Journal of Ptankloo Roearcb Volume 1 Number 3 1979

Grazing of echinoderra larvae (Paracentrotus lividus and Arbacialixula) on naturally occurring particulate matter.

Fereidoun Rassoulzadegan & Lucienne Fenaux

Station Marine, Station Zoologique, 06230 Villefranche-sur-Mer, France(Received February 1979; accepted (revised) September 1979)

Abstract. Larvae (72 hr old) of P. lividus and A. lixula grazed on various suspensions of natural par-ticulate matter with a size range of 2 to 30 microns, and on two species of algae (Phaeodactylum tricor-nulum and Nitzxhia sp.)

— Larvae graze most in the size range where the particle concentration is highest.— If larvae deplete certain size categories of particles they then graze other size ranges in which the con-

centration is still high.— The grazing rate of the two species varied between 988 and 91.949 um' per pluteus per hour.— For A. lixula larvae the grazing rate increases with increasing temperature to a maximum at 22°C.

Introduction

The role of microplanktonic organisms in energy transfer has been particularlyrevealed over the last ten years. According to Beers and Stewart (1969, 1971),microzooplankton forms about 40% of the total planktonic particulate matter andcan graze about 70% of the daily organic carbon production of the phytoplankton.

Recent works concerned mainly with Protozoa has shown that microzooplanktonfeeds on nanoplankton, which is also a facultative food for macrozooplankton(Blackbourn, 1974; Rassoulzadegan, 1978; Heinbokel, 1978). Different groups ofProtozoa tend to succeed the nanoplankton maxima (Ibanez and Rassoulzadegen,1977).

A group of organisms can be defined which, because of the small size of itsmembers, plays a role in the food chain which is complementary to, or competitivewith the microcrustaceans dominating the zooplankton. In most of these organismsthe feeding mechanism is different from that of copepods, being a filter mechanismdepending on ciliary action around a buccal cavity (Protozoa and metazoan larvae).Echinoderm larvae belong to this group of microzooplankton.

Gemmil (1914, 1916) Runnstrdm (1918), Tattersall and Sheppard (1934) andStrathmann (1971) have described the feeding of planktotrophic echinoderm larvae.Like the microzooplankton, these larvae graze phytoplankton of small size (Lebour,1922; Bougis, 1963; Strathmann, 1971), and thus play an important role in thetransfer of substances synthesized by the phytoplankton. Since their rate of growthis considerable, the size range of their particulate food is also considerable, passingfrom small particles at the beginning to large algal cells at the end of their pelagic lifeand thus overlapping the sphere of feeding activity of zooplankton of large size.

Little is known of the size ranges of particles grazed by larvaes at different stages.Strathmann et al. (1972) suggested that larvae cannot capture particles of about 1micron in diameter as efficiently as larger particles. The present work is concernedfirstly with determining the range of particle sizes forming the food of larvae of

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Paracentrotus lividus (Lmk) and Arbacia lixula (L.) when offered natural popula-tions of marine particles, and secondly with comparing the intensity of feeding ac-tivity of larvae fed on mixed particles with those fed unicellular algae (Phaeodac-tylum tricornutum and Nitzschia sp.). The effect of temperature on feeding rateswas also studied.

Materials and methods

Larvae of P. lividus and A. lixula were obtained by artificial fertilization in thelaboratory. Embryos at the 2 or 4 celled stage were placed in beakers of sea waterfiltered through a 0.22 \an Millipore filter, at a temperature of 18-20°C. The concen-tration of embryos was about 10 per ml. At the end of the endotrophic phase (72hours after fertilization at 20°C), healthy larvae were separated by pipetting andplaced in 250 ml or 1 1. beakers containing twice filtered sea water (Millipore 0.22

The dry weight of larvae was measured after fixation in 5% formaldehyde, rinsingin ammonium formiate isosmotic sea water, at pH 8.1 and drying for 48 hours in anover at 60°C.

Plutei were incubated, in a constant temperature chamber, in 250 ml or 11. flaskswith either algal cells or natural particles. Control flasks without larvae were treatedsimilarly. The flasks were rotated slowly to ensure water mixing.

Changes in the proportion of particle size* after larval feeding were estimatedfrom measurements made with particle counters (Coulter counter TA or themultichannel analyser C 1000). Water samples of 2 to 16 ml, depending on diameterof the aperture of the sampling device (100 and 200 \ari) and on the particle concen-tration were taken by aspiration.

Wide ranges of particles sizes were chosen: from 1.3 to 52.1 yon (taken with a 100ion sampler aperture) or from 2.6 to 104 yaa (with a 200 fan), each range being sub-divided into 16 categories. For more detailed analysis, restricted size ranges werechosen, falling into three groups: group 1 from 2.92 to 5.99 /im, subdivided into 18

•When we speak of particle size or counter channel limits, the dimensions correspond to the diameter of asphere whose volume is equal to that of the particle (equivalent sphere).

Experiments were carried out in the following order:

Species

A. lixula

P. lividus

P. lividus

A. lixula

Food

natural particles concentratedby centriTugation(1.1 x 10' x ml- ' )natural particles concentratedon filter paper(1.2x 10* x ml"1)Phaeodactylum +NitzschiaPhaeodactylum

Date

mm

1-6/6/78

20/10/77 *

13-21/6/78

Incubationtemperature ( ° Q

18

18

18

16, 18, 20, 22,24.5

Final concen-tration oflarvae per ml

1.6

1.5

10

13, 11, 5, 7,6 ,8

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Grazing ecfainodera tarrac

classes, group 2 from 5.29 to 11.61 nm, divided into 18 size classes, and group 3from 12.56 to 22.34 ^m, divided into 10 size classes.

For each of the size classes 3 successive measurements were made for all controland experimental flasks. The results shown in various figures represent the meansvalues ± the standard error.

In the experiment concerning the rate of grazing on a culture of Phaeodcatylum,the size classes were grouped in tens from the 51° to the 100th classes. This procedureexplains the shifts in the curve in fig. 4.

Results

I—Size ranges of the naturally-occurring participate matter grazed by P. lividus andA. lixula larvae.a) Grazing of P. lividus larvae on natural particles concentrated by Whatman filter

paper.This experiment showed a greater rate of grazing of particle between 2.92 and11.61 pan in diameteT than of larger particles. Fig. 1 shows that during the first24 hours P. lividus larvae graze on very small particles (2.92 to 10 yaa) with alow feeding rate. Between 24 and 71 hours, the larvae increase their grazing rateon small particles and also take larger ones.

b) Grazing of A. lixula larvae on natural particles concentrated by centrifugation.Fig. 2 shows that from a unimodal distribution of particles of 1.3 to 26.9 \an(peak at 5 \aa), larval grazing was uniform throughout the size range.

J2

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N

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0 to 24 th h

24*10 71 t h h

7 12 1/

Particle diameter Cum)

Flg.l Grazing rate of P. lividus larvae on natural particles (24 to 71 hours).

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Control partick concentration

Larval grazing

10 20

Diameter of •quivalcnt iphars (jm)

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Fig.2 Sizerangeof natural particles concentrated by centrifuge grazed by A. lixula larvae (1.6 plutei perml).

II—Food switching of P. lividus larvae in a mixture of Phaeodactylum andNitzschia.

Fig. 3 shows the changes in grazing activity of larvae presented with a mixture ofPhaeodactylum (3.5 to 5.5 pun in diameter) and Nitzschia (6.5 to 15 j*m in diameter).Particles of intermediate size, or smaller than 3.5 or larger than 15 fim recorded inthis experiment were impurities in the culture. It can be seen that in the first 18 hoursthe larvae grazed mostly particles of small size comprising the Phaeodactylum cells.Then from 18 to 42 hours their grazing shifted into the range containing Nitzschiacells: in the last 24 hours, grazing in this range was very high.Ill—Relation between the algal concentration (Phaedactylum) and the grazing of Alixula larvae.

In this experiment (Fig. 4) grazing was greatest around the mode of Phaeodac-tylum size distribution. An important increase in the quantity of small-sized par-ticles (4 \an) occurred. This effect has been recorded with other filter-feedingorganisms and may be explained by fragmentation, the rejection of fine particles orbacterial proliferation which is encouraged in the presence of filterers(Rassoulzadegan, 1978). In Fig. 4, the correlation can be seen to be strongly positive(r = 0.91, p= 0.99) as the concentration increases to the modal value and becomesnegative (r = 0.95, p = 0.99) beyond. Thus the grazing reflects the normal distribu-tion of the algal cell sizes.IV—Comparison of grazing rates and volumes of water filtered in the two larvalspecies.

From Table 1 it can be seen that the volume of food grazed varies between 998 and91949 um1 per larvae and per hour, and on the whole A lixula larvae showed higher

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rates than P. lividus larvae.The filtration rate, i.e. the volume of water depleted of suspended matter per unit

time, depends on the length of the ciliated band. The value obtained here (0.013 to0.472 u\ per min and per mm ciliated band) were lower than the maximum rates (1.2u\ per min and per mm ciliated band) calculated by Strathmann (1975) from the dataof Whiteley and Baltzer (1958) for these species.

As to the effect of temperature on filtration rate, Fig. 5 shows that, grouping allparticle sizes, the maximum value (0.065 u\ per min and per mm ciliated band) isreached at 22°C.

Discussion

The larvae of the two echinoderms (P. lividus and A. lixula) obtained from Mediter-ranean stock, are capable of grazing very fine particles, down to 2 \tm in diameter. Itis not possible to define the upper size limit of particles grazed in these experiments,since those above 30 um were relatively scarce. Particles at the lower size limit, whensufficiently abundant in the natural suspension, were always grazed in these ex-periments, although according to Strathmann et al. (1972) these cannot be capturedefficiently by the larvae. This is probably explained by the fact that all planktonicfilterers graze largely in the particle size ranges where the concentration is high(Mullin, 1963; Richman and Rogers, 1969; Frost, 1972; Poulet, 1973; 1974; Wilson,

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Fig.4 Grazing of A. lixula larvae on a P. tricomutum suspension (a) and linear regression relationshipsbetween grazing rate of A. lixula larvae and P. tricomutum (b).Y =- 302 X -1102Y - -237 X +1372.

1973). This was seen in the experiment on the grazing of Phaeodactylum by A. lixulalarvae, where the highest grazing rate is a function of particle concentration, amongother factors.

Of the two species chosen for this study, A. lixula has a much higher grazing ratethan P. lividus. From a study of the larval populations in the Bay of "Villefranche-sur-Mer" between 1960 and 1964, Fenaux (1962, 1968a, 1968b) found that A. lixulahas pelagic larvae from the beginning of summer to November, while P. lividus, in

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Table I. Grazing rates and volumes of water filtered by the planktonic larvae of P. IMdus and A. lixula.

Species

A. lixula

P. lividus

P. lividus

A. lixula

Nature ofpaniculatematter

Natural particlescentrifuge-concentratedNatural particlesconcentrated onniter paperPttaeodactylum +NitzchiaPhaeodactylum

FOOD

Concentrationsfun'xml-'

1.1x10*

1.2x10*

10*

3.2x10*

Grazing rateurn1

x plutei - ' x h - '

91949

988-5390(0-24h)(24-71h)

1103-3743(0-18h) (18-42h)2167-10008(16°Q (22°O

Filtration rate\A x plutei - ' xmin-'x(mm ciliated band)-'

0.472

0.017-0.157

0.021-0.082

0.013-0.065

addition to producing a few larvae throughout the year, has two main reproductionperiods: one of 15 days at the end of May and a second of two months in autumn.The larvae are thus mainly present from spring to autumn, with very abundantplutei of A. lixula in the summer. Echinoderm larvae can reach considerable den-sities, especially during their summer peaks (4000 indiv./mJ). Their ecological role isimportant as they constitute the main filterers at a time when other zooplanktonorganisms are largely absent. They thus replace others in energy transfer in neriticecosystems in the summer period when peak polulations of peridinians are present.The experiments on the effects of temperature on grazing rates of A. lixula give anoptimum temperature of 22°C which lies within the normal temperatures recordedbetween mid-summer and mid-autumn. We have attempted to estimate the grazingrate for all larvae per m3 per day, using the conversion rate of particle volume intoorganic carbon of Parsons et al. (1967), assuming that 40% of the dry weight isorganic carbon (Beers et al., 1975) and with the grazing rates of the present study(2.7 as a low rate, 114.7 /ig C per day as a high rate). This gives values from 50.9 to458.8 fig of participate carbon consumption per day per mJ, according to theperiodic abundance of the larvae. Interpreting these results in the light of the knownseasonal cycles of phytoplanktonic biomass in the Bay of Villefranche-sur-Mer, in-dicates that echinoderm larvae can reach a daily grazing of the order of 3°7o of thephytoplanktonic biomass. As to the production of organic matter, the results of thepresent work permit a certain indirect evaluation, namely, that a larvae can grazedaily an amount of organic carbon equivalent to 2 to 72% of its body carbon. Thesevalues are similar to those obtained by Mullin and Brooks (1967) and Petipa et al.(1970) for copepod nauplii, which have a much higher grazing rate per unit weightthan adult copepods.

AcknowledgementsThis work was supported by grants from the "Centre National de la RechercheScientifique" (E.R.A. 228: Ecologie du Plancton marin).

We wish to thank Dr R. Strathmann for this critical reading of the manuscript.

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