A.J. Underwood

Beyond BACI: the detection of environmental impacts on populations in the real, but variable, world

BACI (Before/After and Control/Impact) sampling is widely used in investigations of environmental impacts on mean abundance of a population. The principle is that an anthroppogenic disturbance in the “impact” location will cause a different pattern of change from before to after it starts compared with natural change in the control location. This can be detectable efficiently as a statistical interaction in an analysis of variance of the data. Usually, samples are taken at replicated, random intervals of time before and after the putative impact starts; this ensures that chance temporal fluctuations in either location do not confound the detection of an impact. These designs are, however, insufficient because any location-specific temporal difference that occurs between the two locations will be interpreted as an impact even if it has nothing to do with the human disturbance. Alternatively, abundance in the single control location may change in the same direction, cancelling the effects of an impact. Here, asymmetrical designs are developed that compare the temporal change in a potentially impacted location with those in a randomly-selected set of control locations. An impact must cause a different temporal change in the disturbed location from what would be expected in similar locations. This can be detected for short-term (pulse) or long-term (press) impacts by different patterns of sigficance in the temporal interactions between of sampling and locations. Frolm these novel designs, tests are that demonstrate whether an usual pattern of temporal change in abundance of organisms is specific to the supposedly impacted location and correlated with the onset of the disturbance. Examples are presented of how to use these designs to detect impacts at different spatial scales. Other aspects of their use are discussed.

Experimental Analyses of the Structure and Dynamics of Mid-shore Rocky Intertidal Communities in New South Wales

SummaryAt mid-shore levels on rocky shores in New South Wales, grazing gastropods are the dominant species in sheltered areas. Where wave-exposure is great, barnacles occupy most of the space. At intermediate levels of waveexposure, there are mixtures of grazing gastropods and barnacles, and the patterns of occupancy of space, and structure of the community change from time to time. The major species found in these areas are the coronuloid barnacle Tesseropora rosea, the patellid limpet Cellana tramoserica, the smaller acmaeid limpet, Patelloida latistrigata, which is mostly confined amongst barnacles, and the predatory whelk Morula marginalba. The roles of each of these species in determining the structure and persistence of intertidal communities were investigated by experimental manipulations of the densities of each of these organisms. In most experiments, a range of densities of limpets and barnacles was used, rather than the simple removal of all of one species.Recruitment of Cellana was negatively associated with increasing density of adult limpets, and with increasing density of barnacles. Growth and survival of juvenile Cellana were decreased by increasing densities of barnacles, probably because barnacles occupied space, preventing limpets from grazing. Morula had no effect on recruitment or survival of juvenile Cellana. Recruitment of juvenile Patelloida was not affected by different densities of barnacles, but survival to adult sizes was poor in areas where whelks are active. In areas where whelks were removed, Patelloida showed increased survivorship with increased cover of barnacles, probably because Patelloida amongst barnacles found refuge from the superior competitive effects of Cellana.The settlement and subsequent survival of Tesseropora were affected in complex ways by the activities of Cellana. At great densities, Cellana can have deleterious effects on newly-settled barnacles, probably by crushing them whilst grazing. In some areas, and at some densities, however, limpets can have beneficial effects on the recruitment and/or survival of Tesseropora. The limpets graze the juvenile stages of growth of foliose macroalgae, preventing them from growing up to pre-empt the rock-surface (thus preventing settlement of barnacles) or to smother alreadysettled barnacles. The effect of limpets on the recruitment and survival of barnacles in any area is a function of the densities of limpets and barnacles, and the height on the shore and local weather (the latter factors influence the rates of growth of algae).Increased cover of the rock-surface by adult barnacles caused reductions in the densities of Cellana. Limpets migrated away from areas of great cover of barnacles, and, if confined in such areas, starved and lost weight. The dispersion, as well as the density of the barnacles was important in determining the effects of barnacle cover. Where barnacles occupied half the space, but were scattered, leaving only small patches of bare rock, they had the same deleterious effects on Cellana as in areas where they were spread evenly to occupy most of the rock-surface. Thus, barnacles could invade areas dominated by limpets provided they recruited in sufficient numbers. They did not have to saturate an area to displace the Cellana.In these communities, all of the species can be considered to have important roles in the establishment and maintenance of community structure. We conclude that interpretations of the roles of individual species must be based on direct, experimental investigation. In this system, there was no indication that many of the species were functionally insignificant.The present experiments also revealed that the interactions among even a few species are very varied and complex; proper investigation requires considerable replication and repeated experimentation in different places and years.Finally, although the present studies allow reliable interpretations of observed patterns of occupancy and dominance on natural shores, the experiments did not provide a predictive framework to anticipate the future events in any area. This is because of great variability in the timing and intensity of recruitment of planktonic propagules of all the components in the system, and in the density and activity of predatory whelks in different areas. These results suggest that tightly co-evolved community relationships are not likely to be important, even if they appear to exist, in communities where most of the species have widely dispersed pelagic offspring and interact in diverse and complex ways at different densities.

The effects of grazing by gastropods and physical factors on the upper limits of distribution of intertidal macroalgae

SummaryThe cover of foliose algae is sparse to non-existent above a low-level algal zone on many shores in N.S.W., except in rock-pools. Above this algal zone, encrusting algae, mostly Hildenbrandia prototypus, occupy most of the primary substratum on sheltered shores. Experimental manipulations at midtidal levels were used to test hypotheses about the effects of grazing by molluses and of physical factors during low tide on this pattern of algal community structure.Fences and cages were used to exclude grazers: molluscs grazed under roofs and in open areas. Cages and roofs provided shade, and decreased the harshness of the environment during low tide: fences and open areas had the normal environmental regime.In the absence of grazers, rapid colonization of Ulva and slower colonization by other foliose algae occurred in all experimental areas. The rate of colonization by Ulva sporelings was initially retarded on existing encrusting algae, but after a few months, cover of Ulva equalled that on cleared rock.Most species of algae only grew to maturity inside cages, and remained as a turf of sporelings inside fences. No foliose algae grew to a visible size in open, grazed areas. Grazing thus prevents the establishment of foliose algae above their normal upper limit on the shore, but the effects of physical factors during low tide prevent the growth of algae which become established when grazers are removed. Physical factors thus limit the abundance of foliose algae at mid-tidal levels.The recolonization of cleared areas by Hildenbrandia was not affected by the presence of a turf of sporelings, nor by the shade cast by roofs, but was retarded in cages where mature algae formed a canopy. Even under such a canopy, Hildenbrandia eventually covered as much primary substratum as in open, grazed areas. This encrusting alga is able to escape from the effects of grazing by having a tough thallus, and by its vegetative growth which allows individual plants to cover a lot of substratum, and by the tendency for new individuals to start growing from small cracks and pits in the rock, which are apparently inaccessible to the grazers.Mature foliose algae are removed from the substratum by waves, and many individual plants died during periods of hot weather. Sporelings in a turf were eliminated, after experimental fences were removed, by the combined effects of macroalgal grazers, which invaded the areas, and microalgal grarers which ate the turt from the edges inwards.The results obtained here are discussed with respect to other studies on limits to distribution of intertidal macroalgae, and the role of grazing in the diversity and structure of intertidal algal communities. Some problems of these experimental treatments are also discussed.

Experiments on factors influencing settlement, survival, and growth of two species of barnacles in new south wales

Abstract Adult Tesseropora rosea (Krauss) and Tetraclitella purpurascens (Wood) are mostly found in the eulittoral (barnacle) zone of rocky seashores in New South Wales. Below this zone most space is occupied by the tube-worm Galeolaria caespitosa (Lamarck) or by various species of macroalgae. Within the eulittoral zone, T. rosea are mostly on sunny areas of rock exposed to relatively strong wave-action. T. purpurascens are present mainly in crevices, caves, and under ledges where there is considerable shade. Cyprids of both species settled on sandstone plates and on experimentally cleared areas in the barnacle and Galeolaria zones. Neither species settled where the substratum was already covered by algae or Galeolaria . No spat of T. purpurascens were found in sunny areas of the barnacle zone. T. rosea , however, settled in cleared substrata in sunny and shaded areas. Neither species settled in the littoral fringe above the upper limit of distribution of adults. On boulders transferred to high levels of the shore during a storm, small T. purpurascens died within a few weeks. Barnacles of both species which had settled in experimentally cleared areas in the Galeolaria zone survived and grew. In these areas some T. purpurascens were killed by being smothered by tube-worms which settled after the barnacles. This probably happens to T. rosea , but was not demonstrated experimentally. In the Galeolaria zone, both species of barnacles were very quickly smothered and killed by macroalgae growing over them, except where these were experimentally removed. Within the barnacle zone, all newly-settled spat of T. purpurascens transferred to sunny sites died within two months, whilst many of those in shaded sites survived. In areas where wave-action was strong, spat of T. rosea survived and grew well in sunny areas, but survived better in the shade. Under a ledge, however, where wave-action was reduced, all the T. rosea in sunny sites, and most of those in shaded sites died within two months; many newly-settled T. purpurascens survived in the shade in this area. The grazing limpet Cellana tramoserica (Sowerby) dislodged and crushed some newly-settled T. rosea and reduced survival in some sunny areas. T. rosea settled preferentially on bare rock and were rarely found on the shells of adult barnacles. Thus, the density of spat was greater where adult barnacles were absent. In contrast, many newly-settled T. purpurascens were found on the shells of adults of their own species in shaded areas; they also settled on cleared rock. Because T. purpurascens tended to settle amongst and on adults, and in crevices and confined areas, they were not much affected by limpets. When newly-settled T. purpurascens were in high densities, they had lower survival than in areas with reduced densities, because of squashing and smothering by each other. The upper and lower limits of vertical distribution (zonation) of these two species of barnacles are determined primarily by the settlement of cyprids. Neither species settled at the highest levels on the shore. Whether this was due to the decreasing time of submersion during high tide towards the top of the shore, or a result of preferences for settlement site is unknown. Even if cyprids were to settle in the littoral fringe, the spat would die very quickly probably as a result of desiccation. Below the barnacle zone, the entire substratum is usually occupied by other sessile species, particularly macroalgae, on which the barnacles do not settle. In experimentally cleared areas below the barnacle zone, or in any naturally cleared areas both species settled, and could survive the physical conditions. Newly-settled spat were, however, overgrown and killed by algae and Galeolaria . Within the barnacle zone, T. purpurascens is restricted to shaded areas because of the inability of newly-settled spat to survive the physical stresses of high temperature and desiccation in sunny habitats. T. rosea appears to be excluded from shaded areas by a combination of the lack of suitable substrata on which to settle, and the effects of reduced water-flow in many crevices and under ledges. T. rosea survived better in areas with strong wave-action and can survive in shaded areas where water-flow is not reduced by the topography of the substratum.

Effects of interactions between algae and grazing gastropods on the structure of a low-shore intertidal algal community

SummaryAt low levels on shores in New South Wales, foliose algae are abundant and often occupy all substrata; microalgal grazing gastropods are rare or absent. At higher levels, foliose algae are sparse or absent and grazing gastropods are abundant. Hypotheses for the causes of the lower vertical limits of distribution of these grazers include the effects of increased predation or the deleterious physiological effects of increased period of submergence at lower levels on the shore. Alternatively, the presence of the algae, because they occupy space and deprive the grazers of substratum for feeding, may prevent the downward movement, or survival of the grazers at low levels. Under the first two of these hypotheses, algae are able to colonize and grow in low-shore areas as an indirect result of factors which remove grazers. Under the third hypothesis, the algae are directly responsible for the lack of grazers.Experimental clearings of the low-shore algae and introductions of the mid-shore limpets Cellana tramoserica and Siphonaria denticulata were used to test these hypotheses. C. tramoserica grazes microalgae and removes them from the substratum, preventing colonization. S. denticulata, in contrust, crops the algae, leaving a visible cover of algae on the substratum, which can grow rapidly. Because of its method of feeding, S. denticulata had no measurable impact on the rates of colonization, nor on the dry weights of algae, compared with those of ungrazed areas. C. tramoserica could keep cleared areas tree from foliose algae, but only when the limpets were mainfained in great density (10 per 900 cm2). They were less effective where wave-action was greater.Neither species of limpets could survive when placed onto beds of mature algae, because they had no substratum on which to cling and were swept away by the waves. C. tramoserica did not invade clearings below their lower limit of distribution where they had to move over a bed of foliose algae. Few C. tramoserica moved directly downshore into cleared areas. When placed on bare rock within low-shore beds of algae of different ages, S. denticulata remained amongst the algae and maintained their tissue-weights. Few C. tramoserica remained in areas with well-developed algae, compared with areas having sparse algal growth. Those Cellana which remained amongst well-developed algae lost weight, whereas limpets in areas with less algal growth mammtained their weights. In experimental cages in low-shore beds of algae, where the limpets were inaccessible to potential predators, C. tramoserica lost weight and died. On cleared areas they survived for many weeks, but lost weight and died as algae grew and covered the substratum. In the absence of predation, the micro-algal grazer C. tramoserica could not survive in lowshore areas because algae grew too fast and occupied the substratum, making it inaccessible for the limpets to graze; the algae, once grown beyond small sporelings, are not a suitable food-source for C. tramoserica, and the loss of weight and death of these limpets is attributable to starvation.The lower limit of distribution of C. tramoserica is not due to the direct effects of physical factors associated with prolonged submersion, nor to the impact of predators, but is apparently determined by the presence of rapidly growing, extensive beds of foliose algae at low levels on the shore. The cause of the limit of distribution of S. denticulata is not yet known and predation may prove to be important. Removal of S. denticulata from low-shore algal beds would not, however, affect the domination of substrata by algae. Grazing by S. denticulata at very great density had no effect on algal cover nor weight. In the intertidal community studied, the persistence of a low-shore algal zone, bounded above by abundant grazers is not influenced by the activities of predators, but is a direct result of interactions between the grazers and the algae.

Variability at different spatial scales between a subtidal assemblage exposed to the discharge of sewage and two control assemblages

Abstract Environmental disturbances can alter the variability of assemblages of organisms in impacted sites compared to control sites. It has therefore been proposed that increased variability might be an important feature of stressed populations. Increased variability may be due to changes in the population structure of individual species or changes in the suite of species. In this study, spatial variances of shallow subtidal assemblages of organisms inhabiting vertical cliff-faces were compared among two control locations and one location that had for many years been exposed to the discharge of sewage. These assemblages covered nearly all available space on the substratum and consisted primarily of encrusting and foliose macro-algae and numerous filterfeeding animals, such as ascidians, sponges and bryozoans. Mean differences in abundances between these locations were investigated using Beyond BACI designs. In addition, these locations were used to examine the model that assemblages are more variable in disturbed than undisturbed environments and to try to distinguish differences in variability due to differences in the population structure of individual species from that due to changes in species composition. The assemblages were sampled at two spatial scales at each of three depths in each location. There were significant differences between the polluted location and one or other of the control locations in the mean abundances of some organisms, the variances of certain species (or recognisable types) at each spatial scale and for multivariate measures of species composition. There was, however, no evidence to support the prediction of increased variability in the apparently polluted location compared to the control locations. Importantly, for many measures of abundance and variability, the control locations were as different from each other as they were from the polluted location, suggesting that the latter fell within the range of natural subtidal assemblages separated by these spatial scales. These findings emphasise the need to include more than one control location in any study of a potential environmental impact, so that any effects of that impact can be distinguished from the range of natural variability.

Structure of a rocky intertidal community in New South Wales: Patterns of vertical distribution and seasonal changes

Abstract Patterns of vertical distribution of common intertidal animals and plants were sampled in transects and groups of replicated quadrats on a sandstone rock-platform (Green Point, New South Wales) from October 1972 to October 1976. Zones corresponding to those described in previous qualitative studies were consistent throughout the study. The bottom of the shore was dominated by 100% cover of foliose macroalgae and there were few animals present. Mid-shore levels were dominated by grazing molluscs, sessile animals (notably barnacles and tubeworms) and/or encrusting algae. At the upper levels of the shore was a zone of littorine gastropods of three species. In mid-shore areas, foliose algae were sparse except in pools and were positively correlated with the abundance of sessile animals. The upper limits of vertical distribution of dense cover of foliose algae, the height of peak abundance of mid-shore grazers and the upper limits of these grazers were at higher levels on the shore where exposure to wave-action was greater. There was considerable patchiness in the occupancy of primary substratum from one part of the shore to another, and no clear trends of diversity of species with the gradient of exposure to wave-action were evident. There were, however, clear seasonal trends in the vertical distributions of some algae, which extended to higher levels on the shore during colder months than during the summer. In addition, some species of algae were only present during some seasons of the year, and others showed marked seasonal variability in frequency of occurrence in quadrats. These observations are discussed with respect to known aspects of the ecology of some of the organisms, and provide a background for experimental tests of some hypotheses raised about the structure of this community.

Effects of substratum on the recruitment and development of an intertidal estuarine fouling assemblage

The effect of four substrata (concrete, plywood, fibreglass and aluminium) on the recruitment of species and development of an intertidal estuarine fouling assemblage was examined in Quibray Bay of Botany Bay, New South Wales, Australia. Many species, including the oyster Saccostrea commercialis (Iredale & Roughley) and the barnacles Hexaminius sp., Balanus amphitrite Darwin and Balanus variegatus Darwin, recruited in greater numbers on concrete or plywood surfaces than on fibreglass or aluminium. As a result, patterns of change in the number of species through time were dependent on the substratum. Multivariate analyses indicated that assemblages on different substrata were significantly different after 1 or 2 months of submersion, but became more similar after longer periods (up to 4–5 months). The reasons for this gradual conformity varied depending on the season of submersion and the composition of the species settling in a particular season. The results of this study indicated that the nature of the substratum can affect both initial colonisation of particular species and the development of the assemblage over time. Because the effect of substratum varies with the period of submersion, comparisons of various studies on fouling assemblages using different natural and artificial substrata and for varying lengths of time are likely to be very difficult.

An experimental evaluation of competition between three species of intertidal prosobranch gastropods

SummaryPrevious investigations have shown that competition for space among sessile organisms in rocky intertidal communities is often reduced by predation or harsh environmental factors. Grazing gastropods are unlikely to compete for space, but at high densities might compete for food, unless some factor, such as predation, reduced the densities. The coexisting species of herbivourous gastropods on rock-platforms in New South Wales are not, however, subject to high levels of predation on shores sheltered from waveaction. In this study, three of these species were caged at densities from the natural, to 4 times the natural density on the shore, in different combinations of species, to investigate their competitive interactions. All three species, Nerita atramentosa, Bembicium nanum and the limpet Cellana tramoserica, showed increased mortality and reduced weight at increased density, over 100- or 200-day periods. The effect of high density on Cellana was greater than on Nerita or on Bembicium. In addition, Nerita was competitively superior to the other two species. Cellana, at high densities, adversely affected Bembicium. Nerita was not affected by high densities of either of the other two species, and Cellana was not affected by Bembicium.Under entirely natural conditions, the effects of increased density of Cellana on the mortality and tissue-weight of Bembicium could not occur, because of the high rate of mortality of Cellana when at increased density of its own species. The other effects of increased density of snails would, however, occur. Thus, there can be regulation of numbers of snails because of high densities of their own or other species on the shore.The supply of benthic, microalgal food is proposed as the limiting resource for which the species compete. Hypotheses are proposed to account for the mechanisms by which the three species acquire different amounts of the resource. These are based on aspects of the feeding biology of the snails.The continued coexistence, in intertidal regions, of Cellana, which shows the highest rate of mortality due to members of its own species, with the competitively dominant Nerita, which increases the mortality of Cellana, is apparently due to three factors. These are:(i)the presence of subtidal refuges for breeding populations of Cellana,(ii)regular spatial dispersion of Cellana which would probably decrease intraspecific competition for food, and(iii)the high variability in space and time of recruitment of planktonic larvae of both Cellana and Nerita. This last factor makes it unlikely that high densities of Nerita could occur on all shores in every year. Cellana could always recolonize any area where its density had previously been reduced, and thus, cannot be excluded by competitive interactions. Competitive interactions at high densities of gastropods can therefore cause reductions in the number of each species present on a shore. They cannot, however, lead to exclusion of any species or alter the composition of the community of herbivores on the shore.The difference between competition for space by sessile intertidal organisms, and competition for food by gastropods which graze on microalgae is discussed with respect to the structure of intertidal communities. In the former case, competitively dominant species must be dislodged from the resource, space, by disturbance (e.g. predation or hazards) before recolonization by inferior competitors can occur. In the latter situation, the food resource is renewable without further perturbation of the community, and the competitively dominant species could never consume it completely over a wide enough area, and for a sufficient length of time, to eliminate totally another species.

The effects of tidal height, wave-exposure, seasonality and rock-pools on grazing and the distribution of intertidal macroalgae in New South Wales

Abstract The effects of grazers (mostly gastropods), height on the shore, wave-exposure, season of the year and the presence of shallow rock-pools on the abundance of intertidal macroalgae were examined on shores at Cape Banks (Botany Bay). At the beginning of each of the four seasons, experimental plots with and without grazers were cleared at four heights on three shores, of increasing exposure to waves, The colonization and growth of algae in these plots were monitored (by measurement of per cent cover and dry wt) for approximately the next 3 months in each season. In grazed plots, foliose algae only grew at the lowest levels on the shores. They were more abundant where wave-action was greater, and during the cooler periods of the year, when growth of the plants was enhanced. Higher on the shore, there was a positive correlation between algal cover in grazed plots and the amount of rainfall during the previous 10 days. In all seasons, there was much greater colonization of foliose algae where grazers were excluded. There was greater algal growth at lower levels on the shore, and where wave-action was stronger. Less algae grew in sheltered areas during warmer times of the year. The major seasonal difference found was the more rapid growth and occupancy of the rock by algae during the cooler seasons of the year. Experimental rock-pools were colonized more rapidly at lower levels on the shore, and during the winter. There was no difference between pools and control (non-pool) areas during winter. During summer, however, there was a greater per cent cover and biomass of algae in pools from which grazers had been excluded than in similar control areas. The results can be interpreted as being due to the greater survival and more rapid growth of algae under conditions of increased moisture, decreased emersion and decreased temperatures and light regimes during low tide (i.e. when physical stresses were reduced). These physical factors were, however, less important to the distribution of the algae than were the effects of grazers. Although few algae were present in any experimental plot, the number of species of algae per plot was considerably reduced in grazed areas. The results confirm that the patterns of vertical distribution and abundance of algae on rock-platforms in New South Wales are primarily the result of the activities of grazers. All algae in the present study were capable of living higher on the shore than they were normally found. Much of the variation along a gradient of wave-exposure, from season to season, and small-scale variation from place to place at any time can be explained by the complex interactions between the activities of grazers, and the effects of variations in the physical environment that influence the recruitment, survival and growth of the algae.