LJournal of Experimental Marine Biology and Ecology,235 (1999) 45–53

Effects of trampling by humans on animals inhabitingcoralline algal turf in the rocky intertidal

a b ,*Pam J. Brown , Richard B. TayloraLeigh Marine Laboratory, University of Auckland, P.O. Box 349, Warkworth, New Zealand

bInstitute of Marine Sciences, University of North Carolina at Chapel Hill, 3431 Arendell Street,Morehead City, NC 28557, USA

Received 4 September 1996; received in revised form 10 August 1998; accepted 17 August 1998

Abstract

This paper investigates the effects of trampling by humans on the fauna associated witharticulated coralline algal turf. Patches of intertidal turf in a low-use area of the Cape Rodney toOkakari Point Marine Reserve (in north-eastern New Zealand) were experimentally trampled over5 days at three levels that fell within those measured in a part of the reserve subject to heavy

5visitor use. Two days after trampling ended there were | 2 ? 10 individual macrofauna ( . 5002

mm) per m in control plots, but densities declined with increasing trampling intensity in thetreatment plots, and were reduced to 50% of control values at the highest trampling intensity.Densities of five of the eight commonest taxa were negatively correlated with trampling intensity,with polychaetes being particularly susceptible to low levels of trampling. Three months aftertrampling ended densities of all taxa had returned to control values, with the exception ofpolychaetes. Reductions in animal densities are tentatively attributed to the loss of turf andassociated sand caused by trampling, rather than direct destruction of the organisms. Given thelikely importance of these abundant and productive animals in the rocky reef ecosystem, and theirvulnerability to low levels of trampling by humans, we conclude that the effective management ofmarine protected areas may necessitate total exclusion of humans in some cases. 1999Elsevier Science B.V. All rights reserved.

Keywords: Algae; Coralline turf; Epifauna; Human impact; Intertidal; New Zealand; Marinereserve; Trampling

1. Introduction

Recent studies have shown that trampling by humans can reduce abundances of rocky

*Corresponding author. Tel.: 1 1 252 7266841; fax: 1 1 252 7262426; e-mail: rbtaylor@mail.clis.com

0022-0981/99/$ – see front matter 1999 Elsevier Science B.V. All rights reserved.PI I : S0022-0981( 98 )00186-5

46 P.J. Brown, R.B. Taylor / J. Exp. Mar. Biol. Ecol. 235 (1999) 45 –53

intertidal organisms such as macroalgae, molluscs and barnacles (Beauchamp andGowing, 1982; Ghazanshahi et al., 1983; Povey and Keough, 1991; Brosnan andCrumrine, 1994; Keough and Quinn, 1998). Most of this research has focused on largeconspicuous organisms, but smaller cryptic animals also merit attention due to their greatabundance (Hicks, 1986), high productivity (Edgar and Moore, 1986), and importanceas food for higher trophic levels (Coull and Wells, 1983; Jones, 1988). In the rockyintertidal highest densities of small animals are typically found on macroalgae (Gibbonsand Griffiths, 1986), which provide the epifauna with a range of resources, such as foodand a refuge from predation and desiccation (Gibbons, 1991). Abundances of epifaunaare therefore likely to be reduced where trampling by humans reduces the biomass oftheir host plants.

Coralline algal turfs are a dominant feature of many subtropical and temperate rockyshores (Johansen, 1981). The turf matrix is typically inhabited by high densities of smallmobile and sessile animals (e.g. Chapman, 1955; Dommasnes, 1969; Hicks, 1971).Moderate levels of trampling by humans does not reduce the area occupied by corallinealgal turf, but it does reduce the height of the turf (Povey and Keough, 1991), thusaltering the habitat available for epifauna. In this study we examine the effects oftrampling by humans on the macrofauna inhabiting coralline algal turf within a popularmarine reserve in north-eastern New Zealand.

2. Methods

This study was conducted in articulated coralline algal turf on the intertidal reef flat atKnot Rock, a low-use part of the Cape Rodney to Okakari Point Marine Reserve, innorth-eastern New Zealand (368179S, 1748489E). The reserve receives up to 3000visitors per day during the summer, and large numbers of these people explore rockyintertidal regions adjacent to the main public entry point [Brown and Creese, inpreparation]. During the course of this study few visitors were observed several hundredmeters away on the intertidal flats at Knot Rock. The turf there formed apparentlyhomogeneous patches of several square meters in extent and | 5 mm in height. Four

20.09 m quadrats were placed randomly within each of three patches, and the cornersmarked with small plastic disks nailed into the rock. Within each patch the quadrats weretrampled with a total of 0 (control), 10, 50 or 150 footsteps. These trampling levels weredesigned to fall within the number of footsteps estimated to occur during the 2-monthpeak visitor season (January–February) at various parts of the Channel Reefs, an area ofthe marine reserve subject to heavy use by the public. At three sites on the Channel

2Reefs remote video footage revealed average trampling rates of 45–215 footsteps /m /h,2equivalent to 16–77 footsteps /0.09 m quadrat /4 h low tide period [Brown and Creese,

in preparation]. It is clear therefore, that our experimental trampling intensities were wellwithin the range experienced by some regions of nearby shore, as our maximum totalnumber of footsteps (150) would be reached in only 2 days during the peak visitorseason at some parts of the Channel Reefs. Trampling commenced on September 221995, with quadrats trampled during low tide at 0, 2, 5, or 30 steps per day for 5 days.

P.J. Brown, R.B. Taylor / J. Exp. Mar. Biol. Ecol. 235 (1999) 45 –53 47

The trampler wore rubber-soled shoes and weighed | 60 kg. Four turf samples weretaken from each quadrat on September 29, 1995, 2 days after trampling ended. Samplingwas repeated 3 months (92 days) later on December 28 1995, to determine whether theepifaunal populations had recovered from trampling. Samples were collected by cuttingthrough the coralline algae to the rock surface with an open-ended plastic cylinder

2(internal diameter 5 42 mm, area 5 13.9 cm ). The coralline turf within was collectedusing a metal scraper, with care taken to ensure that all coralline turf and underlyingsediment was removed down to the basal crust or bare rock. This method collects at least95% of meiofaunal individuals associated with coralline turf (McCrone, 1987), andappeared to be at least as effective for the larger animals sampled in the present study(we noticed no remaining animals on the rock that had been scraped clean, and theepifauna had no opportunity to escape following placement of the sampling cylinder).Samples were preserved in 5% formalin in seawater. They were subsequently rinsed on a500-mm mesh sieve, and the animals retained were identified to coarse taxonomic levelsand counted under a stereo microscope.

An additional experiment was run in August 1996 to assess the effects of trampling onphysical attributes of the turf matrix that are likely to be important to epifauna. Wemeasured turf height, biomass, and sand content, all of which could potentially affect theamount of space available for epifauna to inhabit within a given area of rock surface.The experimental site, protocol, and sampling were as described above except thattrampling was carried out over 3 days instead of 5 (with the same total number of steps)from August 12–14 1996, only three samples were taken from each quadrat, andpost-trampling samples were only collected once (2 days after the cessation oftrampling). Samples were preserved in 70% ethanol, then transferred to a beaker forremoval of soft-bodied animals and detritus by decanting in freshwater. The leftovermaterial comprised turf fragments and sand, along with a few large gastropods andpolychaetes that were removed and discarded. The turf and associated sand was washedon a 1-mm mesh sieve that retained the turf, but allowed the sand to pass through, to betrapped on a 100-mm mesh sieve below (following McCrone, 1987). Sand and turf weredried separately to constant weight at 808C.

One-way nested analysis of variance (ANOVA) was used to examine the effects oftrampling on densities of total animals, densities of the eight commonest taxa (averagedacross all trampling levels and both sampling occasions), and physical characteristics ofthe turf (factor 5 trampling intensity (fixed), samples nested within quadrats). IfCochran’s test detected significant heterogeneity of variances (a 5 0.05) data were log(X 1 1) transformed prior to analysis. Since we predicted that trampling would have anegative impact on epifaunal densities (see Section 1), it was possible to increase thepower of the (non-directional) ANOVAs by incorporating information on the ranks ofthe means. Following Rice and Gaines (1994a, 1994b), directional P values werecalculated from the test statistic r P , the product of (1) Spearman’s rank correlations c

between the observed ranking of the means and the expected ranking given thealternative hypothesis (i.e., densities: control $ 10 $ 50 $ 150, with at least oneinequality), and (2) the complement of the P value from the ANOVA. Data for eachsample date were analyzed separately.

48 P.J. Brown, R.B. Taylor / J. Exp. Mar. Biol. Ecol. 235 (1999) 45 –53

3. Results

Total numbers of animals in the control plots ranged from 340662 (mean61 S.E.)2individuals per 13.9 cm sample at the start of the experiment to 288624 3 months later

5when the experiment was terminated. These numbers are equivalent to 2.1–2.5 ? 102individuals /m . The natural epifaunal assemblage (in the control plots at the first

sampling) was dominated by small gastropods [39.863.2% of total individuals (mean61S.E.)], polychaetes (26.863.3), bivalves (15.562.4), gammarid amphipods (7.163.4),nematodes (3.061.5), isopods (2.361.3), anemones (1.960.8), and ostracods(1.560.5). Together these eight taxa comprised 97.9% of total individuals.

There was a strong negative effect of trampling on total animal densities 2 days afterexperimental trampling ceased (P 5 0.004), with densities at the highest tramplingintensity declining to 50% of control values (Fig. 1). There was no apparent effect oftrampling on total animal densities after 3 months (P 5 0.18, Fig. 1).

The effects of trampling on the eight most abundant taxa are shown in Fig. 2. The firstpost-trampling survey (at 2 days) found that trampling caused statistically significant(a , 0.05) reductions in densities of gastropods, polychaetes and ostracods, withdensities at the highest trampling intensity being 54, 44 and 37% of control values forthe three taxa, respectively. Polychaetes appeared to be particularly vulnerable totrampling, with a substantial decline in density evident at the lowest trampling level.Bivalves (P 5 0.09) and nematodes (P 5 0.10) also tended to be negatively affected bytrampling. In contrast, densities of gammarid amphipods, anemones, and isopods wererelatively unaffected by trampling (P $ 0.15), although densities of gammarid am-phipods and isopods were lowest at the highest trampling intensity. By the secondsurvey (3 months after trampling) densities of animals in the trampled quadrats hadreturned to near control values for all taxa except polychaetes, which still showed astrong negative effect of trampling (P 5 0.01). This difference in polychaete densitiesamong treatments was not present in samples collected 1 day prior to experimentaltrampling (data not shown).

Two days after trampling ended (in a separate experiment), turf dry weight and sand

Fig. 1. Densities of total macrofauna 2 days and 3 months after cessation of experimental trampling ofintertidal coralline turf.

P.J. Brown, R.B. Taylor / J. Exp. Mar. Biol. Ecol. 235 (1999) 45 –53 49

Fig. 2. Densities of eight commonest epifaunal taxa 2 days and 3 months after cessation of experimentaltrampling of intertidal coralline turf. Taxa are ranked in decreasing order of abundance.

dry weight showed strong declines with increasing trampling intensity (P 5 0.005 forboth), and turf height showed a similar trend (P 5 0.08) (Fig. 3). The magnitude of thedeclines in these physical variables (values at the highest trampling intensity were41–53% of controls) were comparable to the magnitude of the declines in abundance ofthe taxa most affected by trampling (37–54%).

50 P.J. Brown, R.B. Taylor / J. Exp. Mar. Biol. Ecol. 235 (1999) 45 –53

Fig. 3. Turf height, turf dry weight, and sand dry weight 2 days after cessation of experimental trampling ofintertidal coralline turf. Bars represent means 1 1 S.E.

4. Discussion

5Animals . 500 mm were abundant within the intertidal coralline turf ( | 2 ? 102individuals /m ), but experimental trampling at conservative levels caused immediate

declines in densities of total animals and most common taxa (first measured 2 days aftertrampling ceased).

There are several ways in which trampling may reduce densities of turf-dwellinganimals. The most obvious and direct effect would be the crushing impact of thefootsteps. However, most of the taxa are highly mobile, and should be able to recolonizetrampled patches within hours or days (Sherman and Coull, 1980; Billheimer and Coull,1988), so any short-term reduction in densities should have been rapidly compensatedfor by immigration, at least on the spatial scale of our experiments. Moreover, if thedirect impact of trampling determined subsequent community composition we wouldhave expected the vulnerability of individual taxa to be related to their morphologies, but

P.J. Brown, R.B. Taylor / J. Exp. Mar. Biol. Ecol. 235 (1999) 45 –53 51

this was not always the case. For example, soft-bodied anemones did not appear to beaffected by trampling, but hard-bodied gastropods did. It is more likely that the effectsof trampling were indirect, through changes caused to the turf itself.

In our study trampling reduced the height of the turf by up to 50%. Similar effects ofphysical damage have been found for trampled turf on an Australian shore (Povey andKeough, 1991), and for wave-battered turf on a Norwegian shore (Dommasnes, 1968).Our data show that the height reduction caused by trampling was due to loss of planttissue, not compression. The consequent loss of colonizable habitat is likely to result inlower epifaunal densities, due mainly to the dependence of the animals on their hostplants for food and shelter (see reviews in Edgar and Moore, 1986; Hicks, 1986;Gibbons, 1991). Most seaweed epifaunal populations appear to be limited by theirperiphytal or detrital food supply (Edgar, 1993), which would be depleted in trampledturf due to reduction of plant surface area from which to graze periphyton (Edgar, 1993),and lower quantities of detritus trapped by the thallus matrix (Hicks, 1986). Corallineturf also traps large amounts of sandy sediments (Hicks, 1986). In the present study, theaverage dry weight of sand in the control plots was nearly three times that of the turfitself, which probably explains why coralline turf harbours taxa such as bivalves, whichare more characteristic of sedimentary than phytal habitats. Densities of such taxa mightbe expected to decline following the reductions in sand caused by trampling (Fig. 3), butparadoxically the bivalves were in fact less affected by trampling than many other taxa(Fig. 2). In trampled turf there will also be a reduction in shelter afforded from solarradiation, predation (Coull and Wells, 1983), wave action (Dommasnes, 1968), anddesiccation (Gibbons, 1991). It is also possible that fewer passively drifting animalswould be captured in a turf mat that had its height reduced by trampling (Dean andConnell, 1987). Further manipulative experiments would be required to determine therelative importance of these various mechanisms, which may vary seasonally. If solarradiation and desiccation are important agents of epifaunal decline in trampled turf thenthe animals would be most vulnerable to trampling during the summer, which is alsowhen visitor numbers are highest.

Since biomasses of many other macroalgal species are also reduced by trampling, it ishighly likely that animals inhabiting their fronds will also be detrimentally affected bytrampling. In our study we did not consider meiofauna (animals passing through a500-mm mesh, but trapped on a 63-mm mesh), but they are likely to be more abundantthan macrofauna by at least an order of magnitude in the turf (Gibbons and Griffiths,1986), and are also likely to be negatively affected by reduction of plant biomass due totrampling, for the reasons outlined above.

Three months after trampling ended it was found that densities of total animals, andall taxa except polychaetes, had returned to near control values. Our experimental

2trampling was conducted in 0.09 m quadrats surrounded by patches of relatively naturalcoralline turf. This turf harboured dense populations of animals, which represented alarge pool of potential recolonizers. However, in high-use areas where the entire reef istrampled by large numbers of people this pool may be severely reduced, increasingrecovery time. Time taken for the epifaunal assemblage to fully recover probablydepends ultimately on the recovery rate of the turf itself. Coralline algae grow slowlycompared to other seaweeds (Littler and Littler, 1980) and may not fully recover before

52 P.J. Brown, R.B. Taylor / J. Exp. Mar. Biol. Ecol. 235 (1999) 45 –53

the next visitor season, especially if low levels of trampling by visitors retard itsdevelopment in the interim.

Small mobile invertebrates have high production:biomass ratios (Edgar and Moore,1986) and are extremely abundant on intertidal macroalgae (Gibbons and Griffiths,1986). Common taxa such as amphipods and isopods are major prey items for juvenileand adult fish of many species (Choat and Kingett, 1982; Coull and Wells, 1983; Jones,1988), as well as some decapods (Dean and Connell, 1987), so it is likely that theremoval of a substantial proportion of epifauna from the intertidal by trampling willhave consequences for higher trophic levels.

A function of marine protected areas is to safeguard resident flora and fauna from theactivities of humans. Within such reserves the collection of animals and plants istypically prohibited, but there is normally no restriction on public access, suggesting thatmanagers fail to recognise more subtle impacts of humans such as trampling. Given thepotentially serious implications of damaging an abundant and productive assemblage ofanimals such as the turf-dwelling epifauna, along with the larger organisms alsopotentially affected, the effects of trampling by humans clearly deserve consideration incoastal management plans. This is particularly critical for areas of coastline that areintended to be maintained in ‘‘natural’’ condition for the purposes of conservation orscientific study. To meet these goals it may be necessary to completely restrict humansfrom some areas, since even relatively low levels of trampling can severely damagemany rocky intertidal organisms (Povey and Keough, 1991; Brosnan and Crumrine,1994 and this study).

Acknowledgements

We thank R. Cole, R. Creese and the two referees for their comments on themanuscript. We thank the New Zealand Department of Conservation for funding theproject (Grant 1947), and for permitting us to conduct experiments within the CapeRodney to Okakari Point Marine Reserve.

References

Beauchamp, K.A., Gowing, M.M., 1982. A quantitative assessment of human trampling effects on a rockyintertidal community. Mar. Environ. Res. 7, 279–293.

Billheimer, L.E., Coull, B.C., 1988. Bioturbation and recolonization of meiobenthos in juvenile spot (Pisces)feeding pits. Estuarine Coastal Shelf Sci. 27, 335–340.

Brosnan, D.M., Crumrine, L.L., 1994. Effects of human trampling on marine rocky shore communities. J. Exp.Mar. Biol. Ecol. 177, 79–97.

Chapman, G., 1955. Aspects of the fauna and flora of the Azores.VI. The density of animal life in the corallinealga zone. Ann. Mag. Nat. Hist. 8 (Ser. 12), 801–805.

Choat, J.H., Kingett, P.D., 1982. The influence of fish predation on the abundance cycles of an algal turfinvertebrate fauna. Oecologia 54, 88–95.

Coull, B.C., Wells, J.B.J., 1983. Refuges from fish predation: experiments with phytal meiofauna from the NewZealand rocky intertidal. Ecology 64, 1599–1609.

P.J. Brown, R.B. Taylor / J. Exp. Mar. Biol. Ecol. 235 (1999) 45 –53 53

Dean, R.L., Connell, J.H., 1987. Marine invertebrates in an algal succession. III. Mechanisms linking habitatcomplexity with diversity. J. Exp. Mar. Biol. Ecol. 109, 249–273.

Dommasnes, A., 1968. Variations in the meiofauna of Corallina officinalis L. with wave exposure. Sarsia 34,117–124.

Dommasnes, A., 1969. On the fauna of Corallina officinalis L. in western Norway. Sarsia 38, 71–86.Edgar, G.J., 1993. Measurement of the carrying capacity of benthic habitats using a metabolic-rate based

index. Oecologia 95, 115–121.Edgar, G.J., Moore, P.G., 1986. Macro-algae as habitats for motile macrofauna. Monograp. Biol. 4, 255–277.Ghazanshahi, J., Huchel, T.D., Devinny, J.S., 1983. Alteration of southern California rocky shore ecosystems

by public recreational use. J. Environ. Man. 16, 379–394.Gibbons, M.J., 1991. Rocky shore meiofauna: a brief overview. Trans. Royal Soc. South Africa 47, 595–603.Gibbons, M.J., Griffiths, C.L., 1986. A comparison of macrofaunal and meiofaunal distribution and standing

stock across a rocky shore, with an estimate of their productivities. Mar. Biol. 93, 181–188.Hicks, G.R.F., 1971. Checklist and ecological notes on the fauna associated with some littoral corallinacean

algae. Bull. Natural Sci. 2, 47–58.Hicks, G.R.F., 1986. Meiofauna associated with rocky shore algae. In: Moore, P.G., Seed, R. (Eds.), The

Ecology of Rocky Coasts. Hodder and Stoughton, London, pp. 36–56.Johansen, H.W., 1981. Coralline Algae, A First Synthesis. CRC, Boca Raton, FL.Jones, G.P., 1988. Ecology of rocky reef fish of north-eastern New Zealand: a review. NZ J. Mar. Freshwater

Res. 22, 445–462.Keough, M.J., Quinn, G.P., 1998. Effects of periodic disturbances from trampling on rocky intertidal algal

beds. Ecol. Appl. 8, 141–161.Littler, M.M., Littler, D.S., 1980. The evolution of thallus form and survival strategies in benthic marine

macroalgae: field and laboratory tests of a functional form model. Am. Natural. 116, 25–44.McCrone, A., 1987. Spatial and temporal variation of meiofauna associated with Corallina officinalis

Linnaeus. Unpublished M.Sc. thesis, University of Auckland, Auckland, New Zealand.Povey, A., Keough, M.J., 1991. Effects of trampling on plant and animal populations on rocky shores. Oikos

61, 355–368.Rice, W.R., Gaines, S.D., 1994a. Extending nondirectional heterogeneity tests to evaluate simply ordered

alternative hypotheses. Proc. Nat. Acad. Sci. USA 91, 225–226.Rice, W.R., Gaines, S.D., 1994b. The ordered-heterogeneity family of tests. Biometrics 50, 746–752.Sherman, K.M., Coull, B.C., 1980. The response of meiofauna to sediment disturbance. J. Exp. Mar. Biol.

Ecol. 46, 59–71.