Variability of the bioluminescence characteristics of the Black Sea ctenophores-aliens in connection with different conditions of nutrition

doi:10.4236/abb.2013.411128

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Advances in Bioscience and Biotechnology, 2013, 4, 968-973 ABB

http://dx.doi.org/10.4236/abb.2013.411128 Published Online November 2013 (http://www.scirp.org/journal/abb/)

Variability of the bioluminescence characteristics of the

Black Sea ctenophores-aliens in connection with different

conditions of nutrition

Mashukova Olga*, Tokarev Yuriy

Department of the Biophysical Ecology, Kovalevsky Institute of Biology of the Southern Seas, National Academy of Sciences of

Ukraine, Sevastopol, Ukraine

Email: *[email protected]

Received 12 August 2013; revised 12 September 2013; accepted 1 October 2013

tion License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly

cited.

ABSTRACT

Many ecological-physiological characteristics of cte-

nophores-aliens Mnemiopsis leidyi A. Agassiz, 1865

and Beroe ovata Mayer, 1912 are studied quite well

because they play a very important ecological role in

the Black Sea ecosystem. However, bioluminescence,

one of the most important elements of the cteno-

phores ecology and its connection with feeding re-

gime were not studied sufficiently. Experiments have

shown that characteristics of the ctenophores biolu-

minescence differed considerably in dependence of

food supplies. Thus, amplitude and light-emitting

energy of the fed ctenophores B. ovata are maximal, 3

times more than analogical indices of the just-caught

individuals and 4 times more than ones of starving

individuals. More prolonged flash signal (to 3.5 s),

which exceeds light-emitting duration of the starving

individuals twice, can be registered from the fed

ctenophores. Investigation of the M. leidyi biolumi-

nescence has shown that amplitude and light-emitting

energy of the just-caught ctenop hore s we re two ti mes

more than those of the starving individuals. At the

same time, light-emitting amplitude of the fed indi-

viduals is 6.5 times and light-emitting energy is 3 - 4

times higher than that of the just-caught ctenophores.

The light-emitting duration of the starving and just-

caught organisms is practically the same. The most

prolonged signal is registered from the fed cteno-

phores—up to 2.8 s. The data obtained testify that

characteristics of the ctenophores bioluminescence

can be conditioned not only by nutritional value but

by the composi ti on of the fo od as we l l .

Keywords: Bioluminescence; Beroe ov at a; Mnemiopsis

leidyi; Black Sea; Nutrition

1. INTRODUCTION

Introduced to the Black Sea in 80 - 90 of the last century

ctenophores Mnemiopsis leidyi A. Agassiz, 1865 and

Beroe ovata Mayer, 1912 have made considerable impact

on the Black Sea ecosystem. At the end of 80s’—begin-

ning of 90s’ years ctenophore Mnemiopsis leidyi, being

transferred into the Black Sea water area with ballast

waters, gave mass flash in abundance [1]. Together with

other factors (climatic changes) this alien considerably

influenced biomass of food mesoplankton, deteriorating

food base of plankton-feeding fish—the base of the

Black Sea fishery, pelagic fish [2].

For example, the sharp increase in number of M. leidyi

has caused increase in a share of larval fish with empty

stomachs that has led to the commercial fish population

reducing by 1991 more than 5 times [3]. At the end of

90s’ another ctenophore Beroe ovata invaded the Black

Sea; which fed exclusively by mnemiopsis, and which

meliorated the state of food base for planktonivorous fish

and their larvae [4].

The processes of ctenophores life-activity (metabolism

intensity, food uptake, composition of organic substance

etc) are studied quite completely [5-7]. But there is prac-

tically no information about connection between the

level of M. leidyi and B. ovata being fed and their biolu-

minescence under natural temperature conditions, as well

as about optimal trophic conditions for the ctenophores

bioluminescence [8-10].

Meanwhile, bioluminescence is one of the links in the

organization of general metabolism in living systems,

biochemical mechanisms of which try some modification

under changes of surrounding conditions [11,12]. Ex-

*Corresponding author.

OPEN ACCESS

M. Olga, T. Yuriy / Advances in Bioscience and Biotechnology 4 (2013) 968-973 969

pressness and expressiveness of receiving information

with the help of given test of organisms’ resistance are

undoubted advantages, if compared with criteria, used in

marine planktonology. That’s why the main task of our

work was estimation of ctenophores M. leidyi and B.

ovata light-emission characteristics changes in connection

with conditions of their nutriation.

2. MATERIAL AND METHODS

Experimental studies of the food factor impact on the

light-emitting parameters of ctenophores have been car-

ried out in the Biophysical ecology department of IBSS

of NASU: in July-August of 2006, and in October-No-

vember of 2007 and 2008. Only freshly collected animals

without any damage used for bioluminescence character-

istics study. Total length (mm) of ctenophores B. ovata

and oral-aboral length (mm) of M. leidyi were measured.

Uni-sized (35 - 40 mm—for M. leidyi and 50 mm—for B.

ovata) animals within 1 - 2 h after catching were taken to

the laboratory for the further adaptation to food experi-

ments.

Ctenophores M. leidyi and B. ovata dependence on

food supplies were divided into 3 groups: just-caught

(control), fed and starving for two days specimens. In

each group there were 40 individuals. The dry mass of

ctenophore bodies was determined by weighing on the

microanalitical weighs AN 50 precisely up to 0.1 mg

after drying at 60˚C, wet weight—by the volume of re-

placed brine in measuring cylinder. Dry mass of the

studied bodies of ctenophore M. leidyi—0.86 ± 0.043 g,

B. ovata—2.36 ± 0.11 g. Wet weight of M. leidyi—9.16

± 0.45, B. ovata—10.88 ± 0.54 g. Ctenophores were kept

in glass capacities by volume 3 - 5 l with sea water, fil-

tered through membrane filters with diameter of pores 35

µm in temperature 21 ± 2˚C [11].

Bioluminescence characteristics of the just-caught cte-

nophore—M. leidyi and B. ovata (1 group) were regis-

tered in 2 h after exposition, in the ctenophore of the

second group (starving individuals)—in 2 days. M. leidyi

were food object for B. ovata. To prepare third group of

ctenophore for feeding beroe were set individually into

5-liter capacities with filtered brine. The food (mne-

miopsis) were put 1 ind per each capacity after prelimi-

nary weighing. Then we observed food behavior of beroe.

We fixed the time of capturing the prey and finish of

digesting, directly after which we conducted stimulation

of the ctenophore light emission. Copepoda Acartia

tonsa Dana were an object of nutrition for M. leidyi, as,

first, they dominate in the mesozooplankton composition

at the second half of summer in the Sevastopol bay [13],

and, second—in the food of the Black Sea mnemiopsis

under natural conditions. That is why for feeding M.

leidyi in experimental conditions we used calanoid co-

pepoda Acartia tonsa Dana, grown in the fish cultivation

laboratory, IBSS, NASU [14].

To support the given ctenophore feeding we brought

into experimental vessels food organisms with concen-

tration of copepoda A. tonsa—70 ind·l−1. Concentration

of copepoda in the experimental vessels was determined

before the beginning of the experiment by counting the

individuals in an aliquot of volume in the Bogorov cam-

era. Concentration of food organisms was corrected

every day, keeping it at the level not less than 0.35 mg of

dry mass for l−1. With such level of food supply cteno-

phores are quite mobile (swim actively) and maximally

uptake oxygen, which supposes their ability in intensive

bioluminescence [15].

The amplitude characteristics of the bioluminescence

were investigated, using the laboratory complex “Light”

[16]. The laboratory complex for studying the biophysi-

cal characteristics of ctenophores bioluminescence in-

cluded a high-voltage power device (VS-22), lumine-

scope, consisting of receiver of light radiation (FEU-71)

and dark chamber for an object, and the digital register-

ing device. Cuvette for mechanical and chemical (5

cm3—for ctenophore) stimulation, in which experimental

organisms were placed, is made of transparent plexiglas.

Registration of ctenophores bioluminescence characteris-

tics was conducted at full darkness. The biophysical

characteristics of light-emission of M. leidyi were studied

using mechanical and chemical stimulation.

For reception of irritation adequate to natural stimulus

we used mechanical stimulation ctenophores [17]. The

method of mechanical stimulation was reduced to crea-

tion of a stream of water in a vessel with bioluminescent

by means of the pump electromechanical device. The

changes of hydrophysical characteristics, caused by move-

ment of water masses lead to deformation of ctenophores

cellular membrane which, in turn, induced occurrence of

potential of action and light-emission. To obtain of the

information about maximal [18] ctenophores biolumi-

nescent potential the method of chemical stimulation was

used as well. By means of a syringe we entered into cu-

vette 3 - 5 cm3 of 96% of the ethyl alcohol chosen as

chemical reagent. Amplitude, duration and full energy of

flashes were compared in each group of individuals for

equal temperature conditions (21˚C ± 2˚C).

3. RESULTS AND DISCUSSION

3.1. Mnemiopsis leidyi Bioluminescence

Experiments have shown that characteristics of the

ctenophores M. leidyi и B. ovata bioluminescence dif-

fered considerably in dependence of food supplies. De-

pendence of the ctenophore M. leidyi bioluminescence

characteristics on a degree of organisms being fed is

shown at Figures 2 and 3. Investigation of M. leidyi bio-

luminescence has shown that amplitude and light-emit-

M. Olga, T. Yuriy / Advances in Bioscience and Biotechnology 4 (2013) 968-973

970

ting energy of the just-caught ctenophores were two

times more (p < 0.05), than that of the starving individu-

als (Figure 1).

At the same time, light-emitting amplitude of the fed

species is 6.5 times and light-emitting energy is 3 - 4

times higher than that of the just-caught ctenophores

(Figures 2(a) and (b)).

The light-emitting durations of the starving and just-

caught organisms were practically the same. The most

prolonged signal is registered from the fed ctenophores

M. leidyi—up to 2.8 s (Figure 2(c)).

Nutritive behavior of beroe is studied quite well

[19,20]. In our investigations 90% of B. ovata individu-

als captured the prey (mnemiopsis), eating it in a whole

if it was less in size, and other ate it, pulling it by pieces.

3.2. Beroe ovata Bioluminescence

Capture of food was observed averagely in 2 h after its

setting there. Being eaten by beroe, ctenophore acquired

a ball-form, and the time of digesting in experiments

lasted averagely 4 - 5 h. The characteristics of lumines-

cence in the fed ctenophore beroe were studied after di-

gesting of food and compared with those of the just-

caught and starving individuals. Dependence of biolu-

minescence characteristics in ctenophore B. ovata on a

degree of their organisms being fed is represented at

Figure 3.

Maximal values of bioluminescence amplitude in the

fed B. ovata 3 times exceeded analogous indices in the

just-caught individuals (Figure 4(a)) and 4 times in two

days starving organisms (p < 0.05).

Indices of energy in the just-caught, fed and starving

individuals also differ considerably (Figure 4(b)).

The energy of light emission reaches highest values in

the fed ctenophore, making (348.35 ± 17.41)·108 quan-

tum·cm−2, which is 4 times higher than analogous indices

in the just-caught organisms. But energetic indices in the

Figure 1. The typical bioluminescence signals of M. leidyi

under different nutrition conditions.

just-caught

M. leidyi

(control)

starvi ng for

two days

ctenophores

fe d

ctenophor es

100

200

300

400

500

600

Amplitude of light-emission, *10

quantum*s

-1*

-2

(a)

jus t-caught

M. leidyi

(contr ol)

starving for

two days

cten ophores

fe d

cteno phores

100

200

300

400

500

600

Energy of li ght-emi ssion, *10

quantum*cm

-2

(b)

just- caught

M. leidyi

(control)

starving for

two days

ctenoho r es

fed

cteno phores

0,5

1,5

2,5

Duration of light-emi ssion, s

2.5

1.5

0.5

(c)

Figure 2. (a) The statistical estimation of the light-emission

amplitude ratio of just-caught, starving for two days and fed

ctenophores M. leidyi; (b) The statistical estimation of the

light-emission energy ratio of just-caught, starving for two days

and fed ctenophores M. leidyi; (c) The statistical estimation of

the light-emission duration ratio of just-caught, starving for two

days and fed ctenophores M. leidyi.

M. Olga, T. Yuriy / Advances in Bioscience and Biotechnology 4 (2013) 968-973 971

Figure 3. The typical bioluminescence signals of B. ovata

under different nutrition conditions.

just-caught ctenophores are 2.5 times higher than in

starving individuals, making (122.82 ± 6.14)·108 quan-

tum·cm−2—under mechanical stimulation and (81.10 ±

3.24)·108 quantum·cm−2—under chemical one.

It is known that bioluminescence characteristics in

ctenophores differ considerably under different types of

stimulation [21]. In the given investigations, they ob-

served the highest magnitudes of the light emission am-

plitude and energy in the fed individuals M. leidyi under

chemical stimulation, and in the fed individuals B.

ovata—under mechanical stimulation.

Flashes duration of just-caught and fed individuals

(Figure 4(c)) is practically the same.

But more long flash signal—up to 3.5 s, especially

under the mechanical stimulation, can be observed in the

fed ctenophores, and that exceeds twice (p < 0.05) time

of light emission by the starving for two days individuals.

Thus, maximal energy and time indices of biolumines-

cence in M. leidyi as well as B. ovata are registered in the

fed species and minimal—in starving ctenophores.

We may suppose that the most intensive luminescence

of the fed and just-caught ctenophores is conditioned by

the fact that level of oxygen consumption by them makes

maximal values [16]. For example, the oxygen consump-

tion intensity in starving individuals decrease considera-

bly during two days [22], due to the energetic parameters

of their bioluminescence (amplitude, in particular) de-

crease too.

In addition, taking into account the change of cteno-

phores biochemical composition depending on a degree

of their being fed [23] and biochemical nature of biolu-

minescent reactions we can explain the registered chan-

ges of ctenophores biophysical light-emission character-

istics by a change in food supplies. Observed in experi-

ments depressed condition of ctenophores in connection

with starvation and minimal indices of their biolumines-

cence can be explained by decrease in content of re-

(a)

(b)

3.5

3.0

2.5

2.0

1.5

1.0

0.5

0.0

(c)

Figure 4. (a) The statistical estimation of the light-emission

amplitude ratio of just-caught, starving for two days and fed

ctenophores B. ovata; (b) The statistical estimation of the

energy of light-emission ratio of just-caught, starving for two

days and fed ctenophores B. ovata; (c) The statistical estima-

tion of the light-emission duration ratio of just-caught, starving

for two days and fed ctenophores B. ovata.

M. Olga, T. Yuriy / Advances in Bioscience and Biotechnology 4 (2013) 968-973

972

served polysaccharide—glycogen. The glycogen content

in polysaccharides, reaching maximum in the just-

caught organisms (76.0—in B. ovata and 86.6% in M.

leidyi) reduced substantially under starvation: to 34.4% -

in B. ovata and 18.3% in M. leidyi. Monosaccharide con-

tent under starvation of ctenophores decreases from

39.9% to 13.5% in B. ovata and from 45.8% to 14.3% in

M. leidyi [22]. Fed ctenophores as M. leidyi, as B. ovata,

with ample being fed have maximal concentrations of

organic matter; therefore, in the time of light-emission

they give the most intensive flash. Studied dependences

of ctenophores light-emission characteristics on food

supply make essential contribution to the exposure of

consistent patterns of trophic cooperations predator-prey,

important at the research of water organisms and ecosys-

tems functioning.

4. ACKNOWLEDGEMENTS

The authors express sincere gratitude for help in experiments with M.

leidyi to A. N. Khanaychenko, the leading scientist of the IBSS of NAS

of Ukraine.

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