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Ukrainian Journal of Ecology
UkrainianJournal of Ecology, 2017, 7(4), 473-479, doi: 10.15421/2017_146 ORIGINAL ARTICLE
Amphipod assemblage found on sublittoral hydroids in the White Sea with the special remarks to symbiotic association of stenothoid Metopa alderiwith hydroid Tubularia larynx
I.N. Marin1,2, S. Yu. Sinelnikov3
1A.N. Severtzov Institute of Ecology and Evolution RAS, Moscow, Russia.
2Biological Department, Altai State University, Barnaul, Russia. 3I.D. Pa pan in Institute for Biology of Inland Waters of RAS, Borok, Russia. E-mail: [email protected] (corresponding author) Submitted: 11.09.2017. Accepted:24.11.2017
Data on amphipod assemblage associated with sublittoral hydroids collected in the Kandalaksha Bay in the White Sea are presented in the paper. Eleven species of amphipods were found, among them only M. alderi (Stenothoidae) could be considered as specific symbionts for 3 species of sublittoral hydroid, namely H. falcate, S. mirabilis and T larynx. Aquarium and in situ observation showed that adult females of M. alderi occupy hydrants and protect from other invading females, while males are moving between hydrants showing the absence of any strict territoriality. Probably, the species specifically associated with the habitat on the hydroids polyps allowing feed both on tissues of polyp/hydrant and catching floating particles. Females show no negative reaction to juveniles or males presenting on the same hydrants, and normally co-existed during all time of observations. The males during usually actively move inside the colony of hydroids T. larynx between hydrants and migrating to neighboring colonies showing no negative reaction to females or juvenile; they were numerously catch in plankton in September.
Key words: Hydrozoa; associations; symbiosis; Amphipoda; Stenothoidae; Metopa hydroids; Tubularia White Sea
Introduction
Presently, more and more attention of the world scientific community is devoted to the study of symbiotic relationships, and their role in the functioning of marine ecosystems. The most convenient objects for studying symbiotic interactions are colonial coelenterates, in particular coral polyps, with which a large number of different species of living organisms are associated. Rich communities of coral reefs attract researchers, which contributes to their active study. However, due to the peculiarities of metabolism, coral polyps could not live in cold waters, where their ecological niche is occupied by colonial hydroids. However, the number of scientific works devoted to the study of communities of organisms associated with colonial hydroids is extremely small. Nevertheless, being abundant species, hydroids and associated symbiotic communities play an important role in the ecosystems of the northern seas and in many ecosystems are species-edificators. The amphipod family Stenothoidae Boeck, 1871 (Crustacea: Amphipoda) represent a cosmopolitan group of marine benthic amphipods found from tidal zone to continental shelf, with some species recorded at depths of up to 5000 m (Barnard & Karaman 1991; Krapp-Schickel & Koenemann, 2006). Some species are known to be symbiotic living on hydroids, where they seem to eat hosts' tentacles and eggs (Edgar 1983, Krapp-Schickel 1993). Stenothoids are also known to be commensals of hermit crabs (McGrath 1978; Marin & Sinelnikov 2012, 2016; Marin et al. 2013; Vader & Tandberg, 2015) and bivalve mollusks (Vader 1972; Vader & Tandberg, 2013; Krapp-Schickel & Vader, 2015). At the same time, the records of stenothoids among algae can be probably explained the presence of small hydroids (see Marin & Sinelnikov, in press). Nevertheless, according to the nature of the interaction of amphipods with the host and ecology, there is very little data.
In Russian literary sources, representatives of the family Stenothoidae and, especially, of the genera Metopa Boeck, 1871 and Stenothoe Dana, 1852 are mentioned as a component of various benthic samples. Different stenothoids were found in benthic bottom grab samples taken on hard substrates of the Black Sea (Korshunov, 2002) additionally being the main food resources for fish Thyriscus anoplus (Gilbert & Burke, 1912) (Tokranov, 2009). At the same time, there are no data on the ecology of most of stenothoids in the Russian waters.
The aim of this work is to analyze the amphipod species composition inhabiting various hydroids in the Kandalaksha Bay of the White Sea, as well as the study of host specificity and some features of ecology of symbiotic species inhabiting the most abundant and large White Sea hydroid Tubularia larynx (Ellis & Sollander, 1786) (Cnidaria: Hydrozoa: Tubulariidae). During the study we try to describe the fauna of amphipods associated with 5 most abundant species of colonial hydroids and identify species of symbiotic amphipods specific for these hosts.
An attempt to study the symbiontofauna of the hydroids of the sublittoral of the White Sea is presented for the first time. The work essentially complements the data on ecology of symbiotic animals, the problem of mutual relations in the symbiont-host system and contributes to the study of crustaceans and hydroids as the main components of symbiotic complexes of Arctic and Far Eastern seas.
Material and Methods
The collection of the material has been accomplished the area of the Kandalaksha Bay of the White Sea in the vicinity of the White Sea Biological Station of the M.V. Lomonosov Moscow State University (BBS MSU) from mid-July to mid-September 2009. The symbiotic fauna was collected from most abundant White Sea sublittoral hydroids Gonothyrae loveni (Allman, 1859), Obelia longissima (Alder, 1857), Dynamena pumila (Linnaeus, 1758), Clava multicornis (Forskal, 1775), Hydralmania falcata (Linnaeus, 1758), Sertularia mirabilis (Verrill, 1873) and Tubularia (Ectopleura) larynx (Ellis, Solander, 1786). To study the ecology and population structure of associated animals, 80 colonies of hydroids T. larynx of various sizes were collected. Collection was held with regularity 2 times a week; about 5-10 colonies were collected at each sampling. Hydroids were collected underwater with the help of SCUBA equipment. Underwater hydroid colonies were carefully separated from the substrate and placed in sealed plastic bags, eliminating the loss of symbionts. Flushing of symbionts from hydroids was carried out in the laboratory through a net with a diameter of a screen of 70 pm with a 5-10% solution of ethanol. Further, the collected animals and colonies were fixed in a 70% solution of ethanol.
Processing of material was carried out at the Laboratory of Ecology and Morphology of Marine Invertebrates of the A.N. Severtsov Institute of Ecology and Evolution of RAS, Moscow. The symbiotic assemblage from each colony was viewed under the binocular microscope; fixed animals were sorted into groups. The amphipod species identification was carried out according to Guryanova (1951). For statistical studies of population characteristics, individuals collected during one season at one point were taken. All specimens of amphipods were identified to the species level. The results of the analysis of symbiotic assemblage of individual colonies of Tubullaria larynx were recorded in tables showing the number of males, females, juveniles and their size. The size of the crustaceans was measured from the tip of the rostrum and to the last urosome segment. The sex was determined by the presence or absence of a marsupial bag (available in females only), as well as the structure of the gnathopod II and the length of antenna II. The number of eggs and the expected stage of their development were indicated in females with eggs in marsupium. Semi-permanent glycerol preparations of limbs were prepared for the species identification and then studied under Olympus Bx41 microscope. Worms, mollusks and other organisms found on hydroid colonies were also identified and weighed to determine their biomass. Data on the weight of the size and species composition were recorded in the tables.
Results
Various sublittoral hydroids were collected in order to reveal the specificity of the associated amphipods. Representatives of the family Stenothoidae were found in samples with the colonies of hydroids G. loveni, H. falcata, S. mirabilis and T. larynx (see Table 1). Also other amphipods, namely Amphithoe rubricata (Montagu, 1808), Ischyrocerus cf. enigmatus (Gurjanova, 1934), Crassicorophium bonelli(Milne-Edwards, 1830), Sympleustesglaber (Boeck, 1861), Pleustespanoplus ssp. tuberculatus (Bate, 1858), Eurystheus melanops(G. Sars, 1882), Dulichia bispina (Gurjanova, 1930), Dulichia porrecta (Bate, 1857), Socarnes vahli(Kr0yer, 1838) and caprellids Caprella septentrionalis (Kreyer, 1838), were found in our samples. All these species were also found separately from hydroids on sublittoral algae and the fucales (fucoids) in the littoral zone.
Specificity of collected amphipods
Caprella septentrionalis(Kreyer, 1838) (Caprellidae) lead a sedentary lifestyle and live on various substrates to which they are attached by means of specially adapted pereiopods V-VI. These amphipods specialize in catching detritus particles from the water column with the help of antennas I-II and gnathopod I densely covered with bristles and setose setae (Geptner, 1963). Crassicorophium bonelli (Milne-Edwards, 1830) (Corophiidae) and Ischyrocerus cf. enigmaticus (Gurjanova, 1934) are sedentary animals building muddy tubes on bottom. They create water currents through the tube with the help of pleopods and gnathopods armed with fan-shaped bristles catching detritus particles suspended in water (Gurjanova, E.F., 1951). Their records in the samples can be explained by the fact that when collecting material the colonies were placed in a package together with the surrounding substratum.
Ampithoe rubricata (Montagu, 1818) (Amphitoidae) is one of the most abundant sublittoral species of amphipods in the White Sea. The species is found in large numbers on the rhizoids of Laminaria algae. The diet of A. rubricata includes remains of plant and animal origin (Skutch, 1926).
Sympleustesglaber(Boek, 1861) (Pleustidae), similar to A. rubricata, is an abundant sublittoral species exclusively inhabiting the zone of algae (Gulliksen, 1978). The species was found in almost all samples with colonies T. larynx and other hydroids studied, except D. pumila. It should also be noted that only juvenile specimens were found in our samples. Pleustespanoplusssp. tuberculatus(Bate, 1858) (Pleustidae) is a sublittoral amphipod species found in crimson clusters and bottom fouling communities in the White Sea. Similar to above species, was found only once in the sample from the colony of T. larynx.
Eurystheus melanops (G. Sars, 1882) (Isaeidae) is the White Sea sublittoral species found at depths of 10 to 90 meters. There is no literary data about the lifestyle of the species.
Table 1. The fauna associated with the sublittoral hydroids of the White Sea (only hydroids where stenothoid amphipods were found)
Hydroid host Number of Symbiotic species Number of
collected specimens of
colonies symbionts
Gonothyraea loveni 8 Amphithoe rubricata 91
Caprella septentrionalis 24
Eurystheus melanops 2
Ischirocerus cf. enigmatus 5
Metopa alderi 12
Sympleustes glaber 9
Chironomus f.l. solenarius 12
Nymphon cf. longitarse 13
Obelia longissima 9 Metopa alderi 25
Ischirocerus cf. enigmatus 19
Sympleustes glaber 25
Chironomus f.l. solenarius 40
Nymphon cf. longitarse 7
Hydralmania falcata 7 Caprella septentrionalis 49
Corophium bonelli 25
Eurystheus melanops 10
Ischirocerus cf. enigmatus 12
Sympleustes glaber 97
Metopa alderi 49
Isopoda gen et sp. 6
Dendronotus frondosus 12
Tubularia larinx 44 Amphithoe rubricata 1
Caprella septentrionalis 4
Corophium bonelli 358
Dulichia bispina 60
Dulichia porecta 29
Eurystheus melanops 83
Ishirocerus cf.enigmatus 130
Metopa alderi 1215
Pleustes panoplus 1
Socarnes vahli 1
Sympleustes glaber 846
Mytilis edulis 1142
Coryphella verrucosa 44
Dendronotus frondosus 79
Amphitrite figulus 37
Lepidonotus squamatus 79
Pista maculata 5
Phillodoce maculata 29
Pterosyllis finmarchica 71
Nematoda gen et sp. 156
Nymphon longitarse 8
Phoxichilidium femoratum 47
Sertularia mirabilis 7 Caprella septentrionalis 15
Corophium boneli 25
Eurystheus melanops 5
Ischirocerus cf. enigmatus 12
Metopa alderi 34
Sympleustes glaber 57
Coryphella verrucosa 5
Mytilis edulis 19
Lepidonotus squamatus 8
Nymphon longitarse 4
Dulichia bispina (Gurjanova, 1930) and Dulichia porrecta (Bate, 1857) (Dulichiidae) are benthic amphipods that build sticks of silt particles glued together by a special substance secreted by these crustacean (e.g. Mattson & Cedhagen, 1989.). These species form quite large colonies in the sublittoral of the White Sea at depths of 10-25 meters. The species catch the detritus passing into plankton, using antennas I-II, which are armed with long and strong bristles and setose setae. Amphipods D. bispina and D. porrecta build their constructions on the terminal branches of colonial hydroids quite often explaining their finding in our samples.
Socarnes vahli(Krayer, 1838) (Lysianassidae) is an arctic-boreal shallow water species found on silty substrates and in the area of the red algae in the White Sea (Guryanova, 1951). The species was found only once (one female) in the sample from the colony of T. larynx.
Metopa alderi(Spence Bate, 1857) (Stenothoidae) is a sublittoral species living at depths of 5-25 meters on various hydroids of the White Sea. It has previously been reported only as free living and never before as a symbiont (Lincoln, 1979; Dauvin, 1999; after Tandberg et al., 2010). At the same time, the species was found on almost all of the studied sublittoral hydroids in relatively large number of specimens, except hydroids C. multicornisand D. pumilla. However, the most numerous clusters of the species represented by adult males, females and juveniles of different ages were observed on T. larynx, S. mirabilis and H. falcata. In our samples from colonies of G. loveni and O. longissima, these amphipods were also found, but they were presented by young and immature females only. According to the data obtained after the analysis of samples, the population of the species from mid-June to mid-August is represented by juvenile specimens of different ages and sexually mature females with eggs at different stages of their development. Males appear in samples only at the end of August and are presented at September catching in plankton during the night. The species has been never observed on other substrates than hydroids.
Observations on the behavior of Metopa aderiCBate, 1857) on hydroid hosts.
During the observations in aquarium and in situ it was indicated that each separate hydrant is occupied by adult female attaching to the stalk with the help of thoracic appendages IV-VII, while gnathopods I-II are directed forward and most likely participate in the food collection.
Most of observed time females were sitting on the top of the hydrant, crawling on hypostomal polyp periodically and moving up and down along the perisarc (stalk) of the hydrant. When any large object was flowing into the water near the colony, amphipods crawled to the base of the colony. Periodically the amphipods folded and cleaned something from their pleopods using gnatopods that, we suppose, should be considered as a forming of "food lump". The contents of the "lump" were examined under a microscope showed that it is usually consist of diatoms, plankton algae and transparent mucus, which can be the mucus of hydroids.
A sometimes females of M. alderi were observed to swim from one hydrant to another, sometimes, occupied by another individual. After meeting each individuals felt the opponent with antennas, and then tried to drive the invader from the hydrant pushing it with gnathopods. The winner of such competition returned to normal activity. Females show no negative reaction to juveniles or males presenting on the same hydrants, and normally co-existed during all time of observations. The males during the observations led a more active lifestyle moving inside the colony of hydroids T. larynxbetween hydrants and migrating to neighboring colonies. During the meeting with females, males swam away, not trying to compete for the hydrant in any way. Probably, growing bigger than 2 mm in size, juveniles probably move to an independent way of life, and occupy separate hydrants. Unfortunately, the age of transition to an independent (territorial) way of life was not determined during our observation.
d
Fig. 1. a - colony of sublittoral hydroid Tubularia larynxin the Kandalaksha Bay of the White Sea; b, d- separate hydrant of T. larynx occupied by specimens of M. alderi c-general view of M. alderi
Conclusions
1. Eleven species of amphipods were found on the sublittoral hydroids in the Kandalaksha Bay of the White Sea: Metopa alderi (Bate, 1857), Sympleustes glaber (Boeck, 1861), Pleustes panoplus ssp. tuberculatus (Bate, 1858), Ishyrocerus cf. enigmatus (Gurjanova, 1934), Eurystheus melanops (G. Sars, 1882), Crassicorophium bonelli (Milne-Edwards, 1830), Dulichia bispina (Gurjanova, 1930), Dulichia porrecta (Bate, 1857), Socarnes vahli(Kreyer, 1838), Amphithoe rubricata (Montagu, 1808), Caprella septentrionalis (Kreyer, 1838).
2. Among them only M. alderi (Bate, 1857) could be considered as a specific symbiont for 3 species of sublittoral hydroid, namely H. falcate, S. mirabilis and T. larynx. Representatives of the genus Metopa Boeck, 1871 are specialized on symbiosis with colonial coelenterates (e.g. Krapp-Schickel & Vader, 2015) and bivalve mollusks (Tandberg et al., 2010; Vader & Beehler, 1983). Metopa alderi is a subarctic species distributed along the coast of Europe, from the Southwest. Iceland and Boguslena to the Kara Gates and Ugra Ball, in the White Sea, the Barents Sea, near Spitsbergen and east to Greenland and the Kara Sea (Lincoln, 1979; Dauvin, 1999). In the White Sea, this species occurs on various sublittoral colonial hydroids, but mostly on hydroids T. larynx as it was observed in the Kandalaksha Bay. Our specimens were collected on hydroids, inhabiting biotopes characterized by strong currents. Based on the literature data, as well as on our own observations, we can conclude that M. alderiis a specialized symbiont of the White Sea sublittoral hydroids.
3. Adult individuals of M. alderi prefers to live on sublittoral T. larynx while juvenile specimens can be found on L. flexuosa and G. loveni, which probably indicates that adult individuals are able to expel juveniles from the main host.
4. On T. larynx, each individual hydrant of the colony is occupied by one mature female that protect the territory, while males are moving between hydrants showing the absence of any strict territoriality.
5. Stenothoid M. alderi specifically associated with the habitat on the hydroids polyps allowing feed both on tissues of polyp/hydrant and catching floating particles.
Acknowledgments
The author expresses their sincere gratitude to the Director of the White Sea Biological Station of MV Lomonosov Moscow State University (BBS) Prof. A.B. Tzetlin for providing workplace, equipment for experiments and the possibility of living on the BBS as well as the diving team of the BBS for collecting the material. We are sending our special thanks to Alexander Semenov (BBS) for providing beautiful underwater photographs of hydroids and symbiotic amphipods.
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Citation:
Marin, I.N., Sinelnikov, S.Yu. (2017). Amphipod assemblage found on sublittoral hydroids in the White Sea with the special remarks to symbiotic association ofstenothold Metopa alderi with hydrold Tubularia larynx. Ukrainian Journal of Ecology, 7^4), 473-479. I ("OIS^^MIThk work Is licensed under a Creative Commons Attribution 4.0. License
