- Email: [email protected]
Testate amoebae and nutrient cycling: peering into the black box of soil ecology
Update 5 Rubin, D.B. (1976) Inference and missing data. Biometrika 63, 581– 590 6 Clark, J.S. and Gelfand, A.E. (2006) A future for models and data in environmental science. Trends Ecol. Evol. 21, 375–380 7 Johnson, J.B. and Omland, K.S. (2004) Model selection in ecology and evolution. Trends Ecol. Evol. 19, 101–108 8 Stephens, P.A. et al. (2007) Inference in ecology and evolution. Trends Ecol. Evol. 22, 192–197 9 Grafen, A. (1988) On the uses of data on lifetime reproductive success. In Reproductive Success (Clutton-Brock, T.H., ed.), pp. 454–471, University of Chicago Press 10 Hadfield, J.D. (2008) Estimating evolutionary parameters when viability selection is operating. Proc. R. Soc. Lond. B Biol. Sci. 275, 723–734 11 Lebreton, J.D. et al. (1992) Modeling survival and testing biological hypotheses using marked animals – a unified approach with casestudies. Ecol. Monogr. 62, 67–118 12 Kunin, W.E. and Gaston, K.J. (1997) The Biology of Rarity: Causes and Consequences of Rare-Common Differences, Chapman & Hall 13 Maddison, W.P. et al. (2007) Estimating a binary character’s effect on speciation and extinction. Syst. Biol. 56, 701–710 14 Fisher, D.O. et al. (2003) Extrinsic versus intrinsic factors in the decline and extinction of Australian marsupials. Proc. R. Soc. Lond. B Biol. Sci. 270, 1801–1808 15 Dempster, A.P. et al. (1977) Maximum likelihood from incomplete data via EM algorithm. J. R. Stat. Soc. B 39, 1–38
Trends in Ecology and Evolution Vol.23 No.11 16 Tanner, M.A. and Wing, H.W. (1987) The calculation of posterior distributions by data augmentation. J. Am. Stat. Assoc. 82, 528–540 17 Schafer, J.L. (1997) Analysis of Incomplete Multivariate Data, Chapman & Hall 18 Schafer, J.L. and Graham, J.W. (2002) Missing data: our view of the state of the art. Psychol. Methods 7, 147–177 19 Freckleton, R.P. et al. (2003) Bergmann’s rule and body size in mammals. Am. Nat. 161, 821–825 20 Smith, R.J. and Jungers, W.L. (1997) Body mass in comparative primatology. J. Hum. Evol. 32, 523–559 21 Raghunathan, T.E. (2004) What do we do with missing data? Some options for analysis of incomplete data. Annu. Rev. Public Health 25, 99– 117 22 Burnham, K.P. and Anderson, D.R. (2002) Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach, Springer-Verlag 23 Clark, J.S. and Bjornstad, C.N. (2004) Population time series: process variability, observation errors, missing values, lags, and hidden states. Ecology 85, 3140–3150 24 Rubin, D.B. (1987) Multiple Imputation for Nonresponse in Surveys, John Wiley & Sons 25 Schafer, J.L. (1999) Multiple imputation: a primer. Stat. Methods Med. Res. 8, 3–15 0169-5347/$ – see front matter ß 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.tree.2008.06.014 Available online 25 September 2008
Research Focus
Testate amoebae and nutrient cycling: peering into the black box of soil ecology David M. Wilkinson School of Natural Sciences and Psychology, Liverpool John Moores University, Byrom Street, Liverpool L3 3AF, UK
In some areas of ecology and evolution, such as the behavioural ecology of many well-studied bird species, it is increasingly difficult to make surprising new discoveries. However, this is not the case in many areas of soil and/or microbial ecology. Two recent studies suggest that the testate amoebae, a microbial group unfamiliar to most biologists, might play a much larger role in soil nutrient cycling than has hitherto been suspected.
The importance of soil The soil is largely ‘out of sight’ to an ecologist without a spade and, for much of the 20th century, this meant that it was also ‘out of mind’ to most ecologists. At best, it tended to be treated as a black box, with the behaviour of its inhabitants lumped together under simple labels such as decomposers or nitrogen fixers [1]. Slowly, things are changing: indeed, it has been noticeable that since I started attending major ecology meetings (in the mid-1980 s), the number of papers and sessions on topics such as soil ecology or mycorrhizae has been increasing. One reason for this increase in interest might be the realisation that studying changes in soil respiration is crucial to predicting the future of the soil as a carbon sink [2]. This could be vital for understanding the effects of global warming. Corresponding author: Wilkinson, D.M. ([email protected]).
596
The silica cycle When ecology textbooks describe soil microbiology, it is often in the context of nutrient cycling. One of the cycles Box 1. Testate amoebae Testate amoebae (also known as testate rhizopods or thecamoebians) are protozoa in which the single cell is enclosed within a shell usually referred to as a test, with a size range of 5–300 mm [11]. The tests are usually composed of either self-secreted material – which can be siliceous or proteinaceous – or ‘agglutinated’ tests, which incorporate material from the environment (such as sand grains, diatoms or the scales of smaller siliceous testates which have been consumed as prey) [12]. Like many microbes, testate amoebae have a relatively modest fossil record – for example, occasionally being preserved in amber. However, recently fossils very similar to modern testates have been described from rocks of around 740 million years old [13]. Although polyphyletic (traditionally placed in the phylum Rhizopoda), testates appear to form a reasonably uniform ecological grouping, occurring around the world in a range of terrestrial and freshwater habitats. They are especially common in habitats with high organic matter content, such as organic-rich soils, peats and mosses [12]. Many, but not all, of the identified morphospecies are cosmopolitan in their distribution [14,15]. The presence of tests means that taxa of testate amoebae can be identified by morphology and their populations can be enumerated by direct counting. Testate amoebae thus represent a microbial group whose ecology can be studied by approaches very similar to those used in the study of macroscopic organisms. There is also a long history of studies of testate amoebae autecology, dating back to 19th century microscopists (Figure I).
Update
Trends in Ecology and Evolution
Vol.23 No.11
Figure I. Testate amoebae from the beautifully illustrated 1879 monograph on North American species by Joseph Leidy [16].
that tends to get very limited coverage in these texts is the silica cycle. However, this cycle is crucially interconnected with the more widely discussed carbon cycle. This is because in the long term, silicate weathering is the main
sink for atmospheric CO2 on geological timescales. In addition, on shorter timescales, leakage of silica from soils to the oceans is important for diatom primary production, which in itself represents a carbon sink when the remains 597
Update
Trends in Ecology and Evolution Vol.23 No.11
Figure 1. Testates being utilised by fungi. Continuing, as yet unpublished, work by Martin Vohnı´k and colleagues is showing that testate amoebae might often be colonised by fungi. Here, Phryganella acropodia is being colonised by the hyphae of a saprotrophic fungus in a laboratory culture of Scots Pine (Pinus sylvestris) needles. Culture studies such as these, combined with field data, should extend our understanding of the role of testate amoebae in nutrient cycling. Scale bar 50 mm. Photo courtesy of the Optical Laboratory of the Institute of Botany ASCR, Pru˚honice.
of diatoms become preserved in ocean sediments (a process also vital to the oxygen cycle) [3,4]. A recent paper by Yoshiyuki Aoki and colleagues [5] escapes from the black box approach to soil ecology by looking in detail at the role of one particular microbial group in the silica cycle. These microbes are the testate amoebae (Box 1), in this case cultures isolated from protozoa living in soils in a pine-oak forest on the Nagoya University campus. The authors studied two taxa, Euglypha rotunda and Trinema enchelys (two very common species found from the tropics to the poles), both of which have silica-rich tests (Box 1). They conclude that, although the amount of silica in tests in forest soils at any one time was relatively small (0.45– 1.57 kg SiO2 ha1), because of the rapid turnover of these protists their annual importance in such soils was much greater (10–277 kg SiO2 ha1 yr1). Indeed, these figures are roughly equivalent to the amount of silica entering the soil from plants via leaf litter. This is important because it seems likely that the small silica-rich testate scales easily dissolve in soils, making silica available in a form plants can readily use (increasing Si mineralisation, i.e. the biological availability of this element). Given the global significance of the silica cycle in soils – such as its link to marine diatoms – the suggestion that a group of protists unknown to most ecologists might be significant players in the soil silica system, with an importance matching that of plants, illustrates how little we know about soil processes of potentially global importance. The nitrogen cycle The silica cycle is not the only biogeochemical cycle where testate amoebae have recently been shown to play an 598
unsuspected role. In a paper in Microbial Ecology, Martin Vohnı´k and colleagues [6] suggest a role for testates in the nutrient cycles of nutrient-poor soils via interactions between some plant species, their mycorrhizal fungi and testate amoebae. The plant species in the Ericaceae (including Rhododendron spp) form ericoid mycorrhizae, in which the fungal partners aid the plant in the uptake of nutrients – especially nitrogen compounds. This relationship allows many plants in this family to survive in acidic organic-rich soils, where most of the nitrogen is in forms not readily available to plant roots [7]. The new work by Vohnı´k et al. [6] suggests that the shells of testate amoebae might be providing hotspots of available nutrients in these soils which are being utilised by the plants with the aid of their mycorrhizal symbionts. Vohnı´k and colleagues studied the roots of three species of Rhododendron collected at different sites in Central Europe. In a mix of observational work on field samples and controlled laboratory experiments, they were able to show intimate associations between the hyphae of the ericoid mycorrhizae and testate amoebae shells. For example, in soils associated with all three Rhododendron species, over 40% of the testate amoeba genus Trigonopyxis were colonised by mycelium of soil fungi. These are large testates (and so presumably a good potential source of nutrients) which also appear to be characteristically associated with Rhododendron soils. In a study of the introduced R. ponticum in England, this testate genus was reliably associated with the shrub, but largely absent from soils from the same woodlands which did not support Rhododendron [8]. Ongoing work by Vohnı´k’s group is finding testate shells colonised by fungi in a variety of soils (Figure 1).
Update
Trends in Ecology and Evolution
These observations are reminiscent of earlier work which showed that under laboratory conditions pine seedlings could obtain nitrogen, in this case via ectomycorrhizal fungi, from soil invertebrates such as the springtail Folsomia candida. In this study, radioactive labelling was used to show that ecologically significant amounts of nitrogen from the invertebrates did indeed end up in the plants [9]. Such labelling studies would be an obvious follow-up to the work of Vohnı´k’s team. The future? These two recent studies draw attention to how much we have still to understand about soil ecology and illustrate that taxonomic groups completely absent from the education of most ecologists might be playing important roles in biogeochemical cycles. They add to the very limited, earlier work which suggested an important role for testate amoebae in the mineralisation of carbon and nitrogen in the soils of coniferous forests [10]. The uncertainty over the effects of climate change on soil microbial processes [2] makes our understanding of this aspect of ecology extremely important. Most of the limited studies on testates and nutrient cycling have been on nutrient-poor soils (with mor humus), and hence there is a need to extend this work to more nutrient-rich (mull) soils. The apparent importance of what is to most biologists an obscure group of microbes raises the question: what else is awaiting discovery by ecologists willing to study microbial ecology and peer into the black soil box? Acknowledgements I thank Martin Vohnı´k for commenting on my interpretation of his work and supplying Figure 1. Three anonymous referees also made helpful suggestions on the manuscript.
Vol.23 No.11
2 Lenton, T.M. and Huntinford, C. (2003) Global terrestrial carbon storage and uncertainties in its temperature sensitivity examined with a simple model. Glob. Change Biol. 9, 1333–1352 3 Berner, R.A. (2004) The Phanerozoic Carbon Cycle, Oxford University Press 4 Street-Perrott, F.A. et al. (2008) Towards an understanding of late Quaternary variations in the continental biogeochemical cycle of silicon: multi-isotope and sediment-flux data for Lake Rutundu, Mt Kenya, East Africa, since 38 ka BP. J. Quaternary Sci. 23, 375–387 5 Aoki, Y. et al. (2007) Silica and testate amoebae in a soil under pine-oak forest. Geoderma 142, 29–35 6 Vohnı´k, M. et al. (2008) Testate amoebae (Arcellinida and Euglyphida) vs. ericoid mycorrhizal and DSE fungi: a possible novel interaction in the mycorrhizosphere of ericaceous plants? Microb. Ecol. 10.1007/ s00248-008-92402-y (http://www.springerlink.com/content/100365) 7 Aerts, R. (2002) The role of various types of mycorrhizal fungi in nutrient cycling and plant competition. In Mycorrhizal Ecology (van der Heijden, M.G.A. and Sanders, I.R., eds), pp. 117–133, Springer 8 Sutton, C.A. and Wilkinson, D.M. (2007) The effects of Rhododendron on testate amoebae communities in woodland soils in North West England. Acta Protozool. 46, 333–338 9 Klironomos, J.K. and Hart, M.M. (2001) Food-web dynamics. Animal nitrogen swap for plant carbon. Nature 410, 651–652 10 Schro¨ter, D. et al. (2003) C and N mineralisation in decomposer food webs of a European forest transect. Oikos 102, 294–308 11 Smith, H.G. et al. (2008) Diversity and biogeography of testate amoebae. Biodivers. Conserv. 17, 329–343 12 Ogden, C.G. and Hedley, R.H. (1980) An Atlas of Freshwater Testate Amoebae, British Museum (Natural History) and Oxford University Press 13 Porter, S.H. et al. (2003) Vase-shaped microfossils from the neoproterzoic chuar group, Grand Canyon; a classification guided by modern testate amoebae. J. Paleontol. 77, 409–429 14 Wilkinson, D.M. (2001) What is the upper size limit for cosmopolitan distribution in free living microorganisms? J. Biogeogr. 28, 285–291 15 Smith, H.G. and Wilkinson, D.M. (2007) Not all free-living microorganisms have cosmopolitan distributions – the case of Nebela (Apodera) vas Certes (Protozoa: Amoebozoa: Arcellinida). J. Biogeogr. 34, 1822–1831 16 Leidy, J. (1879) Fresh-Water Rhizopods of North America, U.S.A. Government Printing Office
References 1 Bardgett, R. (2005) The Biology of Soil: A Community and Ecosystem Approach, Oxford University Press
0169-5347/$ – see front matter ß 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.tree.2008.07.006 Available online 27 September 2008
Book Review
Evolution, ecology and terrorism Natural Security: A Darwinian Approach to a Dangerous World edited by Raphael D. Sagarin and Terence Taylor, University of California Press, Berkeley, 2008, US $49.95 hbk (289 pages) ISBN 978-0-520-25347-6
Paul R. Ehrlich Center for Conservation Biology, Department of Biology, Stanford University, Stanford, CA 94305-5020, USA
This is a pioneering and provocative book. It is based on a series of meetings of scientists to answer an important question: what can be learned about national security (traditionally defined) from an understanding of the workings of evolutionary and ecological systems? Here I use the term ‘traditionally defined’ because many of the environmental threats to security (e.g. lessened food Corresponding author: Ehrlich, P.R. ([email protected]).
security because of population growth, climate change and loss of biodiversity and crucial ecosystem services) are not seriously considered in the book. At its best, the book is extremely informative. For instance, the editors set the scene well with two introductory chapters. A chapter by Daniel Blumstein on lessons from antipredator behavior is superb. In addition to being informative about patterns in nature, the chapter makes some interesting suggestions about lessons for national security – such as learning more about balancing detection signaling and habituation to repeated false alarms (e.g. in relation to ‘threat level orange’). Also excellent is a 599
Trends in Ecology and Evolution Vol.23 No.11 16 Tanner, M.A. and Wing, H.W. (1987) The calculation of posterior distributions by data augmentation. J. Am. Stat. Assoc. 82, 528–540 17 Schafer, J.L. (1997) Analysis of Incomplete Multivariate Data, Chapman & Hall 18 Schafer, J.L. and Graham, J.W. (2002) Missing data: our view of the state of the art. Psychol. Methods 7, 147–177 19 Freckleton, R.P. et al. (2003) Bergmann’s rule and body size in mammals. Am. Nat. 161, 821–825 20 Smith, R.J. and Jungers, W.L. (1997) Body mass in comparative primatology. J. Hum. Evol. 32, 523–559 21 Raghunathan, T.E. (2004) What do we do with missing data? Some options for analysis of incomplete data. Annu. Rev. Public Health 25, 99– 117 22 Burnham, K.P. and Anderson, D.R. (2002) Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach, Springer-Verlag 23 Clark, J.S. and Bjornstad, C.N. (2004) Population time series: process variability, observation errors, missing values, lags, and hidden states. Ecology 85, 3140–3150 24 Rubin, D.B. (1987) Multiple Imputation for Nonresponse in Surveys, John Wiley & Sons 25 Schafer, J.L. (1999) Multiple imputation: a primer. Stat. Methods Med. Res. 8, 3–15 0169-5347/$ – see front matter ß 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.tree.2008.06.014 Available online 25 September 2008
Research Focus
Testate amoebae and nutrient cycling: peering into the black box of soil ecology David M. Wilkinson School of Natural Sciences and Psychology, Liverpool John Moores University, Byrom Street, Liverpool L3 3AF, UK
In some areas of ecology and evolution, such as the behavioural ecology of many well-studied bird species, it is increasingly difficult to make surprising new discoveries. However, this is not the case in many areas of soil and/or microbial ecology. Two recent studies suggest that the testate amoebae, a microbial group unfamiliar to most biologists, might play a much larger role in soil nutrient cycling than has hitherto been suspected.
The importance of soil The soil is largely ‘out of sight’ to an ecologist without a spade and, for much of the 20th century, this meant that it was also ‘out of mind’ to most ecologists. At best, it tended to be treated as a black box, with the behaviour of its inhabitants lumped together under simple labels such as decomposers or nitrogen fixers [1]. Slowly, things are changing: indeed, it has been noticeable that since I started attending major ecology meetings (in the mid-1980 s), the number of papers and sessions on topics such as soil ecology or mycorrhizae has been increasing. One reason for this increase in interest might be the realisation that studying changes in soil respiration is crucial to predicting the future of the soil as a carbon sink [2]. This could be vital for understanding the effects of global warming. Corresponding author: Wilkinson, D.M. ([email protected]).
596
The silica cycle When ecology textbooks describe soil microbiology, it is often in the context of nutrient cycling. One of the cycles Box 1. Testate amoebae Testate amoebae (also known as testate rhizopods or thecamoebians) are protozoa in which the single cell is enclosed within a shell usually referred to as a test, with a size range of 5–300 mm [11]. The tests are usually composed of either self-secreted material – which can be siliceous or proteinaceous – or ‘agglutinated’ tests, which incorporate material from the environment (such as sand grains, diatoms or the scales of smaller siliceous testates which have been consumed as prey) [12]. Like many microbes, testate amoebae have a relatively modest fossil record – for example, occasionally being preserved in amber. However, recently fossils very similar to modern testates have been described from rocks of around 740 million years old [13]. Although polyphyletic (traditionally placed in the phylum Rhizopoda), testates appear to form a reasonably uniform ecological grouping, occurring around the world in a range of terrestrial and freshwater habitats. They are especially common in habitats with high organic matter content, such as organic-rich soils, peats and mosses [12]. Many, but not all, of the identified morphospecies are cosmopolitan in their distribution [14,15]. The presence of tests means that taxa of testate amoebae can be identified by morphology and their populations can be enumerated by direct counting. Testate amoebae thus represent a microbial group whose ecology can be studied by approaches very similar to those used in the study of macroscopic organisms. There is also a long history of studies of testate amoebae autecology, dating back to 19th century microscopists (Figure I).
Update
Trends in Ecology and Evolution
Vol.23 No.11
Figure I. Testate amoebae from the beautifully illustrated 1879 monograph on North American species by Joseph Leidy [16].
that tends to get very limited coverage in these texts is the silica cycle. However, this cycle is crucially interconnected with the more widely discussed carbon cycle. This is because in the long term, silicate weathering is the main
sink for atmospheric CO2 on geological timescales. In addition, on shorter timescales, leakage of silica from soils to the oceans is important for diatom primary production, which in itself represents a carbon sink when the remains 597
Update
Trends in Ecology and Evolution Vol.23 No.11
Figure 1. Testates being utilised by fungi. Continuing, as yet unpublished, work by Martin Vohnı´k and colleagues is showing that testate amoebae might often be colonised by fungi. Here, Phryganella acropodia is being colonised by the hyphae of a saprotrophic fungus in a laboratory culture of Scots Pine (Pinus sylvestris) needles. Culture studies such as these, combined with field data, should extend our understanding of the role of testate amoebae in nutrient cycling. Scale bar 50 mm. Photo courtesy of the Optical Laboratory of the Institute of Botany ASCR, Pru˚honice.
of diatoms become preserved in ocean sediments (a process also vital to the oxygen cycle) [3,4]. A recent paper by Yoshiyuki Aoki and colleagues [5] escapes from the black box approach to soil ecology by looking in detail at the role of one particular microbial group in the silica cycle. These microbes are the testate amoebae (Box 1), in this case cultures isolated from protozoa living in soils in a pine-oak forest on the Nagoya University campus. The authors studied two taxa, Euglypha rotunda and Trinema enchelys (two very common species found from the tropics to the poles), both of which have silica-rich tests (Box 1). They conclude that, although the amount of silica in tests in forest soils at any one time was relatively small (0.45– 1.57 kg SiO2 ha1), because of the rapid turnover of these protists their annual importance in such soils was much greater (10–277 kg SiO2 ha1 yr1). Indeed, these figures are roughly equivalent to the amount of silica entering the soil from plants via leaf litter. This is important because it seems likely that the small silica-rich testate scales easily dissolve in soils, making silica available in a form plants can readily use (increasing Si mineralisation, i.e. the biological availability of this element). Given the global significance of the silica cycle in soils – such as its link to marine diatoms – the suggestion that a group of protists unknown to most ecologists might be significant players in the soil silica system, with an importance matching that of plants, illustrates how little we know about soil processes of potentially global importance. The nitrogen cycle The silica cycle is not the only biogeochemical cycle where testate amoebae have recently been shown to play an 598
unsuspected role. In a paper in Microbial Ecology, Martin Vohnı´k and colleagues [6] suggest a role for testates in the nutrient cycles of nutrient-poor soils via interactions between some plant species, their mycorrhizal fungi and testate amoebae. The plant species in the Ericaceae (including Rhododendron spp) form ericoid mycorrhizae, in which the fungal partners aid the plant in the uptake of nutrients – especially nitrogen compounds. This relationship allows many plants in this family to survive in acidic organic-rich soils, where most of the nitrogen is in forms not readily available to plant roots [7]. The new work by Vohnı´k et al. [6] suggests that the shells of testate amoebae might be providing hotspots of available nutrients in these soils which are being utilised by the plants with the aid of their mycorrhizal symbionts. Vohnı´k and colleagues studied the roots of three species of Rhododendron collected at different sites in Central Europe. In a mix of observational work on field samples and controlled laboratory experiments, they were able to show intimate associations between the hyphae of the ericoid mycorrhizae and testate amoebae shells. For example, in soils associated with all three Rhododendron species, over 40% of the testate amoeba genus Trigonopyxis were colonised by mycelium of soil fungi. These are large testates (and so presumably a good potential source of nutrients) which also appear to be characteristically associated with Rhododendron soils. In a study of the introduced R. ponticum in England, this testate genus was reliably associated with the shrub, but largely absent from soils from the same woodlands which did not support Rhododendron [8]. Ongoing work by Vohnı´k’s group is finding testate shells colonised by fungi in a variety of soils (Figure 1).
Update
Trends in Ecology and Evolution
These observations are reminiscent of earlier work which showed that under laboratory conditions pine seedlings could obtain nitrogen, in this case via ectomycorrhizal fungi, from soil invertebrates such as the springtail Folsomia candida. In this study, radioactive labelling was used to show that ecologically significant amounts of nitrogen from the invertebrates did indeed end up in the plants [9]. Such labelling studies would be an obvious follow-up to the work of Vohnı´k’s team. The future? These two recent studies draw attention to how much we have still to understand about soil ecology and illustrate that taxonomic groups completely absent from the education of most ecologists might be playing important roles in biogeochemical cycles. They add to the very limited, earlier work which suggested an important role for testate amoebae in the mineralisation of carbon and nitrogen in the soils of coniferous forests [10]. The uncertainty over the effects of climate change on soil microbial processes [2] makes our understanding of this aspect of ecology extremely important. Most of the limited studies on testates and nutrient cycling have been on nutrient-poor soils (with mor humus), and hence there is a need to extend this work to more nutrient-rich (mull) soils. The apparent importance of what is to most biologists an obscure group of microbes raises the question: what else is awaiting discovery by ecologists willing to study microbial ecology and peer into the black soil box? Acknowledgements I thank Martin Vohnı´k for commenting on my interpretation of his work and supplying Figure 1. Three anonymous referees also made helpful suggestions on the manuscript.
Vol.23 No.11
2 Lenton, T.M. and Huntinford, C. (2003) Global terrestrial carbon storage and uncertainties in its temperature sensitivity examined with a simple model. Glob. Change Biol. 9, 1333–1352 3 Berner, R.A. (2004) The Phanerozoic Carbon Cycle, Oxford University Press 4 Street-Perrott, F.A. et al. (2008) Towards an understanding of late Quaternary variations in the continental biogeochemical cycle of silicon: multi-isotope and sediment-flux data for Lake Rutundu, Mt Kenya, East Africa, since 38 ka BP. J. Quaternary Sci. 23, 375–387 5 Aoki, Y. et al. (2007) Silica and testate amoebae in a soil under pine-oak forest. Geoderma 142, 29–35 6 Vohnı´k, M. et al. (2008) Testate amoebae (Arcellinida and Euglyphida) vs. ericoid mycorrhizal and DSE fungi: a possible novel interaction in the mycorrhizosphere of ericaceous plants? Microb. Ecol. 10.1007/ s00248-008-92402-y (http://www.springerlink.com/content/100365) 7 Aerts, R. (2002) The role of various types of mycorrhizal fungi in nutrient cycling and plant competition. In Mycorrhizal Ecology (van der Heijden, M.G.A. and Sanders, I.R., eds), pp. 117–133, Springer 8 Sutton, C.A. and Wilkinson, D.M. (2007) The effects of Rhododendron on testate amoebae communities in woodland soils in North West England. Acta Protozool. 46, 333–338 9 Klironomos, J.K. and Hart, M.M. (2001) Food-web dynamics. Animal nitrogen swap for plant carbon. Nature 410, 651–652 10 Schro¨ter, D. et al. (2003) C and N mineralisation in decomposer food webs of a European forest transect. Oikos 102, 294–308 11 Smith, H.G. et al. (2008) Diversity and biogeography of testate amoebae. Biodivers. Conserv. 17, 329–343 12 Ogden, C.G. and Hedley, R.H. (1980) An Atlas of Freshwater Testate Amoebae, British Museum (Natural History) and Oxford University Press 13 Porter, S.H. et al. (2003) Vase-shaped microfossils from the neoproterzoic chuar group, Grand Canyon; a classification guided by modern testate amoebae. J. Paleontol. 77, 409–429 14 Wilkinson, D.M. (2001) What is the upper size limit for cosmopolitan distribution in free living microorganisms? J. Biogeogr. 28, 285–291 15 Smith, H.G. and Wilkinson, D.M. (2007) Not all free-living microorganisms have cosmopolitan distributions – the case of Nebela (Apodera) vas Certes (Protozoa: Amoebozoa: Arcellinida). J. Biogeogr. 34, 1822–1831 16 Leidy, J. (1879) Fresh-Water Rhizopods of North America, U.S.A. Government Printing Office
References 1 Bardgett, R. (2005) The Biology of Soil: A Community and Ecosystem Approach, Oxford University Press
0169-5347/$ – see front matter ß 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.tree.2008.07.006 Available online 27 September 2008
Book Review
Evolution, ecology and terrorism Natural Security: A Darwinian Approach to a Dangerous World edited by Raphael D. Sagarin and Terence Taylor, University of California Press, Berkeley, 2008, US $49.95 hbk (289 pages) ISBN 978-0-520-25347-6
Paul R. Ehrlich Center for Conservation Biology, Department of Biology, Stanford University, Stanford, CA 94305-5020, USA
This is a pioneering and provocative book. It is based on a series of meetings of scientists to answer an important question: what can be learned about national security (traditionally defined) from an understanding of the workings of evolutionary and ecological systems? Here I use the term ‘traditionally defined’ because many of the environmental threats to security (e.g. lessened food Corresponding author: Ehrlich, P.R. ([email protected]).
security because of population growth, climate change and loss of biodiversity and crucial ecosystem services) are not seriously considered in the book. At its best, the book is extremely informative. For instance, the editors set the scene well with two introductory chapters. A chapter by Daniel Blumstein on lessons from antipredator behavior is superb. In addition to being informative about patterns in nature, the chapter makes some interesting suggestions about lessons for national security – such as learning more about balancing detection signaling and habituation to repeated false alarms (e.g. in relation to ‘threat level orange’). Also excellent is a 599