Download - Constraints on body-size distributions: an experimental test of the habitat architecture hypothesis

Journal of Animal Ecology

2001

70

, 248–259

© 2001 British Ecological Society

Blackwell Science, Ltd

Constraints on body-size distributions: an experimental test of the habitat architecture hypothesis

REBECCA LEAPER*, DAVE RAFFAELLI*, CHAS EMES* and BRYAN MANLY†

*

Culterty Field Station, Department of Zoology, University of Aberdeen, Newburgh, Ellon, Aberdeenshire, AB41 6AA, UK; and

†

Department of Mathematics and Statistics, University of Otago, PO Box 56, Dunedin, New Zealand

Summary

1.

Holling (1992) has claimed that a range of mechanisms, including habitat architecture,may be responsible for discontinuities in body-size distributions across a broad range ofspatial and temporal scales.

2.

We tested this proposition in the marine benthos by manipulating habitat architecturedirectly. Specifically, we constructed artificial sediments (using glass beads) of uniformlarge or small particles, to change interstitial pore diameters at two estuarine sites.

3.

A combination of kernel estimation and smoothed bootstrap re-sampling showedthat there was a high and varaible degree of modality in body-size (1–5 modes) in theexperimental bead treatments and controls and no obvious evidence for a trough atorganism size 0·5–1 mm ESD.

4.

We propose that habitat architecture may not be as intimately related to body-sizepatterns as originally claimed, at least at smaller scales where experimental tests aretractable.

Key-words

:

body-size spectra, habitat discontinuity, kernel estimation, marine intertidal.


(2001)

70

, 248–259

Introduction

One of the best documented patterns in ecology is therelationship between abundance and body-size, describedfor a wide variety of taxa and habitats (see Blackburn &Gaston 1999 for a review). Most terrestrial studies haveexamined the allometric scaling of abundance withbody-size within taxonomic groups, within communitiesfrom defined areas or in global compilations of data formany taxa and habitats (e.g. Damuth 1981; Peters &Wassenburg 1983; Peters 1983b; Peters & Raelson 1984;Morse, Stork & Lawton 1988; Blackburn, Harvey &Pagel 1990; Marquet, Navarrete & Castilla 1990; Basset& Kitching 1991; Nee

et al

. 1991; Currie & Fritz 1992),while aquatic ecologists have examined the frequencydistributions of different body sizes across all taxa presentin a sample or community (e.g. Sheldon, Prakash &Sutcliffe 1972; Schwinghamer 1981; Peters 1983a; Sprules,Casselman & Shuter 1983; Gerlach, Hahan & Schrange1985; Griffiths 1986; Rodriguez & Mullin 1986; Strayer

1986). Recently, a number of studies have attemptedto bridge the gap between these two approaches (seeStrayer 1994; Cyr, Downing & Peters 1997a; Cyr, Peters& Downing 1997b; Leaper & Raffaelli 1999).

While consistent patterns emerge with respect totaxa, geography and trophic status (see Lawton 1990;Cotgreave 1993; Blackburn & Gaston 1994; Lawton1996; for reviews), there remains uncertainty over theunderlying mechanisms, and this whole area has beenrightly criticized for seeking

post hoc

explanations ofobserved patterns without experimental tests of hypo-theses (Blackburn & Gaston 1999). Holling (1992) hasargued that a range of mechanisms may be respons-ible for the observed body-size distributions, with dif-ferent mechanisms operating at different spatial andtemporal scales. He suggested that abrupt shifts inbody-size reflected, for example, in the ‘humpy’ body-size plots of North American mammals and birds, weredriven by the natural frequencies of particular environ-mental variables, such as habitat architecture (Holling1992).

It is hard to test such hypotheses at the landscapescales of many reported body-size patterns, but marinebenthic systems offer major advantages in this respect(Raffaelli & Moller 2000); they are relatively easy to

Correspondence: Dr Rebecca Leaper, Culterty Field Station,Department of Zoology, University of Aberdeen, Newburgh,Ellon, Aberdeenshire, AB41 6AA, UK. Tel: + 44 (0)1358 789631.Fax: + 44 (0)1358789213. E-mail: [email protected]

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manipulate and discontinuities in body-size spectraseem related to equivalent discontinuities in habitatarchitecture (Schwinghamer 1981). Specifically, thereare two troughs in the body-size plot at organism sizesof 8–16

µ

m and 0·5–1 mm ESD, consistent across arange of sediment grades and benthic environments.Schwinghamer (1981) suggested that this conservatismreflects discontinuities in the way that organisms usethe sediment habitat. Organisms less than a few micronsin size (bacteria) can live on the surface of individualparticles, while large macrofauna (0·5 mm to severalcm in size), perceive the sediment as a solid and eitherlive on it or burrow into it. Intermediate-sized species,the meiofauna (30

µ

m–0·5 mm), are constrained to aninterstitial life as they are too large to exploit particlesurfaces and too small to manipulate bulk sedimentproperties (Schwinghamer 1981).

These patterns in body-size and habitat architectureare consistent with Holling’s thesis, but occur at a muchmore tractable scale than the landscape-scale patternshe described and the hypothesis that habitat architec-ture underpins the benthic body-size spectrum, can beexamined relatively easily. Using an indirect approach,Raffaelli

et al

. (2000) examined the conservatism of thebody-size biomass spectrum by challenging with pertur-bations known to affect body-size, namely size-selectivepredation and organic enrichment. If the spectrum wassensitive to such challenges, then sediment architecturecould not define the location of the peaks and troughs.Raffaelli

et al

. (2000) found little evidence of treatmenteffects and they were thus unable to refute the habitat-architecture proposition. In the present paper, wedescribe a more direct test of the habitat-architecturehypothesis, where we manipulated sediment size ina controlled manner and recorded the effect on themeiofauna–macrofauna region of the spectrum. Specif-ically, we constructed artificial sediments of uniformlarge or uniform small particles, thereby creatingsediments with quite different interstitial (pore) spacediameters. If animal body-sizes are constrained by thesizes of habitat surfaces and pore space then we mightreasonably expect a shift towards larger body sizes inthe large particle treatment and towards smaller bodysizes in the small particle treatment. One further dif-ference between the present study and previous analysesis that all the data were collected at the same spatialscale; usually different-sized organisms are collectedat quite different spatial scales and scaled up to thesame area (e.g. Schwinghamer 1981; Gerlach, Hahan& Schrange 1985; Poff

et al

. 1993; Rasmussen 1993;Duplisea & Hargrave 1996; Ramsay

et al

. 1997; Duplisea1998; Raffaelli

et al

. 2000).

Materials and methods

The experiment was conducted at two sites

c

. 1 km apart,on the Ythan estuary, Aberdeenshire, approximately

20 km north of Aberdeen. The general characteristicsof the estuary and its mudflats have been described else-where (Baird & Milne 1981; Gorman & Raffaelli 1993).At the Snub (Ordnance survey grid reference 005283,and hereafter Site A) the sediment is coarse muddy-sand (median particle size

c

. 250

µ

m) and at the Sleekof Tarty (Ordnance survey grid reference 997281, andhereafter Site B) the sediment is finer, a muddy-sand(median particle size

c.

100

µ

m). Both sites supportedan invertebrate assemblage typical of undisturbedestuarine flats. At each site, nine blocks of three meshcylinders were dispersed over a 30

×

30-m area of homo-geneous mudflat. The cylinders were 8 cm in diameterand 7 cm depth and made from plastic mesh with anaperture of 10 mm, which allowed the free movementof invertebrates and water. The cylinders were open atthe bottom but fitted with a lid of the same mesh andfilled with artificial sediment (glass ballotini beads) ofspecified diameter, or natural sediment from the site.The empty cylinders were located within each blockand placed into similar-sized excavations in the sedi-ment so that the top of each mesh was approximately5 mm above the sediment surface. Within each of theblocks a cylinder was assigned randomly one of the fol-lowing treatments: beads of 1·5–2 mm median particlediameter (hereafter ‘large bead treatment’), beads of0·055–0·1 mm median particle diameter (hereafter‘small bead treatment’) and a core of undisturbed, naturalsediment transferred intact from the adjacent mudflat(hereafter ‘control’). The cylinders were filled flush withthe ambient sediment surface.

The experiment was started in August 1997 and ranfor 8 weeks. Previous studies by the authors prior tothe experiment and Hockin (1981) show that coloniza-tion of artificial bead sediments is rapid, with largenumbers of individuals present after only a few days.We are confident that the asymptote of the colonizationcurve would be reached by the end of the experimentalperiod. At the end of that period, each of the experi-mental units and the controls in six of the blocks weresampled with a 7-cm diameter corer to a depth of 7 cm,thereby ensuring that the edges of the units were notsampled. The material was fixed in 4% formalin withrose bengal. Water content and shear strength weremeasured from each experimental unit and the controlsin the remaining three blocks (Holme & McIntyre1984).

In the present study meiofauna and macrofauna wereextracted from the same core sample (7 cm diameter).The core-sample size we chose reflected a trade-offbetween the logistic constraints faced in processing largesamples for meiofaunal organisms, and the problemsof obtaining reliable density estimates of macrofaunausing very small corers. Based on previous studies by theauthors (and see Gorman & Raffaelli 1993), we are con-fident that a representative sample of both meio- andmacrofauna would be collected with a core this size.This sampling scale was also chosen to facilitate com-parison with a previous body-size study conducted on

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the Ythan (see Raffaelli

et al

. 2000). Our samplingprotocol contrasts with all previous studies (e.g.Schwinghamer 1981; Gerlach

et al

. 1985; Poff

et al

.1993; Rasmussen 1993; Duplisea & Hargrave 1996;Duplisea 1998; Raffaelli

et al

. 2000) where separatesampling protocols were adopted for the meio- andmacrofauna. The majority of these studies used a largercorer to sample macrofauna, which were then sieved overa 500–1000

µ

m mesh (a mesh traditionally used toseparate benthic organisms into meio- and macro-fauna (McIntyre, Elliot & Ellis 1984; Duplisea 1998).Meiofauna were sampled in a much smaller corer,extracted by a range of methods and numbers andbiomass scaled-up to the same area of the core used tosample the macrofauna. The trough proposed bySchwinghamer (1981) occurs in precisely this region,raising the possibility that the trough is an artefactof the sampling protocol (see also Griffiths 1998). Incontrast, our protocol was designed specifically toovercome this potential artefact. The large treatmentwas simply sieved over a series of meshes, 500 (whichretained the beads), 63 and 45

µ

m in size. The smalltreatment cores were elutriated with water in a flaskand sieved over a 63 and 45

µ

m mesh. To extract faunafrom the controls, we used Ludox™ extraction, follow-ing the method of Somerfield & Warwick (1996), andthe supernatant was decanted over a 45-

µ

m mesh. Wealso examined the remaining beads and sediment toconfirm the high efficiency (> 95%) of the extraction.Macrofauna were identified to species, except foroligochaetes, and meiofauna were identified to majortaxa. Because of the high densities of meiofaunalnematodes present, individuals from the entire core hadto be subsampled and numbers scaled appropriately.

Macrofauna were sized by measuring linear dimen-sions under a dissecting microscope, except for oligo-chaetes and the polychaete

Manayunkia aestuarina

which, along with meiofauna, were sized as plan areausing a Joyce–Loebl Magiscan image analyser. Body-size dimensions (linear and plan area) were con-verted to volume (

≡

biomass) using appropriatepublished geometric formulae, and/or empiricalrelationships based on liquid displacement in a grad-uated micropipette or scale plasticine models (seeHiggins & Theil 1988; Duplisea & Hargrave 1996;and Appendix 1).

It is usual practice to convert the volumes of individualsto the diameter of a sphere of an equivalent volume,equivalent spherical diameter (ESD) (Schwinghamer1981; Raffaelli

et al

. 2000). The spectrum can then berepresented as a plot of numbers (density) or biovolume(

≡

biomass) of individuals of different equivalent sphericaldiameters in the sample. The biomass or biovolume ofeach size class is simply the mean number of individualsin that size class multiplied by the volume of an indi-vidual in that size class. In this study we have used log

2

size classes in line with previous studies. Biovolume isexpressed as mm

3

. In the present study, body-size referseither to

µ

m or mm ESD.

At least four methods have been used to examine andmake comparisons between different shaped spectra;simple visual comparisons of plots where both axes arelogarithmic (Schwinghamer 1981), maximum likelihoodmethods (Warwick 1984), a Pareto model approach(Vidondo

et al

. 1997) and kernel estimation (Manly1996). The first three methods all have disadvantages(see Raffaelli

et al

. 2000), and here we used the kernel-estimation technique.

This technique permits the estimation of two import-ant characteristics of body-size spectra; the preciselocation of modes (and intervening troughs) and themost likely number of modes in the distribution (Manly1996). We used smoothed bootstrap re-sampling to seewhether the observed spectra were consistent with acontinuous null distribution of increasing number ofmodes (up to eight). The number of modes in theobserved distribution is consistent with the modelwhen the bootstrap test is not significant at the 5%probability level. The location of modes and (troughs)can then be defined. A full account of the method isprovided by Manly (1996). It should be noted that theassumptions underlying the statistical estimation ofthe number of modes in the distribution probably donot hold when the test is performed on average distri-butions ( i.e. the mean of the six replicates), or formanipulated distributions such as biomass spectra.For this reason, the number of modes in the spectra canonly be properly estimated statistically for the individ-ual replicates of the number body-size spectra.

Results

The pore diameters of the treatment sediments werecalculated as 0·02

µ

m (small), 0·8

µ

m ( large) and 0·1

µ

m(control site A), and 0·04

µ

m (control site B), using theequation provided by Crisp & Williams (1971). Watercontent was significantly different between treatmentsat site A, Kruskal–Wallis

H

= 2·7 d.f. = 2,

P

< 0·05,and site B Kruskal–Wallis

H

= 2·7 d.f. = 2,

P

< 0·05,where small bead treatments had the lowest water con-tent. Similarly, shear strength was significantly differentbetween treatments, site A, Kruskal–Wallis

H

= 2·7d.f. = 2,

P

< 0·05, and site B Kruskal–Wallis

H

= 2·7d.f. = 2,

P

< 0·05 (see Fig. 1). Small bead treatmentshad significantly higher shear strength and large beadtreatments significantly lower shear strength as com-pared to the control. We were therefore confident thatthe treatments differed with respect to their physicalstructure and properties.

-

With respect to the experimental bead treatments,there was no consistency between replicates in the


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most likely number of modes in the number body-sizespectra (Fig. 2 and Table 1). For all the treatments atboth the sites, there was no consistency (with treat-ments) in the number of modes in the distribution(Table 1), although the large bead treatment replicatesseem less variable overall than the small bead treatmentand control spectra in the location of the main ( largest)mode (Fig. 2).

Given the high degree of between-replicate variabil-ity in modality, it is not possible to compare rigorouslythe body-size distributions of large bead vs. small beadtreatments, since it is not obvious which peaks andtroughs should be compared. Notwithstanding theproblems of interpreting and comparing log-log plots,there seems to be no obvious evidence of treatmenteffects on the average body-size spectra at either site,either for numbers or biomass spectra (Figs 3 and 4).

Interestingly, our analysis also highlighted the greatvariability between replicates in the control (undis-turbed) sediment spectra (Fig. 2), and the lack of anyobvious meiofaunal–macrofaunal trough in the sizeregion 0·5–1 mm ESD, for both the number and bio-mass spectra (Figs 3 and 4). The significance of this isdiscussed below.

Between treatment comparisons of total numbersand biomass (Fig. 5), showed that control treatmentsat site A had significantly higher total numbers of indi-viduals [

F

(2,15) = 35·078,

P

< 0·01] compared to thebead treatments. The small bead treatment at site B hadsignificantly lower total biomass [

F

(2,15) = 17·049,

P

< 0·01] compared to both the large bead treatmentand control.

A total of 14 different taxa were identified (Table 2),and those that differed significantly between the treat-ments are shown in Fig. 6a,b. At site A there were sig-nificantly fewer individuals, relative to the controls, of

Manayunkia aestuarina

,

Pygospio elegans

,

Corophium

Fig. 1. Box and whisker plots of median (solid line) watercontent (n = 3) and shear strength (n = 3) of bead treatmentsand controls at site A (white boxes) and site B (grey boxes).(Boxes are the first and third percentiles and the bars representthe data range.)

Table 1. Results of the test of significance for the replicatespectra from the kernel density estimation and smoothedbootstrap re-sampling. h = smoothing constant used in thekernel estimation, m = the smallest number of modes forwhich the bootstrap test was not significant at the 5% level,P = level of significance for each distribution (mode number)

Treatment Replicate h m P

Large beads site A 1 0·167 1 0·0642 0·075 4 0·4373 0·104 3 0·2744 0·080 2 0·4975 0·124 2 0·1156 0·139 1 0·631

Large beads site B 7 0·099 3 0·3708 0·133 1 0·2269 0·216 1 0·105

10 0·072 2 0·56411 0·137 1 0·19912 0·103 2 0·446

Small beads site A 13 0·052 4 0·42014 0·115 1 0·32015 0·050 4 0·33616 0·136 1 0·36617 0·183 1 0·13618 0·105 2 0·229

Small beads site B 19 0·118 2 0·11520 0·091 1 0·12521 0·060 2 0·84322 0·094 3 0·16323 0·134 1 0·79024 0·156 1 0·055

Control site A 25 0·095 2 0·23326 0·048 4 0·63827 0·076 3 0·36328 0·096 1 0·06529 0·133 2 0·07230 0·046 5 0·315

Control site B 31 0·119 1 0·29132 0·085 2 0·27233 0·083 2 0·43934 0·056 5 0·31635 0·087 2 0·48636 0·143 1 0·434


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volutator

and nematodes in both bead treatments,fewer

Nereis diversicolor

and oligochaetes in the smallbead treatment and more

Hydrobia ulvae

in the largebead treatment.

At site B only

M. aestuarina

was less abundant inboth bead treatments, whilst

N. diversicolor

, oligocha-etes and foraminifera were less abundant in the smallbead treatment.

H. ulvae

and ostracods were moreabundant in the large bead treatment. All other taxarecorded at both sites (Table 2), showed no treatmenteffects.

At both sites, nematodes made up a larger propor-tion (up to 90%), of numbers and biomass at 1–1·45 mmin the controls, compared to the small and large beadtreatments Fig. 7a,b. Foraminifera contributed up to40% in numbers and biomass at 128–362

µ

m ESD inthe large (both sites), and small bead treatments (siteB), in comparison to the control, where they only con-tributed a maximum of 2%.

N. diversicolor

dominatedthe largest macrofaunal size classes (> 4·1 mm) in thecontrols and bead treatments, while

C. volutator

wasrelatively more abundant (between 40 and 90%), in thesmaller macrofaunal size classes (1–2·9 mm) in thesmall bead treatments at both sites, compared to 5–60% in the large bead treatments and the controls(Fig. 7a,b).

Table 2. Taxa recorded at sites A and B (+ present, – absent)

Taxon Site A Site B

Foraminifera + +Nematoda + +Oligochaeta + +Nereis diversicolor + +Pygospio elegans + +Capitella capitata – +Manayunkia aestuarina + +Ostracoda + +Harpacticoida + +Corophium volutator + +Carcinus maenas + +Hydrobia ulvae + +Macoma balthica – +Bivalvia + +

Fig. 2. The fitted distributions for the number spectra estimated by the kernel estimation and bootstrapped re-sampling. LA =large beads site A, LB = large beads site B, SA = small beads site A, SB = small beads site B, CA = controls site A, CB = controlsite B. Each line represents a replicate spectrum (six in each treatment). Both axes are scaled as log to base 10 of the original data(i.e. ESD mm). Density function = numbers of individuals per core.


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Fig. 3. Numbers body-size spectra of bead treatments and controls (means of six replicates). Figure legend as Fig. 2.

Fig. 4. Biomass body-size spectra of bead treatments and controls (means of six replicates). Figure legend as Fig. 2.


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Discussion

Our experiment was designed to change unequivocallythe architecture of the sediment habitat, such thathypotheses about its relationship with body-size distri-butions could be rigorously examined. The medianparticle diameter of the experimental treatments wasan order of magnitude larger or smaller than the ambi-ent sediment at our two chosen sites, and hence thepore diameters of the treatment sediments [calculatedusing the Crisp & Williams (1971) formula] were dif-ferent from both the control sites. We are confident thatthe most significant architectural characteristics ( i.e.sizes of particle surfaces and interstitial space) wereindeed changed by our treatments, because they wereprescribed

a priori

and these differences are reflected intheir water content and shear strengths. However, therewas no evidence that either treatment had consistenteffects on body-size spectra. Statistically rigorous esti-mates of the number of modes present in individualreplicates revealed marked variability, such that it wasnot sensible to test for treatment effects

per se

. Much ofthis variability may reflect heterogeneity in the abun-dance of individual taxa at the spatial scale of the rep-licate cores, many macrofaunal species and meiofaunalmajor taxa being patchy at a similar (6 cm diameter)scale on the Ythan (Lawrie, Raffaelli & Emes 1999).It seems unlikely that sediment-architecture hetero-geneity at this scale could be responsible for theobserved variability in the body-size spectra; however,since the two experimental treatments were homogene-

ous. The pattern described by Schwinghamer (1981),that there are two troughs in the body-size plot atorganism sizes of 8–16

µ

m and 0·5–1 mm ESD, con-sistent across a range of sediment grades and benthicenvironments, simply does not occur, at the scale ofthe individual core.

While our results provide no support for a relation-ship between habitat architecture and body-size spec-tra, they also provide no support for Schwinghamer’scontention of a well-defined trough at body-size of0·5–1 mm in the biomass spectrum. Although wewere unable to test formally for bimodality in themeiofaunal–macrofaunal body-size range of thebiomass spectrum, inspection of the spectra for beadtreatments and controls at both sites provides littlesupport for a trough (Figs 3 and 4). In his originalanalysis Schwinghamer (1981), overlaid biomass spectrafrom several localities and the

overall

impression is of atrough at around 0·5–1 mm (see Fig. 7). However, care-ful analysis on a site-by-site basis by the authors showsthat the existence of a trough is not convincing for allthe spectra, and for some of the spectra data are miss-ing from the trough area (Fig. 8). Other authors havealso found it difficult to replicate the pattern describedby Schwinghamer (1981). Thus Strayer (1986) wasunable to find evidence for an obvious meiofaunal–macrofaunal trough in freshwater sediments, as wereRamsay

et al

. (1997) working in marine, estuarine andfreshwater habitats, and Duplisea (1998) in the BalticSea. The only other studies that to our knowledge showevidence for a meiofaunal–macrofaunal trough arethose by Gerlach

et al

. (1985) in the Hegoland Bight,Rasmussen (1993) in freshwater lakes in Quebec andRaffaelli

et al

. (2000) on the Ythan, and then only fornumbers spectra. Clearly, the location of the putativemeiofaunal–macrofaunal trough is less obvious andless consistent than originally claimed.

The spectra derived in the present study were con-structed from analysis of linear or plan area measure-ments of individual organisms and the biovolumescalculated using the relationships detailed in Appendix 1.It could be argued that the use of different relation-ships to those used by Schwinghamer (1981), where ameiofaunal–macrofaunal trough has been reported,may have obscured the trough. This seems unlikely,since the same relationships and sizing protocols wereused by Raffaelli

et al

. (2000), where there is in factevidence of a trough (in the numbers spectra) consistentwith Schwinghamer’s claims. However, a potentially sig-nificant methodological difference between the presentstudy and most others involving marine benthic bio-mass spectra is in the sampling protocol for meiofaunaand macrofauna. The standard protocol is to takeseparate samples for these two major groups, given theoften order of magnitude difference between them inabundance and the amount of work required to processlarge samples for meiofaunal organisms. Macrofaunalsamples are sieved over a mesh a few hundred micronsin size and then their densities pooled with scaled-up

Fig. 5. Mean total numbers and biomass of individuals inbead treatments and controls (means of six replicates) at site A(open circles) and site B (closed circles). Error bars are 95%confidence intervals.


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estimates from the meiofaunal samples. In the presentstudy meiofauna and macrofauna were extracted fromthe same core (7 cm diameter), the same core size usedby Raffaelli

et al

. (2000) to sample macrofauna. Giventhat the densities of the most common macrofauna inthis study were similar to those reported for other studieson the Ythan (listed in Gorman & Raffaelli 1993), we areconfident that a representative sample of both meiofaunaand macrofauna was collected with a core this size.

Mesh size not only truncates the body-size distribu-tion at the aperture size used (which is undesirable inthe study of body-size spectra), but can strongly influ-ence density and biomass estimates; for example, largemesh sizes can severely underestimate juvenile andsmaller macrofauna taxa (see Schlacher & Wooldridge1996). In the present study the most commonly foundmacrofaunal species,

M. aestuarina

, typically had a

modal body-size of 250

µ

m ESD. If macrofauna hadbeen sampled separately and sieved over a 500-

µ

m mesh,the numbers and biomass of this taxon would havebeen substantially underestimated. Therefore, in studiesof community size-spectra, it is important to collect allthe data at the same spatial scale, since it is possible thatthe meiofaunal–macrofauanal trough seen in otherstudies may be emphasized by the protocols adopted(Griffiths 1998). We are also confident that the experi-ment ran for a sufficient length of time, given that num-bers and biomass in the treatment cores did not generallydiffer significantly from the controls.

With respect to the habitat-architecture hypothesis,the critical discontinuity is generated by the step shiftfrom an interstitial lifestyle to one where the sedimentmatrix is seen as a solid. Warwick (1984) has arguedthat there is little potential for intermediate body plans

Fig. 6. Mean densities of taxa in bead treatments and controls at (a) site A and (b) site B. (Error bars are 95% confidence limits,n = 6 and shaded bars are homogenous subsets).


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Fig. 6. Continued.

Fig. 7. Relative contribution of taxa to numbers and biomass (mean of six replicates). Figure legend as Fig. 2.


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Fig. 7. continued.

Fig. 8. Benthic biomass spectra for six sites in Nova Scotia after Schwinghamer (1981).


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in this size region, so that the trough represents a bot-tleneck in the benthic spectrum. However, in fine-grainedmuddy environments large nematodes and other ‘inter-stitial’ taxa are able to move through the sediment bysliding (Williams 1972) and the discontinuity betweenthe interstitial and sediment-matrix habitat may actu-ally no longer exist. Under such conditions, therefore,one might not expect to find a pronounced troughbetween meio- and macrofaunal taxa. In the presentstudy, this may certainly hold for the small bead habitatand possibly the controls. The latter are composed ofvery fine particles and a mixture of natural sedimentparticles, faecal pellets and an organic matrix which isextremely difficult to resolve quantitatively (Watling1991; Hallberg 1992) and probably not well character-ized by simple measures such as median particle size. Ifthis is correct, then only in large bead treatment mightwe expect to see a trough.

In conclusion, the most parsimonious explanationfor the difference in shape between the spectra pre-sented here and those of Schwinghamer (1981) or sub-sequent workers is that the meiofaunal–macrofaunalpart of the spectrum is not as conservative as originallythought and that under appropriate mixtures of thecomponents that comprise the sediment matrix, thediscontinuity between interstitial and a more solid sed-iment habitat may cease to exist and, with it, the meio-faunal–macrofaunal trough.

The implications of our results for Holling’s (1992)proposition are unclear. Holling’s body-size patternswere defined at large spatial scales (continental) andthe presence of peaks and troughs only broadly attrib-uted to similar frequencies in environmental variables.No formal test of associations between body-size andenvironmental variables was carried out, but Hollingdrew heavily on Schwinghamers’s benthic biomassspectra analyses to support his proposition. The datapresented here indicate that if such associations doexist at macro-scales, it is difficult to demonstrate them atsmaller scales where experimental tests are tractable.

Acknowledgements

We would like to thank Sue Way and Mark Emmersonfor help in the field, and Sandra Telfer for comments onearlier drafts of this manuscript. We would also like tothank two anonymous referees for the comments thatgreatly improved this manuscript. Scottish NaturalHeritage gave us permission to work on the Sands ofForvie and Ythan Estuary National Nature Reserve.Rebecca Leaper is supported by a NERC StudentshipGT/96/13/M.

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Appendix 1. Empirical relationships used to convert body-size dimensions to volume. L is the length of the organism (mm), A isthe area of the organism (mm2), Wt is the wet weight of the organism (mg) and V is volume of the organism (µL). All volumes wereconverted to ESD using a formula provided by Schwinghamer (1981), where volume (V ) expressed as (µL) and ESD as (mm)

Taxon L (mm) Wt (mg) V (µL)

Foraminifera A ^ 2·29Nematoda A ^ 2·29Oligochaeta A ^ 1·4Nereis diversicolor L ^ 2·899*83·8 Wt/specific gravityPygospio elegans A ^ 1·4Capitella capitata A ^ 1·4Manayunkia aestuarina A ^ 2·23Ostracoda A ^ 2·44Harpacticoida A ^ 2·35Corophium volutator L *0·2978 ^ 1·38Carcinus maenas Liquid displacementHydrobia ulvae A ^ 0·8485 L *0·851 ^ 1·91Macoma balthica A ^ 2·44Bivalvia A ^ 2·44

A: measured as plan area using image analysis; L measured using a dissecting microscope; Nereis diversicolor (width of the firstchaetiger); Corophium volutator (tip of the rostrum to the tip of the telson); Hydrobia ulvae (apex of the spire to the base).Wtcalculated from (1) empirical relationship relating L to dry weight (constant weight of animals dried at 70 °C) provided byChambers & Milne (1979), and (2) conversion to wet weight using a specific gravity of 1·05 provided by Ramsay et al. (1997).
