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All animals are equal, but some animals are more equal than others
Journal of Experimental Marine Biology and Ecology 366 (2008) 184–186
Contents lists available at ScienceDirect
Journal of Experimental Marine Biology and Ecology j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / j e m b e
All animals are equal, but some animals are more equal than others R.M. Warwick ⁎, P.J. Somerfield Plymouth Marine Laboratory, Prospect Place, West Hoe, Plymouth, PL1 3DH, UK
a r t i c l e
i n f o
Keywords: Biodiversity Classification Marine animals Species Taxonomic distinctness Taxonomy
a b s t r a c t If the number of animal species is to be used as a measure of ‘biodiversity’, or if distributions of species among taxa of higher rank are to be used to infer evolutionary or ecological patterns, then we need to know whether animal phyla are consistently subdivided in such a way that each species represents an equal division of life's diversity. It is widely assumed, intuitively, that the traditional Linnean classification of marine animals is inconsistent between different major groups. We demonstrate formally that this is the case. For this exercise we use a consistent taxonomic hierarchy for all marine phyla within a relatively large region, the UK. The value of average taxonomic distinctness Δ+ is shown to vary considerably between phyla. There is a highly significant relationship between the number of species within a phylum and the average distance through the taxonomic hierarchy between those species. This implies that larger phyla are broken up into relatively small units at higher taxonomic levels. Interestingly, this occurs independently of the perceived taxonomic difficulty within phyla. Species number is therefore a poor unit of currency for evaluating biodiversity, and studies which infer patterns using distributions of, or ratios between, higher taxa through time should take phyletic differences into account. © 2008 Elsevier B.V. All rights reserved.
1. Introduction Most explicit attempts to quantify biodiversity, the diversity of ecosystems, species and genes, have concentrated on the specific and genetic levels in the hierarchy of biological organisation (Gaston, 1996). Amongst animals two taxonomic levels may be considered fundamental, species and phyla. Between these two levels mankind, for convenience, inserts a taxonomic hierarchy which allows the classification of animals. This hierarchy may also be considered as a surrogate for genetic diversity, in that species within the same genus, for example, may be expected to be less genetically distinct than species in separate families, orders or classes. If the number of animal species in a sampling unit (be that a quadrat, a national park, or a region of the globe) is to be used as a measure of ‘biodiversity’ then we need to know whether animal phyla are consistently subdivided in such a way that each species represents an equal division of life's diversity. This is particularly important for studies of marine benthic biodiversity, because the marine benthos comprise a higher number of phyla that any other realm on the globe (Ray, 1988; May, 1988; Norse, 1993; Warwick, 1996). It is widely assumed, intuitively, that the traditional Linnean classification of animals is inconsistent between different major groups (Ricklefs and Schluter, 1993). Further, this inconsistency is perceived to relate to the taxonomic difficulty within groups of animals and the intensity to
⁎ Corresponding author. Tel.: +44 1752 633100; fax: +44 1752 633101. E-mail address: [email protected] (R.M. Warwick). 0022-0981/$ – see front matter © 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.jembe.2008.07.023
which that group has been studied (May, 1988). Among marine animals, for example, the Mollusca, with their abundance of hard parts and long history of professional and amateur attention, might be expected to be more finely split into smaller taxonomic units than, say, the Annelida, the taxonomy of which is considered the preserve of specialists. These notions are frequently voiced among marine benthic ecologists, but never appear in print because the potential inconsistencies have not been formally demonstrated or quantified. Here we describe an analysis which addresses the question of whether species in different phyla differ in the extent to which they are assigned to taxonomic levels of higher rank. 2. Methods As a measure of inter-relatedness between species we use Δ+, the average taxonomic distinctness (Clarke and Warwick, 1998; Warwick and Clarke, 2001) of species, within phyla. Essentially this is the average path length between every pair of species traced through a taxonomic tree: h i Δþ ¼ ∑∑ibj ωij =½SðS−1Þ=2 where S is the number of species, ωij is the taxonomic distances through the classification tree between every pair of species (the first from species i and the second from species j), and the double summation ranges over all pairs i and j of these species (i b j). For a standard Linnean classification these are discrete distances, the simple trees in Fig. 1 illustrating path lengths of one step (species
R.M. Warwick, P.J. Somerfield / Journal of Experimental Marine Biology and Ecology 366 (2008) 184–186
185
3. Results
Fig. 1. Three simple taxonomic trees illustrating the calculation of Δ+. There are three equal steps. In A all seven species belong to the same genus so that the average step length between them is 1. In B all seven species belong to different genera but the same family, so the average step length is 2. C shows that this same value of 2 can be derived from different configurations of the taxonomic hierarchy.
The value of average taxonomic distinctness is shown to vary considerably between phyla (Fig. 2). There is a highly significant relationship (Δ+ = 39.0 + 9.95 log10(S), F1,17 = 16.87, p = 0.001) between the number of species within a phylum, and the average distance through the taxonomic hierarchy between those species. Larger phyla are broken up into relatively small units at higher taxonomic levels. Interestingly, this occurs somewhat independently of the perceived taxonomic difficulty within phyla. For example, Mollusca and Annelida both lie close to the regression line. Nevertheless, it must be said that the Echinodermata, which have also received a great deal of both professional and amateur attention, have the Δ+ value that is highest above the regression line, while the Sipuncula and Entoprocta, lacking in both hard parts and charisma, have the lowest values and are well below the regression line. 4. Discussion
in the same genus), two steps (different genera but same family) and three steps (different families but same order). The trees can obviously be extended up to higher taxonomic levels. Fig. 1 uses a simple linear scaling whereby the largest number of steps in the tree (two species at greatest taxonomic distance apart) has a value of 3. Clearly a phylogenetic classification would be preferable to a simple Linnean one (Pleijel and Rouse, 2003), but unfortunately fully resolved cladograms for the benthic phyla involved here are not available. High values indicate that on average species are distinct, low values indicate that on average they are closely related. For this exercise we need a consistent taxonomic hierarchy for all phyla within a relatively large region. Most phyla are marine and for the UK a marine species a directory exists (Howson and Picton, 1997) which includes the necessary information. We have calculated average taxonomic distinctness (Δ+) of all marine invertebrate species recorded from UK waters within each phylum containing more than 10 species. The taxonomic levels used for each phylum were species, genus, family, order, class and phylum, i.e. 5 steps each of value 1. For species, as units of biodiversity, to have equal worth across phyla then the average taxonomic distinctness within each phylum should be the same.
This study focuses on marine phyla, and it should be remembered that in addition to the fact that most phyla are found in the marine realm, particularly the benthos (May, 1988), the distribution of diversity among higher taxa differs greatly between the land and the sea. Although only 20% of animal species are marine, the sea contains systematically higher proportions of higher taxonomic units, culminating in more than 90% of classes (Ray, 1985). Most recorded animal species are insects, and 40% of those are beetles (May, 1988) so it would seem likely that terrestrial species within phyla should be more closely related to each other than marine species, continuing the relationship observed here to higher taxa with greater numbers of species. This would be an interesting basis for a further study. As noted by May (1988) any information about diversity is clouded by uncertainties about how different two groups of organisms have to be before someone assigns them to different species, by the fact that some taxa have been studied in much more detail than others, and by the recognition that even within well studied taxa some workers recognise more species than others. If it is to be believed that higher taxa are biologically meaningful, and not some construct of convenience to assist humans in their desire to classify things, then we need some assurance that the assignment of species to higher
Fig. 2. Average taxonomic distinctness (Δ+) of all marine invertebrate species recorded from UK waters within each phylum containing more than 10 species, plotted against the number of species (S) recorded in each phylum. The dashed line is a least squares regression of the data.
186
R.M. Warwick, P.J. Somerfield / Journal of Experimental Marine Biology and Ecology 366 (2008) 184–186
taxonomic levels is, in some sense, consistent. We have demonstrated that the classification of species is inconsistent between different animal groups, and as a basic unit for evaluating biodiversity species number is, therefore, a poor measure. Species that are closely related may be considered to be less ‘unique’, and therefore to have less conservation value, than species that have few close living relatives (May, 1990; Faith, 1994; Humphries et al., 1995). Species from large phyla appear to be more unique than they should, whereas species from small phyla, which greatly increase the overall genetic diversity within assemblages where they occur, appear to be less unique than they should. The fact that larger phyla are broken up into relatively small units at higher taxonomic levels is probably an inherent attribute of any classification system. It has to do with the management of the classification: the hierarchical model accommodates the need for an efficient management of the categories and taxa in the Linnean system. Studies which use the number of species as the currency of biodiversity neglect the fact that the currency varies in value depending on the overall composition of the assemblages being studied. Criticism could similarly be levelled at studies in which overall values of Δ+ are determined for samples comprising differing proportions of these phyla (e.g. Ellingsen et al., 2005). However, in ecological studies of soft-bottom macrobenthos, it should be noted that the four major phyla encountered (annelids, molluscs, crustaceans and echinoderms) have approximately equivalent values of Δ+ within their regional species pools, so that calculations of overall taxonomic distinctness based on samples comprising differing proportions of them will usually be valid. Taxa of higher rank are considered to be older than taxa of lower rank, and a considerable body of work has focused on the distribution of species among taxa of higher rank to elucidate the origins of differences in diversity among communities (Ricklefs and Schluter, 1993). Such approaches are often applied to palaeontological data. For example, Jablonski et al. (1983) demonstrated that higher taxa of marine invertebrates arise in near-shore environments and subsequently spread offshore and ultimately to the deep sea, whereas lower-level taxa (families, genera) originate more evenly across the environmental gradient. The validity of such studies depends on higher taxa in different phyla having equivalent weight. We are not sure that they do. It may be that the distributions of taxa of lower rank among taxa of higher rank result from a time-dependent branching process (Chu and Adami, 1999), it may be that higher taxa represent a window into the evolution of species and communities (May, 1988; Ricklefs and Schluter, 1993), it may be that decreasing subtaxon-taxon ratios are simply a non-linear function of increasing sample size (Gotelli and Colwell, 2001), or it may be that the distribution of species among higher taxa tells us more about taxonomists than it does about relationships among species. Whatever the truth, this study tells us
that the relative weighting of higher taxa differs between phyla, and this should be taken into account in studies examining patterns in diversity in time or space. Acknowledgements In the spirit of Steinbeck's dedication of Cannery Row to his friend Ed Ricketts, this offering is for our friend John Gray, who would have known why or should. It is a contribution to the Plymouth Marine Laboratory's core strategic research programme and was supported by the UK Natural Environment Research Council (NERC) and the UK Department for Environment, Food and Rural Affairs (Defra) through project ME3109. We are grateful to Dr. Christos Arvanitidis for helpful comments on an earlier draft. RMW acknowledges his position as an honorary fellow of the Plymouth Marine Laboratory. [SS] References Chu, J., Adami, C., 1999. A simple explanation for taxon abundance patterns. Proc. Natl. Acad. Sci. 96, 15017–15019. Clarke, K.R., Warwick, R.M., 1998. A taxonomic distinctness index and its statistical properties. J. Appl. Ecol. 35, 523–531. Ellingsen, K.E., Clarke, K.R., Somerfield, P.J., Warwick, R.M., 2005. Taxonomic distinctness as a measure of diversity applied over a large scale: the benthos of the Norwegian continental shelf. J. Anim. Ecol. 74, 1069–1079. Faith, D.P., 1994. Phylogenetic pattern and the quantification of organismal biodiversity. Philos. Trans. R. Soc. Lond., Ser. B Biol. Sci. 345, 45–58. Gaston, K.J. (Ed.), 1996. Biodiversity: a biology of numbers and difference. Blackwell Science, Oxford. Gotelli, N.J., Colwell, R.K., 2001. Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecol. Lett. 4, 379–391. Howson, C.M., Picton, B.E., 1997. The Species Directory of the Marine Fauna and Flora of the British Isles and Surrounding Seas. Ulster Museum and Marine Conservation Society, Belfast and Ross-on-Wye. Humphries, C.J., Williams, P.H., Vane-Wright, R.I., 1995. Measuring biodiversity value for conservation. Ann. Rev. Ecol. Syst. 26, 93–111. Jablonski, D., Sepowski, J.J., Botjer, D.J., Sheehan, D.M., 1983. Onshore-offshore patterns in the evolution of Phanerozoic shelf communities. Science 222, 1123–1125. May, R.M., 1988. How many species are there on Earth? Science 241, 1441–1449. May, R.M., 1990. Taxonomy as destiny. Nature 347, 129–130. Norse, E.A., 1993. Global marine biological diversity: a strategy for building conservation into decision making. Island Press, Washington, D.C. Pleijel, F., Rouse, G.W., 2003. Ceci n'est pas une pipe: names, clades and phylogenetic nomenclature. J. Zool. Syst. Evol. Res. 41, 162–174. Ray, G.C., 1985. Man and the sea – the ecological challenge. Am. Zool. 25, 451–468. Ray, G.C., 1988. Ecological diversity in coastal zones and oceans. In: Wison, E.O. (Ed.), Biodiversity. National Academy Press, Washington, D.C., pp. 36–50. Ricklefs, R.E., Schluter, D., 1993. Species diversity: regional and historical influences. In: Ricklefs, R.E., Schluter, D. (Eds.), Species diversity in ecological communities: historical and geographical perspectives. The University of Chicago Press, Chicago. Warwick, R.M., 1996. Biodiversity and production on the sea floor. In: Hempel, G. (Ed.), The oceans and the poles. Gustav Fischer Verlag, Jena, pp. 217–227. Warwick, R.M., Clarke, K.R., 2001. Practical measures of marine biodiversity based on relatedness of species. Oceanogr. Mar. Biol. Ann. Rev. 39, 207–231.
Contents lists available at ScienceDirect
Journal of Experimental Marine Biology and Ecology j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / j e m b e
All animals are equal, but some animals are more equal than others R.M. Warwick ⁎, P.J. Somerfield Plymouth Marine Laboratory, Prospect Place, West Hoe, Plymouth, PL1 3DH, UK
a r t i c l e
i n f o
Keywords: Biodiversity Classification Marine animals Species Taxonomic distinctness Taxonomy
a b s t r a c t If the number of animal species is to be used as a measure of ‘biodiversity’, or if distributions of species among taxa of higher rank are to be used to infer evolutionary or ecological patterns, then we need to know whether animal phyla are consistently subdivided in such a way that each species represents an equal division of life's diversity. It is widely assumed, intuitively, that the traditional Linnean classification of marine animals is inconsistent between different major groups. We demonstrate formally that this is the case. For this exercise we use a consistent taxonomic hierarchy for all marine phyla within a relatively large region, the UK. The value of average taxonomic distinctness Δ+ is shown to vary considerably between phyla. There is a highly significant relationship between the number of species within a phylum and the average distance through the taxonomic hierarchy between those species. This implies that larger phyla are broken up into relatively small units at higher taxonomic levels. Interestingly, this occurs independently of the perceived taxonomic difficulty within phyla. Species number is therefore a poor unit of currency for evaluating biodiversity, and studies which infer patterns using distributions of, or ratios between, higher taxa through time should take phyletic differences into account. © 2008 Elsevier B.V. All rights reserved.
1. Introduction Most explicit attempts to quantify biodiversity, the diversity of ecosystems, species and genes, have concentrated on the specific and genetic levels in the hierarchy of biological organisation (Gaston, 1996). Amongst animals two taxonomic levels may be considered fundamental, species and phyla. Between these two levels mankind, for convenience, inserts a taxonomic hierarchy which allows the classification of animals. This hierarchy may also be considered as a surrogate for genetic diversity, in that species within the same genus, for example, may be expected to be less genetically distinct than species in separate families, orders or classes. If the number of animal species in a sampling unit (be that a quadrat, a national park, or a region of the globe) is to be used as a measure of ‘biodiversity’ then we need to know whether animal phyla are consistently subdivided in such a way that each species represents an equal division of life's diversity. This is particularly important for studies of marine benthic biodiversity, because the marine benthos comprise a higher number of phyla that any other realm on the globe (Ray, 1988; May, 1988; Norse, 1993; Warwick, 1996). It is widely assumed, intuitively, that the traditional Linnean classification of animals is inconsistent between different major groups (Ricklefs and Schluter, 1993). Further, this inconsistency is perceived to relate to the taxonomic difficulty within groups of animals and the intensity to
⁎ Corresponding author. Tel.: +44 1752 633100; fax: +44 1752 633101. E-mail address: [email protected] (R.M. Warwick). 0022-0981/$ – see front matter © 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.jembe.2008.07.023
which that group has been studied (May, 1988). Among marine animals, for example, the Mollusca, with their abundance of hard parts and long history of professional and amateur attention, might be expected to be more finely split into smaller taxonomic units than, say, the Annelida, the taxonomy of which is considered the preserve of specialists. These notions are frequently voiced among marine benthic ecologists, but never appear in print because the potential inconsistencies have not been formally demonstrated or quantified. Here we describe an analysis which addresses the question of whether species in different phyla differ in the extent to which they are assigned to taxonomic levels of higher rank. 2. Methods As a measure of inter-relatedness between species we use Δ+, the average taxonomic distinctness (Clarke and Warwick, 1998; Warwick and Clarke, 2001) of species, within phyla. Essentially this is the average path length between every pair of species traced through a taxonomic tree: h i Δþ ¼ ∑∑ibj ωij =½SðS−1Þ=2 where S is the number of species, ωij is the taxonomic distances through the classification tree between every pair of species (the first from species i and the second from species j), and the double summation ranges over all pairs i and j of these species (i b j). For a standard Linnean classification these are discrete distances, the simple trees in Fig. 1 illustrating path lengths of one step (species
R.M. Warwick, P.J. Somerfield / Journal of Experimental Marine Biology and Ecology 366 (2008) 184–186
185
3. Results
Fig. 1. Three simple taxonomic trees illustrating the calculation of Δ+. There are three equal steps. In A all seven species belong to the same genus so that the average step length between them is 1. In B all seven species belong to different genera but the same family, so the average step length is 2. C shows that this same value of 2 can be derived from different configurations of the taxonomic hierarchy.
The value of average taxonomic distinctness is shown to vary considerably between phyla (Fig. 2). There is a highly significant relationship (Δ+ = 39.0 + 9.95 log10(S), F1,17 = 16.87, p = 0.001) between the number of species within a phylum, and the average distance through the taxonomic hierarchy between those species. Larger phyla are broken up into relatively small units at higher taxonomic levels. Interestingly, this occurs somewhat independently of the perceived taxonomic difficulty within phyla. For example, Mollusca and Annelida both lie close to the regression line. Nevertheless, it must be said that the Echinodermata, which have also received a great deal of both professional and amateur attention, have the Δ+ value that is highest above the regression line, while the Sipuncula and Entoprocta, lacking in both hard parts and charisma, have the lowest values and are well below the regression line. 4. Discussion
in the same genus), two steps (different genera but same family) and three steps (different families but same order). The trees can obviously be extended up to higher taxonomic levels. Fig. 1 uses a simple linear scaling whereby the largest number of steps in the tree (two species at greatest taxonomic distance apart) has a value of 3. Clearly a phylogenetic classification would be preferable to a simple Linnean one (Pleijel and Rouse, 2003), but unfortunately fully resolved cladograms for the benthic phyla involved here are not available. High values indicate that on average species are distinct, low values indicate that on average they are closely related. For this exercise we need a consistent taxonomic hierarchy for all phyla within a relatively large region. Most phyla are marine and for the UK a marine species a directory exists (Howson and Picton, 1997) which includes the necessary information. We have calculated average taxonomic distinctness (Δ+) of all marine invertebrate species recorded from UK waters within each phylum containing more than 10 species. The taxonomic levels used for each phylum were species, genus, family, order, class and phylum, i.e. 5 steps each of value 1. For species, as units of biodiversity, to have equal worth across phyla then the average taxonomic distinctness within each phylum should be the same.
This study focuses on marine phyla, and it should be remembered that in addition to the fact that most phyla are found in the marine realm, particularly the benthos (May, 1988), the distribution of diversity among higher taxa differs greatly between the land and the sea. Although only 20% of animal species are marine, the sea contains systematically higher proportions of higher taxonomic units, culminating in more than 90% of classes (Ray, 1985). Most recorded animal species are insects, and 40% of those are beetles (May, 1988) so it would seem likely that terrestrial species within phyla should be more closely related to each other than marine species, continuing the relationship observed here to higher taxa with greater numbers of species. This would be an interesting basis for a further study. As noted by May (1988) any information about diversity is clouded by uncertainties about how different two groups of organisms have to be before someone assigns them to different species, by the fact that some taxa have been studied in much more detail than others, and by the recognition that even within well studied taxa some workers recognise more species than others. If it is to be believed that higher taxa are biologically meaningful, and not some construct of convenience to assist humans in their desire to classify things, then we need some assurance that the assignment of species to higher
Fig. 2. Average taxonomic distinctness (Δ+) of all marine invertebrate species recorded from UK waters within each phylum containing more than 10 species, plotted against the number of species (S) recorded in each phylum. The dashed line is a least squares regression of the data.
186
R.M. Warwick, P.J. Somerfield / Journal of Experimental Marine Biology and Ecology 366 (2008) 184–186
taxonomic levels is, in some sense, consistent. We have demonstrated that the classification of species is inconsistent between different animal groups, and as a basic unit for evaluating biodiversity species number is, therefore, a poor measure. Species that are closely related may be considered to be less ‘unique’, and therefore to have less conservation value, than species that have few close living relatives (May, 1990; Faith, 1994; Humphries et al., 1995). Species from large phyla appear to be more unique than they should, whereas species from small phyla, which greatly increase the overall genetic diversity within assemblages where they occur, appear to be less unique than they should. The fact that larger phyla are broken up into relatively small units at higher taxonomic levels is probably an inherent attribute of any classification system. It has to do with the management of the classification: the hierarchical model accommodates the need for an efficient management of the categories and taxa in the Linnean system. Studies which use the number of species as the currency of biodiversity neglect the fact that the currency varies in value depending on the overall composition of the assemblages being studied. Criticism could similarly be levelled at studies in which overall values of Δ+ are determined for samples comprising differing proportions of these phyla (e.g. Ellingsen et al., 2005). However, in ecological studies of soft-bottom macrobenthos, it should be noted that the four major phyla encountered (annelids, molluscs, crustaceans and echinoderms) have approximately equivalent values of Δ+ within their regional species pools, so that calculations of overall taxonomic distinctness based on samples comprising differing proportions of them will usually be valid. Taxa of higher rank are considered to be older than taxa of lower rank, and a considerable body of work has focused on the distribution of species among taxa of higher rank to elucidate the origins of differences in diversity among communities (Ricklefs and Schluter, 1993). Such approaches are often applied to palaeontological data. For example, Jablonski et al. (1983) demonstrated that higher taxa of marine invertebrates arise in near-shore environments and subsequently spread offshore and ultimately to the deep sea, whereas lower-level taxa (families, genera) originate more evenly across the environmental gradient. The validity of such studies depends on higher taxa in different phyla having equivalent weight. We are not sure that they do. It may be that the distributions of taxa of lower rank among taxa of higher rank result from a time-dependent branching process (Chu and Adami, 1999), it may be that higher taxa represent a window into the evolution of species and communities (May, 1988; Ricklefs and Schluter, 1993), it may be that decreasing subtaxon-taxon ratios are simply a non-linear function of increasing sample size (Gotelli and Colwell, 2001), or it may be that the distribution of species among higher taxa tells us more about taxonomists than it does about relationships among species. Whatever the truth, this study tells us
that the relative weighting of higher taxa differs between phyla, and this should be taken into account in studies examining patterns in diversity in time or space. Acknowledgements In the spirit of Steinbeck's dedication of Cannery Row to his friend Ed Ricketts, this offering is for our friend John Gray, who would have known why or should. It is a contribution to the Plymouth Marine Laboratory's core strategic research programme and was supported by the UK Natural Environment Research Council (NERC) and the UK Department for Environment, Food and Rural Affairs (Defra) through project ME3109. We are grateful to Dr. Christos Arvanitidis for helpful comments on an earlier draft. RMW acknowledges his position as an honorary fellow of the Plymouth Marine Laboratory. [SS] References Chu, J., Adami, C., 1999. A simple explanation for taxon abundance patterns. Proc. Natl. Acad. Sci. 96, 15017–15019. Clarke, K.R., Warwick, R.M., 1998. A taxonomic distinctness index and its statistical properties. J. Appl. Ecol. 35, 523–531. Ellingsen, K.E., Clarke, K.R., Somerfield, P.J., Warwick, R.M., 2005. Taxonomic distinctness as a measure of diversity applied over a large scale: the benthos of the Norwegian continental shelf. J. Anim. Ecol. 74, 1069–1079. Faith, D.P., 1994. Phylogenetic pattern and the quantification of organismal biodiversity. Philos. Trans. R. Soc. Lond., Ser. B Biol. Sci. 345, 45–58. Gaston, K.J. (Ed.), 1996. Biodiversity: a biology of numbers and difference. Blackwell Science, Oxford. Gotelli, N.J., Colwell, R.K., 2001. Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecol. Lett. 4, 379–391. Howson, C.M., Picton, B.E., 1997. The Species Directory of the Marine Fauna and Flora of the British Isles and Surrounding Seas. Ulster Museum and Marine Conservation Society, Belfast and Ross-on-Wye. Humphries, C.J., Williams, P.H., Vane-Wright, R.I., 1995. Measuring biodiversity value for conservation. Ann. Rev. Ecol. Syst. 26, 93–111. Jablonski, D., Sepowski, J.J., Botjer, D.J., Sheehan, D.M., 1983. Onshore-offshore patterns in the evolution of Phanerozoic shelf communities. Science 222, 1123–1125. May, R.M., 1988. How many species are there on Earth? Science 241, 1441–1449. May, R.M., 1990. Taxonomy as destiny. Nature 347, 129–130. Norse, E.A., 1993. Global marine biological diversity: a strategy for building conservation into decision making. Island Press, Washington, D.C. Pleijel, F., Rouse, G.W., 2003. Ceci n'est pas une pipe: names, clades and phylogenetic nomenclature. J. Zool. Syst. Evol. Res. 41, 162–174. Ray, G.C., 1985. Man and the sea – the ecological challenge. Am. Zool. 25, 451–468. Ray, G.C., 1988. Ecological diversity in coastal zones and oceans. In: Wison, E.O. (Ed.), Biodiversity. National Academy Press, Washington, D.C., pp. 36–50. Ricklefs, R.E., Schluter, D., 1993. Species diversity: regional and historical influences. In: Ricklefs, R.E., Schluter, D. (Eds.), Species diversity in ecological communities: historical and geographical perspectives. The University of Chicago Press, Chicago. Warwick, R.M., 1996. Biodiversity and production on the sea floor. In: Hempel, G. (Ed.), The oceans and the poles. Gustav Fischer Verlag, Jena, pp. 217–227. Warwick, R.M., Clarke, K.R., 2001. Practical measures of marine biodiversity based on relatedness of species. Oceanogr. Mar. Biol. Ann. Rev. 39, 207–231.