P.S.Z.N. I: Marine Ecology, 170-3): 67-75 (1996) © 1996 B lackwell Wi o$chafts-Verla , Berlin ISSN 0173-9565

Accepted: May 9,1995

Habitat Provision for Meiofauna by Fucus serratus Epifauna with Particular Data on the Flatworm Monocelis lineata

PAT 1. S. BOADEN

The Queen's University of B Ifast School of Biology and Biochemistry, Marine Biology Stalion. Portaferry, Co. Down, BT22 JPF, Northern Ireland, U. K.

Witl'fl figure and 5 tables

Key words: Fucus serratus, meiofauna, epifauoa , Turbel/aria. Monoceli lineata.

Abstract. Fucus serratus provides a habitable site For much epifauna if conditions are right. Epifaunal colonies in their turn as wen Provide habitats in which meiofauna can dwell. Thus micro-environment i provided which is D pendent on colony-&pecies, - ize and silt for its riches. Analysis of population data shows the facts are Turbcllarian abundance rarely relates to other taxa. However the flatworms' population count Closely relates to total meiofauna.! amount. Experiments on bryozoall-choice by Monocelis lineara show This wonn prefers Flustrellidra as a place to go. This may in part be due to thigmotactic deference But mainly seems related to a feeding preference. In addition to behaviour towards food and concavity, Responses are shown to light, temperature, CUlTent and gravity. In the discussion thus it is partly explained How meiofauna finds epifauna and thee' i maintained.

Problem

When working in science one seldom ha time To work up the data then put it in rhyme, But if science se ms dull perhaps we should alter And bring back the methods of GARSTANG, WALTER (1951). A note on uch brackets (e.g.) by this token Thing may be read which should not be spoken. The next authors I mention according (hem honour For reviewing algal epifauna are SEED & O'CONNOR (1981). Their paper summa.rises earlier ref fences To algal epifauna' habitat preferences.

U. S. Copyright Cl afance Cenler Cod Statement: 0173-9565/96/170 I - 0067 $ 11.50/0

68

For meiofauna on seaweeds the old entrance visa Was work e.g. by COLMAN (1940) and WIESER (l952),. But HICKS (1985) now summarizes what's gone before Though for meiofauna on epifauna the lit rature's poor, This lack recently, with co-authors, I ought to redr\!ss By giving a paper - see later - at the last EMI3S The problem now posed is weed and epifauna's role Re meiofaunal occurence. So, towards this goal, Fucus serratus CL.) has been collected and data On its fauna, especially Monocelis lineata (MULLER), Analysed to try to determine the extent and way that The weed and epifauna mak:e meiofaunal habitat. lW. lineata (Plathelminthes. Seriata) is an euryoecious form, See LUTHER (1960) who says that weed is its norm.

Material and Methods

The plants were collected from SITangford Lough> s shore -

See BOADEN et al. (in press) if YOll want to know more. For behavioural studies and more information, 1994 work was at the 9A Station (54°23' N: 5°33' W).

To determine the area provided by one plant alone It was cut in 10 lengths, then out of each zone Ten random pieces of frond or. if bJ L!, frond ,md stem Had area determined from tracing made round them This was after each had had meiofaunal extraction By the method below, which gives satisfaction. For each of the pieces' epifaunal species an estimate Of % cover was made and from the ratio of weight After blotting, of each zone to each sample It was estimated - simple mathematics were ample -How much habitat for meiofauna one plant of F. serratus

Through its area and epifauna could really impart us. Note: This plant was collected 011 the 13th of July Abundance may cbange as rh C.1sons go by.

Three extractions - two by a 7 min, 7% MgCh SOllse and One with sea water of salinity thirty-three pan per thousand -With the shJk n upemat:lnt poured through a 65 Jl ,ie\e And tIns rin cd wilh s awater into a dish, were found to give A meiofaunal count with mmlbers that were sufficient To show the extraction was about 85% efficient. Worms for Lab w rk were kept dark and quite cold (S° C) And care taken to u e them before a day old. For two or three hours before use, you should mark, Th y were I ft in the lab (18-20° C) in daylight or dark

In choice experiments MOJl(J(.cli'i was given the test To see which epifauna they se rn d to Jik b st;

Colonie� of about equal size were placed in a dish • nd 15 worrm add d (left for 2 h) to go where t11 y'd \\ j�h.

For gravity and light experiments a worm's position W< s easily tracked through th", :-tctdilion Of graph paper undemeath or .1 grid scr:Hched on the base

BOADEN

Meiof3.una OD Fucus serratus

Of a Petri dish or plastic slope (40°). This meant the pJace Could be marked on a graph paper pad trace Every 15 seconds recording turning and pace; Mean turning was detenn ined for each 2 min from the score Of actllal track/straight-line to each mark from that before.

For current OTT (1967) used tbermistors - I'd none of that ilk So I m aSllred the speed with small blobs of milk Relea�ed from the end of a long fine pipette As they passed Cl wire m J nre attached to its jet. This was done before low water with a11 hour still to go, At 65 cm water depth wilh w�ed in its flow. In the lab, worms in a 5 01111 bore glass tube of 30 cm length Were subjected to currents from 0-80 cm· s-1 strength.

The same tube closed off' made a simple device, With one end in warm water, the other in ice, To see if Monocelis placed (F h.' 94) in a gradient show Temperature prd rence high, middle or low. One rainy day (31.1.94) - nearly cold enough to freeze­Temperature was recorded at low tide in Celsius degrees By a thermometer plac d on a plant's surface in the air And down through the Fucus bed (25 cm) each 5 cm layer. One hot sUJruner day (13.7.94) - one without rain! -I went back to the shore 8Jld did it again.

Results

With method explained, the results come at last -The surface of weed was surprisingly vast The plant that wa measured was of a size such To 1 m2 of shore it added 4 times as much,

But since there were really more plants on the shor Plant area in the weed bed was many times more. Analy is of data (Table 1) shows epifauna's the need If much meiofauna's to be found on the weed, So what was important was the mean cover made By the epifaunal species (19%) all over the blade (Fig. 1 A), Bryozoans dominated, e.g., Alcyonidium hirsutwn (FLEMING) The numb rs were such you could not disput them Hydroids had also found themselves room-Young fronds and holdfast letting them bloom (Fig. IB). Lenglh and breadth of fronds and epifaunal cover Will have varied from one plant to another, Howevcr the plant selecled had, to the author's yes, A vc rag epifaunal cover and was of average size. Thu alth ugh there was no whole-plant r plication, This plant hould give a quit good approximation.

The influence of species will now be addre sed On Flu trellidra hispida (F BRICIUS) m iofauna did b �st At two of the sites this dif[�r nee wa cl ar (TabJe 1).

69

llD C

L9

Ut 'l!I! !3 m

LT 0 •

i?� L6

L.S

L4

La

L2

1..1

soon 10000 individuals [nj

others Nematoda Acarina other Turbellaria Monocelis Ostracoda Copepoda

200 400

B

.l3ClADEN

E3 others !W Fiustrellida III Alcyonidium gelalinosum

Electra lE:!! Hydrozoa Em' Alcyonidium fJirsulum

600 BOO lODO 1200 1400 1600 colony area [cm']

Fig. l. A) Surface 3rea and epiraunal cover of, B) epifaunal CO\t�r on, and Ci abundance of meiofaun<l on a �ing1e Pileus scrruJIIS plant from site 9A, Slrangford Lougb Narrows, July 1994. Levels l--IO arc equal length seclions, taken from the plant lo()�ely

bunched togeLher laterally. The planl wasl20 cm long and the calcubted [olal surface 4.0 I 1112 Calculated [otal of the epifaullal cover \vas 0.76 m-2 (i.c.,@:? nl [he plant surface) and of the number of mciofauna! inrJi,·idll,1].; 90.323 Qiving a mean densil\ of 2.25 per cm} of plant sur! aL" , la a are s h(�\vn i � order of overail abundance.

Meiofauna on Fucus serratus 71 Table 1. Meiofaunal dens i ty and mean silt concentration on epifaunal and control samples (frond without any epifauna or flora) from Funis serratus fTom sites in the Strangford Lough Narrows, means of all samples, September 1992 - August 1993; Hest significant statistical differences (unequal variances), *: P < 0.05, **: P < 0.01, ***: P < 0.001, AI: Alcyonidhlm hirsutwn, El: Electra pilosa, FI: Flustrellidra hicl}Jida, C: control, NS: no significant differences.

meiofaul1iL rindiv . . cm-2] silt fmg . cm-2] Alcyonidium Electra Flustre llidra controls all samples

site 194 7.3 t 0.9 10,9 t 2.6 15.2 t 1.3 0.9 t 0.2 30.4 t 4.2 within site FI &C"'** C*** Al & C*** AI, El & Fl*** between site NS WD*** 9A & WD** 9A* WD**

site 9A 8.4 t 0.8 9.7 t 1.1 10.3 t 1.0 O.StO,1 25.6 t 2.8 within site C"*'!' C*** C*** AI, El & FI*** between site NS WD*** 194**. WD·' 194* NS

siteWD 8.2 t 1.0 5.3 ± 0,7 24,8 t 2.9 0.8 t 0.2 49.1 t 6.5 within site E1*, FI & C*** AI", Fl & C*** AI, El & C*** AI, El & Fl*** between site NS 194 & 9A·" 194**,9A*** NS NS

Table 2. Turbellarian density (indiv . . cm-2] on epifaunal and control. smnples (frond without any eplfauna or flora) fi:om Fucus serratus from sites in the Strangford Lough Narrows, meems of all samples, September 1992 - August 1993; Hest significant statistical differences, *: P < 0.05, **: P < 0.01, ***: P < 0.001, AI: Alcyonidium hirsutum, El: Electra pilosa, FI: Flustrellidra hispida, C: control, NS: no statistical difference.

Alcyonidium Electra Flustrellidra

Site 194 1.I7 t 0.28 1.52 t 0,54 2,03 to.32 within site FI*, C**'� C**'" AI*, C**'� between site NS NS \VD * *

Site 9A 1.52 t 0.23 2.18 t 0.57 1.62tO.22 within site C*** C*** C*,�* between site WD** WD"'* \VD**

SiteWD 0.82 t 0.16 0.59 t 0.14 S.17 t 1.25 \>;"ithin site Fl&C· Fl&C'i ** AI, El & C*** between site 9A** 9A"* 9A & WD*'"

A. hirsutum and Electra pilosa (L.) though eame near At 9A. This is the site which for silt was the cleanest And meiofauna on Fluslrellidra was at its lean t. Previous analyses (BOADEN et al., l.e.) I hereby remind For ach of the species at all sik. combined Showed meiofaunal densities had (rong correlations (+) With the epifaunal surfaces' silt concentrations.

I'm intere led in ecology of marine 'fr . Plalyhelminth S Ba DE (1995) for the most recent synthesis, So now I'll present the results and the daw With a particular view to MorlOcelis lineafa.

In J 992/3 turbeIlarian abundance meant Of the total mciofauna they comprised about 14%; I did not check all samples but from several my feel is 70-80% of flatworms founu in fact w r MrJllocelis. The numbers of Turbellaria w [ given some inflation

controls 0.09 t 0.04 AI, El & FI*** NS

0.10 t 0.03 AI, El & Fl**'" NS

0.12 t 0,03 AI, El & FI***

NS

J!t �\ 1L "il"U �";;;;-<4.. Jl� ..i::t'ol-.- .. I,.....--", ���-, t.!� ,�

72

In July 1994 by an acoel population (Fig. le), Nevertheless it can be expected as being quite normal To have 1-21v1. lineata . cm-2 of the surfa e pifaunal. Did worm density (1992/3) relate to epifaunal taxa? See Table 2 to find out what the facts are. Examination of data shows a propensity For small colonies to have a high worm d n 'ily (Table 3).

BOADEN

Table 3. Turbellarian density CD in iudiv . . cnr2) on epifaunal colonies of lesser «) or greater (» than mean area, perimeter, or perimeter to area ratio (of the sample taken) from Fucus serratus from sites in the Strftngford Lough-Nanows, September 1992 - August 1993. AI: Alcyonidium hiT': utum, El: Electra pilosa, FI: Flustrellidra hispida. Separate site data not presented for area and perimeter since only significantly different (Hest) values were for FI at WD (area at **) and for El at 9A (area and perimeter, both at *"').

area perimeter perimeter: area ratio

all sites all sites site 194 site 9A site WD Ai 3.53 ± 0.28 6.90 ± 0.32 2.53 ± 0.22 2.61 ± 0.11 2.09 ± 0.1 1

< > < > < > < > < >

D 1.28 ± 0.92± 1.33 ± 0.94± 1.33 ± 0.99 ± 1.61 ± 1.41± 0.86± 0.79±

0.18 0.17 0.18 0.18 0.39 0.40 0.32 0.11 0.24 0.11

NS IS NS NS NS El 2.87 ± 0.43 7.08 ± 0.67 4.55 ± 0.35 4.45 ± 0.49 3.81 ±0.31

< > < > < > < > < >

D 1.69± 0.72± 1.73 ± 0.68 ± 0.52 ± 2.66± 1.20 ± 3.87 ± 0.62± 0.55 ±

0.37 0.01 0.18 0.10 0.11 1.09 0.27 1.38 0.15 0.29

** ** * '" NS Pi 2.57 ± 0.22 5.58 ± 0.31 2.70±0.lS 2.19 ± 0.11 5.00± 0.61

< > < > < > < >

D 3.71 ± 1.79 ± 3.99 ± 1.69 ± 1.82 ± 2.40± 1.54 ± 1.76 ±

0.73 0.23 0.80 0.22 0.32 0.67 0.23 0.47

** ** NS NS

The nematodes, ostracods copepods and mites Were common meiofauna at each of the sites; With the total of the taxa's densities combined Regression with Oatworms' was the usual thing to find But with each taxon separately the chance was very poor Except on A. hirsutwl1 at the site named 194 (Tabie 4).

<

2.27±

0.73

**

The choice for Flustrellidra found was rather small (Table 5) Worms tended to find something then not move at all But a colony of Flu. trellidra was better than plain frond; To F. hispida d;)maged by cutting most worms would abscond. Light and dark adapted worms responded to laterallight When put on or increased they glid away then left or light. Dark adapted may d the fa ter and turned a little more But for confilTI1ation by statistics probability was too poor.

>

11.9 ±

2.77

all sites 2.41 ± 0.09

< >

\1:07 i·' 1 .30l:� '0:11--0:21 NS 4.27 ± 0.22

< >

0.75± 2.44 ±

0.11 0.63

**

3.30± 0.25

< >

1.91± 5.96±

0.20 1.57

**

Meiofauna on FUCllS serratus 73

Table 4. Regression coefficients between turbellarial1 density, densi ty of other taxa, and si] t concentration (incliv . . cur2 and mg . cm·2 of epifauoal sW'face, respectively). Samples from Fucus serratus from sites in the Strangford Lough Narrows, S plember 1992 - August 1993. Abbreviations as in Table 3.

N mawda Copepoda Ostracoda Acarida total silt meiofauna

Al

site 194 0.37 * 0.45 * 0.62 *** 0.63 *** 0.54 ** 0.34

site9A 0.03 0.20 0.11 0.'19 0.39 :� 0.02

siteWD 0.17 0.30 0.17 0.28 0.33 0.09

El

site 194 0.01 0.29 0.07 0.l9 0.44 * 0.13

site 9A 0.34 0.10 0.12 0.20 0.65 **:,< 0.34

site \VD 0.09 0.08 0.01 0.44 * 0.30 0.0]

FI

site 194 0.08 0.47 ** 0.08 0.10 0.43 * 0.01

site9A 0.06 0.55 ** 0.22 0.31 0.68 • • 0.37 *

siteWD 0.24 0.24 0.12 0.19 0.62 *** 0.69 ***

control

site 194 0.01 0.06 0.17 0.09 0.24 0.23

site9A 0.09 0.01 0.02 0.36 0.42 * 0.18

silt::WD 0.01 0.21 0.13 0.15 0.25 0045 '"

Table 5. Choice experiments with Monocelis lineata from epifaunal colonies on Fucus serratus from site 9A Strangford Lough NaJ.TOWS, March 1994 Botches of 15 worms were placed in seawater in Petri dishes and the numbers which had moved onto the alteruative sllliaces (previously washed free of meiofauna) after 2 h recorded. Abbreviations as before.

choices

Al vs El Al vs Fl El vs Fl control vs Ft

no. of Monocelis 6 8 4 10 6 9 5

5 9 6 9 7 8 4

7 7 5 9 7 7 5

Chi2 s of above

total (df 5) 1.43 4.31 0.67

heterogeneity Cdf 4) 0.S7 0.38 0.30 0.45

overall (df 1) 0.86 3.93 * 0.36 4.12 *

With light above (60 W at 50 cm) speeds were equal rated

But from the straight and narrow 'dark-w rms'deviated; ('Light and dark' speeds 0.55 ± 0.02,0 .59 ± 0.05 cm . S-l, NS and turning rates 1.48 ± 0.01, 1.98 ± 0.42, P < 0.05, n = 5).

When test<:d in a current of up to 40 cm . S·l Monocelis moved and tovirard the source were b ckoned However, above these speeds current proved too strong

All the worms 10 t th ir hold and got swept along. Surface currenluc ,t the hore had a 40 m· ··i sp cd But only 7.5 at th ba of, anclless than 5 with.in, the weed.

10

10

7

4.57

F1 vs cut Ft

6 9

5 9

4 10

4.31

0.38

3.93 *

74

In a t mperatur gradient no matter where they starfed, If not there already, to 17-18° the worms departed .

Relevant her , heat down through weed on the shore In summer was from 31 to 12°, in winter from 0 to 4. On lit slopes dark-adapted worms rapidly descended 'Light-wonns' moved at random. Thus the tests were ended.

Discussion

Fucus serratus itself does not seem to give A habitat where much meiofauna can live But, conditions being right, plant �rrowth is intense

And cpifauna can colonise an area immense (See earlier and SEED & BOADEN, 1977), When the tide's in it's raised of the ground Into the current where food can abound. It is likely that hydroids are round the plant's fringe Since this is where cunents and food most impinge.

In the c nlrc of plants speed may be less But here bryozoan have their greatest success Conver e1y with tide out weed gives insulation From temperature, fr m rain, and from desiccation. In turn it is th extent of epifauna which is R spon ible for the plant's meiofaunal riches.

BOADEN et al. (1995) discussed meiofauna's relation

With epifaunal species' perimeter and surface configuration, As readily observed, e.g., in choice experiments, a fact is That species like MOJlocelis display strong thigmotaxis At other times the worm will glide about of course-I presume for overriding needs or shortage of resource.

The greater density on colonies of high perimeter/area order Implies worms get to colonies by going across their border. ]1.1. lineata is a general predator and scavenger as far as I know S BOADGN (1977) for <lod and for marshes BILIO(l967), So relation with meiofauna or choice of Flustrellidra-cut (Table 5) May well re ult from pr dation

- i. e., what worms need inside in their gut. + geo- and -photo-taxis I've (BOADEN l.c.) found before In IvJoJlocelis from coarse sand on a western Swedi h shor�.

This kept worms from the surface avoiding dangers' chance; Similarly in Strangford it would h Ip keep them in the plants. Migration in a temperature gradient iL xplained with ease In emersed plants worms move not to ov\;rhea.t or freeze.

When in tidal current, since plants ._lrt:am out in its' sp �ed W mm movement should be towards the hasal part of W 'd

BOADEN

Mei ofauna on FUCLlS serratus

But, once uncovered, the weed' s holdfast may be worse For desiccation, h at and other factors quite adverse. Studies here were probably at fault and fail B ecause worm exist in quite another scale -Inst ad of experiencing the cunents ' broad geography They ' re wi thin cpifauna' s boundary-layer micro-topograph y. RlEDL & FORSTNER ( 1 968) say for flatworms in the ph ylal 0.3 mm body height or less may be vital.

Thus simple factors such as light and heat may drive WonTIs to inner and basal fronds where epifauna thrive, Having got there Monocelis lineata can react By staying where i ts food is and keeping colony contact.

Acknowledgements

SlOBHAN McCLUSKEY and others helped with data To these students my tllanks are given pro rata -But even more thanks to JORG OTT and commi ttee For allotti ng m tim :md sp:1ce for this ditly .

References

75

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