Effects of trampling by humans on animals inhabiting coralline algal turf in the rocky intertidal
Post on 14-Sep-2016
LJournal of Experimental Marine Biology and Ecology,235 (1999) 4553
Effects of trampling by humans on animals inhabitingcoralline algal turf in the rocky intertidal
a b ,*Pam J. Brown , Richard B. Taylora
Leigh Marine Laboratory, University of Auckland, P.O. Box 349, Warkworth, New ZealandbInstitute 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
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 ( . 500
2mm) 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
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: email@example.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.
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 (JanuaryFebruary) 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 45215 footsteps /m /h,2
equivalent to 1677 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 1214 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). IfCochrans 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) Spearmans rank correlations cbetween 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
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 2.12.5 ? 10
2individuals /m . The natural epifaunal assemblage (in the control plots at the firstsampling) 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 were4153% of controls) were comparable to the magnitude of the declines in abundance ofthe taxa most affected by trampling (3754%).
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.
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 presen...