T A N E 29, 1983

R E A D I N G A S E A S H O R E

by J . E . Morton * and J . R. Walsby t * Department of Zoology, University of Auckland, Private Bag, Auckland

t Leigh Marine Laboratory, R. D., Leigh

S U M M A R Y

The Auckland intertidal shore has been analysed to show the similarities in the sequence of its zonation in space (both vertically down the open shore, and from the upper to lower surface of a boulder), and the sequence in time (by which colonisation and ecological succession take place). The course of colonisation is described from data from Milford, Castor Bay and Goat Island Bay, Leigh, and its rate and progression compared for different levels on the shore.

The distinctive encrusting communities living under boulders are described, as are their succession during colonisation and the factors determining their spatial distribution.

The idea of "climax" in ecological succession is discussed for the community between tides, with the recognition of a polyclimax situation according to position on the shore.

The concept of "zonation" is found to apply reliably, though with fundamental changes in its controlling factors, in the subtidal. Sublittoral communities are described in the light of recent S C U B A studies in the Cape Rodney-Goat Island area. The equivalence is established between the sublittoral encrusting communities on open rock surfaces, and the sciaphilic communities or "general sublittoral hypobion" between tides.

INTRODUCTION

Narrow though it is, the intertidal shore is one of the richest of the Earth's major biomes. Few other sorts of biospace can be so tightly organised. Not only are the animals small and numerous, and in large part sedentary or even sessile; their patterns and processes are also miniaturised, both in space and time. Both dimensions show steep gradients of change. It is a truism that a walk up a shore from low water will reveal a scale of change as great as on a mountain climb, or (as Alexander von Humboldt was the first to envisage) on a journey from the tropics to the tundra.

The sea shore is not only a compact system, but is beautifully accessible for study. It is the best place school students and amateur naturalists can go for examples of almost all the animal phyla. In its taxonomic luxuriance the intertidal shore is, for the animals, virtually

51

what the equatorial forest is for the plants. But it is a far more manageable frame than a forest, in which most of the grand properties of the community can be compactly exemplified in space and time: not only the trophic and energetic relations constitutive of the "ecosystem", but also the concepts of competition and exclusion, and ontogeny and succession. '

With the hard intertidal shore we are evidently dealing with a single spatial community, but one by itself metabolically highly incomplete. Despite the macro-algae on the shore, most of the productivity it relies on takes place remote from the site, in the open waters or ultimately the oceans at large. The processes of "reduction" are also largely "off-site", with the washing away of dead and moribund material and its accumulation subtidally, or on sheltered soft shores.

Temporal succession has so far been little studied on hard shores. Even their spatial succession is not yet fully described and understood. Yet these complex changes in community composition run with such a discernible order that the Stephensons (1949) were able to build up for the shores of the world a "Universal System" of plant and animal zonation. This was perhaps the most creative generalisation of descriptive ecology since Humboldt or Wallace.

This paper takes its title from a phrase of Alan Stephenson's in the introduction to "Life Between Tidemarks on Rocky Shores" by Stephenson and Stephenson (1972). It is written with the hope that biologists at home or in schools may be encouraged into ongoing studies, where some important principles of ecology can be followed up, with few resources for travel or need of expensive equipment. It will show too how much shore work can still be possible for those unfitted by age or opportunity for S C U B A diving.

ZONATION

Between tidal limits the ecocline of spatial succession follows the now well-established order. Fig. Ia shows the sequence of changes for an east northern Auckland shore of moderate shelter. The patterns and species composition alter with temperature and other geographical changes, as between Auckland and Otago. Further, within each region, or even around a single locality, there are variations due to differences in water movement, bringing to bear at successive levels up the shore the modifying effects of surge, splash and spray. Thus, as well as the vertical axis denoting changes in the total amount and continuous duration of emersion/immersion, embodying the Stephenson concept of the shore, there is the second (horizontal) axis employed by Ballantine (1961) and by many others since, giving a seven point biological scale from high wave exposure to extreme wave shelter (Fig. Ib). Its use in New Zealand and overseas is today a standard part of shore description.

52

(a)

H W N

Fig. 1. (a). Zonation pattern of a moderately sheltered Auckland intertidal shore, showing the location of the "barnacle line", "red line" and "brown algal line". (b). Elevation of zonal limits with increased exposure in relation to the 7-point biological exposure scale introduced by Ballantyne (1961).

There are three important thresholds, the barnacle line, the "red line" of encrusting calcareous alga, and the brown algal line. These mark the upper limits of biotic zones arranged as follows: Barnacle Zone: This runs through upper and middle eulittoral zones.

Other shelled animals (Crassostrea followed by Pomatoceros) may be interpolated in the middle eulittoral zone.

Pink Zone: This runs, in its full extent, from the beginning of the low eulittoral zone to the limit of photosynthesis subtidally. Important sub-zones interpolated within its limit as are: Lower eulittoral zone - Corallina turf, with Hormosira; Sublittoral fringe - the brown algal zone of Fucales (Carpophyllum, Cystophora, Sargassum); Sublittoral zone - Laminariales (Ecklonia).

COLONISATION

The succession in space exhibited in the passage down the shore is

53

clearly reflected also in the events that happen in time, with the colonisation of cleared or bare settlement surfaces. The ontogeny of the intertidal community was first studied by us at Castor Bay over a period of 30 months at three levels on the shore shown in Fig. 2: the middle eulittoral zone with oysters; the lower eulittoral zone with Corallina; and the sublittoral zone, just below E . L. W. N. under permanent submersion, with Ecklonia.

Fig. 2. Colonisation of intertidal surfaces at Milford, Castor, and Goat Island Bays, from data obtained over 24 months from January 1970.

The settling surfaces used were slabs of prismatic basalt (obtained from Smales' Quarry, Takapuna), measuring c. 0. 5 m x 0. 2 m. These were lifted monthly for inspection during low spring tides, and replaced in the same sites. Slabs with "half-holes" that had been drilled for splitting were especially convenient beyond low water, where they had to be felt for by hand amongst dense brown algae. Fig. 3 shows the temporal course of succession, compared with a terrestrial succession and also its comparability with the spatial order of the organisms over the intertidal range. The three threshold levels, barnacle line, and pink and brown algal lines, became established in that order, with progressive retardation higher on the shore.

54

Fig. 3. The course of ecological succession in the intertidal (b), compared with a longer term grassland-to-forests succession (a). Compare (b) also with the spatial order of organisms over the intertidal range in Fig. Ia.

All communities are subject to direction change in composition over extended time. Whittaker's (1971) sequence of changes characteristic of the major vegetational successions on land, agrees essential with those operating in the intertidal. The sequence in the intertidal is as follows: i. The substrate becomes altered and developed from the initial bare soil

or rock. ii. Biotic strata develop with increased height, massiveness and

differentiation rate. iii Productivity, or rate of formation of new organic matter, increases

with development of community structure. iv. As height and complexity increase, microclimates are increasingly

determined by the characteristics of the community itself. v. Species diversity increases from earlier to later stages, sometimes

declining before climax. vi. Populations rise and fall to replace each other along a time gradient,

just as stable communities may do along a spatial gradient. This process may slow down as larger and longer-lived species appear.

vii. Not only diversity but stability increases as the succession advances. Earlier stages are very unstable, with rapid replacement.

55

The final community is stable, with long-lived dominants, that maintain their composition, showing oscillation but no longer directional change. Some authors would restrict the term "ecological succession", in its

useful application, to the changes brought about in a community by the modification of the substratum and microclimate by a previous dominant, so as to effect its own supersession by a later dominant species. A n ultimate example of the tightly integrated changes in substratum and community, with back and forth interplay of effects, could be shown, for a "reducing" community, by the ripening of a blue cheese, with the succession of saprophytes (bacteria and fungi) occupying and altering the chemo-substrate ensuing from the decomposition of the proteins, fats and lactose of milk.

There are probably few cases where succession does not owe much of its course to the activities of the sequential occupants of the space. On marine settling plates, just below L. W. S. on Devonport Wharf. Harger (1963) recognised four stages of an ecological succession. These are shown in Fig. 4. For settlement of mussels, a complex substratum was

Fig. 4. Ecological succession of fouling community at Devonport Wharf, based on data obtained by Harger (1963). The panel at top represents 30 months of fouling.

first needed, and this could be provided by algae, bryozoans, or artificial frayed fibres. The kelp Ecklonia settled on plates with a pre-existing primary cover of arborescent bryozoans, but would not settle on climax or sub-climax plates with simple or compound ascidians.

Quite evidently, the location of a particular species in intertidal space cannot be explained adequately as a simple function of shore height or immersion time. It is instructive to find how the same sequence of

56

succession is imposed upon both a mid-eulittoral boulder, 0. 5 m high, and a wharf pile with a vertical tidal range of 3 m. These are illustrated in Fig. 5. Where a whole intertidal shore could represent a microcosm of a mountain-side, the ecocline upon a boulder is a condensation of the whole shore, under conditions provided by the geometry of the boulder with its effectual gradations of temperature and illumination.

It is important to notice both upon boulders, and upon a whole shore,

3

Fig. 5. Vertical zonation on a wharf pile compared with that on an intertidal boulder.

57

the influence of "aspectation", with the variations due to differences between (a) shade and strong isolation and (b) wave exposure and shelter. Fig. 6 represents the two sides of the island of Motu Arohia, Bay of Islands, where wave exposure effects, extending high up the shore, make the rock face not only a picture, but an "exposure-gram" as well (cf. Fig. Ib).

Fig. 6. Elevation effect under strong exposure on Motu Arohia Island, Bay of Islands.

U N D E R B O U L D E R S

While a community is building up on the top of a settling plate, colonisation of an entirely different sort is going on underneath. Such under-bouldcr communities have not yet been taken into account in any systematic way in explanations of shore zonation. Even in the work of the Stephensons, life beneath movable cover has generally escaped all mention. Yet these communities are the richest and most faunistically diverse of any on the shore. They are as important to the total appreciation of the habitat as would be all those deeper or shaded communities of a forest that pass un-noticed by aerial mapping.

Among the reasons for neglect must be the sheer profusion of entities, and the poor taxonomic coverage (until recently) of most of their groups, especially sponges, hydroids, ectoprocts, sessile polychaetes and ascidians. In addition to their diversity, there is the apparent spatial confusion of their settled communities that is only today being reduced to understanding.

The lower face of a boulder is unlighted beyond its immediate periphery, and is protected both from high temperatures and wide fluctuations of temperature. The under surfaces of stable boulders will

58

thus be immune not only from insolation and desiccation, but also from wave impact. However, open spaces beneath them will be periodically washed by strong laminar current flow.

Wholly distinct from those on open bedrock, under-bouldcr communities include no autotrophic "producers". Their support comes ultimately from photosynthesis of phytoplankton, spatially disjunct from its consumers. Almost all the primary consumers are sessile, relying on a wide diversity of current-promoting and filtering devices for sorting and concentrating planktonic food and conveying it to the mouth. Sessile sponges, ectoprocts, tubeworms, and ascidians build up a substrate that is entirely biotic. This forms a food resource for a wide range of specialist carnivores, secondary consumers grazing with maximum economy of effort on a ubiquitous and potentially unlimited protein substrate. The principal carnivores are gastropod molluscs. Specialised mesogastropods can take a diversity of foods, ranging over all the sessile filter feeders, including the cnidarians which themselves feed as micro-carnivores. The Opisthobranchia have evolved as even more specialist carnivores, feeding most numerously on sponges (both by grazing and suctorial modes) but also widely upon ectoprocts, ascidians and even polychaetes. Asteroids and ophiuroids may also subsist as "grazing carnivores", but most of the former, like the Neogastropoda, tend to be predators taking a diet of mobile gastropods.

Like the community of the open surface, the under-bouldcr community reaches its greatest complexity at low water mark. For the proper study of its ontogeny, careful consideration should be given to the choice of localities. Its development will proceed to completion in places where there are large stable boulders, often irregular in shape and secure against periodic wave overturn, yet with water movement strong enough to prevent the lodgment or accumulation of sand or silt. Such shores (3-6 in the Ballantine exposure scale, Fig. Ib) will be characterised in northern New Zealand by Carpophyllum maschalocarpum in the sublittoral fringe, succeeded by Ecklonia radiata immediately beyond low water.

Towards increasing exposure, boulders are smoothly rounded, and so regularly subject to wave overturn as to be termed "mobile". At the sheltered extreme, boulders rest permanently in anaerobic black sand or silt/clay mixtures, and are shown in Fig. 7 as "embedded". Colonisation ceases beneath, but sponges may become increasingly important at the sides.

The following stages in the ecological succession have been established from observations made at Whangarei Heads, Goat Island Bay and - within the Gulf - Milford, Castor Bay and Takapuna: 1. Bare boulder surface; 2. barnacles (in the Gulf Elminius modestus, on outer coasts Balanus

trigonus) associated with serpulid tube-worms {Hydroides sp.

59

Fig. 7. The shore distribution of boulders in relation to exposure/shelter.

sheltered, Spirorbis sp. exposed); 3. encrusting ectoprocts (Bryozoa); 4. enrichment with first compound and later simple ascidians, later

serpulids and sessile molluscs; 5. crustose sponges enter the scene in quantity, especially red

Microciona, halichondrines and golf-balls {Tethya); 6. sponges become massive, fusing between the sides of adjacent

boulders, including penetrant-massive Cliona, and Spongia and Anchorina; also cup corals {Flabellum) and brachiopods (Terebratella). The climax, (stage 6), with boulders fused into an immobile pavement

by Lithophyllum algal crusts above and massive sponges below, will not be reached in situations where either: (a) high wave energy is sufficient to overturn boulders repeatedly, with

60

succession consequently reverting to an initial baseline, or (b) sediment accumulates in the absence of clearing currents, so as to

impede the operation of respiratory or food-collecting mechanisms. Situation (a) is well exemplified from Smuggler's Bay, Whangarei

Heads. The boulders are smoothed and flattened beneath by long abrasion and regular wave-dragging, with less frequent overturn. Though fast-growing Carpophyllum plumosum is present on top, the underboulder succession does not, on the vast majority of rocks, proceed beyond Stage 3 (or 4), with crustose ectoproct Bryozoa predominant. At Goat Island Bay, Leigh, with a strong current regime, early development is passed through rapidly to give a well-grown ectoproct community in 12 months.

The extreme of boulder mobility is to be seen at the Little Barrier Island landing place, where the boulders are being constantly over­turned. With the exception of the largest at the lowest level (c. 1 m in diameter), they are devoid of encrusting communities.

In the second situation (b) sand under boulders becomes black and anaerobic. The boulder is left azoic beneath, save for certain species (tubeworms, Thelepus and Flabelligera affinis; anemones, Paractis ferox and Anthopleura aureoradiata). Two chitons, Ischnochiton maorianus and Terenochiton inquinatus, from the boulder periphery, regularly shelter in anaerobic sediments.

Irregular scoria boulders on a silted bottom at Westmere Reef, Auckland Harbour, present an interestingly modified succession. With suspended silt restricting light penetration, life forms of Stage 5, especially ascidians (Microcosmus claudicans) with long siphons clear of the silt, and low tidal oysters (Ostrea lutaria) move to the sides (even the tops) of the boulders. Stage 6 is achieved only with the fusing sponge Halichondria moorei, typical of turbid waters.

In Fig. 8 the rates of under-bouldcr succession in the sub-littoral fringe are compared at Castor Bay (sheltered with high silt content) and Goat Island Bay (clean with high turbulence).

The rate and extent of progress in the scenario of the boulder hypobion involves, then, the following parameters: (i) Mobility of the boulder, as affected by its size, shape and shore

position and the local wave energy; (ii) immersion time available for filtering or other feeding; (iii) water clarity as related to exposure/shelter.

At Leigh Cove, the sizes (greatest diameter) of reef boulders, and then-positions in the scenario of succession were plotted (Fig. 9) for three levels in the eulittoral zone. It will be seen that none of the upper eulittoral boulders reach the later stages of the succession; and that for equivalent boulder size later stages have been attained at lower levels. The prospect of a boulder of given size attaining an advanced stage is enhanced by its size (= stability) and its lowness on the shore.

61

Idyanthyrsus

Compound ascidians

Fig. S. Colonisation of sublittoral fringe (S. L . F . ) boulders at Castor Bay and Goat Island Bay, Leigh, from data obtained over 24 months from January 1970.

The ratios of the areas occupied by the successive groups of encrusting species are compared in Fig. 10 for two Whangarei Heads localities; High Island in shelter, with good development of crusting and fusing sponges (stages 5 and 6), and Smugglers' Bay in moderate exposure, with the succession held predominantly by bryozoans (stage 3).

The organisms of the encrusting community of a boulder show regular changes in location with regression down the shore. On an idealised subspherical boulder, with a convention of "latitude" from 180° at the lowest pole to 0° at the top, a given species or species cluster will occupy progressively higher latitudes with further distance downshore, from E . H . W. S. to E . L . W. S. Such a pattern of change is shown in Fig. 11 for boulders from the maritime zone (over 10 feet above L. W. S. ) to the sublittoral zone, at Taurikura Bay, Whangarei Heads. Its controlling factors are evidently insolation/humidity.

62

2 3 4 5 STAGES IN SUCCESSION •

LOWER

1 2 3 4 5 6 Fig. 9. Size and succession on boulders at Leigh Cove, from three levels on the shore.

Some interesting extensions of range can occur with aspectational or seasonal variation. Within the Hauraki Gulf, for example, the black bryozoan Watersipora cucullata can in winter months rapidly and aggressively extend its range upwards, to grow over the tubeworm Pomatoceros caeruleus and the chiton Sypharochiton pelliserpentis; these animals and even coralline turf may remain still living beneath the brittle advancing cover of Watersipora cucullata.

The underboulder community is part of a more widely ranging "sciaphilic" (= shade-loving) community, designated the "general sub­littoral hypobion". Its distribution involves a third axis on a continuum of intertidal space, in addition to those introduced by Stephenson (for vertical height) and Ballantine (for water movement). This parameter is included in Fig. 12 and expresses the degree of enclosure ("interiority") from solar radiance, with its effects on illumination, insolation and

63

desiccation. It could be quantified by the open angle to the exterior, or subtidally as a product of the depth, water clarity and angle of inclination of the surface.

HIGH ISLAND (sheltered)

STAGES < 1 > < 2 > < 3 > < 4 > < 5 > < 6 >

SMUGGLERS BAY (semi-exposed) Fig. 10. Percentage ratios of succession stages on boulders in shelter and moderate exposure, showing the mean of 50 boulders at High Island and Smuggler's Bay (Whangarei

64

1 8 0

Fig. 11. Location of encrusting organisms on boulders, with regression down the shore. "Latitude" is measured from 180° at the lower pole to 0° at the top.

As well as boulder, there are obviously other intertidal sites suited to sciaphilic communities. These will include overhangs formed by the differential weathering of hard and soft sedimentary strata, and intertidal caves and shaded gullys, both marked by a regular succession of encrusting species with increasing interiority.

Sciaphilic sequences are also developed upon wharf piles, and horizontal stringers with increasing shade. With stronger current flow, and more open space, life-forms will show freer growth than their analogues in the narrow space under boulders. Sponges become elaborately branched; flat ascidians of boulders (Corella eumyota and Asterocarpa spp. ) give place to long siphoned Microcosmus claudicans and pendent, tubular Ciona intestinalis. Anemones (Actinothoe albocincta and Diadumene neozelandica) are long and pendent. The short stubble of boulder hydroids (species of Clytia, Orthopyxis, Hydractinia) is replaced by bushy species of Aglaophenia, Pennaria and Tubularia Crustose ascophoran Ectoprocta are exchanged for bushy and tufted Anasca (species of Bugula, Caberea, Scrupocellaria). Gelatinous and elongate ctenostomes enter the scene, such as

65

Fig. 12. A diagrammatic representation suggesting how wave exposure (= water movement), tidal height or subtidal depth, and illumination (in caves, under boulders and on subtidal surfaces) affects the distribution of littoral and shallow offshore organisms.

66

Zoobotryon pellucidum. Equally characteristic as the encrusting hypobion is the wealth of

crabs under boulders. The Brachyura and the porcellanid Anomura are diversely engineered for life in narrow places. For each shore level and degree of shelter there are crabs as indicator species, with distinct adaptive strategies. Their design and adaptive strategy are distinctive for each shore level and each degree of exposure. They are illustrated in Fig. 13, and listed in Table 1.

Table 1. The zonation of crabs (Brachyura) on northern New Zealand shores

Family

Grapsidae:

Xanthidae:

Cancridae:

Oxyrhyncha:

Dromiidae:

Porcellanidae:

Habitat and shore zone

Fast, Littoral fringe and upper eulittoral zone:

Slow, mid eulittoral zone:

Fast, sublittoral fringe: Active, mid and lower eulittoral zones: Slow, lower eulittoral

Slow, mid eulittoral zone:

Slow, lower eulittoral zone and sublittoral fringe: Slow, lower eulittoral zone:

Slow, sublittoral fringe:

Slow, sublittoral fringe:

Fast, mid and lower eulittoral zones: Slow, sublittoral fringe:

Species

Leptograpsus variegatus, Cyclograpsus lavauxi Cyclograpsus insularum

Hemigrapsus edwardsi (in clean habitats), Hemigrapsus crenulatus (in silty habitats) Plagusia capensis (with brown algae) Ozius truncatus

Pilumnopeus serratifrons (in silty habitats), Pilumnus spp. (in silty holdfasts and cavities) Heterozius rotundifrons (among clean boulders) Cancer novaezelandiae (with silty sand), sometimes also the portunid Liocarcinus corrugatus Neomithrax minor, Hymenicus pubescens, Elamena producta (with small red algae), Halicarcinus planatus (with brown algae), Neomithrax urceus, N. peroni - all clingng against boulder surface Eurynolambrus australis (among clean boulders and in inter-spaces) Petalomera wilsoni (with sponges in interspaces) Petrolisthes elongatus (against boulder surface) Petrocheles spinosus (in holdfasts)

C L I M A X

As the end stage of a directional change, the "climax" state of a community is usually held to be marked by the attainment of various sorts of stability. Assimilation and growth, biomass and productivity, the generation of diversity, are all, at climax, said to have reached steady equilibrium. There can be little doubt that stability is a property

67

of high community organisation. In many land habitats, the climax situation is recognised to be

minor

Fig. 13. Schematic representation of boulders from high to low water, showing the distribution of crabs.

68

complex. A n area may contain a number of types of climax, corresponding with a diverse mosaic of habitats. There may also be patches of pre-climax successional communities. A "polyclimax" situation thus results, varying according to aspectation, soil type, wind action and drainage, and other climatic or edaphic parameters. The most prevalent or representative sort of climax condition is then known as the "climatic climax". A n example, is the flax, manuka and Myrsine association on the windswept slope of Goat Island where a multi-storeyed coastal forest community cannot establish.

With an intertidal shore, nothing is evidently owed to edaphic factors (in the sense of soil properties), though the geological nature of the bedrock can obviously switch development in alternative ways. Across its steep ecocline from low to high water mark there is essentially one community, expressed by a sequence of sub-climax states (barnacles, bivalve molluscs, tubeworms, coralline algae with associates and finally large brown algae), according to position down the shore, and other spatial or climatic influences. The steepness of the ecocline and the strictness of the climatic regime have thus in a remarkable way imparted a predictable order to the intertidal rocky shore. The virtual identity of the directional sequence in space and in time has already been noted.

On subtidal rock faces and in soft benthic environments, with climatic controls no longer primary, such regularity may be looked for in vain. Gray (1976), in an important discussion of the implications of climax states for monitoring programmes, shows that the marine benthic fauna may present spatial mosaics varying in dominance over narrow areas. In Fig. 14, the ball represents a community, and the side of the valley

time Fig. 14. Equilibrium of climax communities (after Gray, 1976).

69

the scale of perturbation. In model A the community is in stable (climax) equilibrium as shown, and after disturbance it will return to this position which represents "global stability". Model B takes into account "neighbourhood stability", and is considered more realistic for soft benthic communities. The community is locally stable in stage 1, but a slight perturbation may send it into stage 2, with a different species dominating. It would then require a larger perturbation to change the stage from 2 to 1 or 3. Such situations of neighbourhood stability are held to occur not only on soft flats and amongst fouling organisms, but also on some rocky shores.

T H E S U B L I T T O R A L

The sequence we have been describing does not terminate at low water mark. Indeed boulders and overhangs could be regarded (like hedgerows leading from woodland into meadow) as small salients from a more extensive protected habitat into the harder and more stringent climatic regime of the intertidal zone. Below low water, the climatic constraints of insolation and evaporation and (below wave-base) of strong water movement, are altogether removed. The residual climatic factor is that of illumination, which rapidly falls off in quantity and alters in spectral quality beyond the intertidal. Its modifying influences are depth, water transparency, and angle of presentation of the substrate.

Here the hypobion of the hemispheric sublittoral fringe boulder has become spread out flat; just as we may find the mid eulittoral under-bouldcr community with barnacles (Tetraclitella purpurascens, Calantica spinosa), a red anemone (Isactinia tenebrosa), and a limpet (Gadinia conica) redeployed on the wall of an intertidal cave.

Infra tidal rocky surfaces are generally highly irregular, with the angle of presentation constantly varying. In the earliest of his subtidal studies, Ayling (1969) sought to demonstrate the relation between local illuminance and distribution of organisms. The resultant diagram (Fig. 15) is thus an abstraction from a dappled and uneven species mosaic; it cannot possess the actual pictorial quality of a Ballantine exposure/shelter diagram.

S U B T I D A L ZONATION

The S C U B A divers' world is obviously one where the strict ( = narrowly defined) zonation, so familiar between tides, is not generally a sufficient working concept. There have been strip diagrams drawn to take account of certain harmonies, e. g. by Doak (1979) and Morton and Miller (1973), and these in their colour sequence undoubtedly bear a relation to the patterns beneath boulders, or in caves or overhangs (see

70

SLOPE

0° 30 ° 60° 90° 120°

? ' / . 0 2 5 7 . or/o

Fig. 15. Distribution of some subtidal encrusting organisms in relation to light, as affected by depth and angle of presentation (after Ayling 1976).

Fig. 18). Thus, in the strongest illumination the colours are laminarian brown, followed as we recede from the light by coralline pink, the pallid colours of polyzoans and ascidians, the rich brown, red, tangerine and bright yellow of sponges, and at furthest depths, the zone of pallid white relieved with scarlet. Only with the gorgonians and, deeper still, the antipatharians can there be recognised any truly novel life-forms not already familiar from sciaphilic enclaves in the intertidal.

Diagrams of the subtidal, such as those of Morton and Miller (1973) from a pre-SCUBA generation, are a little like the preacher's exposition of celestial realms not yet personally visited. (Perhaps Linnaeus began the fashion, by staying at home when he despatched his students to the Arctic rigours of Lapland. )

Where it is possible to identify sub-tidal zones, they often have confused horizontal borders and run imperceptibly into each other. Their vertical limits, while related to physical factors, cannot be so regularly fixed as in the intertidal. They are dependent upon a complex of factors: (i) the level of illumination as a function of depth and water clarity, and also of the angle of the bedrock slope (see Fig. 15);

71

(ii) amounts of water movement; (iii) settlement of sediment; (iv) biotic factors involving competition, opportunism of settlement, and

seasonal or long-term cyclic changes. In the intertidal, and increasingly with distance up the shore, it is

rigorous climatic restraints that predominantly control zonation. Below the tides, it is biotic factors that play the major role in facilitating or inhibiting colonisation in a zonal pattern. In the second of his studies, Ayling (1976) began a search for regularities dependent on the factor of illumination, but finally revealed the high importance of biotic factors with their perturbations and oscillations introduced into the sub-tidal community, superimposed upon the physical regulators.

There is thus, in the sub-tidal, along with a freeing of the climatic constraints of zonation, a shift to the establishment of biologically imposed habitat structure, within the limits of graded rather than sharp physical changes. The current studies of J . H . Choat and colleagues (e. g. Choat and Schiel 1982, Schiel and Choat 1980) emphasise the importance of biotic disturbance or pressure on the establishment or stability of distinct sublittoral communities.

A more panoramic overview of a zoning regime operating subtidally has emerged from the survey and mapping of the Cape Rodney to Okakari Point Marine Reserve (Ayling, Cumming and Ballantine 1981). A part of these is given in Fig. 16, showing that the biological habitats have a clear sequence or zonation, though their extents are unpredictable. Such "zonation" is not immediately appreciated by the diver in the water when the field of panoramic vision is very limited.

For these maps, habitats were identified with a biological base, relating habitats to combinations of biotic and physical factors as a subsequent step.

The common sequence (Fig. 17) from low water mark downwards runs: (i) Shallow broken rock which immediately beyond low water, swathed

in tresses or large fucacean brown algae {Carpophyllum spp. and Sargassum sinclairii), with an under-world of reds (Pterocladia spp., and Melanthalia abscissa). Always submerged but well-illuminated, they owe their lower limit to restriction by urchin-grazing.

(ii) Bare-rock flats which are quite variable in extent, with the urchin Evechinus chloroticus. These are a biotic interruption of the continuation of the laminarian Ecklonia radiata that would normally follow the fucaceans. The rocks have been cleared of large algae, initially by the sea-eggs felling the kelp forest, always from the edge. The productivity of the cleared areas increases considerably (Schiel 1982) just as a grazed meadow is much more productive than the same area in bush or forest. The pink coralline-encrusted rocks are kept clear of macro-algae by continued urchin grazing, and by the

72

Fig. 16. Sequence of subtidal communities off Goat Island, Leigh, compiled from photographic data from various workers.

opportunistic occupation and grazing by gastropods such as Cellana stellifera, Trochus viridis, Cantharidus purpureus and Cookia sulcata, all of which can exploit this new open living-space once it has been cleared.

(iii) A kelp forest of Ecklonia radiata, which is restricted at its upper border by urchin grazing and in deep-water by eventual insufficiency of light levels.

(iv) Deep reefs undisturbed below the level of wave base and light are the habitat centre of the "general sublittoral hypobion", encountered only in securely sheltered salients and enclaves between tides. Here the growth of sessile filter feeders (tube-worms, barnacles,

73

74

ectoprocts, ascidians, sedentary molluscs and sponges) forms a complex mosaic over the rock surface. The trigger-fish Navodon scaber is now the important "disturber", constantly nibbling at encrusting species and releasing vacant living space to promote further diversity of opportunistic settlement. Of all the general sublittoral hypobion it is the sponges that penetrate furthest into turbid waters and ultimately monopolise situations where other filter feeders could not survive. As it is at Westmere in the upper Waitemata Harbour, so we find sub-tidal sponge gardens in an over­burden of sediment from 1 to 5 cm deep. Closely encrusting filterers have yielded here to massive and tubular sponges, that can survive by protruding upwards through the sediment.

SYNTHESIS

Fig. 18 brings together the sequence of zoning through the intertidal beyond low water the vertical axis, and that of the sides of intertidal and subtidal boulders. Distribution upon boulder surfaces has already been related with the position of the boulder in the intertidal zone (Fig. 11). The following zones can be characterised, and conveniently referred to by their colour: I. W H I T E ZONE of sessile shelled invertebrates. Basically an

operculate barnacle zone, marking (by its beginning) the threshold of the upper eulittoral zone. In the middle eulittoral zone it is entered by oysters {Crassostrea spp. ) above and tubeworms (Pomatoceros caeruleus) below. Heavy white shells are probably radiation-reflecting during long emersion. On colder shores, or on shaded slopes, mussels (Mytilidae) appear, with shell colours blue or black.

II. M A U V E - P I N K ZONE of calcareous red algae. This marks at its upper limit the threshold of the lower eulittoral zone, and except in extreme exposure is clad at this level with Corallina turf. Subtidal studies have revealed this zone to extend sublittorally as far as the limit of illumination for photosynthesis. Though classically regarded as distinct and characteristic entities, the following three B R O W N A L G A L ZONES appear as interpolations into the full continuity of the calcareous algal zone (the second and third are variously distributed across low water mark, essentially according to conditions of turbidity and light penetrance).

II. i FUCOID B R O W N A L G A E , especially Hormosira banksii, and in increasing exposure Xiphophora chondrophylla, with coralline turf in the lower eulittoral.

II. ii C A R P O P H Y L L O I D B R O W N A L G A E , constituting the sublittoral fringe, but often extending slightly beyond L. W. S.

II. iii L A M I N A R I A N B R O W N A L G A E , of Ecklonia radiata in the north (sometimes with Lessonia variegatus). In shelter and with

75

turbid water this kelp may enter the intertidal. Subtidally, its tall forests may be invaded and cleared by echinoid (and gastropod) grazing, to expose a coralline-pink "echinoid flat". Beneath Ecklonia develop the shade-loving non-calcareous red algae, Pterocladia spp. and Melanthalia abscissa.

I l l B R O W N ZONE dominated essentially by Ectoprocta. This is subtidally represented by bushy Anasca (Bugula spp. and related forms), and beneath intertidal boulders by Beania spp. (flat, modified anascans) and numerous crustose Ascophora. In the sheltered intertidal, this zone typically begins with a threshold strip of the black, red-edged ascophoran Watersipora cucullata. The zone is also entered by sponges, especially orange and brown species of Tethya and Suberites, and brick red ones of Microciona, Ophlitaspongia and Holoplocamia. Red sponges, like others, show more luxuriant branched growth subtidally. Typical also are anemones (Actinothoe albocincta and Diadumene neozelandica) and thick-test ascidians (Cnemidocarpa bicornuata and Asterocarpa cerea).

IV. R E D - Y E L L O W Z O N E developing the full diversity and form range of the "general sublittoral hypobion". Life forms are essentially comparable on subtidal open surfaces and beneath boulders. They comprise a wide range of yellow- orange, brown and red sponges, including tuberose grey Ancorina alata and brown Spongia reticulata; variously coloured heads and crusts of compound ascidians; the thin-test simple ascidian Corella eumyota; and numerous sessile molluscs. Subtidal growth and branching is far more luxuriant subtidally than beneath boulders. This is the "sponge garden" of the S C U B A world.

V. WHITE-with-RED ZONE with organisms characteristic of low illumination, and a high proportion colourless or white. The organisms are calcareous sponges, crusting didemnid ascidians, pallid ascophoran Ectoprocta, and clusters of tubeworms, especially Filograna sp. The supporting colour is generally vivid red, from the crowns or opercular of serpulids, brachiopods (Terebratella inconspicua) and the oral discs of cup corals (Flabellum rubrum).

VI W H I T E or PINK ZONE on sloping rock faces, always the deepest component of the sublittoral "shore". This zone is gorgonian dominated, with Primnoides and other sea fans, and at greater depths the "black" coral Apanipathes (white when living). The zone is never represented by any intertidal enclave, and is assigned by Morton and Miller 1973) to the lower sublittoral zone. It will be noticed that the term "zone" has been employed here in a

biological sense that could cut across its standard use, as by Morton and Miller (1973), to denote the basic subdividions of the intertidal (eulittoral zone) and the subtidal (sublittoral zone). With the tentative

76

B O U L D E R S

Fig. 18. Schematic sequences of zoning on open faces (intertidal and subtidal) and on boulders. Three examples of boulders are shown with their undersurface hypobion.

77

role of this paper in exploring an idea, it is hoped that such provisional, non-definitive terminology will be self-explaining and avoid confusion.

A C K N O W L E D G E M E N T S

We are indebted to Dr W. J . Ballantine for continuing and stimulating discussion of the questions dealt with in this paper. We also record our thanks to Mr Jonathan Jull (research assistant to the senior author) for his assistance and care in the preparation of the illustrations.

R E F E R E N C E S

Ayling, A . M . 1969: The ecology of sublittoral rocky surfaces in northern New Zealand. B. Sc (Hons. ) thesis, University of Auckland. 65 p.

Ayling, A . M . 1976: The role of biological disturbance in determining the organisation of the sub-tidal encrusting community in temperate waters. Ph. D. thesis, University of Auckland. 114 p.

Ayling, A . M . ; Cumming, A . & Ballantyne, W. J . 1981: Map of shore and sub-tidal habitats of the Cape Rodney-Okakari Pont Marine Reserve, North Island, New Zealand in 3 sheets, scale 1: 2 000. Department of Lands and Survey, Wellington.

Ballantine, W. J . 1961: A biologically defined exposure scale for the comparative description of rocky shores. Field Studies 1: 1-19.

Choat, J . H . & Schiel, D. R. 1982: Patterns of distribution and abundance of large brown algae and invertebrate herbivores in the sub-tidal region of northern New Zealand. Journal of Experimental Marine Biology and Ecology (in press).

Doak, W. T. 1979: "The Cliff Dwellers". Hodder and Stoughton, Auckland. 80 p. Gray, J . 1976: Are marine baseline surveys worthwhile? New Scientist. 219-221. Harger, J . R. E . 1963: The settlement and development of fouling communities on vertical

bouyant surfaces in the Auckland Harbour, with notes on the adjacent wharf-pile fauna. M . Sc, thesis, University of Auckland. 98 p.

Morton, J . E . & Miller, M . C. 1973: "The New Zealand Sea Shore" 2nd edition. Collins. London. 653 p.

Schiel, D. R. 1982: Selective feeding by the echinoid Evechinus chloroticus and the removal of plants from sub-tidal algal stands in northern New Zealand. Oecologia 54: 379-388.

Schiel, D. R. & Choat, J . H . 1980: Effects of density on monospecific stands of marine algae. Nature 285: 324-326.

Stephenson, T. A . & Stephenson, A . 1949: The universal features of zonation between tide-marks on rocky coasts. Journal of Animal Ecology 37: 289-305.

Stephenson, T. A . & Stephenson, A . 1972: "Life Between the Tide-marks on Rocky Shores". W. H . Freeman & Co., San Francisco. 425 p.

Whittaker, R. H . 1970: "Communities and Ecosystems". Macmillan. London. 158 p.

78