The flora and fauna associated with Himanthalia elongata (L.) S. F. Gray in relation to water current and wave action in the Lough Hyne marine nature reserve

Estuarine,

Coastal

and Shelf

Science

(1987) 25,663-676

The Flora and Fauna Associated with Himanthalia elongata (L.) S. F. Gray in Relation to Water Current and Wave Action in the Lough Hyne Marine Nature Reservea

J. A. Kitching School

of Biological

Received

6 March

Sciences, University 1987 and in revised

of East Anglia, form

12 June

Norwich,

U.K.

1987

Keywords: algae; epiphytes; water; currents; wave-exposure;

Lough Hyne

The growth of epiphytes (plant and animal) was investigated at various stages in the development of the low littoral alga Himanthalia elongata. The vegetative thallus, or button, is very resistant to the settlement of epiphytes on its upper surface, but susceptible to extensive coverage on its lower surface and stalk, especially by Bryozoa and spirorbid worms. The receptacles or straps are invaded by a microforest of filamentous algae, which in turn provides accommodation and in many cases food for many invertebrates, including gastropods, amphipods and larval Diptera. Spirorbid worms on the underbuttons are confined to sites sheltered from strong water currents and wave action, but other epiphytes of the underbuttons show little regard for these features. Microforest and its associated fauna are restricted to sheltered sites. Perspex discs set up as imitation Himanthalia buttons were colonized by the same epiphytes as real Himanthalia buttons, but on both sides, indicating the existence of a special protective mechanism for the upper surfaces of real Himanthalia buttons.

Introduction The life of the alga Himanthalia elongata (L.) S. F. Gray (Phaeophyceae, Fucales) usually extends over a period of about two years, during which time it passesthrough a seriesof stages(Figure 1, modified and metricated from Moss, 1952). According to Gibb (1937), at Aberdeen ova and sperm are liberated during the period from July to the following January. The young vegetative thallus or button grows through stages 1 to 4, and the receptacles or straps first appear (stage 5A) in the following July, grow in length (5B), begin to branch (5B, 5C) in October, and reach their full length (often over 2 m) by the following July, when discharge of ova and sperm begins. Discharge may be delayed until January.

The whole

plant finally

disintegrates.

The numerous epiphytic algae which are associatedwith H. elongata at Roscoff were surveyed by van den Ende and Linskens (1962). The algae are distributed preferentially “Paper No. 24 in the series ‘ The ecology of Lough

Ine ‘.

663 0272-7714/87/060663

+ 14 $03.00/O

@ 1987 Academic

Press Limited

664

J. A. Kitching

a 3

Figure 1. Stages in the development of H. elongata, modified from scheme used by Moss (1952). Stages: 1, up to 10 mm in height; 2, over 10 mm but apex still rounded; 3, apex flattened; 4, fully grown vegetative button but no straps; 5A, with straps up to 1 cm in length; 5B, strap length l-5 cm; XI, strap length 5-25 cm; 6, strap length 25-100cm; 7, straps more than 1OOcm long; 8, straps spent and plant breaking up.

to particular parts or levels of the Himanthalia, some to the stalk or underside of the button, some to the top of the button, and some to the strap either near to the base or further up. The histological structure of H. dongata was studied by van den Ende and van Oorschot (1963). The top of the vegetative button was found to be covered by a layer of slime which, from its staining reactions, was thought to consist of alginate. According to Al-Ogily (1983, the top of the button has antibiotic properties which discourage the growth of bacteria. Spirorbid larvae will not settle on the tops, however oriented, but will readily settle on the bottoms of the buttons. A skin consisting of the outer cell walls of surface cells is shed from time to time, especially from the straps, less frequently from the button tops, and not at all from the under-buttons (Russell 8z Veltkamp, 1984). Algae epiphytic on the straps may evade skin-shedding by anchoring themselves within the cryptostomata. The tops of the buttons, important for photosynthesis in the growing Himanthalia, are normally clean until they reach a late stage in their lives, but it is not yet clear by which of these characteristics they repel epiphytes.

665

Epiphytes and H. elongata

Bullock

r)

Island

(,,

100

200

m

Figure 2. Map of part of Lough Hyne Marine which samples of H. elongaca were collected, Bassindale et al. (1948). Inset, the Rapids.

Nature Reserve, showing the sites from in accordance with the scheme used by

This paper surveys the distribution of plant and (especially) animal epiphytes of in relation to wave action, water current, and shelter in the Lough Hyne Marine Nature Reserve, Ireland (map reference 51”29’N, 9”2o’W). Himanthalia

Methods

Samples of H. elongata were comlete collections taken from defined areas, at positions shown in Figure 2. Defined areaswere the tops of one or more rocks, amounting to about

666

J. A. Kitching

4-N

I

1

i

J

0

-

0 I

1 I

of UB

various

sites in the Lough

-

-

4

Hyne

I

Nature

n

-

17

5814

Reserve,

c I

-

7

786

m

-

I -

I

6

?a6

Moderate

all collected

12

5R4

current

in September.

I

n

-

-

26

584

current

-

I

5

786

-

-I

(south)

II

-

n

78

6

pool

(west)

-

II

786

3.

-

-

8

564

Very wave exposed

6 Sep. 1985

Long

as for Figure

I

-

3

584

very wove exposed

information

I6

584

eddy

Other

Gentle

Pool

I5 sap. 1982

Long

0 %

100 %

100%

0%

i 0 %

F

100% c r 0 %

- 0 %

7 100%

I

- 0 %

- 50%

-100%

-0

-50

-100

-0 %

-50%

-100%

100%

from

I

-

7

786

Strong

Rock

7 Sep. 1985

Nlfa’s

0 %

I

I

-

I

4

5R4

Very strong current

D7 14 Sep. 1983

0 %

4 Hintnnthulia

I

I

-

-

II

786

current

D4 ‘/2 9 Sep. 1985

100 %

Figure

p;/osa

ryiandi

-

I

5

584

Strong

D31/2 13 Sep. 1983

I00 %

Elecm7

Callopom

with :

hyalma of U8 )

% UBs Infested

Cellepmllo ( % coverage

Ant,clockv/se spworblds (No. per UB)

Clochww splrorbnds (No. per UB)

Coverage

Button tops wth animal eplphytes

Button tops wth plant epiphytes

No. of Nm. in stage

?a6

02

I4 sep. 1982

0%

100%

0 %

100 %

0 %

IO0 %

0

50

100

0 %

50%

100 %

0 %

50%

100%

stage

Gentle

Water

current

I I Sep. 1982

movement

E 19 (south)

Site

Date collected

El9 Rapids D2 Rapids DG Rapids D4’, Rapids D7 Nita’s Rock Holly Creek Long Pool (South) Long Pool (West)

Station

5 4 4 7 7 5 18 11

11

6 Sep. 1985

Sep. Sep. Sep. Sep. Sep. Sep. Sep. Sep.

0.83 kO.06

1.76kO.16 2.78 i 0.48 1.31 kO.26 1.26kO.33 1.82kO.26 1.84+0.24 1.32kO.06 0.94+0.09

235 + 101

636k 157 1414*439 155+81 391 f 199 686F230 633 k 287 166,24 125+28

Strap weight k)

Strap length (m)

(n)

and epifauna

1. Characteristics

1982 1982 1983 1985 1983 1985 1982 1982

11 14 13 9 14 7 17 15

Date collected

TABLE

0,25+0.15

41+12 11.5k4.7
42+12 4.9k4.9 0.0 +_o.o 0.36 kO.36 30.6* 17.7 o.o+o.o 1.3kO.7 5.Ok5.0

Amphithoe (Reonexes) (N:;akpg)-’

(mean i- standard

Filamentous epiphyte weight (9)

of straps Jam falcata (No. kg-’ strap)

o.o_+o.o

2.1k1.6 7.4+ 7.2 o~o+o.o o.o*o.o 33.9k30.7 0.0 + 0.0 o.o&-0.0 o~o+o.o

error)

7.8k4.4

8.1 k2.1 25211 lO.Sk3.6 7.8 k 4.4 6.3k2.9 0.0 +o.o 2.95 1.0 85 + 14.6

Patina pellucida (No. kg-’ strap)

o.o+o.o

0.3kO.3 0.0 5 0.0 1.9*0-9 o.o*o.o

o.o+o.o 0.0 + 0.0 o.o+o.o

1.9f0.7

Cingulopsis fulgida (No. kg-’ strap)

o.o+o.o

681_+ 174 o.o+o.o 0.0 + 0.0 o-0+0.0 0.2kO.2 8.1 k5.8 41_+17 o~o+o~o

Rissoa parva (No. kg-’ strap)

O.O_fO~O

18.6k8.6 o.o+o.o 0.0 1.0.0 o.o_+o.o 0.3kO.3 74k25 0.7+0.5 o.o+o~o

Halocladius (No. kg-’ strap)

o~o+o~o

4.5k2.1 o.o*o.o O.O&O.O 0.0 f 0.0 O~O&O~O 41*19 o.o+o.o o.o+o.o

Clunio marinus (No. kg-’ strap)

Epiphytes and H. elongata

TABLE 2. Fauna

of perspex

669

discs set up in Himanthalia

zone at Dl

Tops 18 Sep. 1983

20Apr. 1984

on 21 July 1983 Bottoms

21 Jul. 1984

8 Sep. 1984

18 Sep. 20Apr. 1983 1984

21 Jul. 1984

of discs collected

6

6

5

7

6

6

5

Number of discs having: Corallina o@%uzlis Fosliella lejolisii Unidentified algal mat Himanthalia (stage 1) Algae of any kind Anticlockwise spirorbids Pomatoceros Celleporella hyalina Electra pilosa Cryptosula pallasiana Scrupocellaria reptans Anomiid Musculus sp.

0 0 3 0 3 0 0 0 0 0 0 1 0

2 0 4 0 5 0 2 0 0 0 0 1 0

4 1 2 2 4 0 1 3 0 0 0 0 0

3 4 2 5 6 0 2 6 0 0 0 4 1

0 0 0 0 0 0 0 0 0 0 0 3 0

0 0 1 0 1 1 2 6 3 0 4 1 1

0 0 0 0 1 0 5 5 0 1 1 0 0

O-20

l-70

O-30

5-75

c-30

&65

10-65

Number

Total

cover

(range

“CI) “All on transparent

8 Sep. 1984

0 3” 0 0

25-60

discs.

1 m2 where Himanthalia was abundant, but larger areas in places with strong currents where Himanthalia is rarer. Samples taken in Holly Creek, and those taken in the lower Rapids, where tidal conditions are similar to those in the sea, were on flat rocks in the middle of the Himanthalia zone. Those taken in the lough and in the upper Rapids (E19, D2), where the tidal rise and fall is much less, extended over the full height of the narrow Himanthalia zone. Within each sample, all specimensof Himanthalia were kept separate. Each specimen was classified by its stage of growth, as defined in Figure 1. The flora and fauna of each specimen was examined for the upper side of the vegetative thallus, or ‘ top ‘, for the lower side of the vegetative thallus and the stalk, together forming the ‘ underbutton ‘, and for the receptacles or ‘straps ‘. The filamentous epiphytes were removed from the straps together with their associated fauna by squeezing the straps between finger and thumb and drawing them through from end to end. The epiphytes so removed were blotted and weighed damp. Extremely short close-fitting filamentous epiphytes such as Myriactula areschougii remained attached to the straps. Quantities of sessile animals attached to the underbuttons were estimated as percentage area of underbutton covered. Imitation Himanthalia buttons, consisting of circular perspex discs mounted on rigid nylon stalks, were set up at site D 1 in the upper Rapids, in their proper zone, on a cuboidal dexion steel frame weighed down with a heavy slab of rock inside, in order to discover whether the sameepifauna developed ason real Himanthalia buttons. The discs were of four kinds: clear glossy, clear but buffed with sand-paper, black glossy, and black buffed with sand-paper. They measured 3 cm in diameter, with stalks 2.5 cm in height and 0.4 cm between the discs.

3.

670

A. Kitching

TABLE 3. List of species associated Algae” (Parke & Dixon, 1976) Rhodophyta Audouinella corymbifera Audouinella secundata Calliblepharis ciliata Rhodophyllis divaricata Phyllophora pseudoceranoides Corallina oficinalis Fosliella lejolisii Jania rubens Champia par&a Lomencaria articulata Ceramium pedicellacum Ceramium rubrum Polysiphonia violacea Goniotrichium alsidii

with Himanchalia

E19, D7, Holly Holly Holly Holly Dl, E19, E19, Holly Holly D7, Holly E19,

straps straps Creek Creek Creek Creek perspex straps straps Creek Creek straps Creek straps

(Sep.), (Sep.), (Apr.), (Sep.), discs

elongaca (UB = underbutton)

UB UB UB E19, Long

Pool, UB

(Sep. and Apr.), UB (Sep.), E19, D7, straps (Sep.),

straps

Phaeophyta Eccocarpus siliculosus Feldmannia irregularis Elachista scuculata Myriaccula areschougii Myriotrichia clavaeformis Sphacelaria cirrosa

Holly Creek (Sep.), E19, D7, straps D7, straps D7, Long Pool, straps Holly Creek (Sep.), Long Pool, straps Holly Creek (Sep.), E19, Long Pool, straps E19, UB

Chlorophyta Chlorochytrium cohnii Ulothrixflacca Enceromorpha clathraca Enteromorpha flexuosa Enteromorpha intestinalislcompressa Enteromorphaprolifera Ulva lactuca Ulva rigida Cladophora sp.

Holly Creek (Sep.), E19, in diatom tubes on straps Holly Creek (Apr.), straps E19, straps Nita’s Rock, UB E19, Long Pool, straps Holly Creek (Sep.), E19, straps Holly Creek (Sep.), straps Holly Creek (Sep.), Nita’s Rock, straps E19, straps

Porifera Halichondria

D3;,

Hydrozoa Dynamena

paniceab

pumila

(Pallas)

Janus

D7, UB

(L.)

Polychaeta (Fauvel, 1923,1927; Eteone picca Grubea sp. Enogonegemmafera Nereidae, small Pomacoceros criqueter Spirorbis inornacus

Knight-Jones

pagenscecheri

Bryozoa’ (Ryland, 1970; Ryland Tubulipora sp. Crisia eburnea Bowerbankia sp. Aecea cruncata Scruparia chelata Callopora lineata

UB

& Hayward,

and Knight Jones, 1977) El9 Holly Creek (Sep.), El9 Holly Creek (Sep.), El9 D7, UB D3& Nita’s Rock, UB Holly Creek (Sep.), Nita’s spirorbids. Figs 3 and 4 Holly Creek (Sep.), Nita’s spirorbids. Figs 3 and 4 1977; Hayward & Ryland, Holly Creek (Apr.), D3f, UB Holly Creek (Sep.), Nita’s Rock, UB Holly Creek (Sep.), Holly Creek (Sep.),

Rock,

UB; clockwise

Rock,

UB; anticlockwise

1979) UB UB UB D7, Nita’s

Rock,

UB

671

and H. elongata

Epiphytes

TABLE 3. Continued Bryozoa’

(Ryland,

1970; Ryland

& Hayward,

Callopora rvlandi Electra pilosa Scrupocellaria reptans Escharoides coccineus Umbonula littoralis Haplopomagraniferum C~ll~porella hvalina

1977; Hayward & Ryland, 1979) Holly Creek iApr.), E19, UB Figs 3 and 4; occasionally on tops at D2, D4:, D7 Figs 3 and 4; occasionally on tops at D2, D7 Holly Creek (Apr. and Sep.), UB Holly Creek (Sep.), UB D7, UB Table 2; Figs 3 and 4; occasionally on tops at D3:

Crustacea Cirripedia Verruca

(0. F. Miller)

stroemia

Isopoda

(Naylor,

Figs 3 and 4, on top at D2

1972) E19, D2, Nita’s Rock, Long E19, D7, straps E19, Long Pool, straps

D.vnamene bidentata Idotea pelagica Idotea granulosa

Amphipoda:

Gammaridea’

(Lincoln,

Stenothoe monoculoides Me&a obtusara Apherusa jurinri Dexamine spinosa Amphithoe rubricata Amphithoe i Pleonexes) Aora gracilis Lembos sp. Jassaf~alcata

Amphipoda: Caprella Caprella

1979) E 19, Holly E19, Holly Holly E19, Holly Holly Table

gammaroides

Caprellidea

(Harrison,

D7, straps D2, D7 (many),

(King,

Achelia echinata Phoxvchilidium End& 1aeeG

D7, straps Creek (Sep.), straps Creek (Sep.), Creek (Sep.), D4:, D7, Long Creek (Sep.), Creek (Sep.), 1, straps

straps E19, straps E19, Nita’s Rock, straps Pool, straps E19, straps Long Pool, straps

1944)

acutifrons acanthifera

Pycnogonida

Pool, straps

straps

1974) Holly Creek E19, straps E19, straps

sp.

(Sep.),

straps

Insecta (:ollembola Lipura

Diptera

maritima

(Laboulbtne)

Rock

J

Hulocladius erartabilis Staeger (larvae) Clunio marinus Haliday (larvae)

I’rosobranchia

Nita’s

(Graham,

Aonaea virginea Patina pellucida Cibbula cineraria Calliostoma zizqphinum Lacuna pallid& Lacuna vincta I‘ittorina littoralis Rissoa parva Cmgula cingillus Cingula remicostata Cingulopsis fulgida Skeneopsisplanorbis Bittium reticulatum

E19, Nita’s E19, Nita’s

Rock, Rock,

straps straps

1971) Nita’s Rock, straps Table 1 E19, Nita’s Rock, straps D7, straps Holly Creek (Sep.), E19, straps Holly Creek (Sep.), Long Pool, straps E19, Nita’s Rock, straps Table 4, straps E19, straps Holly Creek (Sep.), E19, straps Table 1, straps Nita’s Rock, straps Nita’s Rock, straps

672

J. A. Kitchirtg

TABLE 3. Continued Prosobranchia (Graham, Nassarius incrassatus Onoba semicostata Barleeia rubra Opisthobranchia Doto coronata

1971) E19, D7, straps Holly Creek (Sep.), Holly Creek (Sep.),

(Thompson

& Brown,

E19, straps E19, straps

1976)

4

E19, straps

,amellibranchia (Tebble, 1966) Anomiidae, small Mytilus sp., very small Musculus discorsg, small Musculus marmoratt&‘, small Hiatella sp.“, probably H. arctica, Ophiuroidea (Mortensen, Ophiothrix fragilis Amphipholis squamata

small

Table 2; Figs 3 and 4 D7, UB; E19, straps Nita’s Rock, UB Nita’s Rock, UB Nita’s Rock, UB

1927)

Ascidiacea” (Millar, 1970) Polyclinum aurantium Sidnyum turbinatum Aplidium pallidum Trididemnum tenerum Didemnum sp. Diplosoma listerianum Ascidiella aspersa Botryllus schlosseri Botrylloides leachi

D4:, straps Holly Creek

(Sep.),

E19, straps

Fig. 3, UB Nita’s Rock, UB Table 2, UB D3’,, UB and tops Holly Creek (Sep.), UB D3;, D4;, UB Table 1, Nita’s Rock, UB Figs 3 and 4, UB; on tops at D2, D4: Fig. 4, UB

“All identifications of algae were made by Dr E. M. Burrows, ( = Pneophyllum Zejolisii (Rosano@ Chamberlain), identified *Identified by Miss S. M. Stone. ‘Some specimens were identified by Dr Phyllis Knight-Jones. dSome specimens were identified by Dr P. J. Hayward. ‘Some specimens were identified by Dr R. J. Lincoln. ‘Some specimens were identified by Dr R. S. Wilson. ‘Some specimens were identified by Dr T. E. Thompson. “Identified by Dr Paul Kingston. ‘Some of each species were identified by Dr R. H. Millar.

except for Fosliella lejolisii by Dr Y. M. Chamberlain.

Results The flora and fauna associated with Himanthalia were first studied in Holly Creek, which is a very sheltered site yet having fully marine tidal conditions. Complete collections of all Himanthalia on single flat rocks were made in September 1982 and in April 1983, and the results for the buttons are summarized in Figure 3. The April collection contained very many stage 1 and stage 2 plants, many of them attached to other algae, while the September collection contained no plants from these two categories. Small numbers of Himanthalia in late stages (up to 6 and 7) were present in both samples. In the April collection there were few plants in stages 5A, 5B, and 5C, these having (presumably) moved up into stage 6, and in September these had reached stage 7. No plants above stage 4 were found in April 1983 on a rock previously scraped clean in April 1982. Button tops were most often free of epiphytes. Occasionally there were scraps of

Epiphytes and H. elongata

673

immature algae and small colonies of Bryozoa, these almost entirely on the later stages (6 and 7). Sometimes algae were attached to the rim of the underbutton, reaching upwards. Underbuttons carried many epiphytes, some algae, including Calliblepharis ciliata, Lomentaria articufata and Ulva rigida, but mostly animals. Coverage of underbuttons in Holly Creek was greatest on the later stagesand reached an average of around 70’,, at stage 7 in September (Figure 3). Clockwise Spirorbidae were found on most underbuttons from stage 3 onwards, and those examined proved to be Spirorbis inornatus. Anticlockwise Spirorbidae oanua pagenstecheri) were lessabundant. Bryozoa were the most extensive colonists of underbuttons, especially from stage 4 onwards. Celleporella hyalina, Electra pilosa and Callopora lineata were found on many underbuttons, along with the barnacle Verruca stroemia (often found on the stalk) and very small Anomiidae (saddle oysters). Colonial ascidians spread over the other epifauna. The fauna associatedwith Himanthalia buttons at other sitesin September is summarized in Figure 4 for stages6 and 7 (well into their secondyear) and for stages4 and 5 (well into their first year). As in Holly Creek, the button tops were mostly clean, although Bryozoa (Electra pilosa) and colonial tunicates (Botryllus schlosserz) sometimes spread over them in the Rapids (D2 to D7). Underbuttons were more heavily infested in the Rapids; Celleporella hyalina was the most prevalent but by no meansthe only bryozoan. Spirorbids, both clockwise and anticlockwise, were almost entirely missing from Himanthalia buttons exposed to strong current in the Rapids, and also from Long Pool, which is exposed to severe wave action. They were abundant at El9 (south end) and at Nita’s Rock, both subject to very weak current caused by eddies from the main stream. All strapsfrom the September Holly Creek samplewere examined for their epiflora and for the animals associated with it. Filamentous algae included Ectocarpus siliculosus, Ceramium pedicellatum and Enteromorpha prolifera, which were populated by various gastropods, including especially Rissoa parva, and by amphipods. The straps also carried the short close-fitting brown algae Myriactula areschougii. The limpet Patina pellucida was found with feeding excavations on some straps. The principal animal species associatedwith straps in Holly Creek are summarized in Table 1. The straps of Himanthalia were clothed with a microforest of filamentous algae at El9 (south end) (Table l), where the current is weak, including Ceramium pedicellatuvn, Ectocarpus siliculosus and Enteromorpha spp. This microforest accommodated a considerable fauna, including large numbers of the gastropod Rissoa parva and of the amphipod Amphithoe (Pleonexes). Microforest diminished greatly southwards along the Rapids, but rose again in less turbulent water at D7, where on some straps there was much Ceramium and with it considerable numbers of the amphipods Amphithoe (Pleovzexes)and Jassa falcata. In Long Pool, which is exposed to severe wave action, there was little microforest and little associated fauna. At Nita’s Rock there is a gentle direct current during inflow and a slow eddy during outflow. The microforest of Ceramium was completely choked by fine sediment, and the usual associatedfauna was almost entirely missing; instead there were many larvae of Halocladius variabilis and Clunio marinus (Diptera). The artificial ‘ Himanthalia ’ discs, 24 in all (six of each type) were set up at Dl on 21 July 1983, at a site unlikely to be disturbed by smallboats. Setsof discswere collected from the frame on 18 September 1983,20 April 1984,21 July 1984, and 8 September 1984. Each collection contained not lessthan one not more than two of each kind of disc (transparent

674

J. A. Kitchirrg

or black, glossy or matt). The discs were placed in 6”,, formaldehyde solution for later examination. The results are summarized in Table 2. As (with one possible exception) no difference was found between different kinds of discs collected at the sametime, they have been grouped together in this summary. Discs collected in September 1983 carried very little except small anomiids. In subsequent collections, nine months and more from the time when the discswere set up, algae were beginning to grow on the tops of nearly all the discsbut on the bottoms of only a few. They included one species, Fosliella lejolesii, normally found on the leaves of Zostera, which grows in the sheltered creek below the Rapids. Several speciesof Bryozoa became establishedon the discs.The most extensive wasCelleporellahyalina, which first appeared on the bottoms but ultimately occupied parts of both sides. Pomatocerosand anomiids grew on both sides. The flora and fauna of the artificial discs are compared with those of natural Himanthalia in the Discussion. A list of all the speciesfound associatedwith Himanthalia is given in Table 3. No doubt further work would add considerably to this list.

Discussion Himanthalia elongata occupies a zone near the bottom of the littoral region, where the adverse effects of exposure to air would be exercised much lessseverely than at higher levels on the shore. The result is that a much larger community of plants and animals is associatedwith Himanthalia than with most other zone-forming Fucales higher up the shore. For instance, Hazlett and Seed (1976) report only 14animal speciesassociatedwith Fucus spiralis in Strangford Lough, Northern Ireland, all of them mobile and presumably able to retreat to damper places, if necessary, during low water. Ninety-three species are reported in association with Fucus serratus in Strangford Lough (Boaden et al., 1975), many of them attached; desiccation is much less of a problem. In the present paper (Table 3) 105 species are reported in association with Himanthalia, many of them attached; 32 species are shared with Fucus serratus as reported from Strangford Lough. Himanthalia lives for about two years; Fucus plants have a life span of 3-5 years (Chapman, 1974), during which time more blade is added distally. For most animal epiphytes two years would be expected to be a sufficient amount of time for settlement, growth and maturity, and this probably holds for epiphytes of the underbutton. There must be a defense mechanism (whether alginate film, antibiotic, or skin shedding) against epiphytes which protects the top of the button until a late stageis reached, sothat the time available may be too short for someepiphytes to reach maturity. In the second year of life the straps develop, and epiphytes such asmicroforest and its numerous associatedanimals must settle and grow rapidly. The most striking difference between the communities associatedwith Fucus serratusand Himanthalia lies in the fact that asF. serratusgrows it merely provides more of the samesubstrate, whereasHimanthalia after one year ceasesto provide more button but provides a completely new substrate, the strap, with surfaces suitable for quite different plant and, in turn, animal epiphytes. With the microforest comes an entirely different community. The form of protection-skin shedding, as demonstrated by Russell and Vellkamp (1984)-fails to deter filamentous epiphytes, becausethey can settle in the cryptostomata.

Epiphytes and H. elongata

675

Settlement of epiphytes is the result of interaction between larval behaviour and plant defenses.Except in the latest stages,the upper surface of the buttons is normally clean. It clearly has effective protection, whether by the mechanical effect of a film of slime, or by antibiotic action or by the shedding of skin. It is possible that several mechanisms are involved, and that they differ in their contribution to different parts of the Himanthalia. A number of animals (Pomatoceros, Celleporella hyalina, small anomiids, Musculus sp.: which normally grow on the underbuttons of Himanthalia also grew on the artificial Himanthalia buttons, both on the tops and on the undersides. The almost complete absenceof spirorbids from theartificial buttons may beascribed to the water current at site D I. The artificial buttons Iacked the specia1protection characteristic of rea1Himanthafia tops. Although many more tests would be necessary before any conclusions could be drawn about settling behaviour, the earlier development of Celleporella hyalina on bottoms than on tops of artificial buttons might reflect the tendency to settle on undersurfaces and away from light: reported by Ryland (1960). Normal underbuttons of Himanthalia evidently lack the special protection characteristic of the tops and become densely covered with organisms such as Bryozoa, anomiids and Pomatoceros. Most of these animals adhere strongly, and it is not surprising that they show little sensitivity to vigorous water movement. Only the two spirorbids are obviously restricted by current and by wave exposure; Callopora rylandi may be similarly restricted, but the evidence for this is insufficient. In contrast, the fauna associated with straps is greatly affected by water movement. Under quiet conditions the straps become covered with a miniature forest of filamentous algal epiphytes, which apparently avoid the skin-shedding activity of the straps. These filamentous epiphytes provide shelter, and in some casesfood also, for many small animals. In the Rapids and in a tide pool on the open coast the straps have few filamentous epiphytes and their associatedfauna is very limited. A few of the algae growing on Himanthalia straps are especially associated with Himanthalia (the close-fitting Elachista scutulata and Myriactula areschougii), but the remaining plants and ail the animals found on Himanthalia straps are general low-level intertidal species.Not surprisingly, the animal population of the microforest is controlled by the amount of microforest available. Nita’s Rock is a specialcase.The microforest there is smothered in fine sediment. Conditions are therefore unsuitable for the normal animal population of the microforest; instead they encourage larvae of the Diptera Halocladius variabilis and Clunio marinus. The silt doesnot form a bottom deposit, which would be expected to prevent colonization by Himanthalia (Moss et al., 1973); it isfiltered out by the microforest. The distribution of stagesin Holly Creek in April and September indicates that very large numbers of young buttons (stages 1 and 2) are produced early in the year, and that most of these are subsequently lost. A small number survive, reaching stages4-5A by September, and many of thesemature during the following year. Observations carried out in the lower Rapids area have confirmed the high turnover in young stages,and suggest that it is due to weak attachment and to abrasion by other algae.

Acknowledgements

I am grateful to all those systematic specialists-cited in Table 3-who have determined material for me, and especially to Dr E. M. Burrows, without whose expert help this work

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could not have been undertaken. I am happy to acknowledge the assistance of students of the University of East Anglia in the field work, and helpful correspondence with Professor T. A. Norton.

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