LARGE SCALE TEMPORAL PATTERNS IN THE COMMUNITY STRUCTURE OF SUBTIDAL SOFT-SEDIMENT MACROFAUNAL COMMUNITIES
A REVIEW
CHRISTOPHER LOWE
Introduction
Since Edward Forbes' work in 1815 much research has been produced concerning short-term patterns in sub-tidal macrofauna (Irish Sea Study Group)19. Many species follow the seasonal cycle, such as Sepia officinalis (Linn.) and Aplysia punctata (Cuvier), which migrate into shallow water to breed during the summer (Hayward et al)17. However more recently it has become evident that large-scale patterns, recurring over a period of more than a year, can also be important. Lewis23 pointed out that if larval recruitment disturbance is short term relative to the lifespan of organisms it is likely to have a short term impact on the population which quickly recovers. If the disturbance is significantly longer than the organism lifespan then the species would be removed and recolonisation would take longer, requiring immigration from external populations.
Ramsay28 defines the community as "an assemblage of species populations which occur together in space and time." Over the past ten years work has been published linking long term community patterns with characteristics of benthic marine habitats. Such patterns are generally caused by disturbance leading to change in the environment. Morrisey et al26 showed that changes in a small area relative to the habitat generally have short term effects but larger disturbances tend to cause longer term changes.
Large scale patterns can be manifested either as cycles or trends; natural patterns are usually cycles. Changes from anthropogenic inputs often result in damage to communities from accidental inputs and the degradation of community diversity. Where this is followed by adaptation it can appear to form a cycle. However most degradation from anthropogenic inputs appear as trends. In this review I will cover these long term effects on soft-sediment macrofauna, defined as those animals retained in a 0.5mm sieve which live on or in a non-solid substrate.
GESAMP17 found that natural deep-sea cycles tend to be annual, following the fall of algal detritus. Due to the massive volumes of water, concentration changes are small and the effects of anthropogenic inputs are negligible. This review therefore concentrates on continental shelf communities.
The models which have been put forward of long-term change are on small spatial scales cannot be transferred to different systems. They take the form of species x is followed by species y as a description of succession rather than an attempt to explain these changes. In this review I will discuss the likely impact of different factors on communities and the problems of attempting to extrapolate these changes onto larger scales.
Though community change is always due to disturbance, studies (Warwick and Uncles39, Rasmussen29, Irish Sea Study Group19) have shown that causes of temporal patterns in the benthic environment arise from four main causes.
1) Changes in the physical environment. Strength of currents and sediment composition and stability define which organisms are physically able to persist in the habitat. Patterns in these factors affect patterns in the community.
2) Changes in the food supply. The amount of food and nutrients which come into the system determine what species and how many organisms can survive in the habitat.
3) Periodic population loss from pathogens and natural environmental changes, this is usually followed by recovery.
4) Anthropogenic inputs. These are extremely varied and population losses may not be followed by full recovery.
Temporal patterns due to physical parameters
In 1977 Warwick and Davis38 found a correlation between the physical and chemical character of sediments and the communities found in them. Further work by Warwick and Uncles39 suggested that sediment type and stability have a great impact on which communities are able to exploit a habitat. Creutzberg et al7 found that sediment character was the primary physical factor setting community type. Elliot and O'Reilly10 found that in the Forth Estuary, bioturbation, such as the production of faecal piles and worm casts, altered the stability of the sediment. This appeared to affect the community dynamics by reducing the rate of substrate movement in the area. Rees and Walker30 found changes in the communities of Liverpool Bay in the period 1978-86 which mirrored those of the North Sea suggesting that community dynamics can be an amplification of large scale oceanographic events.
All of these studies indicated that the tidal current regime of the area, which can be regarded as the "super parameter", dictates natural variation in soft sediment, benthic macrofaunal communities and that cycles or changes in the current in an area would lead to cyclical or permanent changes in the community.
Temporal patterns due changes in the food supply
Warwick and Uncles39 considered that type and amount of food has a major impact on populations in a community. Kube et al22 also found the concentration of sediment chlorophyll (an indication of activity of phytoplankton and micro-organisms which act as food for some benthic organisms) to be a major biological factor affecting the community. Therefore climate changes which affect the food supply will also have a major impact on the community.
Morrisey et al26 stated that the major food source of most macrofauna is from the plankton whose production in temperate waters varies over an annual cycle. However longer term trends are likely. The Canary Report1 indicated that increased UV irradiation from the hole in the ozone layer is starting to interfere with the reproduction of plankton, reducing the food available to benthic organisms.
Often one species dominates an area but the species that dominates changes over time. Eagle9 suggested this is due to a high density of larvae of one species being present and settling when disturbance opens an area for colonisation. Once established this species will prevent colonisation by other species by feeding on planktonic larvae (including their own species). Change of dominant species occurs when the dominant species dies due to age or disturbance; leaving the area open to colonisation from larvae that could be different species to the original inhabitants. The dominant species is therefore dependent on which species' larvae are present in the plankton when living space becomes vacant. Frequency of change depends on either frequency of disturbances or the lifespan of the dominant species. Large numbers of random events determine these factors and so they are difficult to predict and model.
The El Niño-Southern oscillation (ENSO)
Trade winds over the Pacific Ocean move surface waters leading to a bulge of water in the West which in some years can become large enough to force surface water back to the East. This is known as El Niño, and drastically affects the surface currents of the East Coast of America. Deep currents carrying nutrients that normally surface off the coast are stopped from doing so (Fig 1, bottom) and micro-organisms cannot then reproduce at their normal rate, reducing the food source for other animals. Planktonic animals migrate with the currents but benthic communities shrink in size because of the lack of food.
Warm El Niño waters are able to dissolve less oxygen than normal waters and as such the depth of penetration of oxygen into the sediment is reduced. Sevice and Feller32 showed that in El Niño conditions organisms are forced to live shallower in the sediment than normal, this leaves them open to attack from predators and reduces the volume of sediment in which organisms can live, so again the number of benthic organisms is reduced.
The temperature of surface waters then decreases to below normal (Fig 1, top) before the trade winds bring warm water again back to the East. This is known as La Niña or the cold phase (NOAA)27. The entire cycle has a variable period of between four and seven years and is known as the El Niño-Southern Oscillation (ENSO).
Since these events profoundly affect the economically-important marine communities of the East Pacific much research has been carried out on ENSO, although little has been based around soft sediment macrofauna. Nevertheless these will be affected, although because this is presumably a natural long-term cycle communities will have evolved to cycle with these conditions with the result that diversity will be less affected than if it were a new phenomenon. In fact Houston's 1979 Intermediate Disturbance Hypothesis suggests that diversity would in fact be higher than that of a community under under conditions as disturbance allows the survival of species which would otherwise be less competitive.
Figure 1, Surface temperatures relating to current in the Pacific Ocean during one ENSO from NOAA 199827
Changes to the North Atlantic Drift (NAD)
Atmospheric emissions are now considered to be causing an increase in global temperature, leading to an increase in sea levels. Over the next half a century, low lying areas may become submerged by the sea, opening a large area of shallow water to colonisation by marine organisms thus creating new communities (ENN)11.
Another apparent effect is a reduction in the cycle of freezing and thawing of the Arctic ice cap that is thought to drive the North Atlantic Drift which brings warmer, nutrient rich water from the Gulf of Mexico to NW Europe. Disruption of the NAD could lead to European waters becoming much less productive, and previous reversals of the NAD have been associated with temperature changes in the North Atlantic (Gribbin)14. Since this is still a theoretical change the effects of this process are uncertain (GESAMP)18.
Temporal patterns due to disease and recovery
Temperature change
During the early 1930's a severe wasting disease affected approximately 90% of seagrass communities in the North Atlantic, but not the Pacific or Mediterranean. The reduction resulted in the loss of the macrofauna associated with the beds, though they returned to almost pre crash levels by the 1950's. This was originally attributed to a pathogen but current research suggests the cause was increased water temperature; this was recorded in the North Atlantic but not in the Pacific or the Mediterranean. It is likely that this is not an isolated event and will happen again (Rasmussen)29, perhaps more permanently as a result of climate change. This effect may be more widespread; recent work by Sanford31 suggests that feeding in the keystone predator on Oregon shores Pisaster ochraceus is inhibited by small increases in temperature.
Pathogens
Laukner23 has shown that bacterial pathogens and parasitic nematodes, can decimate entire populations of gastropods Following the destruction of the animals in a habitat a succession will begin. For example if the species affected is a keystone predator then the entire structure of the community can change. However as with the seagrass beds the situation is likely to return to normal under natural conditions.
Anthropogenic inputs
Introduction
According to GESAMP18 pollution is "..the introduction by man, directly or indirectly, of substances or energy into the marine environment (including estuaries) resulting in such deleterious effects as harm to living resources, hazards to human health, hindrance to human activities including fishing, impairment of quality of use of seawater and reduction of amenities." The Irish Sea Study Group19 suggest that anthropogenic inputs such as sewage outfalls and solid waste dumps have the greatest effect on benthic macrofaunal communities on the continental shelves of the western world.
Such pollution has been considered so important that it has formed the basis of most studies of the benthic environment, usually by Before After Control Impact (BACI) studies. These utilise a set of samples taken before a disturbance as a base line and assume any significant deviance from this is due to the disturbance. However; soft sediment macrofauna communities may undergo significant variations in time periods as short as one day under natural conditions (Morrisey et al)26. So recently data has been collected for longer periods before impact so deviation from normal temporal cycles can be measured and a more reliable comparison made (Thrush et al)36.
Sewage & Fertiliser
Untreated sewage causes an increase in carbonaceous nutrients allowing huge increases in the numbers of micro-organisms. These use all the oxygen in the sediments around the outfall, killing the macrofauna (SOE)35. Further from the outfall a relatively small number of species tolerant of low oxygen levels exploit the food source, dominating that habitat, and reducing community diversity. Fertilisers from agriculture run off into rivers and estuaries, causing eutrophication by the same mechanism (Irish Sea Study Group)20. The polluting effects can be extended by the development of algal blooms which can produce lethal toxins, which can knock out entire communities or be very specific. For example in North Cornwall an algal bloom, probably precipitated by a change in the regime of sewage outfalls, exterminated two species of gastropod while leaving all other species unaffected (Gibbs et al)12.
Sludge dumping is known to be a cause of lowering diversity by silting up feeding apparatus and smothering infauna (Comprehensive Studies Task Team)4.
The effects of sewage and sludge have been controlled within the European Union by the 1991 Urban Waste Water Treatment Directive6. Water undertakers in member states are required to provide biological sewage treatment for coastal towns and to remove nitrogen from effluents in areas designated as "sensitive". At the end of 1998 dumping of sewage sludge at sea was outlawed by the same directive.
Such legislation and improved environmental awareness has lead to the reduction of inputs into some areas, allowing recovery from their effects. Mathison and Berry25 found increased diversity in benthic populations in the Forth Estuary coinciding with the reduction of industrial inputs in the early 1980's and Rees et al30 found similar trends in the community composition of Liverpool Bay following reduction of inputs in the mid 1970's.
Organic Pollutants
Organic pollution can take on many forms, from universally lethal to very selective effects. In 1994 UKWIR published a report37 suggesting that although chemicals like DDT might not have a direct effect on benthic populations the levels of these chemicals could build up in the tissues of predators feeding on these organisms leading to death or infertility. Following a reduction in predator number, species normally held in check by predation could become dominant, reducing diversity.
Gibbs and Bryan12 worked on the antifouling agent TBT which causes female dog whelk Nucella lapilis (Linn.) to grow male gonads which, in extreme cases, may physically prevent mating from occurring. Several populations became extinct before the use of TBT paints on small boats became illegal in British waters (Irish Sea Study Group)20. The effect of these chemicals is not known on benthic invertebrate organisms but other gastropods could be affected in the same way as N. lapilis.
Heavy metals
Wigham40 suggests that since heavy metals from industrial processes and wastewater outflows are concentrated by benthic organisms, particularly those that feed in sediments, the presence or absence of low tolerance shell fish could be an indicator of the level of heavy metals. These, being insoluble, can remain in the sediment for long periods and the community may return to its normal structure only very slowly. Predators on these species can also bioaccumulate metals to toxic levels.
Dredging
Harvey et al15 showed that the removal and dumping of sediments changed the substrate composition in dredge sites. Opportunistic species increased in number, reducing the biodiversity, and it took more than two years for sediment characteristics and the faunal community to return to normal. Dredging may resuspend heavy metals which had fallen into the sediments, causing the death of organisms around the dredging site (Irish Sea Study Group)21.
The impact of sewage and heavy metals on infaunal communities is summarised in Fig. 2.
Fishing for shellfish by dredging also decreases the diversity of benthic communities. The Irish Sea Study Group20 showed that otter trawling reduced species numbers by 40%, infaunal density by 65% and total biomass by up to 90%. Service et al33 found soft corals and hydroids to be particularly affected, leading to the virtual destruction of communities in heavily fished zones. Recovery may be slowed or permanently changed by resuspension of sediments (Churchill)2, changing the character of the sea floor.
Fig. 2. The Affects of anthropogenic inputs on infaunal communities. From Conneely 19885
Oil spills
Large oil spills from tankers and pipelines are greatly publicised by the media. The Irish Sea Study Group20 however showed that these account for only approximately 60% of the oil lost to sea, the remainder arising from frequent small spills and intentional dumping. Whatever the size of the spill dense fractions of oil will sink and much will fall to the sea floor where their direct toxicity and smothering effects cause community destruction. The group pointed out that most reports of this effect relate to in the littoral environment but it is also evident in the sublittoral where entire benthic communities can be wiped out by a major spill.
Radionuclides
Clark3 suggested that any radioactive contact will result in the degradation of susceptible species but that due to the difficulty of monitoring benthic population over time and the naturally high mortality in these systems it would be difficult to prove. However MAFF34 which reported that the levels of radioactivity found in the sediments around the outflow of Sellafield nuclear power plant were several orders of magnitude too low to have an effect even in gulls, the top predators of the food chain.
Haux and Forlion15 commented that most work on toxic effects has been on single organisms in industrial species so the effect on the community is difficult to predict. (Fig. 3).
Figure 3.Effects of toxicants occur at different levels of biological organisation. Toxic effects are best known and understood at the cell and organ level, while the ecosystem and community levels are least understood although most relevant (from Haux and Forlin, 198816).
Discussion
Changing patterns in the marine benthic macrofaunal community are caused by either natural or anthropogenic environmental changes. Some natural changes are cyclic; others such as disease and recovery are irregular. In either case the population will remain constant or recover to a similar level of diversity since the community has evolved with these changes. Due to large short-term variation of benthic communities it is difficult to model with any certainty long-term patterns and trends from field data as these variations swamp the longer term change. Some changes can however be modelled in some cases, such as when the cause is changes in the current profile. However pathogenic kills are difficult to model, since the extent to which the pathogen will spread is less easily predicted.
Most community changes on continental shelves are caused by anthropogenic inputs. Due to continual degradation by these inputs long-term changes are more easily followed than with natural changes. Anthropogenic inputs can often be measured and their effects predicted. For example a trawl of the sea bed affects a known area, removing all organisms above a certain size, from which the time taken to return to normality can be predicted (Harvey et al)15. Single incidents cause a similar effect to disease, killing a few or all of the species in the community; long-term inputs tend to cause degradation of the habitat, reducing diversity gradually over time.
For toxins, most work covers single organisms rather than communities which would be more relevant to this review. Such anthropogenic inputs often persist in the environment and prevent normal re-establishment of the community long after the input has stopped.
Natural and anthropogenic types of disturbance often differ in the level within the community which feels the major impact. Natural cyclic change usually first affect organisms lower in the food chain which feed on detritus or plankton that currents bring in. This causes bottom-up control of the system; if the smaller animals are reduced in number so are the predators and diversity is maintained. Anthropogenic factors tend either to be universally lethal or remove predators by bioaccumulation of toxins. The removal of predators can be almost as detrimental as more widespread mortality in that a species which may have been held in check by the predator can become dominant, resulting in severely reduced diversity.
It is clear that community change due to anthropogenic effects can have a severe and lasting effect, partly because toxins remain in the environment and partly because the communities have not adapted to resist the effects. It can therefore be concluded that decrease in diversity due to mans disposal of waste and chemicals into the sea is the major pattern in benthic soft sediment communities.
Future work
Most work so far undertaken on benthic communities has been too short term to show patterns. However works such as COST 47 project (see Lewis)24 may allow more clarity to be shed on this area.
Equally little work has been carried out on the movement of benthic organisms from warm water to cooler temperate regions. This could be a valuable measure of global warming.
I have shown that anthropogenic inputs are an important cause of community changes. However although some work has been done on single organisms, little is known of the quantitative effects they could have on benthic communities which is vital if we are to understand the nature of community change in this environment.
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