within different crab species in the coastal Barents Sea.
TaxaComparisons
Lithodes vs. HyasParalithodes vs. HyasParalithodes vs. Lithodes
Acrosiphonia sp.1.942.42
Chordaria flagelliformis2.773.46
Desmarestia aculeata1.391.73
Dictyosiphon foeniculaceus2.493.11
Palmaria palmata3.053.80
Ptilota gunneri3.334.15
Saccharina latissima1.38
Ulvaria obscura2.493.11
Obelia geniculata4.1510.02
Obelia longissima8.296.576.37
Peraclistus oophagus2.493.11
Nemertini g. sp.1.061.92
Circeis armoricana2.275.96
Harmothoe imbricata7.604.508.43
Placostegus tridentatus2.305.8814.81
Protula tubularia0.84
Spirobranchus triqueter1.342.771.85
Johanssonia arctica1.612.10
Heteranomia scuamula4.438.93
Hiatella arctica1.462.00
Mytilus edulis2.402.151.42
Ectinosoma neglectum2.483.46
Harpacticus uniremis4.995.90
Tisbe furcata2.453.83
Gamarellus homari1.06
Ischyrocerus anguipes3.875.34
Ischyrocerus commensalis9.6712.80
Balanus balanus3.526.93
Balanus crenatus3.513.531.42
Callopora lineata2.385.70
Crisia denticulata1.172.47
Lichenopora hispida5.08
Lichenopora verrucaria2.091.752.54
Scrupocellaria arctica0.743.23
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Dvoretsky, A.G.; Dvoretsky, V.G. Epibiotic Communities of Common Crab Species in the Coastal Barents Sea: Biodiversity and Infestation Patterns. Diversity 2022, 14, 6. https://doi.org/10.3390/d14010006

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Dvoretsky AG, Dvoretsky VG. Epibiotic Communities of Common Crab Species in the Coastal Barents Sea: Biodiversity and Infestation Patterns. Diversity. 2022; 14(1):6. https://doi.org/10.3390/d14010006

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Dvoretsky, Alexander G., and Vladimir G. Dvoretsky. 2022. "Epibiotic Communities of Common Crab Species in the Coastal Barents Sea: Biodiversity and Infestation Patterns" Diversity 14, no. 1: 6. https://doi.org/10.3390/d14010006

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