Role of colonization in spatio-temporal patchiness of microgastropods in coralline turf habitat

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Abstract

The ability of benthic macrofauna to disperse and colonize new habitats throughout their life may contribute substantially to small-scale patchiness in abundances in different habitats. Microgastropods in coralline turf on rocky shores in Australia are very patchy in abundance at different spatio-temporal scales. They therefore represent an ideal assemblage for testing hypotheses about processes of colonization. Patterns and rates of colonization of 10 species of microgastropods were investigated in one intertidal habitat (coralline turf) in Botany Bay, New South Wales, Australia, using artificial substrata, which are considered to be a good mimic of natural coralline turfs. The experiment was designed to test the hypotheses that (1) patterns (abundance of colonizing individuals) and mode (juveniles vs. adults) of colonization depends on the proximity of a patch to a potential source of dispersing colonists (i.e. patch of natural coralline turf), (2) different species show different rates of colonization, and (3) patterns of succession are not repeatable among different patches of natural algae. Seven different plots (natural patches of coralline turf) were randomly chosen in the area of study. Artificial units (called patches) were placed at different distances around each plot (within the plot and 0, 50 or 100 cm away from the edge). Samples were collected 6, 13, and 27 days after the experiment started. Colonization was rapid (i.e. within 6 days) for most species. Pattern (number of individuals) and mode of colonization (adults vs. juveniles) varied among algal plots. Most species responded differently across patches causing no consistent patterns of colonization. Furthermore, patterns of colonization of artificial units were not always synchronous with, or in the same direction as, changes in abundances in the nearest algal plots, which themselves showed no consistent spatio-temporal pattern.

Introduction

Over the past several years, many ecologists have turned their attention to understanding how ecological processes vary at different spatial and temporal scales (e.g. Dayton and Tegner, 1984, Barry and Dayton, 1991, Dayton et al., 1992, Levin, 1992, Thrush et al., 1996). Ecological communities are commonly affected by disturbances that vary in extent, intensity, and frequency. These disturbances consequently, can have effects that vary in spatial and temporal scale (Hall et al., 1994). Disturbances are often considered to play a central role in dynamics of assemblages by creating a mosaic of patches at different stages of recovery Van Blaricom, 1982, Underwood, 1999. To understand and model the functioning of mosaics of patches (e.g. Paine and Levin, 1981), one must understand the mechanisms and rates of arrival of new organisms into disturbed patches.

Although benthic marine research has emphasized species that colonize areas as planktonic larvae, individuals of many taxa disperse as adults and/or juveniles (e.g. Santos and Simon, 1980, Highsmith, 1985, Martel and Chia, 1991, Norkko et al., 2001). The ability of benthic macrofauna to disperse throughout their life may contribute substantially to species reacting to local heterogeneity of habitats (Günther, 1992). High rates of post-settlement movement are considered important in providing a mechanism for rapid dispersal and recolonization of patches by macrofauna, contributing to small-scale patchiness in different habitats (Cummings et al., 1995). Recent research has shown that some macrofauna and meiofauna are highly mobile as adults. Many benthic species undertake regular nocturnal excursions into the water column Ohlhorst, 1982, Howard, 1985 and defaunated sites often may be colonized within a few hours, days or weeks Sherman and Coull, 1980, Leber, 1985, Virnstein and Curran, 1986. In addition, transport of bedload and suspended load may move post-settlement juvenile and adult benthic stages of soft-bottom macrofauna, particularly bivalves and gastropods (e.g. Sörlin, 1988, Highsmith, 1985, Commito et al., 1995, Cummings et al., 1995, Norkko et al., 2001). It is now widely recognized that above-sediment movement by post-settlement macrofauna is an important process structuring soft-sediment systems and can have a significant influence on patterns of macrofaunal distribution and abundance Günther, 1992, Snelgrove et al., 1993.

Therefore, knowledge of the ability of macrofauna at different stages of their life cycles to colonize new habitats is generally important in determining responses of assemblages to disturbance. Experiments investigating colonization may provide useful information about rates of movement into unoccupied habitat Bell and Devlin, 1983, Howard, 1985 and can be used to measure distances over, which fauna can disperse.

Studies of colonization have primarily focused on macrofauna in soft-bottom communities (e.g. Sherman and Coull, 1980, Zajac and Whitlatch, 1982, Bell and Devlin, 1983, Virnstein and Curran, 1986, Thrush et al., 1996, Turner et al., 1997) or large components of the fauna on rocky intertidal habitats (e.g. McGuinness, 1988, Lagadeuc and Colbeaux, 1992, Hockey and Schurink, 1992, Davenport and Stevenson, 1998). To date, relatively little attention has been paid to the influence of colonization on the population dynamics of microfauna on intertidal rocky shores.

Microfaunal assemblages have great potential for measuring changes to biodiversity (Gee and Warwick, 1996) and assessing environmental impacts (Smith and Simpson, 1993). A diverse assemblage can be found in small patches of habitat under different environmental conditions and can develop in both natural and artificial habitats placed in different areas (Gee and Warwick, 1996). Coralline turfs (i.e. turfs composed of tightly packed upright branches of coralline algae, forming a stiff matrix that holds quantities of sand) are a common type of habitat on rocky shores in Australia. Microgastropods (i.e. gastropods with adult size <2 mm) are a common component of assemblage in algal turf. As their abundances are patchy at different spatial (Olabarria and Chapman, 2001a) and temporal scales (Olabarria and Chapman, 2002), they represent an ideal assemblage to test models of ecological processes, including colonization. Particularly, abundances of microgastropods vary largely at small spatial scale in coralline turf habitat (Olabarria and Chapman, 2001a). This variation may be caused by processes of recruitment and/or mortality (Underwood and McFadyen, 1983) or short-term dynamic patterns of immigration and emigration among patches of habitat (Barnes, 1998). Because coralline turfs range from beds of algae that extend over several hundreds of meters, to fragmented patches <0.25 m2 Stewart, 1982, Akioka et al., 1999, coralline turf is, therefore, an ideal system for evaluating the role of colonization in determining patterns of distribution in fragmented habitats.

Until now, studies on patch dynamics of soft-sediment (reviewed by Thrush et al., 1996) and intertidal rocky shores (reviewed by Sousa, 1985) have focused primarily on the influence of the size, shape, and location of the patch on colonization and changes in colonization overtime (i.e. succession) Virnstein and Curran, 1986, Farrell, 1991, Benedetti-Cecchi and Cinelli, 1994. For example, a patch's position with respect to various environmental gradients (tidal height, velocity of currents, degree of insolation) can influence greatly the mode and rate of colonization (e.g. Denley and Underwood, 1979).

To my knowledge, not much attention has been paid to the location of patches on succession of microfaunal assemblages in algal beds on rocky shores (but see Dean and Connell, 1987a, Dean and Connell, 1987b). In this study, colonization of artificial patches of turf by species of microgastropods that normally inhabit coralline turfs is documented. Habitat-mimics, such as artificial turf possess similar structural characteristics to natural habitat, but do not exhibit any of the biological characteristics of natural habitats. Various types of habitat-mimics have been used to test hypotheses about faunal assemblages associated with different habitats on rocky intertidal shores (e.g. Myers and Southgate, 1980, Davenport and Stevenson, 1998). Artificial patches of coralline turf provide a good mimic of natural algal turf and avoid potential artefacts associated with defaunating natural coralline turf to measure colonization and confounding effects, such as shape or size of patch because patches can be made to measure. These patches also accumulate sediment as the natural algal turf, but it is very dynamic over time (Kelaher, 2000). Moreover, artificial turfs are colonized by a similar suite of species as are found in natural habitats Bell and Hicks, 1991, Edgar, 1991.

The microgastropods used in this study represented different species within a range of families, with likely different life-history traits with respect to feeding modes, reproduction, development, mobility, and dispersal (Beesley et al., 1998). Life histories and the stage of the life cycle which disperses, can change rates or patterns of colonization (Smith and Brumsickle, 1989). For example, organisms that disperse over long distances may colonize small, isolated patches more efficiently than do individuals with limited dispersal ability (Sousa, 1984, Butler, 1991, but see Johannesson, 1988).

This experimental study was designed to test the hypotheses that (1) patterns (i.e. abundance of colonizing individuals) and mode of colonization (i.e. juveniles vs. adults) depend on the proximity of a patch to a potential source of dispersing colonists (i.e. a patch of natural coralline turf), (2) different species show different rates of colonization, and (3) patterns of succession (i.e. sequence of arrival of each species) are not repeatable among patches of natural coralline turf because of variability in physical and biological processes experienced by each patch.

Section snippets

Study area

The experiment was done in the Cape Banks Scientific Marine Research Area on the northern headland of Botany Bay, New South Wales, Australia (site described in Olabarria and Chapman, 2001a). The area (∼1500 m2) was orientated to the west with a slope of 30° and was semiexposed to wave-action. This intertidal rock platform had many patches of coralline turf, composed of tightly packed upright branches of coralline algae, primarily Corallina officinalis Linnaeus, forming a stiff matrix that held

Natural coralline turf

Five species, E. atropurpurea, E. rubrilabiata, P. g. gregaria, A. incidata and S. luteofuscus, were the most abundant and widespread across different plots of coralline turf. The abundance of each species varied across plots and through time. There was no clear temporal trend in abundances for most species, and patterns of change (increases or decreases) were not in the same direction in the different plots (Fig. 1a–b; illustrated by E. atropurpurea and S. luteofuscus; Time×Plot, F12, 21=2.29,

Discussion

The assemblages of microgastropods found in coralline turf are certainly not static (Olabarria and Chapman, 2002). Artificial turfs provide convenient, easily manipulated units to demonstrate that colonization of new habitat by microgastropods was rapid (i.e. within 6 days) for most species in most patches. The pattern (number of individuals) and mode (adults vs. juveniles) of colonization were generally independent of the proximity to a potential source of colonists, i.e. natural coralline

Acknowledgements

This research was supported by funds from the Australian Research Council, the Institute of Marine Ecology and the Centre for Research on Ecological Impacts of Coastal Cities. I am grateful to Sonia Monteiro, Elena Lazzarotto, David Blockley, Francesca Rossi for their help in the field and also to Grant Kaplan and Andrés Grigaliunas who helped with sorting in the laboratory. This paper also benefited from comments by Gee Chapman and Theresa Lasiak. [RW]

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