Body size does not predict species richness among the metazoanphyla

C. D. L. ORME, D. L. J. QUICKE, J. M. COOK & A. PURVIS

Department of Biology, Imperial College, London, UK

Introduction

Highly uneven distributions of species richness within

higher taxa are a common feature of natural assemblages

(Dial & Marzluff, 1989). Simulation studies, however,

have shown that such extreme overdominance of taxa is

not expected from null models of the distribution of

species among higher taxa in which all contemporaneous

species have the same probability of speciation (Dial &

Marzluff, 1989; Nee et al., 1996). Consequently, com-

parative studies have set out to identify traits correlated

with increased species richness. Many of these studies

have focused on the effects of body size on species

richness, because body size subsumes a great deal of

other ecological variation (Peters, 1983). Early work

frequently suggested, at a wide range of taxonomic

scales, that diversity is highest amongst the smallest

bodied taxa. For example, Van Valen (1973) demonstra-

ted this for angiosperms, mammals and birds and May

(1986) suggested that this was the case for all terrestrial

animals. In contrast, Dial & Marzluff (1988) examined a

wide range of body size distributions and proposed that

taxonomic diversity was highest at a small intermediate

body size.

Comparative studies can be confounded by problems of

phylogenetic nonindependence of the traits under study

(Felsenstein, 1985). Independent contrasts circumvent

this problem by using the differences in traits between

sister taxa identified from phylogenies rather than the

trait values themselves (Felsenstein, 1985). Phylogenetic

studies of the correlation between body size and diversity

have been carried out among the families of birds (Nee

et al., 1992), mammals (Gardezi & da Silva, 1999), and

species of primates and carnivores (Gittleman & Purvis,

1998). Of these studies, only Gittleman & Purvis (1998)

found support for increased diversity in small bodied

clades, and then only in a subclade of the Carnivora. A

possible limitation of these studies is that they only

examine taxa at the rank of class or below and may be at

too fine a scale to detect patterns of diversity resulting

from body size differences.

In this study we have therefore used the phyla of the

Metazoa to examine the relationship between body size

and diversity at a scale which is comparable with

previous studies by May (1986) and Dial & Marzluff

(1988) but with the inclusion of phylogenetic informa-

tion resulting from recent intense scrutiny of the meta-

zoan relationships. The Metazoa includes organisms

ranging from a few hundred microns to tens of metres

in length. To our knowledge, this is the first study

to re-address the questions discussed above at such a

large scale and with appropriate corrections for the effects

of phylogenetic relatedness.

Keywords:

independent contrasts;

macroevolution;

Metazoa.

Abstract

We present a comparative study of the relationship between body size and

described taxonomic diversity in the Metazoa. We find no pattern between

body size and taxonomic diversity; neither the smallest organisms nor

organisms at an intermediate body size are consistently more diverse than

their closest relatives. This conclusion holds for both nonphylogenetic analysis,

in which phyla are treated as independent points, and analysis of independent

contrasts using several recent hypotheses of metazoan phylogeny. These

results appear surprising in the context of existing models of body size

distributions. However, such models are built around the prevalence of right-

skewed distributions and we find no evidence for such a distribution.

Correspondence: C. David L. Orme, Department of Biology, Imperial

College, Silwood Park, Ascot, Berkshire, UK, SL5 7PY.

Tel.: +44 20759442446; fax: +44 20759442339;

e-mail: d.orme@ic.ac.uk

J . E V O L . B I O L . 1 5 ( 2 0 0 2 ) 2 3 5 – 2 4 7 ª 2 0 0 2 B L A C K W E L L S C I E N C E L T D 235

Phylogeny

Recent studies, using both molecular and morphological

data, have proposed many alternative statements of

relationships amongst the Metazoa as whole, or of taxa

within the Metazoa. In order to assess whether our

results are sensitive to the differences between these

statements, we repeat all our analyses using several

phylum-level phylogenies. The first two are the preferred

trees of Zrzavy et al. (1998), based on morphological and

18S rDNA data, and Nielsen et al. (1996), based on

morphological data, because both are fully resolved and

contain the vast majority of the metazoan phyla. How-

ever, neither presents the hypothesis, supported by

recent work using morphology and embryology (Eernisse

et al., 1992), 18S rDNA (Aguinaldo et al., 1997;

Ruiz-Trillo et al., 1999) and Hox genes (de Rosa et al.,

1999), that the Bilateria can be divided into protostome

and deuterostome clades and, further, that the protost-

omes are split into the Ecdysozoa and Lophotrochozoa.

We have therefore also taken the summary phylogeny

presented by Holland (1999) as a basis and used several

variant resolutions of the areas of uncertainty. One

variant is shown in Fig. 1 and the alternative topologies

used are described below.

Diploblasts

We have adopted two variant topologies for the

resolution of the diploblasts, both of which present

the Porifera as a paraphyletic grouping of the Calcarea

and Demospongiae, but omitting the Hexactinellida

(Zrzavy et al., 1998; Borchiellini et al., 2001). The

variants differ in the branching order of the remaining

diploblasts:

D1 (Calcarea (Placozoa (Cnidaria (Ctenophora, Bilate-

ria)))) (Nielsen et al., 1996; Zrzavy et al., 1998)

D2 (Calcarea (Ctenophora (Placozoa (Cnidaria, Bilate-

ria)))) (Cavalier-Smith et al., 1996; Kim et al., 1999).

Ecdysozoa

M1 The Nematoda and Nematomorpha form a sister

taxon to the Panarthropoda as shown in Fig. 1: (Ceph-

aloryncha ((Nematoda, Nematomorpha) Panarthro-

poda)) (Zrzavy et al., 1998).

M2 The Nematoda and Nematomorpha form a sister

taxon to the Cephaloryncha: ((Cephaloryncha (Nema-

toda, Nematomorpha)) Panarthropoda) (Nielsen et al.,

1996; Garey et al., 1998).

Lophotrochozoa

These variants mainly reflect differences in the degree of

resolution of the lophotrochozoan taxa (Halanych et al.,

1995; Aguinaldo et al., 1997; de Rosa et al., 1999; Ruiz-

Trillo et al., 1999; Stechmann & Schlegel, 1999) shown in

Fig. 1.

L1 is the least resolved variant, consisting of a poly-

tomy with resolution only of two pairs of sister taxa:

(Acanthocephala, Rotifera) (Winnepenninckx et al.,

1995; Garey et al., 1998) and (Annelida, Echiura) (Rouse,

1999).

L2 and L3 add the sister group relationship (Cyclio-

phora, Entoprocta) (Funch & Kristensen, 1995; Zrzavy

et al., 1997) and two groupings of the Annelida, Echiura,

Sipuncula and Mollusca. The L2 variant uses (Mollusca

(Sipuncula (Annelida, Echiura))) (Eernisse et al., 1992),

whereas the L3 variant uses ((Mollusca, Sipuncula)

(Annelida, Echiura)) (Zrzavy et al., 1998).

L4 and L5 use the resolution seen in Fig. 1, based on

work by Eernisse et al. (19921 ), Funch & Kristensen

(1995), Garey et al. (1998) and Zrzavy et al. (1998). They

Fig. 1 One variant (D1M1L5)of the composite phylogeny used in

our analyses. The variable regions (D, L, M) are marked and the

alternative topologies are described in the text.

236 C. D. L. ORME ET AL .

J . E V O L . B I O L . 1 5 ( 2 0 0 2 ) 2 3 5 – 2 4 7 ª 2 0 0 2 B L A C K W E L L S C I E N C E L T D

differ only in the placement of the Sipuncula with L4

mirroring L2 and L5 mirroring L3.

In the absence of any reliable estimate of the branch

lengths within metazoan phylogenies we have assumed

that all branch lengths are equal (Ackerly, 2000), a point

we return to in the discussion.

Data

Body form varies considerably within the Metazoa and

so we use biological volume (Siemann et al., 1996;

Poulin & Morand, 2000), rather than length (May

1986) or area (Poulin, 1996, 1998), as a measure of

body size. Where possible we take data from existing

studies of body size distribution within taxa but for the

remaining taxa we take measurements from original

descriptions or from reviews. We use the maximum

recorded dimensions from individual species, as this is

most commonly reported. We use the median as a

measure of central tendency for the linear dimensions

and these are reported in Table 1, along with the

number of species contributing to each value. Where

width and/or height were not recorded in a source, we

make assumptions based on body form and the

remaining dimensions: such values are indicated in

parentheses in Table 1. Volume is calculated as the

product of these linear dimensions. In some cases, we

convert a mass to a volume: we assume a density of

1 g cm–1 in all cases and these conversions are noted in

Table 1. The analyses below use the natural logarithm

of these volumes.

In some cases, subtaxa show considerable differences

in body form or a terminal taxon in a phylogeny

comprises a group of phyla. Here we calculate the

volumes of each subtaxon and then use the mean of

the natural logarithms of the volumes of the subtaxa,

weighted by the number of described species, as the

volume of the taxon itself. All taxa used in calculations

are shown in Table 1 with indentation indicating where

values have been calculated from a group of subtaxa. An

electronic appendix provides further details on the body

size data collected and our data set is available from the

authors on request.

Numbers of described species are taken from a range of

recent reviews of taxa and estimates of described species.

Where estimates differ between sources, we prefer the

most recent estimates or estimates from reviews focusing

on a particular taxon. The described species numbers

used and the sources from which they are taken are also

shown in Table 1.

Analyses

The number of described species in the Arthropoda is

very large in comparison with all other metazoan phyla.

In order to test that our regressions are robust to the

possible leverage exerted by the arthropods, we have

performed all the analyses described below with the

arthropods both included and excluded.

We used linear regression to assess whether ln(biovol-

ume) is a predictor of species richness in the absence of

phylogenetic information. We initially fitted a quadratic

linear model to test for the existence of an intermediate

optimum body size and then performed model simplifi-

cation and diagnostic plots using the statistical program R

(Ihaka & Gentleman, 1996). Since species richness has a

highly right-skewed distribution, we used the natural

logarithm of species numbers as the response variable.

We have also approximated a histogram of body sizes

amongst species; for this figure we have used the

subdivisions of taxa shown in Table 1 in order to

represent the range of body sizes within the larger phyla

more accurately.

We next used MacroCAIC v.0.8.3 (Agapow & Isaac,

2002) to calculate phylogenetically independent con-

trasts of both ln(biovolume) and species richness. The

body size contrasts and nodal values of body size are

calculated, and the contrasts scaled by branch length to

standardize variance, according to the methods described

by Felsenstein (1985) and Pagel (1992).

Two contrasts of species richness are recommended

when using MacroCAIC (Isaac N. J. B et al., unpublished

work): the relative rate difference (RRD), calculated as

ln(Ni/Nj); and, the proportional dominance index (PDI),

calculated as Ni/Nt–0.5, where Ni and Nj are the number

of species in the larger and smaller bodied clade,

respectively, and Nt ¼ Ni + Nj. These measures vary little

in their performance in simulation studies (Isaac N.J.B.,

et al. unpublished work); here we have used the diag-

nostic tests described below to decide which is most

suited to our analyses. Contrasts are not calculated at

polytomous nodes. MacroCAIC is available from the

following URL: http://www.bio.ic.ac.uk/evolve/soft-

ware/macrocaic/index.html.

We performed two diagnostic analyses using the

output from MacroCAIC:

We used linear regression to test whether nodal body

size is correlated with the scaled body size contrasts. A

significant result would indicate that the variance in the

contrasts is not constant across the full range of body

sizes (Purvis & Rambaut, 1995).

We used linear regression to test whether total species

richness at a node (Nt) predicts the scaled species richness

contrasts (PDI or RRD) for that node. Again, a significant

result indicates that the variance in the contrasts is not

constant across the full range of total clade sizes (Isaac

N.J.B, et al. unpublished work).

MacroCAIC also reports the standardized residuals for

the regression through the origin in terms of the number

of standard deviations (Garland et al., 1992). We exam-

ined these residuals to check for data points with

standard deviations greater than ±1.96.

We used linear regression through the origin (Garland

et al., 1992) to test whether species richness contrasts are

Body size among metazoan phyla 237

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Table 1 Body size and species richness data used in these analyses. The dimensions used to calculate biovolume (B) are given where available and

brackets indicate values estimated from the dimensions. The terminal taxa used by (a) Nielsen et al. (1996), (b) Zrzavy et al. (1998) and (c) the composite

phylogeny are indicated. Indentation indicates where subtaxa have been combined to calculate a volume for a higher taxon. The sources used are:

1 (Adis, 2000), 2 (Alford et al., 2000), 3 (Ball & Reynoldson, 1981), 4 (Barnes et al., 1993), 5 (Blackburn & Gaston, 1994b), 6 (Bonnet & Naulleau, 1994),

7 (Brown, 2000), 8 (Brunton & Curry, 1979), 9 (Cameron & Redfern, 1976), 10 (Clark, 1970), 11 (Clark & Courtman-Stock, 1976), 12 (Clarke &

Johnston, 1999), 13 (Dilly & Ryland, 1985), 14 (Dorjes, 1968), 15 (Ellis, 1978), 16 (Emig, 1979), 17 (Funch & Kristensen, 1995), 18 (Furuya et al., 1992),

19 (Gibson, 1982), 20 (Gibson, 1995), 21 (Ginsberg, 2000), 22 (Giray & King, 1996), 23 (Greenwood, 2000), 24 (Haukisalmi et al., 1998), 25 (Hayward &

Ryland, 1979), 26 (Hayward & Ryland, 1985), 27 (Hayward, 1985), 28 (Hayward & Ryland, 1990), 29 (Helfman, 2000), 30 (Higgins & Kristensen, 1986),

31 (Higgins & Kristensen, 1988), 32 (Hochberg & Short, 1983), 33 (Israelsson, 1999), 34 (Ivanov, 1963), 35 (Jones & Baxter, 1987), 36 (Kalavati et al.,

1984), 37 (King et al., 1994), 38 (Kozloff, 1992), 39 (Kozloff, 1993), 40 (Lester, 1985), 41 (Madsen & Hansen, 1994), 42 (Markham, 1971), 43 (Millar,

1970), 44 (Minelli, 1993), 45 (Morgan & King, 1976), 46 (Neubert & Nesemann, 1999), 47 (Nielsen, 1989), 48 (Nielsen, 1995), 49 (Nordsieck, 1969),

50 (Petrochenko, 1956), 51 (Petrochenko, 1958), 52 (Pierrot-Bults & Chidgey, 1988), 53 (Platt & Warwick, 1988), 54 (Pontin, 1978), 55 (Poss &

Boschung, 1996), 56 (Pough, 2000), 57 (Poulin, 1997), 58 (Poulin, 1998), 59 (Prudhoe, 1982), 60 (Reaka-Kudla, 2000), 61 (Robson, 1929), 62 (Robson,

1932), 63 (Rohde, 2001), 64 (Ruhberg, 1985), 65 (Ryland & Hayward, 1977), 66 (Schmidt-Rhaesa, 1997), 67 (Schwank & Bartsch, 1990), 68 (Siemann

et al., 1999), 69 (Silva & Downing, 1995), 70 (Smith, 1961), 71 (Stafford & Meyer 2000), 72 (Stephen & Edmonds, 1972), 73 (Sterrer, 1991a), 74 (Sterrer,

1991b), 75 (Sterrer, 1991c), 76 (Stokes & Holland, 1996), 77 (Thompson & Brown, 1976), 78 (Trouve et al., 1998), 79 (Tyler & Bush, 1998), 80 (Warwick

et al., 1998), 81 (Wheeler, 1978), 82 (Wilcke, 1967), 83 (Woodwick & Sensenbaugh, 1985), 84 (Yamaguchi, 1963).

Biovolume Length Width Height

(a) (b) (c) Taxa ln(B) (mm3) (mm) n (mm) n (mm) n Sources Species Sources Notes

� � Choanoflagellata – – – – – – – – – 140 48

� Porifera – – – – – – – – – 10 000 4

� � Demospongia – – – – – – – – – 9000 4

� � Calcarea – – – – – – – – – 1000 4

� � � Placozoa –0.11 0.9 3 3 (0.1) 4 1 48

� � � Cnidaria – – – – – – – – – 15 000 44

� � � Ctenophora – – – – – – – – – 80 48

� Orthonectida –8.95 0.00013 0.205 19 0.03 17 (0.03) – 38, 39 20 38, 39

� Dicyemida –4.67 0.0094 1.67 7 0.08 7 (0.08) – 18, 32, 36 70 4

� Platyhelminthes –0.10 0.91 55 436

� Platyhelminthes –0.08 0.93 55 117

� Platyhelminthes –0.07 0.93 55 000 63

Turbellaria 2.58 13.2 22 47 6 37 – – 3, 59 15 000 63

Monogenea –2.50 0.082 2 169 0.41 143 – – 84 10 000 63

Trematoda –2.08 0.125 57 20 000 63

Cestoda 2.42 11.213 75 53 1.5 34 – – 24, 78 10 000 63

� � Acoela –3.86 0.021 1.05 74 0.2 62 (0.1) – 14 319 79

� Nemertodermatida –3.86 10 79

� Catenulida –3.86 107 79

� Chordata 10.90 51 297

� � Cephalochordata 5.44 231 53 25 – – – – 55, 76 25 48

� � Urochordata 8.41 4500 20 57 15 57 (15) – 43 1990 4

� � Vertebrata 11.01 60 314 49 282 (i)

Agnatha 13.8 984467 550 4 (42.3) – (42.3) – 81 84 29

Chondrichthyes 17.78 5.3E + 07 1500 43 (187) – (187) – 81 848 29

Osteichthyes 11.16 70 000 – – – – – – 12 23 460 29

Amphibia 10.74 46 298 57 21 (28.5) – (28.5) – 70 4780 2

Snakes 11.63 112 500 850 62 – – – – 6, 71 2500 56

Lizards 8.61 5500 – – – – – – 56 3000 56

Aves 10.54 37 600 – – – – – – 5 9672 23

Mammalia 11.44 92 500 – – – – – – 69 4649 21

� � � Echinodermata 10.22 27 488 6227 4 (ii)

Holothuroidea 9.70 16 352 70 41 15.28 28 (15.28) – 41 1150 4

Echinoidea 12.17 193 365 69.5 59 66.7 19 41.7 49 11 950 4

Asteroidea 12.05 171806 – – – – – – 11 1500 4

Ophiurioidea 8.75 6283.2 – – – – – – 11 2000 4

Crinoidea 8.54 5097.7 – – – – – – 10 625 4

� Hemichordata 5.91 95

� � Enteropneusta 7.35 1557 173 3 3 3 (3) – 22, 37, 83 70 4

� � Pterobranchia 1.89 6.6 6.6 3 1 1 (1) – 13, 40, 42 25 48

� Cephalorhyncha –5.46 199

� � Kinoryncha –6.81 0.0011 0.38 7 0.05 7 (0.05) – 31 150 48

� � Loricifera –6.65 0.0013 0.205 7 0.08 7 (0.08) – 30 32 4

238 C. D. L. ORME ET AL .

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Table 1 (continued)

Biovolume Length Width Height

(a) (b) (c) Taxa ln(B) (mm3) (mm) n (mm) n (mm) n Sources Species Sources Notes

� � Priapulida 8.76 6353 52.5 2 11 2 (11) – 28 17 48

� � � Nematoda –5.99 0.0025 1.4 285 0.042 239 (0.042) – 53, 80 20 000 48

� � � Nematomorpha 4.42 83.3 170 84 0.7 72 (0.7) – 66 304 66

� � � Onychophora 6.75 850.5 42 55 4.5 51 (4.5) – 64 70 44

� � � Tardigrada –5.95 0.0026 0.375 65 0.08 2 (0.08) – 45 600 48

� � � Arthropoda 3.81 45.21 1 074 577 (iii)

Arenae 4.48 88.2 – – – – – – 68 37 000 1

Acari 3.00 20.1 – – – – – – 58 45 000 1

Orthoptera 6.17 480 – – – – – – 68 20 000 7

Hemiptera 3.75 42.5 – – – – – – 68 98 000 7

Coleoptera 3.79 44.3 – – – – – – 68 350 000 7

Diptera 2.24 9.4 – – – – – – 68 120 000 7

Lepidoptera 5.09 162 – – – – – – 68 160 000 7

Hymenoptera 3.91 50 – – – – – – 68 120 000 7

Copepoda –2.67 0.069 1.04 15 (0.26) – (0.26) – 28 9000 60

Ostracoda –4.14 0.016 0.64 22 (0.16) – (0.16) – 28 8000 60

Eucarida 9.73 16 896 33 151 32 34 (16) – 28 10 566 60

Pericarida 3.47 32 8 315 (2) – (2) – 28 12 706 60

� � Phoronozoa 8.48 347

� Brachiopoda 8.55 5175 15 18 23 4 (15) – 8 335 44

� Phoronida 6.36 580 145 8 2 10 (2) – 16 12 48

� Syndermata –3.12 2700

� � Acanthocephala 2.13 8.4 8.4 413 1 358 (1) – 50, 51 900 48

� � Rotifera –5.74 0.0032 0.3 79 0.1 12 (0.1) – 54 1800 48

� � � Nemertea 5.46 234.38 75 70 2.5 55 (1.25) – 19 1149 20

� � � Mollusca 6.31 550 – – – – – 97 814 4 (iv)

Solenogastres 5.05 156 25 6 2.5 6 (2.5) – 35 180 4

Caudofoveata 4.00 54.7 35 3 1.25 3 (1.25) – 35 70 4

Polyplacophora 6.76 858 22 11 13 11 3 11 35 550 4

Cephalopoda 11.20 73 332 47 129 39.5 127 (39.5) – 61, 62 656 4

Prosobranchia 6.38 588 12 128 7 127 7 13 28 55 000 4

Opisthobranchia 5.40 221 20 124 4.7 124 (2.35) – 77 1000 4

Pulmonata 4.50 90.3 5 84 4.25 84 (4.25) – 9 20 000 4

Scaphopoda 1.58 4.86 6 7 0.9 7 (0.9) – 35 350 4

Bivalvia 7.91 2715 20 708 14 646 10 540 15, 49 20 000 4

� � � Sipuncula 6.62 750 30 273 5 118 (5) – 72 320 48

� Annelida 4.16 64.36 18 750 (v)

Polychaeta 6.17 480 60 220 4 23 (2) – 28 12 000 44

Oligochaeta 2.92 18.55 20 251 0.96 80 (0.96) – 82 6000 44

Hirudinea 6.27 529.39 35 84 5.5 16 (2.75) – 46 600 44

� Annelida 4.14 19 130 (vi)

� Annelida 4.14 18 890 (vii)

� � Gnathostomula –5.91 0.0027 0.759 31 0.06 31 (0.06) – 73–75 100 4

� � Echiura 10.35 31104 96 63 18 8 (18) – 72 140 44

� Pogonophora 1.34 3.81 72.1 60 0.23 62 (0.23) – 34 140 4

� � � Chaetognatha 4.22 67.92 23.5 20 1.7 20 (1.7) – 52 200 48

� � Cycliophora –5.43 0.0044 0.347 1 0.11 1 (0.11) – 17 1 17

� � � Ectoprocta –2.85 0.0576 0.64 253 0.3 241 (0.3) – 25–27, 65 4000 48

� � � Entoprocta –3.51 0.03 0.685 32 0.21 33 (0.21) – 47 150 48

� � � Gastrotricha –8.25 0.00026 0.16 181 0.04 146 (0.04) – 67 510 67

� Xenoturbellida 7.00 1098.5 26 2 6.5 2 (6.5) – 33 2 33

i. The total species richness for the vertebrates includes all species of Crocodylia (22), Sphenodon (2) and Chelonia (265), in addition to the species taxa listed above (Pough 2000).

ii. The total species richness for the echinoderms includes 2 species of Concentricycloidea (Rowe et al., 1988).

iii. The total species richness for the Arthropods includes, in addition to the taxa listed above, further species from the Merostomata (4) and Pycnogonida (1000) (Minelli, 1993),

Arachnida (9303) and Myriapoda (15096) (Adis, 2000), Crustacea (2672) (Reaka-Kudla, 2000) and Insecta (56230) (Brown, 2000).

iv. The total species richness for the Mollusca includes 8 species of Monoplacophora (Barnes et al., 1993).

v. The total species richness for the Annelida includes 150 species of Myzostomida (Eeckhaut et al. 2000).

vi. Includes Gnathostomula, Echiura and Pogonophora.

vii. Includes Echiura.

Body size among metazoan phyla 239

J . E V O L . B I O L . 1 5 ( 2 0 0 2 ) 2 3 5 – 2 4 7 ª 2 0 0 2 B L A C K W E L L S C I E N C E L T D

predicted by body size contrasts. We also used linear

regression, not through the origin, to test whether

species richness contrasts are predicted by the nodal

values of body size. A significant result indicates that

diversity is the greatest at an intermediate body size

(Gittleman & Purvis, 1998). Visual Basic for Applications

programs running within Microsoft Excel were used to

automate all the tests above, apart from the regression

through the origin which is calculated within Macro-

CAIC. R (Ihaka & Gentleman, 1996) was also used to

perform diagnostic plots on linear regressions.

Results

Simplification of the quadratic model showed that

neither ln(biovolume) nor [ln(biovolume)]2 are signifi-

cant predictors of ln(species richness) in the absence of

phylogenetic information. Diagnostic plots indicated that

the models were suitable for the data. The data are

plotted in Fig. 2(a), showing regression lines for the data

plotted, both including (solid line) and excluding (dot-

ted line) the Arthropoda (shown as a filled circle). The

lines shown are those for models using ln(biovolume)

alone; neither regression is significant, with P > 0.3 for

both data sets. Figure 2(b) shows the distribution of

body sizes amongst phyla and Fig. 2(c) shows the

approximate distribution of body size amongst species

from our data.

The variance in the scaled body size contrasts does not

vary markedly over the range of nodal body sizes for any

of the test phylogenies. However, the variance in RRD

increases slightly but significantly with Nt in all the full

analyses and in two (Zrzavy et al., 1998 and variant

D1M1L1) of the analyses with Arthropoda excluded. We

therefore prefer PDI as a species richness contrast in this

study as it shows no increase in variance with Nt, and so

report only results for PDI below. The results are

qualitatively identical if RRD is used instead of PDI in

the analysis.

Results of regression through the origin of PDI on

body size contrasts for all the test phylogenies are

shown in Table 2. None show any significant relation-

ship between body size and species richness, irrespect-

ive of whether the Arthropoda are included. The

standardized residuals show that outliers are never

greater than 2.87 SD from the predicted values and are

almost exclusively found at contrasts within the diplo-

blasts or at the base of the Bilateria. The results of the

regressions presented in Tables 2 and 3 do not change

qualitatively when contrasts from the bilaterian taxa

alone are used.

In addition, regressions of PDI against estimated nodal

body size show that there is no significant variation in

the relationship between body size and species richness

as body size varies (see Table 3). Again, the exclusion of

the arthropods from the analysis does not qualitatively

change our results.

Discussion

There are two key issues arising from our findings. The

first is the apparent discrepancy between the results

presented here and previous studies on the relationship

between body size and species richness. The second is the

robustness of our findings given both the analytical

approach and the data used. We address these points in

turn.

Fig. 2 (a) Scatterplot of ln(biovolume)(ln(B))in mm3 against

ln(number of described species) (ln(S))for the terminal taxa of the

composite phylogeny. The plot also shows regression lines for the

full data set [solid line – ln(S) ¼ 6.12 + 0.09.ln(B), P ¼ 0.35] and

with the Arthropoda (shown as a solid circle) omitted [dashed line )ln(S) ¼ 5.90 + 0.08. ln(B), P ¼ 0.38].

(b) Body size distribution of the phyla of the Metazoa, using the

terminal taxa from the composite phylogeny

(c) Approximate body size distribution of the species of the Metazoa,

calculated using the subtaxa in Table 1.

240 C. D. L. ORME ET AL .

J . E V O L . B I O L . 1 5 ( 2 0 0 2 ) 2 3 5 – 2 4 7 ª 2 0 0 2 B L A C K W E L L S C I E N C E L T D

Body size and species richness

Our study does not support any correlation between the

median body size of a phylum and the number of species

in that phylum, counter to statements either that the

smallest bodied taxa tend to be most diverse (Van Valen,

1973; May, 1986; Kochmer & Wagner, 1988) or that

diversity is highest in taxa of some median size (Dial &

Marzluff, 1988). Although a nonphylogenetic approach

can be criticized on grounds of the nonindependence

of the comparisons used, there remains a contradic-

tion between our findings and the robust ecological

observation that species richness decreases with increas-

ing body size (e.g. Hutchinson & MacArthur, 1959; May,

Table 2 Results of regression through the origin for PDI against body

size contrasts. N indicates the number of contrasts used to calculate

the regression coefficient (b) and the F ratio is therefore F2,N)1. The

number of positive (+) and negative (–) contrasts are indicated.

Phylogeny N + – b F p

Arthropods included

D1M1L1 18 8 10 –0.013 0.16 0.69

D1M1L2 21 9 12 –0.012 0.13 0.73

D1M1L3 21 10 11 –0.011 0.10 0.76

D1M1L4 26 15 11 0.004 0.02 0.89

D1M1L5 26 14 12 0.004 0.01 0.91

D1M2L1 18 8 10 –0.017 0.26 0.61

D1M2L2 21 9 12 –0.016 0.22 0.65

D1M2L3 21 10 11 –0.014 0.18 0.67

D1M2L4 26 15 11 0.001 <0.01 0.97

D1M2L5 26 14 12 <0.001 <0.01 0.99

D2M1L1 18 8 10 –0.014 0.16 0.69

D2M1L2 21 9 12 –0.012 0.13 0.72

D2M1L3 21 10 11 –0.011 0.10 0.75

D2M1L4 26 15 11 0.004 0.02 0.89

D2M1L5 26 14 12 0.004 0.01 0.91

D2M2L1 18 8 10 –0.017 0.27 0.61

D2M2L2 21 9 12 –0.016 0.22 0.64

D2M2L3 21 10 11 –0.014 0.19 0.67

D2M2L4 26 15 11 0.001 <0.01 0.98

D2M2L5 26 14 12 <0.001 <0.01 1.00

Zrzavy 30 16 14 0.006 0.03 0.87

Nielsen 27 12 15 –0.008 0.07 0.80

Arthropods excluded

D1M1L1 17 5 12 –0.038 1.48 0.24

D1M1L2 20 6 14 –0.037 1.39 0.25

D1M1L3 20 7 13 –0.035 1.29 0.27

D1M1L4 25 12 13 –0.018 0.33 0.57

D1M1L5 25 11 14 –0.018 0.37 0.55

D1M2L1 17 7 10 –0.036 1.38 0.26

D1M2L2 20 7 13 –0.035 1.30 0.27

D1M2L3 20 8 12 –0.034 1.20 0.29

D1M2L4 25 14 11 –0.017 0.29 0.59

D1M2L5 25 13 12 –0.017 0.32 0.57

D2M1L1 17 5 12 –0.038 1.49 0.24

D2M1L2 20 6 14 –0.037 1.40 0.25

D2M1L3 20 7 13 –0.035 1.30 0.27

D2M1L4 25 12 13 –0.018 0.34 0.57

D2M1L5 25 11 14 –0.019 0.37 0.55

D2M2L1 17 7 10 –0.036 1.39 0.26

D2M2L2 20 7 13 –0.036 1.30 0.27

D2M2L3 20 8 12 –0.034 1.21 0.29

D2M2L4 25 14 11 –0.017 0.30 0.59

D2M2L5 25 13 12 –0.017 0.33 0.57

Zrzavy 29 15 14 –0.009 0.08 0.79

Nielsen 26 13 13 –0.015 0.26 0.61

Table 3 Results of regression of PDI against the nodal values

calculated for each phylogeny. N indicates the number of contrasts

used to calculate the intercept (a) and regression coefficient (b) and

the F ratio is therefore F2,N)2

Phylogeny N a b F P

Arthropods included

D1M1L1 18 –0.08 0.01 0.27 0.61

D1M1L2 21 –0.04 –0.01 0.08 0.78

D1M1L3 21 –0.02 <0.01 0.02 0.88

D1M1L4 26 0.09 –0.01 0.17 0.68

D1M1L5 26 0.07 –0.02 0.74 0.40

D1M2L1 18 –0.09 0.02 0.43 0.52

D1M2L2 21 –0.05 <0.01 0.03 0.86

D1M2L3 21 –0.03 0.01 0.07 0.79

D1M2L4 26 0.08 –0.01 0.10 0.76

D1M2L5 26 0.07 –0.02 0.57 0.46

D2M1L1 18 –0.08 0.01 0.28 0.61

D2M1L2 21 –0.04 –0.01 0.08 0.78

D2M1L3 21 –0.02 <0.01 0.02 0.88

D2M1L4 26 0.09 –0.01 0.17 0.68

D2M1L5 26 0.07 –0.02 0.74 0.40

D2M2L1 18 –0.09 0.02 0.43 0.52

D2M2L2 21 –0.05 <0.01 0.03 0.87

D2M2L3 21 –0.03 0.01 0.07 0.79

D2M2L4 26 0.08 –0.01 0.09 0.76

D2M2L5 26 0.07 –0.02 0.56 0.46

Zrzavy 30 0.06 –0.01 0.25 0.62

Nielsen 27 –0.02 <0.01 0.04 0.85

Arthropods excluded

D1M1L1 17 –0.25 0.04 2.70 0.12

D1M1L2 20 –0.18 0.01 0.29 0.59

D1M1L3 20 –0.16 0.02 1.05 0.32

D1M1L4 25 –0.01 0.00 0.04 0.85

D1M1L5 25 –0.03 –0.01 0.07 0.79

D1M2L1 17 –0.12 0.03 1.04 0.32

D1M2L2 20 –0.13 0.01 0.09 0.77

D1M2L3 20 –0.10 0.02 0.60 0.45

D1M2L4 25 0.07 <0.01 0.00 0.96

D1M2L5 25 0.05 –0.01 0.27 0.61

D2M1L1 17 –0.25 0.04 2.71 0.12

D2M1L2 20 –0.18 0.01 0.30 0.59

D2M1L3 20 –0.16 0.02 1.06 0.32

D2M1L4 25 –0.01 <0.01 0.04 0.84

D2M1L5 25 –0.03 –0.01 0.07 0.79

D2M2L1 17 –0.12 0.03 1.04 0.32

D2M2L2 20 –0.13 0.01 0.09 0.77

D2M2L3 20 –0.10 0.02 0.60 0.45

D2M2L4 25 0.07 <0.01 0.00 0.96

D2M2L5 25 0.05 –0.01 0.26 0.61

Zrzavy 29 0.04 –0.01 0.08 0.77

Nielsen 26 –0.01 0.01 0.20 0.66

Body size among metazoan phyla 241

J . E V O L . B I O L . 1 5 ( 2 0 0 2 ) 2 3 5 – 2 4 7 ª 2 0 0 2 B L A C K W E L L S C I E N C E L T D

1986). As neither the body size distribution of the phyla

nor our approximate body size distribution for species

show the right skewed distribution expected from a

pattern of decreasing species number with body size, it is

perhaps unsurprising that our results contradict expec-

tations based on such a pattern. It could be argued,

however, that our data do show such a decline for body

sizes of greater than 4 mm3 and that the absence of

pattern below that size is the result of a bias in sampling

towards large bodied organisms (May, 1986), a point we

return to later in this discussion.

An alternative explanation is that small body size is

necessary but not sufficient for a radiation in species

numbers. Gardezi & da Silva (1999) found that diversi-

fication rates decreased significantly with increases in

body size among the lightest mammalian orders but not

among the mammals in general or among the remaining

heavier orders by themselves. The pattern that the

relationship between body size and species richness will

be most marked among lighter bodied subtaxa is consis-

tent with a model of body size evolution of passive

diffusion from a constrained minimum size (Gardezi & da

Silva, 1999). However, our analysis of estimated nodal

values shows no change in the relationship between

body size and species richness across the range of body

sizes: it is not the case that, in comparisons among the

very smallest lineages, larger-bodied clades are more

diverse. Our results also reject the existence of a single

intermediate optimum body size for the Metazoa, as

might be predicted by a reproductive fitness model like

that of Brown et al. (1993) and also by mosaic models of

the subdivision of the environment among taxa of

differing sizes (Hutchinson & MacArthur, 1959).

Although body size may well affect diversification rates,

ecological differences between all but closely related taxa

may obscure such effects. In the case of the Metazoa,

even such gross ecological factors as whether a taxon is

marine, freshwater, symbiotic or terrestrial vary both

within and between phyla (May, 1994).

Although we accept that the distribution of the median

body sizes within the phyla (Fig. 2b) is crude, it is clearly

bimodal. This could result from ecological differences:

Kirchner et al. (1980) suggest that bimodality in the

distribution of nematode body sizes is a result of

differences between vertebrate parasites and invertebrate

parasites. Alroy (1998) suggests that a similar pattern in

the body size of recent mammals may result from

evolution away from an unstable intermediate size.

Similar phylogenetic comparative studies examining

the relationship between body size and species richness

have found at best weak support for a correlation.

Gittleman & Purvis (1998) used species level phylogenies

of the Carnivora and Primates and found a significant

correlation only within the caniform carnivores. Other

studies, focusing on mammalian (Gardezi & da Silva,

1999) and bird (Nee et al., 1992; Owens et al., 1999)

family phylogenies and a phylogeny of hoverfly genera

(Katzourakis et al., 2001), have failed to find any consis-

tent correlation. The results presented here therefore

corroborate the general pattern emerging from phyloge-

netic comparative studies that there is no simple evolu-

tionary rule relating body size to species richness.

Analysis and data

The reliability of such studies is contingent on the

accuracy of the phylogenies used. The use of multiple

phylogenies in our analyses shows that our findings are

insensitive to several different proposals of the topology

of metazoan phylogeny and we believe that they are

therefore unlikely to be invalidated by further phyloge-

netic studies. A commonly perceived problem is that the

definition of the metazoan phyla is essentially arbitrary.

However, as independent contrasts are calculated

between sister taxa identified from a phylogeny, the

formal taxonomic level of groups under study is irrelev-

ant as long as the branching pattern is correctly identi-

fied. In addition, the calculation of contrasts at internal

nodes provides data about the relationship under study at

taxonomic levels higher than that of the terminal taxa.

The number of contrasts available would be increased by

using lower taxonomic levels (e.g. Class) as the terminal

taxa and might reveal correlations between body size and

diversity within, rather than between, phyla. Such an

analysis would, however, be considerably complicated

over questions of the phylogeny and monophyly of the

classes of the Metazoa.

Dates for the major steps in metazoan evolution are

currently a contentious issue, dictating our use of equal

branch lengths (Ackerly, 2000). Molecular estimates of

the date of the division between protostomes and

deuterostomes vary greatly, from around 1200 million

years ago (mya) (Wray et al., 1996) to 670 mya (Ayala

et al., 1998). The common palaeontological view that the

majority of the metazoan phyla arose at, or before,

the Cambrian may underestimate the later origin of the

crown groups now recognized as extant phyla (Budd &

Jensen, 2000), but it is clear that many metazoan phyla

are extremely old. Benton (1993) reports first fossil

representatives for 18 extant phyla that are older than

500 million years: branches leading to the terminal taxa

are therefore likely to be considerably longer than the

internal branches.

In contrast, the use of units reflecting morphological

disparity, rather than units of time, for branch lengths is

likely to lead to longer internal branches. Rates of

morphological diversification are typically concentrated

early in the history of many animal groups (Foote, 1996),

including the diversification of skeletal elements across

the Metazoa (Thomas et al., 2000). Given these problems,

we believe that equal branch lengths are an acceptable

assumption and that the availability of a reliably dated

phylogeny of the Metazoa would not qualitatively

change the results of our analysis. We would also expect

242 C. D. L. ORME ET AL .

J . E V O L . B I O L . 1 5 ( 2 0 0 2 ) 2 3 5 – 2 4 7 ª 2 0 0 2 B L A C K W E L L S C I E N C E L T D

the outliers in our contrast plots to be from comparisons

between tips if our use of equal branch lengths under-

estimated terminal branch lengths (Purvis & Webster,

1999) whereas, in fact, we find that outliers represent

comparisons at deeper branches.

Our body size data is drawn from a wide range of

sources and, where morphological diversity dictates,

incorporates detail of size differences within phyla. As

discussed above, we are constrained to a phylum level

analysis by the availability of suitable phylogenies and

hence to the use of a single measure of body size for each

of the metazoan phyla, concealing within-phylum vari-

ation in body size. The same, however, is true for any

estimate of a central tendency and we see no reason why

our estimation of median phylum body sizes would show

a consistent bias.

Perhaps a more intractable problem of the approach

used here is the reliance on numbers of described species

(Purvis & Hector, 2000). Our analyses hold true as long as

the relative diversities of these phyla remain the same but

some phyla are considerably less well known than others

(Hawksworth & Kalin-Arroyo, 1995). Perhaps the most

serious problem lies in the diversity estimates of marine

fauna. The largest estimate of total marine diversity is that

of Grassle & Maciolek (1992) who, based on extrapolation

from boxcore samples of deep (1500–2500 m) benthic

communities off the east coast of the USA, predicted

upward of 10 million species of marine Metazoa. Later

work suggests that the sampling area used by Grassle &

Maciolek (1992) may not be representative of all latitudes

(Gage & May, 1993; Rex et al., 1993) or, indeed,

comparable latitudes (Poore & Wilson, 1993) and that

the estimate uses inaccurate assumptions about species

replacement across global gradients (May, 1992). It

nevertheless seems likely that species number estimates

for the marine taxa are likely to be greater underestimates

than those for terrestrial taxa. In particular, it seems

certain that the described diversity of the Nematoda is

highly unrepresentative of their true diversity. Hawks-

worth & Kalin-Arroyo (1995) estimate that the diversity

of the chordates is known to within a factor of two, the

arthropods and molluscs to within a factor of five but that

the diversity of nematodes is only known to within a

factor of 10. Neither Grassle & Maciolek (1992) nor Rex

et al. (1993) report nematode diversities from their

sampling but Lambshead (1993) has estimated a total

diversity of marine nematodes of up to 1 · 108 species.

This exceeds even the larger estimates of total arthropod

diversity, e.g. 1.5 · 107 species (Odegaard et al., 2000).

Another concern is that, within a taxon, the larger

species are generally described first leading to a decrease

in modal size and an increase in skew as more species are

described (Blackburn & Gaston, 1994a). This may mean

that our species richness estimates of the smallest bodied

phyla are systematically biased; certainly the

most recently described phyla, Cycliophora (Funch &

Kristensen, 1995) and Loricifera (Kristensen, 1983), are

only some hundred microns in length. Unfortunately, we

have no earlier estimate with which to compare our

distribution of body sizes. The closest is May’s (1986)

estimate of the distribution of terrestrial animals which

uses length as a metric; however, our study includes both

marine and terrestrial organisms and uses volume.

One possible solution is to use a randomization

procedure to resample species richness from within a

range of estimates of total diversity for each phylum. In

the absence of methodical estimates of total diversity for

the majority of phyla, however, it is not apparent that

this approach would introduce anything except noise

into our analyses. Another possibility is to systematically

inflate described species numbers for the phyla based on

some measure of the ease with which new species can be

detected. Unfortunately it is difficult to propose a metric

other than body size itself; an approach which is

evidently circular.

Phylogenetically independent contrasts have been

used to investigate putative correlates of species richness

other than body size. Such studies have revealed signi-

ficant correlates of species richness across a range of

organisms including: sexual dimorphism (Barraclough

et al., 1995; Owens et al., 1999), generalist feeding habits

and dispersal capabilities (Owens et al., 1999) in birds;

sexual selection and diet breadth in hoverflies

(Katzourakis et al., 2001); rates of genetic change in

flowering plants (Barraclough et al., 1996); and latitude

in birds and butterflies (Cardillo, 1999). Given the success

of this approach in revealing other correlates of species

richness, we feel that the, at best, weak support for a

correlation between species richness and body size at a

wide range of scales indicates a genuine lack of any strong

general relationship between diversification rate and size.

Acknowledgments

We especially thank Armand Leroi for constructive

criticism and help during the course of this research.

We thank Kate Jones and Rob Belshaw for insightful

comments on versions of the manuscript and Nick Isaac,

Paul Agapow and Paul Harvey for advice and help with

MacroCAIC and for access to their unpublished simula-

tion studies. We also thank two anonymous referees for

helpful and constructive comments on the manuscript.

This work is supported by funding from the Natural

Environment Research Council to CDLO (GT04/98/MS/

154) and AP (GR3/11526).

Supplementary Material

The following material is available from http://

www.blackwell-science.com/products/journals/suppmat

/JEB/379/JEB379sm.htm

Appendix

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References

Ackerly, D.D. 2000. Taxon sampling, correlated evolution, and

independent contrasts. Evolution 54: 1480–1492.

Adis, J. 2000. Amazonian Arthropods (Terrestrial). In: Encyclo-

pedia of Biodiversity, Vol. 1 (S. Levin, ed.), pp. 249–260.

Academic Press, New York.

Agapow, P.-M. & Isaac, N.J.B. (2002). MacroCAIC: correlates of

species richness. Diversity Distributions 8: 41–43.

Aguinaldo, A.M.A., Turbeville, J.M., Linford, L.S., Rivera, M.C.,

Garey, J.R., Raff, R.A. & Lake, J.A. 1997. Evidence for a clade

of nematodes, arthropods and other moulting animals. Nature

387: 489–493.

Alford, R.A., Richards, S.J. & MacDonald, K.R. 2000. Bio-

diversity of amphibians. In: Encyclopedia of Biodiversity,

Vol. 1 (S. Levin, ed.), pp. 159–169. Academic Press,

New York.

Alroy, J. 1998. Cope’s rule and the dynamics of body mass

evolution in North American fossil mammals. Science 280:

731–734.

Ayala, F.J., Rzhetsky, A. & Ayala, F.J. 1998. Origin of the

metazoan phyla: molecular clocks confirm paleontological

estimates. PNAS 95: 606–611.

Ball, I.R. & Reynoldson, T.B. 1981. British Planarians. Synopses

of the British Fauna (New Series) no. 19. Cambridge Univer-

sity Press, Cambridge.

Barnes, R., Calow, P. & Olive, P. 1993. The Invertebrates: a New

Synthesis. Blackwell Science, Oxford.

Barraclough, T.G., Harvey, P.H. & Nee, S. 1995. Sexual selection

and taxonomic diversity in passerine birds. Proceedings R. Soc.

Lond. Series B. Biol. Sci. 259: 211–215.

Barraclough, T.G., Harvey, P.H. & Nee, S. 1996. Rate of rbcL gene

sequence evolution and species diversification in flowering

plants (angiosperms). Proceedings R. Soc. Lond. Series B. Biol. Sci.

263: 589–591.

Benton, M.J. 1993. The Fossil Record 2. Chapman & Hall, London.

Blackburn, T.M. & Gaston, K.J. 1994a. Animal body size

distributions change as more species are described. Proc. R.

Soc. Lond. Series B. Biol. Sci. 257: 293–297.

Blackburn, T.M. & Gaston, K.J. 1994b. The distribution of body

sizes of the world’s bird species. Oikos 70: 127–130.

Bonnet, X. & Naulleau, G. 1994. A body condition index (BCI) in

snakes to study reproduction. C. R. Acad. Sci. Serie III – Sci. Vie.

317: 34–41.

Borchiellini, C., Manuel, M., Alivon, E., Boury-Esnault, N.,

Vacelet, J. & Parco, Y.L. 2001. Sponge paraphyly and the

origin of Metazoa. J. Evol. Biol. 14: 171–179.

Brown, B.V. 2000. Insects, Overview. In: Encyclopedia of Biodi-

versity, Vol. 2 (S. Levin, ed.), pp. 479–484. Academic Press,

New York.

Brown, J.H., Marquet, P.A. & Taper, M.L. 1993. Evolution of

body-size – consequences of an energetic definition of fitness.

Am. Nat. 142: 573–584.

Brunton, C.H.C. & Curry, G.B. 1979. British Brachipods. Synopses

of the British Fauna (New Series) no. 17. Academic Press,

London.

Budd, G.E. & Jensen, S. 2000. A critical reappraisal of the fossil

record of the bilaterian phyla. Biol. Rev. Cam. Phil. Soc. 75:

253–295.

Cameron, R.A.D. & Redfern, M. 1976. British Land Snails.

Synopses of the British Fauna (New Series) no. 6. Academic

Press, London.

Cardillo, M. 1999. Latitude and rates of diversification in birds

and butterflies. Proceedings R. Soc. Lond. Series B. Biol. Sci. 266:

1221–1225.

Cavalier-Smith, T., Chao, E.E., Boury-Esnault, N. & Vacelet, J.

1996. Sponge phylogeny, animal monophyly, and the origin

of the nervous system: 18S rRNA evidence. Can J. Zool.-Revue

Can Zool. 74: 2031–2045.

Clark, A.M. 1970. Echinodermata: Crinoidea. Marine Invertebrates

of Scandanavia no. 3. Universitetsforlaget, Oslo.

Clark, A.M. & Courtman-Stock, J. 1976. The Echinoderms of South

Africa. British Museum (Natural History), London.

Clarke, A. & Johnston, N.M. 1999. Scaling of metabolic rate with

body mass and temperature in teleost fish. J. Anim Ecol. 68:

893–905.

Dial, K.P. & Marzluff, J.M. 1988. Are the smallest organisms the

most diverse? Ecology 69: 1620–1624.

Dial, K.P. & Marzluff, J.M. 1989. Nonrandom diversification

within taxonomic assemblages. Syst Zool. 38: 26–37.

Dilly, P.N. & Ryland, J.S. 1985. An intertidal Rhabdopleura

(Hemichordata, Pterobranchia) from Fiji. J. Zool. 205:

611–623.

Dorjes, J. 1968. Die Acoela (Turbellaria) der Deustchen Nord-

seekuste und ein neues system der Ordnung. Z Zool. Syst Evol

6: 56–452.

Eeckhaut, I., McHugh, D., Mardulyn, P., Tiedemann, R.,

Monteyne, D., Jangoux, M. & Milinkovitch, M.C. 2000.

Myzostomida: a link between trochozoans and flatworms?

Proceedings R. Soc. Lond. Series B. Biol. Sci. 267: 1383–1392.

Eernisse, D.J., Albert, J.S. & Anderson, F.E. 1992. Annelida and

arthropoda are not sister taxa – a phylogenetic analysis of

spiralian metazoan morphology. Syst Biol. 41: 305–330.

Ellis, A.E. 1978. British Freshwater Bivalve Molluscs. Synopses of

the British Fauna (New Series) no. 11. Academic Press,

London.

Emig, C.C. 1979. British and Other Phoronids. Synopses of the

British Fauna (New Series) no. 13. Academic Press, London.

Felsenstein, J. 1985. Phylogenies and the comparative method.

Am. Nat. 125: 1–15.

Foote, M. 1996. Models of morphological diversification. In:

Evolutionary Paleobiology (D. Jablonski, D. Erwin & J. Lipps,

eds), pp. 62–86. University of Chicago Press, Chicago.

Funch, P. & Kristensen, R. 1995. Cycliophora is a new phylum

with affinities to the Entoprocta and Ectoprocta. Nature 378:

711–714.

Furuya, H., Tsuneki, K. & Koshida, Y. 1992. 2 New species of the

genus Dicyema (Mesozoa) from octopuses of Japan with notes

on D. misakiense and D. acuticephalum. Zool. Sci. 9: 423–437.

Gage, J.D. & May, R.M. 1993. Biodiversity – a dip into the deep

seas. Nature 365: 609–610.

Gardezi, T. & da Silva, J. 1999. Diversity in relation to body size

in mammals: a comparative study. Am. Nat. 153: 110–123.

Garey, J.R., Schmidt Rhaesa, A., Near, T.J. & Nadler, S.A. 1998.

The evolutionary relationships of rotifers and acanthocepha-

lans. Hydrobiologia 387: 83–91.

Garland, T., Harvey, P.H. & Ives, A.R. 1992. Procedures for the

analysis of comparative data using phylogenetically inde-

pendent contrasts. Syst. Biol. 41: 18–32.

Gibson, R. 1982. British Nemerteans: Keys and Notes for the

Identification of the Species. Synopses of the British Fauna

(New Series) no. 24. Field Studies Council, Shrewbury.

Gibson, R. 1995. Nemertean genera and species of the world – an

annotated checklist of original names and description

244 C. D. L. ORME ET AL .

J . E V O L . B I O L . 1 5 ( 2 0 0 2 ) 2 3 5 – 2 4 7 ª 2 0 0 2 B L A C K W E L L S C I E N C E L T D

citations, synonyms, current taxonomic status, habitats and

recorded zoogeographic distribution. J. Nat. Hist. 29: 271–562.

Ginsberg, J.R. 2000. Biodiversity of mammals. In: Encyclopedia of

Biodiversity (S. Levin, ed.), pp. 777–810. Academic Press, New

York.

Giray, C. & King, G.M. 1996. Protoglossus graveolens, a new

hemichordate (Hemichordata: Enteropneusta: Harrimanidae)

from the northwest Atlantic. Proc. Biol. Soc. Wash. 109:

430–445.

Gittleman, J. & Purvis, A. 1998. Body size and species-richness

in carnivores and primates. Proceedings R. Soc. Lond. Series B.

Biol. Sci. 265: 113–119.

Grassle, J.F. & Maciolek, N.J. 1992. Deep-sea species richness –

regional and local diversity estimates from quantitative

bottom samples. Am. Nat. 139: 313–341.

Greenwood, J.J.D. 2000. Biodiversity of birds. In: Encyclopedia of

Biodiversity, Vol. 1 (S. Levin, ed.), pp. 489–520. Academic

Press, New York.

Halanych, K.M., Bacheller, J.D., Aguinaldo, A.M.A., Liva, S.M.,

Hillis, D.M. & Lake, J.A. 1995. Evidence from 18s ribosomal

DNA that the lophophorates are protostome animals inarti-

culate. Science 267: 1641–1643.

Haukisalmi, V., Heino, M. & Kaitala, V. 1998. Body size variation

in tapeworms (Cestoda): adaptation to intestinal gradients?

Oikos 83: 152–160.

Hawksworth, D. & Kalin-Arroyo, M. 1995. Magnitude and

distribution of biodiversity. In: Global Biodiversity Assessment

(UNEP) (V. Heywood, ed.), pp. 107–192. Cambridge Univer-

sity Press, Cambridge.

Hayward, P.J. 1985. Ctenostome Bryzoans. Synopses of the British

Fauna (New Series) no. 33. Academic Press, London.

Hayward, P.J. & Ryland, J.S. 1979. British Ascophoran Bryzoans.

Synopses of the British Fauna (New Series) no. 14. Academic

Press, London.

Hayward, P.J. & Ryland, J.S. 1985. Cyclostome Bryzoans. Synopses

of the British Fauna (New Series) no. 34. Academic Press,

London.

Hayward, P.J. & Ryland, J.S. 1990. The Marine Fauna of the British

Isles and North-West Europe. Oxford University Press, Oxford.

Helfman, G.S. 2000. Biodiversity of fish. In: Encyclopedia of

Biodiversity, Vol. 1 (S. Levin, ed.), pp. 755–782. Academic

Press, New York.

Higgins, R.P. & Kristensen, R.M. 1986. New Loricifera from

southeastern United States coastal waters. Smithson. Contrib.

Zool. 438: 1–70.

Higgins, R.P. & Kristensen, R.M. 1988. Kinorhyncha from Disko

Island, West Greenland. Smithson. Contrib. Zool. 458: 1–56.

Hochberg, F.G. & Short, R.B. 1983. Dicyemennea discocephala Sp-N

(Mesozoa, Dicyemidae) in a finned Octopod from the

Antarctic. J. Parasit. 69: 963–966.

Holland, P.W.H. 1999. The future of evolutionary developmen-

tal biology. Nature 402: C41–C44.

Hutchinson, G.E. & MacArthur, R.H. 1959. A theoretical

ecological model of size distributions among species of

animals. Am. Nat. 93: 117–125.

Ihaka, R. & Gentleman, R. 1996. R: a language for data analysis

and graphics. J. Comp. Graph. Stat. 5: 299–314.

Israelsson, O. 1999. New light on the enigmatic Xenoturbella

(phylum uncertain): ontogeny and phylogeny. Proceedings R.

Soc. Lond. Series B. Biol. Sci. 266: 835–841.

Ivanov, A.V. 1963. Pogonophora. Academic Press, London.

Jones, A.M. & Baxter, J.M. 1987. Molluscs: Caudofoveata, Soleno-

gastres, Polyplacophora and Scaphopoda. Synopses of the British

Fauna (New Series) no. 37. E.J. Brill Publishing Co., Leiden.

Kalavati, C., Narasimhamurti, C.C. & Suseela, T. 1984. 4 new

species of Mesozoan parasites (Mesozoa, Dicyemidae) from

Cephalopods of Bay of Bengal. Proc. Ind. Acad. Sci. Anim. Sci.

93: 639–654.

Katzourakis, A., Purvis, A., Azmeh, S., Rotheray, G. & Gilbert, F.

2001. Macroevolution of hoverflies (Diptera: Syrphidae): the

effect of using higher-level taxa in studies of biodiversity, and

correlates of species richness. J. Evol. Biol. 14: 219–227.

Kim, J.H., Kim, W. & Cunningham, C.W. 1999. A new

perspective on lower metazoan relationships from 18S rDNA

sequences. Mol. Biol. Evol. 16: 423–427.

King, G.M., Giray, C. & Kornfield, I. 1994. A new Hemichordate,

Saccoglossus bromophenolosus (Hemichordata, Enteropneusta,

Harrimaniidae), from North America. Proc. Biol. Soc. Wash.

107: 383–390.

Kirchner, T.B., Anderson, R.V. & Ingham, R.E. 1980. Natural

selection and the distribution of nematode sizes. Ecology 61:

232–237.

Kochmer, J.P. & Wagner, R.H. 1988. Why are there so many

kinds of passerine birds? Because they are small. A reply to

Raikow. Syst. Zool. 37: 68–69.

Kozloff, E.N. 1992. The genera of the phylum Orthonectida. Cah.

Biol. 33: 377–406.

Kozloff, E.N. 1993. 3 New Species of Stoecharthrum (Phylum

Orthonectida). Cah. Biol. 34: 523–534.

Kristensen, R.M. 1983. Loricifera, a new phylum with Aschel-

minthes characters from the Meiobenthos. Z. Zool. Syst. Evol.

21: 163–180.

Lambshead, P.J.D. 1993. Recent developments in marine ben-

thic biodiversity research. Oceanis 19: 5–24.

Lester, S.M. 1985. Cephalodiscus sp. (Hemichordata, Pterobran-

chia): observations of functional morphology, behavior and

occurrence in shallow water around Bermuda. Mar. Biol. 85:

263–268.

Madsen, F.J. & Hansen, B. 1994. Echinodermata: Holothuroidea.

Marine Invertebrates of Scandanavia no. 9. Universitetsforla-

get, Oslo

Markham, J.C. 1971. The species of Cephalodiscus collected

during Operation Deep Freeze, 1956–59. Ant. Res. Series 17:

83–110.

May, R.H. 1986. The search for patterns in the balance of nature:

advances and retreats. Ecology 67: 1115–1126.

May, R.M. 1992. Biodiversity – bottoms up for the oceans.

Nature 357: 278–279.

May, R.M. 1994. Biological diversity – differences between land

and sea. Proceedings R. Soc. Lond. Series B. Biol. Sci. 343:

105–111.

Millar, R.H. 1970. British Ascidians. Synopses of the British Fauna

(New Series) no. 1. Academic Press, London.

Minelli, A. 1993. Biological Systematics: the State of the Art.

Chapman & Hall, London.3

Morgan, C.I. & King, P.E. 1976. British Tardigrades. Synopses of

the British Fauna (New Series) no. 9. Academic Press,

London.

Nee, S., Barraclough, T. & Harvey, P. 1996. Temporal changes in

biodiversity: detecting patterns and identifying causes. In:

Biodiversity: a Biology of Numbers and Difference (K. Gaston, ed.),

pp. 230–252. Blackwell Science, Oxford.

Body size among metazoan phyla 245

J . E V O L . B I O L . 1 5 ( 2 0 0 2 ) 2 3 5 – 2 4 7 ª 2 0 0 2 B L A C K W E L L S C I E N C E L T D

Nee, S., Mooers, A. & Harvey, P. 1992. Tempo and mode of

evolution revealed from molecular phylogenies. PNAS 89:

8322–8326.

Neubert, E. & Nesemann, H. 1999. Annelida, Clitellata – Bran-

chiobdellida, Acanthbdellea, Hirudinea. Sußwasserfauna von Mitte-

leuropa, Band 6/2. Spectrum. Academischer Verlag,

Heidelberg.

Nielsen, C. 1989. Entoprocts. Synopses of the British Fauna (New

Series) no. 41. E.J. Brill Publishing Co., Leiden.

Nielsen, C. 1995. Animal Evolution: Interrelationships of the Living

Phyla. Oxford University Press, Oxford.

Nielsen, C., Scharff, N. & Eibye-Jacobsen, D. 1996. Cladistic

analyses of the animal kingdom. Biol. J. Linn. Soc. 57: 385–410.

Nordsieck, F. 1969. Der Europaischen Meeresmuscheln (Bivalvia)

Vom Eismeer Bis Kapverden, Mittelmeer und Schwarzes Meer.

Gustav Fischer Verlag, Stuttgart.

Odegaard, F., Diserud, O.H., Engen, S. & Aagaard, K. 2000. The

magnitude of local host specificity for phytophagous insects

and its implications for estimates of global species richness.

Cons. Biol. 14: 1182–1186.

Owens, I.P.F., Bennett, P.M. & Harvey, P.H. 1999. Species

richness among birds: body size, life history, sexual selection

or ecology? Proceedings R. Soc. Lond. Series B. Biol. Sci. 266:

933–939.

Pagel, M.D. 1992. A method for the analysis of comparative data.

J. Theor. Biol. 156: 431–442.

Peters, R.H. 1983. The Ecological Implications of Body Size. Cam-

bridge Studies in Ecology. Cambridge University Press, Cam-

bridge.

Petrochenko, V.I. 1956. Acanthocephala of Domestic and Wild

Animals. Academy of Sciences of the USSR, Moscow.

Petrochenko, V.I. 1958. Acanthocephala of Domestic and Wild

Animals. Academy of Sciences of the USSR, Moscow.

Pierrot-Bults, A.C. & Chidgey, K.C. 1988. Chaetognatha. Synopses

of the British Fauna (New Series) no. 39. E. J. Brill Publishing

Co., Leiden.

Platt, H.M. & Warwick, R.M. 1988. Free Living Marine Nematodes

Part II British Chromadorids. Synopses of the British Fauna

(New Series) no. 38. E. J. Brill Publishing Co., Leiden.

Pontin, R.M. 1978. A Key to the British Freshwater Planktonic

Rotifera. Freshwater Biological Association Scientific Publica-

tion no. 38. Titus Wilson & Son, Kendal.

Poore, G.C.B. & Wilson, G.D.F. 1993. Marine species richness.

Nature 361: 597–598.

Poss, S.G. & Boschung, H.T. 1996. Lancelets (Cephalochordata:

Branchiostomatidae): How many species are valid? Israel

J. Zool. 42: S13–S66.

Pough, F.H. 2000. Biodiversity of reptiles. In: Encyclopedia of

Biodiversity, Vol. 1 (S. Levin, ed.), pp. 145–160. Academic

Press, New York.

Poulin, R. 1996. The evolution of body size in the Monoge-

nea: the role of host size and latitude. Can. J. Zool. 74:

726–732.

Poulin, R. 1997. Egg production in adult trematodes: adaptation

or constraint? Parasitology 114: 195–204.

Poulin, R. 1998. Host and environmental correlates of body size

in ticks (Acari: Argasidae and Ixodidae). Can. J. Zool. 76:

925–930.

Poulin, R. & Morand, S. 2000. Testes size, body size and male-

male competition in acanthocephalan parasites. J. Zool. 250:

551–558.

Prudhoe, S. 1982. British Polyclad Turbellarians. Synopses of the

British Fauna (New Series) no. 26. Cambridge University

Press, Cambridge.

Purvis, A. & Hector, A. 2000. Getting the measure of biodiver-

sity. Nature 405: 212–219.

Purvis, A. & Rambaut, A. 1995. Comparative analysis by

independent contrasts (CAIC): an Apple Macintosh applica-

tion for analysing comparative data. CABIOS 11: 247–251.

Purvis, A. & Webster, A.J. 1999. Phylogenetically independent

comparisons and primate phylogeny. In: Comparative Primate

Socioecology (P. Lee, ed.), pp. 44–70. Cambridge University

Press, Cambridge.

Reaka-Kudla, M.L. 2000. Crustaceans. In: Encyclopedia of Biodi-

versity, Vol. 1 (S. Levin, ed.), pp. 915–943. Academic Press,

New York.

Rex, M.A., Stuart, C.T., Hessler, R.R., Allen, J.A., Sanders, H.L. &

Wilson, G.D.F. 1993. Global-scale latitudinal patterns of

species diversity in the deep sea benthos. Nature 365:

636–639.

Robson, G. 1929. A monograph of the Recent Cephalopoda. Part 1:

Octopodinae. British Museum (Natural History), London.

Robson, G. 1932. A monograph of the Recent Cephalopoda. Part 1: the

Octopoda. British Museum (Natural History), London.

Rohde, K. 2001. Platyhelminthes (Flatuolms). In: Encyclopedia of

Life Sciences, www.els.net. Native Publishing Group, London.6

de Rosa, R., Grenier, J.K., Andreeva, T., Cook, C.E., Adoutte, A.,

Akam, M., Carroll, S.B. & Balavoine, G. 1999. Hox genes in

brachiopods and priapulids and protostome evolution. Nature

399: 772–776.

Rouse, G.W. 1999. Trochophore concepts: ciliary bands and the

evolution of larvae in spiralian Metazoa. Biol. J. Linn. Soc. 66:

411–464.

Rowe, F.W.E., Baker, A.N. & Clark, H.E.S. 1988. The morphol-

ogy, development and taxonomic status of Xyloplax Baker,

Rowe and Clark (1986), with the description of a new species.

Proceedings R. Soc. Lond. Series B. Biol. Sci. 233: 431–459.

Ruhberg, H. 1985. Die Peripatopsidae (Onychophora): Systema-

tik, kologie, Chorologie und phylogenetisch Aspekte. Zoologica

46: 1–184.

Ruiz-Trillo, I., Riutort, M., Littlewood, D.T.J., Herniou, E.A. &

Baguna, J. 1999. Acoel flatworms: earliest extant bilaterian

metazoans, not members of Platyhelminthes. Science 283:

1919–1923.

Ryland, J.S. & Hayward, P.J. 1977. British Anascan Bryzoans.

Synopses of the British Fauna (New Series) no. 10. Academic

Press, London.

Schmidt-Rhaesa, A. 1997. Nematomorpha. Sußwasserfauna von

Mitteleuropa, Band 4/4. Gustav Fischer Verlag, Stuttgart.

Schwank, P. & Bartsch, I. 1990. Gastrotricha und Nemertini.

Sußwasserfauna von Mitteleuropa, Band 3/1+2. Gustav Fischer

Verlag, Stuttgart.

Siemann, E., Tilman, D. & Haarstad, J. 1996. Insect species

diversity, abundance and body size relationships. Nature 380:

704–706.

Siemann, E., Tilman, D. & Haarstad, J. 1999. Abundance,

diversity and body size: patterns from a grassland arthropod

community. J. Anim. Ecol. 68: 824–835.

Silva, M. & Downing, J.A. 1995. CRC Handbook of Mammalian

Body Masses. CRC Press, Boca Raton.

Smith, P.W. 1961. The amphibians and reptiles of Illinois. Ill.

Nat. Hist. Soc. Bull. 28: 1–298.

246 C. D. L. ORME ET AL .

J . E V O L . B I O L . 1 5 ( 2 0 0 2 ) 2 3 5 – 2 4 7 ª 2 0 0 2 B L A C K W E L L S C I E N C E L T D

Stafford, P.J. & Meyer, J.R. 2000. A Guide to the Reptiles of Belize.

Academic Press, New York.

Stechmann, A. & Schlegel, M. 1999. Analysis of the complete

mitochondrial DNA sequence of the brachiopod Terebratulina

retusa places Brachiopoda within the protostomes. Proceedings

R. Soc. Lond. Series B. Biol. Sci. 266: 2043–2052.

Stephen, A.C. & Edmonds, S.J. 1972. The Phyla Sipuncula and

Echiura. Trustees of the Btitish Museum (Natural History),

London.

Sterrer, W. 1991a. Gnathostomulida From Fiji, Tonga and New-

Zealand. Zool. Scripta 20: 107–128.

Sterrer, W. 1991b. Gnathostomulida from Hawaii. Zool. Scripta

20: 129–136.

Sterrer, W. 1991c. Gnathostomulida from Tahiti. Zool. Scripta 20:

137–146.

Stokes, M.D. & Holland, N.D. 1996. Life history characteristics of

the Florida Lancelet, Branchiostoma floridae: some factors

affecting population dynamics in Tampa Bay. Israel J. Zool.

42: S67–S86.

Thomas, R.D.N.K., Shearman, R.M. & Stewart, G.W. 2000.

Evolutionary exploitation of design options by the first

animals with hard skeletons. Science 288: 1239–1242.

Thompson, T.E. & Brown, G.H. 1976. British Opisthobranch

Molluscs. Synopses of the British Fauna (New Series) no. 8.

Academic Press, London.

Trouve, S., Sasal, P., Jourdane, J., Renaud, F. & Morand, S.

1998. The evolution of life history traits in parasitic and free-

living platyhelminthes: a new perspective. Oecologia 115:

370–378.

Tyler, S. & Bush, L. 1998. Turbellarian platyhelminths: taxonomy.

[WWW document] URL http://www.umesci.maine.edu/bio-

logy/turb/index.html.

Van Valen, L. 1973. Body size and numbers of plants and

animals. Evolution 27: 27–35.

Warwick, R.M., Platt, H.M. & Somerfield, P.J. 1998. Free Living

Marine Nematodes Part III Monhysterids. Synopses of the British

Fauna (New Series) no. 53. Field Studies Council, Shrews-

bury.

Wheeler, A. 1978. Key to the Fishes of Northern Europe. Frederick

Warne Ltd, London.

Wilcke, D.E. 1967. Oligochaeta. Die Tierwelt Mitteleuropas. Verlag

Von Quelle & Meyer, Leipzig.

Winnepenninckx, B., Backeljau, T., Mackey, L.Y., Brooks, J.M.,

Dewachter, R., Kumar, S. & Garey, J.R. 1995. 18S Ribosomal-

RNA data indicate that Aschelminthes are polyphyletic in

origin and consist of at least 3 distinct clades. Mol. Biol. Evol.

12: 1132–1137.

Woodwick, K.H. & Sensenbaugh, T. 1985. Saxipendium corona-

tum, new genus, new species (Hemichordata, Enteropneusta)

– the unusual spaghetti worms of the Galapagos rift hydro-

thermal vents. Proc. Biol. Soc. Wash. 98: 351–365.

Wray, G.A., Levinton, J.S. & Shapiro, L.H. 1996. Molecular

evidence for deep Precambrian divergences among metazoan

phyla. Science 274: 568–573.

Yamaguchi, S. 1963. Monogenea and Aspidocotylea. Systema

Helminthum. Interscience Publishers, New York.

Zrzavy, J., Hypsa, V. & Vlaskova, M. 1997. Arthropod phylo-

geny: taxonomic congruence, total evidence and conditional

combination approaches to morphological and molecular data

sets. In: Arthropod Relationships (R. A. Fortey & R. H. Thomas,

eds), pp. 97–107. Chapman & Hall, London.

Zrzavy, J., Mihulka, S., Kepka, P., Bezdek, A. & Tietz, D. 1998.

Phylogeny of the Metazoa based on morphological and 18S

ribosomal DNA evidence. Cladistics 14: 249–285.

Received 23 May 2001; revised 29 October 2001; accepted 1 December

20017

Body size among metazoan phyla 247

J . E V O L . B I O L . 1 5 ( 2 0 0 2 ) 2 3 5 – 2 4 7 ª 2 0 0 2 B L A C K W E L L S C I E N C E L T D