JOURNAL OF

EXPERIMENTAL
MARINE BK)LOGY
Journal of Experimental Marine Biology and Ecology, AND ECOLOGY
ELSEVIER 202 (1996) 63-71

Relationships between body-size, species abundance and

diversity in marine benthic assemblages: facts or artefacts?
R.M. Warwick*, K.R. Clarke
Plymouth Marine Laboratory, Prospect Place, West Hoe, Plymouth PLI 3DH, UK

Received 4 May 1995; revised 5 January 1996; accepted 5 January 1996

Abstract

Plots of the number of species against body size for a wide range of undisturbed macrobenthic
assemblages on the European continental shelf have an approximately lognormal distribution, i.e.
there are more species of intermediate size than of either larger or smaller sizes. The total
abundance of all macrobenthic species combined also peaks at an intermediate size. The
abundance of individual species in relation to their average body size has a pattern similar to that
observed for terrestrial guilds of animals; high abundances are found in some intermediate sized
species but do not tend to be found in small or large sized species. This does not appear to be a
purely statistical consequence of the greater number of intermediate sized species in the
assemblage. We show (as these plots imply) that for a given number of individuals there are fewer
species of intermediate size but the possibility of sampling artefacts cannot be discounted here.
Plots of the number of species per 100 individuals against body-size are J-shaped, the minimum of
the curve corresponding to the size of animals for which retention on a 0.5 or 1 mm mesh sieve
starts to become inefficient and juveniles will pass through while adults are retained. Thus the real
number of species per 100 individuals at these small sizes will tend to be lower than the sample
data suggest. At larger body sizes there is a more or less linear increase in the curve (on a log/log
scale). This would be an inevitable consequence, in a sample of fixed area1 cover (e.g. a 0.1 m’
grab), of patterns of spatial dispersion scaling with organism size. This problem is of fundamental
importance for the sampling of biodiversity and could be examined by scale-stratified sampling
and model simulations.

Keywords: Macrobenthos; Body-size; Diversity; Abundance; Dispersion pattern

1. Introduction

Terrestrial ecologists have long been concerned with establishing generalities about

*Corresponding author.

0022-0981/96/$15.00 0 1996 Elsevier Science B.V. All rights reserved

PII SOO22-0981(96)00031-7
64 R.M. Warwick, K.R. Clarke I J. Exp. Mar. Bid. Ed. 202 (1996) 63-71

the numbers of species and individuals of different body-size that co-occur in natural
assemblages or geographic regions. Hutchinson and MacArthur (1959) found that for “a
given level of organisation” (e.g. birds, mammals) “the size distribution by species
appears to be a roughly symmetrical logarithmic distribution curve”, i.e. there are more
species of intermediate size than either larger or smaller species. More recently, it has
been shown that some intermediate sized species have high abundances, whereas smaller
or larger species do not (Lawton, 1989, 1990; Blackburn et al., 1993). Blackbum et al.
(1990) concluded that, at least in some cases, this may be a statistical effect resulting
from there being more intermediate-sized species in the communities they studied
(feeding guilds of birds and beetles). These relationships have not been so extensively
explored for marine organisms, although Fenchel (1993) illustrates truncated lognormal
distributions of species numbers against size for several groups of marine organisms
from Danish waters. Warwick (1984) sampled a number of sublittoral benthic com-
munities using various sample sizes, and sieve meshes ranging from 63 ,um to 0.5 mm,
and found a highly conservative pattern with two separate lognormal distributions,
corresponding to the traditional categories of meiofauna and macrofauna, with a trough
between them.
Marine macrobenthic communities comprise a range of species of different sizes, the
abundance and diversity of which are usually determined from samples of fixed
dimensions (typically 0.1 m2 grabs or box-cores), extracted from the sediment using
sieves of standard mesh-size (typically 0.5 or 1 mm). The sieve cut-off is obviously not
a sharp one, and there will be some small species whose juveniles will pass through the
sieve and whose adults will be retained on it, thus giving an underestimate of the true
number of individuals of that species present in the original sample. In the larger size
range, where all individuals including the smallest juveniles are retained on the sieve,
the sampling precision will vary with organism size if the dispersion patterns (patch
sizes) are related to organism size. Thus, all else being equal, we might expect to find
more species of large organisms than of smaller organisms for a given number of
individuals in a standard area sample, if the patch sizes of the larger species are bigger
than those of the smaller species: we will sample fewer whole patches and more small
parts of patches for the larger species.
The purpose of this paper is to examine the empirical relationships between body size,
species diversity and abundance for some macrobenthic assemblages from non-perturbed
situations, to see whether they conform to the patterns found in terrestrial communities
and to discuss which, if any, of these patterns are likely to be artefacts of the traditional
methods of sampling and extraction, rather than real attributes of the assemblages.

2. Methods

We have used all the published data available to us on undisturbed NE Atlantic shelf
macrobenthos in which both species abundance and species biomass data are provided;
the latter information is required in order to determine an average weight (proxy for
size) of each species in each study. Essentially this is the same data-base as was used for
our meta-analysis of disturbance effects (Warwick and Clarke, 1993), and our categori-
sation of non-perturbed situations is based on that analysis. These are:
 R.M. Warwick, K.R. Clarke I J. Exp. Mar. Bid. Ed. 202 (1996) 63-71 65

1. Station ‘Pierre Noire’ in the Bay of Morlaix. Dauvin (1984) (Annexe 3.2), sampled
this station on the Brittany coast of France on 21 occasions at roughly 3 month
intervals between April 1977 and February 1982, spanning the period of the oil spill
of the ‘Amoco Cadiz’ some 50 km west of the station in March 1978. Samples have
been aggregated into years and the immediate post-spill year (1978) was omitted
from this analysis.
2. Northumberland. A station off the coast of NE England (Buchanan and Warwick,
1974).
3. Carmarthen Bay. A station off S. Wales (Warwick et al., 1978).
4. Oslofjord. Samples were collected at 6 stations in Frierfjord/Langesundfjord (con-
necting to Oslofjord), Norway (Gray et al., 1988). Only stations A, E and G have
been used in this analysis, the other 3 suffering from the effects of seasonal anoxia.
5. Lochs Linnhe and Eil. A time series of samples from 1963 to 1973 in 2 western
Scottish sea-lochs, covering the period of commissioning of a pulp mill (Pearson,
1975). We have used averaged data for the pre-pollution years 1963- 1968.
6. Firth of Clyde. A transect of 12 stations sampled in 1983 on a west-east transect
across a sewage sludge dump ground off Garroch Head, Scotland (Pearson and
Blackstock, 1984). Only the terminal unpolluted stations 1, 11 and 12 have been used
(combined) here.
7. Kiel Bay. A station in Kiel Bay, Germany; mean of 22 sets of samples at the control
station for the experimental study of Amtz and Rumohr (1982).
8. Skagerrak. The 100 m station of Josefson (1981).

The units for the biomass determinations differ between studies (ash-free dry weight,
blotted wet weight, etc.) and we have individually scaled the size axis for each separate
study using the original units, rather than using potentially spurious conversion factors in
an attempt to produce a single standardised weight unit. Four types of plot have been
produced:

1. Number of species, expressed as a percentage of the total, against body weight class.
The latter is obtained from the observed mean body weight (B/A) for each species in
the sample, discretised into whole log, integers, so that the mid-point of each class is
2.72 times the weight of the previous class.
2. Log 1 + total abundance over all species in each weight class (weight axis as in 1).
3. Log abundance of each individual species against log body weight, with the weight
axis on a continuous (non-discretised) scale.
4. Log number of species per 100 individuals in each weight class (weight axis as in 1).

Plots 1 and 3 are presented for all studies but, for economy of space, only the Morlaix
data are presented as examples of plots 2 and 4.

3. Results

The numbers of species in each body-weight class (type 1 curves) approximate to a

66 R.M. Warwick, K.R. Clarke I J. Exp. Mar. Biol. Ecol. 202 (1996) 63-71

lognormal distribution (fitted curve) in all examples (Fig. l), except that in a few cases it
seems to be right-skewed even on log scales (Morlaix, Northumberland). The total
abundance of all species against body size (type 2 curves) takes the form of a
right-skewed unimodal curve in all cases (Fig. 2). In the Morlaix example, the mode
occurs at a log body weight of about - 1.5 or 0.22 mg ash-free dry weight. Larger or
smaller than this, organisms are less abundant. Type 3 curves also show that the most
abundant species are of intermediate size in all examples (Fig. 3). Although the position
of the upper bound of abundance is rather difficult to define, it does appear to decline
strongly with increasing body weight and also decline, less clearly, at the smallest body
weights (cf. Lawton, 1989, 1990), and in cases where ash-free dry weight units have
been used, as at Morlaix, the most abundant species are in the same size category as the
mode of the type 2 curves. These plots imply that, for a given number of individuals,
there are fewer species of intermediate size and type 4 plots confirm this (Fig. 4). These
are J-shaped with the fewest species per 100 individuals again occurring at a body
weight of about 0.22 mg dry weight in the Morlaix example.

4. Discussion

Numbers of species-size relationships and species abundance-size relationships for

entire macrobenthic assemblages in general seem to conform to the well-established
patterns for guilds of terrestrial animals. It is unlikely that the smaller number of
macrofauna species observed in the smaller size range is a processing artefact since the
lognormal pattern is the same as that found by Warwick (1984) for the macrofaunal
component of entire benthic metazoan communities, and for that study the numbers of
smaller species (measured as adult body size rather than average size) were determined
using smaller meshed sieves. Inspection of Fig. 3 suggests that the apparently higher
abundances of some intermediate sized species is not simply a statistical effect resulting
from there being more intermediate sized species in the community (Fig. 1). This is
confirmed by computation, from the type 3 graphs, of standard deviations of the log
abundances over the species in each weight class. These standard deviations measure the
spread of abundance values but remove any dependence of that spread on the number of
species in the weight class. The pattern which results is of decreasing standard deviation
as body weight increases, confirming the presence of a decreasing upper bound in the
type 3 plots.
The J-shaped plots of number of species per 100 individuals against body size (Fig. 4)
are arguably counter-intuitive and the possibility of sampling artefacts cannot be
excluded. They imply that, if we sieved a sample through a very coarse-meshed sieve
and examined 100 randomly chosen individuals retained on this sieve, we would get
more species than if we sieved the same sample through a finer sieve and examined 100
individuals. The J-shaped nature of this curve could be artefactual in two respects:

1. The upturn to the left, i.e. an increase in the number of species per 100 individuals
for the smallest animals could result from the sieve cut-off problem mentioned above.
The total number of individuals of each species is not efficiently sampled as the
 R.M. Warwick, K.R. Clarke I J. Exp. Mar. Biol. Ecol. 202 (1996) 63-71 67

Eli. LlNN"E

nCLvDE
LOCH LOCH
40
t t t

LOG BODY WEIGHT

Fig. I. ‘Type I ’ plots of number of species, expressed as a percentage of the total, against body weight class
for all examples listed in the text. The weight axis is discretised into integers on a log<, scale.
68 R.M. Warwick, K.R. Clarke I J. Exp. Mar. Biol. Ecol. 202 (1996) 63-71

LOG BODY WEIGHT

Fig. 2. Morlaix samples. ‘Type 2’ plots of log= (1 + total abundance) of all organisms (irrespective of species)
in each weight class for each year. The weight axis is discretised into integers on a log_ scale.

smaller individuals are lost through the sieve. The minimum value of the number of
species per 100 individuals (type 4 curves) and the maximum values for numbers of
species (type l), total numbers of individuals (type 2) and abundances of individual
species (type 3) all occur at a dry weight of around 0.22 mg or an equivalent
spherical diameter of 1.2 mm. This is about the size at which smaller individuals of a
species will start to become lost through a 0.5 or 1 mm mesh sieve. The upturn to the
left cannot be explained as the beginning of the second meiofauna peak in species
abundances described by Warwick (1984) since it is not reflected in either the type 1
or type 2 curves (Figs. 1 and 2).
2. The increase in numbers of species per 100 individuals at sizes larger than 0.22 mg
ash-free dry weight could result from a plausible hypothesis that many species are
distributed according to clustered spatial processes rather than randomly dispersed
ones (Poisson fields), with patch sizes which are scaled to organism size. If small
species are distributed as a mosaic of small patches relative to the, say, 0.1 m* sample
area, then many whole patches and rather few part-patches are likely to be sampled
and each whole patch will contribute sizeable numbers of individuals of the same
species. If larger organisms are distributed in bigger patches, then many part-patches
and few whole patches will be sampled and the part-patches will tend to contribute
individuals of different species.

These observations imply that diversity measures are likely to be rather dependent on
a complex combination of the sieve mesh size used, the area of the sample and the size
distribution of the organisms present. This makes comparison of diversity measures from
different studies difficult to interpret. For example, recently Gray (1994) compared
 R.M. Warwick, K.R. Clarke I .I. Exp. Mar. Bid. Ed. 202 (1996) 63-71 69

l l
. l

Fig. 3. ‘Type 3’ plots of log= (abundance) of each individual species against log (weight) for all examples
listed in the text. The weight axis is on a continuous loge scale.
70 R.M. Warwick, K.R. Clarke I J. Exp. Mar. Bid. Ed. 202 (1996) 63-71

0 0.
-5 -3 -1 1 3 5 7 9 -5 -3 -1 1 3 s 7 9

LOG BODY WEIGHT

Fig. 4. Morlaix samples. ‘Type 4’ plots of log, (number of species per 100 individuals) in each weight class for
each year. The weight axis is discretised into integers on a log, scale.

diversity profiles of the benthic fauna on the Norwegian continental shelf with data from
the deep-sea (Grassle and Maciolek, 1992), suggesting that the species diversity was
comparable. However, Gray’s samples were taken with a 0.1 m2 grab and sieved
through a 1 mm mesh, whereas Grassle and Maciolek’s samples were taken with a 0.25
m2 box core and sieved through a 0.3 mm mesh. If the size distribution of the fauna in
the two areas was equivalent, these differences in sampling procedure, from the evidence
presented above, could inflate the apparent Norwegian diversity relative to the deep-sea.
The fact that the deep sea benthic fauna is on average smaller than the shelf fauna (Gage
and Tyler, 1991) will tend to correct for the discrepancy in mesh size. However, the
different area1 cover of the two samplers acts in the other direction, tending to negate
this correction and this only serves to highlight the difficulty inherent in such
comparisons.
Clearly the question of whether the true number of species per 100 individuals really
varies with body size in the way suggested by Fig. 4, or whether this is a consequence of
the methods of sampling and sample processing, needs further investigation. This could
be achieved by varying the sampling area and sieve size to see whether this affects the
form of the curves, by scale stratified sub-samplin g and by computer simulation studies
where standard-sized samples are taken from modelled assemblages in which patch size
varies with organism size in a uniform way.

Acknowledgments

This work was joint-funded by the UK Natural Environment Research Council and
the UK Ministry of Agriculture, Fisheries and Food.
 R.M. Warwick, K.R. Clarke I J. Exp. Mar. Biol. Gol. 202 (1996) 63- 71 71

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