The Symbiotic Association of Starfish Asterias rubens and Copepod Scottomyzon gibberum

Journal of Environmental Treatment Techniques

2020, Volume 8, Issue 4, Pages: 1545-1548

J. Environ. Treat. Tech.

ISSN: 2309-1185

Journal web link: http://www.jett.dormaj.com

https://doi.org/10.47277/JETT/1548

The Symbiotic Association of Starfish Asterias

rubens and Copepod Scottomyzon gibberum

Artem POROMOV, Vladimir FEDYUNIN*, Andrey SMUROV

Lomonosov Moscow State University, Faculty of Biology, Department of General Ecology. Leninskiye Gory 1-12, Moscow, 119991,

Russian Federation.

Received: 06/08/2020

Accepted: 10/08/2020

Published: 20/10/2020

Abstract

In this paper we study the specifics of the population of copepods Scottomyzon gibberum Scott dwell in starfish Asterias rubens L.

in Kandalaksha Bay of the White Sea near the N.A.Pertsov White Sea Biological Station. We singled out the "average" most populated

starfish size class. The distribution of copepods on the surface and the proportion of individuals in the galls depend on the type of the

biotope in which populations of starfish live and salinity of the water. In the area of Polovie islands and "Babie Sea" population of

starfish is higher as well as the number of cells in their coelomic fluid. The area of the carapace of copepods in the researched water area

varies.

Keywords: Asterias rubens, Scottomyzon gibberum, population indices, coelomocytes, White Sea, an area of the carapace

classes of starfishes, and the properties of the location of

Introduction

copepods on the body surface of A. rubens. The data of the

population supplemented with the research results of starfish

coelomic liquid cells and dimensional characteristics of

copepods.

Symbiosis is widely common in nature, and symbiotic

associations often play a key role in maintaining normal

functioning of terrestrial, freshwater, and marine ecosystems

(

Smurov, 2003). To understand the nature of symbiotic

associations, interactions in the system "symbiont-host", their

place and role in the existence and dynamics of communities it

is necessary to study various aspects, including topical and

trophic interactions, the seasonal and spatial dynamics, the

influence of biotope conditions and host defense mechanisms

2 Materials and methods

Starfishes were collected in plastic bags near NA Pertsov

White Sea Biological Station (Murmansk region, Russia

(66.55359 °N, 33.10403 °E). The stations are presented in

Table 1. Each starfish was placed into an individual pack. The

sample size was 1015 specimens. We selected intact five-

pointed starfishes from eight stations during the whole

vegetation period of 2012-2013, with the average frequency of

once every three weeks and 30-40 specimens for a time. At the

depth of up to two meters the starfishes were collected by a net,

at the depth of 3-8 meters - using diving equipment. Salinity

and water temperature were measured. We measured

dimensional parameters of the starfishes: Hr (the distance from

madreporic plate to the inner circle, contrradius), r (the distance

from the center to the inner circle, a small radius), R (the

distance from the center to the great circle, a large radius).

Copepods S. gibberum were collected from the surface of the

starfish by a microscopic needle with binocular glasses with

1.8-fold increase. Female copepods were placed in 50 mm-

diameter Petri dishes and fixed with 5% formalin solution for

one day. After fixing females S. gibberum were viewed through

a binocular microscope, we measured the length and the width

of the carapace, and calculated the area, according to the

formula for the area of an ellipse. To characterize the

population of copepods on the surface of the starfish the main

indicators of the number of symbionts were calculated:

extensiveness, intensity, variation index, the character of

distribution of the copepods on the surface of starfishes was

determined as one of the proxy indicators of population status

(

Ieshko, Bugmyrin, & Pavlov, 2009). The object of the study is

the symbiocenosis of mass littoral species of starfish Asterias

rubens L. and copepods Scottomyzon gibberum Scott dwelling

in them. The area of the studied species is distributed in the

territory of the northern seas (Vevers, 1949). Adult females S.

gibberum live on the surface of the starfish A. rubens and

induce the formation of galls. Larval stage, males and young

females are free-living planktonic organisms (Rettger, 1969).

S. gibberum in the White Sea is first described by AV Smurov

(

Smurov, 1993). Copepods of the northern seas typically have

.5-year life cycle with the death of females in October and

November (Rettger, 1969). S. gibberum on the surface of

starfish lead to the formation of galls due to the growth of soft

host covers, in which one or more females are present (Rettger,

969).

A. rubens is characterized by a cyclical population of

copepods during the vegetative period, increasing from June to

October, and during this period the proportion of males on the

surface of starfish increases (A.A. Poromov&Smurov, 2014).

Copepods S. gibberum are sensitive to low salinity, that is why

migration of starfishes to the freshened areas lead to decrease

in their population (Poromov & Smurov, 2014). We studied the

features of the population of copepods S. gibberum living on

the surface of starfishes A. rubens, the character of distribution

of the copepods, described the population of different size

Corresponding author: Vladimir FEDYUNIN, Lomonosov Moscow State University, Faculty of Biology, Department of General

Ecology. Leninskiye Gory 1-12, Moscow, 119991, Russian Federation. E-mail: v-fedyunin@mail.ru

1545

Journal of Environmental Treatment Techniques

2020, Volume 8, Issue 4, Pages: 1545-1548

(

Rózsa, Reiczigel, &Majoros, 2000). Coelomic fluid was

each station by a 1 ml syringe fitted with a 21 mm needle. The

average volume of the collected liquid was 0.6 ml.

extracted from the cavity of not fewer than 10 starfishes from

Table 1: Collection stations of starfish Asterias rubens

№

Collection station

The "Babie Sea"

Coordinates

Type of bottom communities

Type of biotope

Mytilus edulis and Fucus

vesiculosus on rocky ground

N66.602 E33.195

Rocky muddy ground

Mytilus edulis and Fucus

vesiculosus on rocky ground

Fucus vesiculosus on rocky

ground

Zoostera marina, Arenicola

marina on sandy ground

Laminaria saccharina on sandy

muddy ground

Zoster marina, Arenicola marina

on sandy ground

Mytilus edulis on sandy ground in

the estuary

Polovie islands

N65.573 E33.003

Rocky muddy ground

Black gap-

Ermolinskaya bay

N66.332

E033.025

Sandy ground with eelgrass

MSU WSBS pier

N66.331 E33.060

N66.325 E33.071

N66.321 E33.052

N66.311 E32.580

N66.520 E33.198

Eremeevskie

islands

Rocky ground with thickets of

laminaria

Kislaya bay

Sandy ground with eelgrass

Chernaya river

Krestovie islands

Laminaria saccharina on sandy

muddy ground

Rocky ground with thickets of

laminaria

The number of cells in the coelomic fluid was counted in

the boundaries of - 0.5 - 2.2, which corresponds to bands Hr

20.9-32.50 mm., R 14.9-23.9 mm, R 52.1-80 mm. For

copepods it is typical to have negative binomial distribution

on the surface of starfishes.

Hemocytometer in duplication using Romanowsky-Giemsa

staining solution (Venier, Maron, & Canova, 1997). The

statistical analysis was done using the software IBM SPSS

Statistics 20, Quantitative Parasitology 3.0. The level of

significance was set as less than 0.05.

3.2 Spatial differences in the population

Using the values of intensity, extensiveness, it is possible

to select points with high indices of the population - in Polovie

islands and "Babie Sea". The lowest value is typical for the area

of Eremeevskie Islands and Chernaya river. Using the values of

the variation index the same group of points were distinguished

Results

.1 Population of starfishes by size classes

The analysis of size structure of starfishes was conducted

using principal component analysis, which allowed to convert

three measured parameters into one. This conversion makes it

possible to evaluate the connection between the three-

dimensional parameters altogether and the population of

copepods. The regression analysis of the integral size indicator

of the first component (which determines the age variability -

an increase in size with age) was further conducted and the

number of copepods was estimated.

(

Figure 2). In the area of Eremeevskie islands only one adult S.

gibberum female was found on the surface of starfishes.

Figure 2: Spatial differences of the population of starfish Asterias

rubens by copepods Scottomyzon gibberum 1 – the "Babie Sea", 2 -

Polovie islands, 3 - Black gap-Ermolinskaya bay, 4 - MSU WSBS pier,

- in the area of Eremeevskie islands, 6 – Kislaya bay, 7 – Chernaya

Figure 1: The connection of the integral size (calculated during the

factor analysis) of starfish A. rubens and the number of copepods S.

gibberum; on top – the histogram of size classes of starfishes; on the

right – the histogram of distribution of starfishes by the number of

copepods

river, at the entrance to the bay, 8 - Krestovie islands

.3 Distribution of copepods on the surface of the starfish

Asterias rubens

Copepods mostly live on the lateral side of the rays and the

oral side of starfishes (Figure 3). Our observations have shown

that pedicellariae which are greater on the aboral side are able

to capture and hold the copepods while moving planktonic

stages are settling on the surface of starfishes. Depending on

Figure 1 shows a scatter diagram for the dependence of

"integral size index - the number of copepods" and histograms

for these characteristics. An isolated class of medium size

individuals had a relatively greater number of copepods, with

1546

Journal of Environmental Treatment Techniques

2020, Volume 8, Issue 4, Pages: 1545-1548

the ratio of single individuals and individuals in galls the Babie

sea points stand out.

stands for its hydrological characteristics and processes of

bioaccumulation of organic matter in sediments that reach

similar levels with a major port city such as Kandalaksha

(

Peresypkin, 2003). The area of Eremeevskie islands is

characterized by laminaria kelp and strong currents that affect

living organisms at this point. Kislaya bay is a broad sandy

littoral with thickets of eelgrass. Starfishes at this point have

different food ration and color. Chernaya river estuary forms a

"bath" with stratified salt water, which the population of

starfish living at the bottom in low salinity (21 ‰) and intense

rushing river nutrients runoff. In the area of the pier of MSU

Biological Station anthropogenic impact takes place due to the

prolonged economic activity and intensive use of small and

medium-sized boats. The salinity of the water varies within the

range of 21-26 ‰. The points in the area of Lomonosov MSU

biological station, Polovie islands and the "Babie sea" are

located in the area with high anthropogenic load. Females of S.

gibberum can settle on the oral, aboral and lateral sides of the

starfish. When salinity is lowering the population of individuals

on the aboral side increases (t [1, 19] = 2.6, P <0.01). In the

previous studies (Smurov, 1993) it was noted that the copepods

on the aboral side are not revealed. The population depends on

the age of starfishes which can be conventionally defined

basing on the size. To evaluate the population of S. gibberum

in starfish A. rubens the most populated "average" size class of

starfishes was selected. Juveniles are almost unpopulated, big

adult individuals are populated insignificantly as well. For the

studied area the population is connected to the type of biotope.

The highest values of the population indices are relevant for

stony silty soils found in the sea near the "Babie sea" and

Polovie islands. The lowest values are relevant for Krestovi and

Eremeevskie islands which are characterized by thickets of

laminaria and the domination of small specimens (Figure 5).

The observed high values of the variation index near Polovie

islands and the "Babie sea" suggest low individual resistance

and poor immune response (Ieshko, 2009). In the most

contaminated areas (the “Babie Sea” and Polovie islands) of the

studied area the population is higher.

Figure 3: Percentage of individuals of Scottomyzon gibberum on

different surfaces of the starfish Asterias rubens body and the number

of single individuals. 1 – the "Babie Sea", 2 - Polovie islands, 3 - Black

gap-Ermolinskaya bay, 4 - MSU WSBS pier, 5 - in the area of

Eremeevskie islands, 6 – Kislaya bay, 7 – Chernaya river, at the

entrance to the bay, 8 - Krestovie islands

Seasonal dynamics in increase or decrease of the

individuals’ proportion in the galls and the distribution of

copepods on the body surface of starfishes were not observed

for any of the stations across the studied area.

.4 The number of cells in the starfish coelomic fluid

Both the number of cells and the proportion of micronuclei

in cells are different in starfishes collected from different

stations. There are two points in Polovie Islands (77.8 ± 15.6 ×

5 cells/ml) and in the "Babie Sea" (86 ± 10.6 × 10 cells/ml)

characterized by high values of the number of cells in the

coelomic fluid. There are three points with relatively low values

in the central areas (the average value of 35 × 15 cells/ml), the

values do not differ. And there is a point in the estuary of

Chernaya river (54.3 ± 15.6 × 6.7 cells/ml) with higher values

in comparison with the mentioned above.

.5 The area of the carapace copepods

There are differences in the size of the carapace for

different points of the studied area (Figure 4). The largest

copepods are observed in Kislaya bay area.

Figure 5: The spatial differences in the population of Asterias rubens

starfish by copepods Scottomyzon gibberum (ordination analysis: Bray-

Curtis index of similarity, cluster analysis for group average and

Kruskal ordination analysis with non-metric scaling procedure (MSD

Kruskal's nonmetric scaling procedure)). The types of biotopes: 1 -

rocky ground with thickets of laminaria, 2 - sandy ground with eelgrass,

Figure 4. The area of the carapace of copepods Scottomyzon gibberum.

– the "Babie Sea", 2 - Polovie islands, 3 - Black gap-Ermolinskaya

bay, 4 - MSU WSBS pier, 5 - in the area of Eremeevskie islands, 6 –

Kislaya bay, 7 – Chernaya river, at the entrance to the bay, 8 - Krestovie

island

- rocky muddy ground

The conditions of biotope also affect copepods themselves.

The area of the carapaceis wider in the areas with low salinity

t [1, 762] = 0.2, P <0.01). In the area of Kislaya bay, where

there are the greatest sizes of the carapace, sandy soil is

prevailing, the current speed is slow, there are Eelgrass

Discussion

(

The study area includes several biotopes with different

physical, chemical, and hydrological conditions as well as the

sources and levels of anthropogenic influence. The "Babie Sea"

1547

Journal of Environmental Treatment Techniques

2020, Volume 8, Issue 4, Pages: 1545-1548

meadows, the starfishes differ in color (they are lighter). Sandy

soil and Eelgrass meadows are characteristic also for the rest of

the points where there is a relatively large area of the carapace

Authors’ contribution

All authors of this study have a complete contribution for

data collection, data analyses and manuscript writing.

"black gaps", WSBS pier and Chernaya river. Starfishes differ

in terms of the amount of cells in the coelomic fluid, these

values are higher in the areas with a greater population of

copepods (F [2, 5] = 14.2; P <0.029) - Polovie islands and the

References

Poromov, A. A., & Smurov, A. V. (2014). Characterization of copepod

Scottomyzon gibberum scott population on Asterias rubens L.

starfishes under different anthropogenic load conditions. Moscow

University Biological Sciences Bulletin, 69(2), 74–79.

doi:10.3103/S0096392514020126

"Babie sea" .The relatively high number of cells in the coelomic

fluid is also typical for the area of Chernaya river, in the

population of starfishes that live in low salinity. Under

experimental conditions with low salinity the toxic effect of

metals is revealed through the appearance of bacterial

contamination of the coelomic fluid (Poromov, Smurov, 2014).

The symbiotic association of starfishes Asterias rubens and

copepods Scottomyzon gibberum Scott even in small areas have

differences in the populations that may be associated with both

the levels of anthropogenic load, and the features of biotopes.

In this association the host and the symbiont influence each

other. Starfishes affect the distribution of copepods on the

surface due to the activity of pedicellariae. The increased

number of copepods thus leads to the activation of immune

processes with the increase in cell number in the coelomic fluid

of the starfish in the most populated areas. At the same time,

these processes may bepedicellariae greatly affected by both

the natural features of biotopes (salinity, depth, current speed,

and the type of biotope) and the anthropogenic factor.

Poromov, A.,

& Smurov, A. (2014). Scottomyzon Gibberum

(Copepoda) Associated With White Sea Starfish Asterias Rubens

in Spatial and Temporal Aspects. Water Research and

Management,

4(1),

43–46.

Retrieved

from

http://www.wrmjournal.com/index.php?option=com_content&vie

w=article&id=192:scottomyzon-gibberum-copepoda-associated-

with-white-sea-starfish-asterias-rubens-in-spatial-and-temporal-

aspects&catid=49:no-13&Itemid=213

Rettger, R. (1969). Ekologie und Postlarvalentwicklung von

Scottomyzon gibberum, eines auf Asterias rubens parasitisch

lebenden Copepoden (Cyclopoida siphonostoma). Marine

Biology, 2(2), 145–202. doi:10.1007/BF00347013

Rózsa, L., Reiczigel, J., & Majoros, G. (2000). Quantifying parasites in

samples of hosts. The Journal of Parasitology, 86(2), 228–32.

doi:10.1645/0022-3395(2000)086[0228:QPISOH]2.0.CO;2

Venier, P., Maron, S., & Canova, S. (1997). Detection of micronuclei

in gill cells and haemocytes of mussels exposed to benzo[a]pyrene.

Mutation Research/Genetic Toxicology and Environmental

Ethical issue

Mutagenesis,

218(96)00162-0

390(1-2),

33–44.

doi:10.1016/S0165-

Authors are aware of, and comply with, best practice in

publication ethics specifically with regard to authorship

Vevers, H. G. (1949). The Biology of Asterias Rubens L.: Growth And

Reproduction. Journal of the Marine Biological Association of the

United Kingdom, 28(01), 165. doi:10.1017/S0025315400055272

Ieshko E.P., Bugmyrin S.V. (2009) FEATURES OF POPULATION

DYNAMICS AND DISTRIBUTION. PARASITES OF SMALL

MAMMALS. Proceedings of the Zoological Institute of the

Russian Academy of Sciences, 313(3), 319-328.

(

avoidance of guest authorship), dual submission, manipulation

of figures, competing interests and compliance with policies on

research ethics. Authors adhere to publication requirements

that submitted work is original and has not been published

elsewhere in any language.

Smurov A.V. (1993). The first discovery of the symbiotic copepod

Scottomizon gibberum (Scott) (Siphonostomatoida) associated

with the starfish Asterias rubens in the White sea. Reports of The

Academy of Sciences, 333(5), 684 – 686.

Competing interests

The authors declare that there is no conflict of interest that

would prejudice the impartiality of this scientific work.

Smurov A.V. (2003). Fundamentals of environmental diagnostics.

1548