- Email: [email protected]
Naturally eutrophic lakes: reality, myth or myopia?
NEWS
4% COMMENT
tural practices on lakes and the increased nutrient loadings associated with medieval agriculture. There is evidence for the long-term expansion of agriculture in the North Shropshire area? the pollen record at Crose Mere indicates that hemp retting took are >300 p,g 1-l. Today, many of the meres place at this lake from the Iron Age onare dominated by blue-green algal (cyano- ward@. Combined with deforestation, soil bacterial) crop+, like many other eu- erosion and presumably manuring of the trophic systems, It is, of course, blueprimitive agriculture systems, this retting greens that create the widely held public must have resulted in a substantial transimage of a eutrophic lake: pea-green with fer of P from the terrestrial to the aquatic algal scums accumulating along the shore- ecosystem: in part, it is the legacy of this line. type of perturbation that is seen in the One wonders, however, what the aver- meres today. This conclusion is confirmed age European peasant farmer during the by diatom analyses at two other nearby medieval period thought of the bluelakes, Ellesmere and Rotherne Mere, where green algal problem, because it appears oligo-mesotrophic diatom floras are respecies indicative that it has been around for some time. In a placed by Stephanodiscus second and contrasting paper, van Gee1 of enriched systems (R.J. Nelms, unpubet al.5 have documented the abundance of lished PhD thesis, Liverpool Polytechnic, two blue-green genera (AphQnizo~enon 1984). As with many other lowland lakes and A~Q~eRa)over hundreds of years, by in Europe~“,ll, the meres are not naturally identifying their akinetes preserved in the eutrophic systems, they have merely been sediments of Lake Cosciaz in the Na Jazach eutrophic for a long time - probably hunlake district of central Poland. Akinetes are dreds of years. resting stages produced by blue-green algae: because of their resistant cell wall, Phosphorus sources they preserve well in lake sediment@. AklnAs it was difficult to identify a contemetes are, in fact, produced by only a few porary source to account for the high P blue-green algal species, but the fossil concentrations in some of the seepage record of these important contributors to lakes, Moss et al.3 concluded that some the phytoplankton can be extended by use of the meres are probably naturally euof the pigment record7. trophic, with the local bedrockas the most By present-day standards, Gosciaz likely P source. While there must be a natuwould have been considered eutrophic ral background contribution to the nufrom the 15th century onwards, but im- trient budget, such an assumption may portantly its sediment record indicates that underestimate the role of 1000 years of culit is a cultural, not a naturally eutrophic, tural disturbance and the build-up of an lake. Aphu~izo~e~o~and A~a~ena had internal P pool. It is also a reflection of the been present in Gosciaz at low abundances commonly held belief that soils have a for some time, but underwent a substan- near-infinite ability to retain P. There is, tial increase in abundance from about however, increasing evidence that mod1000.~ - an increase that is highly corre- ern agriculture is beginning to saturate lated with the expansion of agriculture in soils with nutrients, substantially alter the catchment as recorded by the pollen soil properties, as well as increasing soil record. Van Geel ef ~1.~ interpret this in- erosion and, hence, nutrient 10~~~2~1:~ - so crease in nitrogen-fixing blue-greens as much so, that winter rainfall can remove a trend towards nitrogen limitation, as a considerable amounts of P from the result of the substantial P loading to the surrounding farmland and transfer it into lake from the medieval period onwards, a the aquatic systems. For these seepage situation clearly similar to that occurring lakes, the internal P load is probably supin the deeper Shropshire-Cheshire meres plemented by nutrient transfer during the todaya. winter months when the soils are waterlogged.
Naturally eutrophic lakes: reality, myth or myopia? ake eutrophication is creeping back Lcourse, onto the environmental agenda. Of the problem has never ceased to exist - it has merely been overshadowed in the past 15 years or so by acid precipitation and, recently, by concerns about climatic warming. High nutrient loadings to lakes and the resultant increased productivity, however, still cost the water supply industry considerable sums of money’. Highly productive systems also tend to have reduced amenity value: few people seem to like swimming in bluegreen algal blooms, and that is without consideration of the health risks associated with algal toxins: even if the owner survives the dog might not (15 dogs died after swimming in a ~~crocys~~sbloom in Rutland Water, UK)*. The toxic blue-green scares of the 1980s were important in refocusing attention on lake eutrophication. Reduced biotic diversity is also of concern to conservation and nature management agencies. The process-response of lake eutropht cation is reasonably well understood, and has been for some time, following the re search initiatives of the 1960s and 1970s. Lake eutrophication has generally been perceived as a cultural or anthropogenic phenomenon: the currently high nutrient loadings to lakes today are the result of man’s activities in the catchment, or so it is assumed. Given this history of eutrophication research, and the global scale of cultural impacts on both terrestrial and aquatic ecosystems, it is surprising, in the 199Os,to run into the concept of natural eutrophic lakes, described in a new paper by Moss, McGowan and Carvalhos. Examples of lakes with high phosphorus concentrations in relatively pristine catchments do existe, and tend to be associated with local bedrock rich in phosphorus (P). Pristine, however, is not the word one would choose to describe the landscape in which the ShropshireCheshire meres of central England are Iocated. The meres are a collection of 60 or so lakes that lie in a cultural landscape of intense agricultural activity. The mean total phosphorus (TP) concentrations of these lakes range between 50 and 15OO~gl-1 (Ref. 3): they are clearly eutrophic and some of them are assumed to be naturally eutrophics. Many of the deeper lakes are also nitrogen-limited, and there is a strong top-down (grazing) control of ph~oplan~on crops in the shallower lakes, where mean TP concentrations TREE
vol.
10,
no.
4 April
1995
Blue-green folklore
The presence of blue-greens in the Shropshire-Cheshire meres is assumed (in part) to be natural because of its ap pearance in folklore (‘breaking of the meres’*) dating back to the Middle Ages. The Gosciaz sediment record clearly illustrates that such records of blue-green blooms are true but are merely part of the cultural heritage of the area. They are a reflection of the impact of early agricul-
M~~erne~t implications There is more than an abstract, ecological issue at stake here - conservation and restoration cost money. The longterm and presumed natural state of some eutrophic lakes contrasts with the cultural record preserved in their sediments and leads to the question of nature management, conservation and lake restoration ol eutrophic lakes. If the lakes are naturally
0 1995. Elsevier
Science
Ltd
137
NEWS
&
COMMENT-
eutrophic, they can safely be left alone the cheapest and preferred option for some agencies. If they have been disturbed over long timescales, the leave-alone option is also a realistic one: achieving the halcyon status that existed before deforestation and development of medieval agriculture is clearly not feasible. The inertia of the internal P load combined with contemporary nutrient loadings maintains lakes in their current eutrophic state. Besides that, the dominant communities of 2000 or more years ago have, in all probability, disappeared long ago; as a result, inocula to form the basis of natural restoration may not be available. On a slightly shorter timescale, however, there is the problem of restoration goals. It is in these instances that a temporal perspective is important for defining background conditions - ‘natural’ background TP concentrations for restoration projects, using sediment records14 and nutrient transfer functions15 or other hindcasting method+.
wider view of the top-down, bottom-up debate in limnology; similarly, a lengthening of the temporal perspective can be useful in defining natural and cultural. These two contrasting papers3*5 illustrate the importance of longer-term temporal perspectives, both for understanding the contemporary status of a lake (or any other ecosystem for that matter) and its management. For most lowland eutrophic lakes in northwest Europe, ‘natural’ should probably be used with extreme caution: ‘cultural’ is likely to be more apposite. The sediment record in lakes provides an easy means of testing assumptions about the current status of a lake (i.e. natural versus culturaP4), by use of microfossils such as akinete@, pigments7 and nutrient transfer functionsl5. There is, then, a clear need for combining a variety of different ap proaches and including a longer temporal perspective to assist in the understanding of contemporary systems. Sometimes at least, the past can be the key to the present.
Temporal myopia The reluctance to accept that many of these presently eutrophic systems have actually been in a similar condition for hundreds of years is, in part, a reflection of the myopia of contemporary ecologists. It is only recently that the importance of long-term temporal perspectives has been acknowledged. Moss et al.3 argued for a
Acknowledgements I am grateful to Suzanne McGowan for help with the blue-green algae toxins literature and to John Birks and Bas van Gee1for their comments.
12
N. John Anderson
15
Geobotany Thoravej
16
Division, Danish Geological Survey, 8, DK 2400 Copenhagen NV, Denmark
Genetic conflicts and parasitism
I
t has been argued that the interaction between a parasite and its host can lead to an ‘arms race’ between them, in which adaptations in each of the protagonists are successively neutralized by counteradaptations in the other. There are analogies between such an interaction and that between different DNA lineages existing within the same cell. Some such ‘genomic conflicts’ have been demonstrated. For example, geneticists have described systems showing meiotic drive, such as the mouse t-locus and Segregation Distorter systems in Drosophila. Here, individuals heterozygous for the ‘driving’ allele pass it on to much more than 50% of the offspring. This is despite the driving allele having a low homozygous fitness. More recently, it has been discovered that transposable genetic elements increase their abundance through transposition, and rarely, if ever, confer any benefits on their hosts, thus stimulating another genomic conflict. 138
0 1995, Elsevier
Science
Ltd
There is thus a spectrum of genetic conflicts, running from those between different DNA sequences in the same cell to those between parasite species and their hosts. Could all share similar underlying explanations? Exploring the parallels between these diverse systems was one of the goals of a recent European Science Foundation Workshop on genetic conflicts and parasitism. The meeting was organized by researchers at the Laboratoire de dynamique du genome et evolution, and the Institut d’ecologie, at the Parisian Universities VII and VI, respectively. The meeting, held in Paris in October 1994, was attended by around 40 scientists from 11 countries. One of the best examples of genomic conflicts is generated by cytoplasmic male sterility mutations in hermaphrodite plants. As organelle DNAs pass solely through the ovules, a mutation in an organelle genome that caused male sterility
References 1
Sutcliffe, D.W. and Jones, J.G., eds (1992) Eutrophication: WaterSupply,
Research
and Application
to
Freshwater Biological
Association Codd, GA. and Beattie, K.A. (1991) PALS Microbial. Digest 8,82-86 3 Moss, B., McGowan, S. and Carvalho, L. (1994) Limnot. Oceanogr. 39, 1020-1029 4 Murphy, T.P., Hall, K.J. and Yesaki, I. (1983) 2
Limnol. 5
Oceanogr
2958-69
van Geel, B., Mur, L.R., Ralska-Jasiewiczowa,M. and Goslar, T. (1994) Reu. falaeobot. Palynol. 83,97-105
Livingstone, D. (1984) in Lake Sediments and Environmental History (Haworth, E.Y. and Lund, J.W.G.,eds), pp. 191-202, Leicester University Press 7 Swain, E.B. (1985) Freshw. Biol. 15, 6
53-75 8
Reynolds, C.S.(1971) FieldStud.
3,
409-432 9 10 11
13 14
Beales, P.W. (1980) New Phytot. 85, 133-161 Fritz, S.C.(1989) J. Ecol. 77, 182-202 Gaillard, M-J. et al. (1991) .t Paleolimnol. 6, 51-81 Krug, A. (1993) Hydrobiologia 251, 285-296 Sharpley, A.N. et al. (1994) J. Enuiron. Qua/. 23, 437-451 Anderson, N.J. (1993) Trends Ecol. Euol. 8, 356-361 Bennion, H. (1994) Hydrobiotogia 275/276, 391-410 Heathwaite, A.L. (1994) J. Hydrol. 159, 395-421
but an increase in female fertility could spread through the organelle population. The resulting high frequency of female plants in the population would strongly favour nuclear genes restoring male fertility. It is therefore unsurprising that systems of cytoplasmic male sterility and nuclear restorer genes have been observed in many plant species. The molecular causes of cytoplasmic male sterility are very variable, consisting usually of the formation of chimaeric genes in mitochondrial DNAs, as was described by P. SaumitouLaprade (University of Lille, France). MitochondriaI DNA variants will be subject to selection at different levels, and different models for the process were described by B. Godelle and B. Albert (respectively from the University of Paris XI, and the University of Orsay, France). A hymenopteran example of cytoplasmic sex ratio distorters was also discussed by J. Breewer (University of Amsterdam, The Netherlands). One unexpected discovery (described here by E. Zouros, University of Crete, lraklion, Greece) is that the mussel Mytilus has two different lineages of mitochondrial TREE
vol.
IO,
RO. 4 April
1995
4% COMMENT
tural practices on lakes and the increased nutrient loadings associated with medieval agriculture. There is evidence for the long-term expansion of agriculture in the North Shropshire area? the pollen record at Crose Mere indicates that hemp retting took are >300 p,g 1-l. Today, many of the meres place at this lake from the Iron Age onare dominated by blue-green algal (cyano- ward@. Combined with deforestation, soil bacterial) crop+, like many other eu- erosion and presumably manuring of the trophic systems, It is, of course, blueprimitive agriculture systems, this retting greens that create the widely held public must have resulted in a substantial transimage of a eutrophic lake: pea-green with fer of P from the terrestrial to the aquatic algal scums accumulating along the shore- ecosystem: in part, it is the legacy of this line. type of perturbation that is seen in the One wonders, however, what the aver- meres today. This conclusion is confirmed age European peasant farmer during the by diatom analyses at two other nearby medieval period thought of the bluelakes, Ellesmere and Rotherne Mere, where green algal problem, because it appears oligo-mesotrophic diatom floras are respecies indicative that it has been around for some time. In a placed by Stephanodiscus second and contrasting paper, van Gee1 of enriched systems (R.J. Nelms, unpubet al.5 have documented the abundance of lished PhD thesis, Liverpool Polytechnic, two blue-green genera (AphQnizo~enon 1984). As with many other lowland lakes and A~Q~eRa)over hundreds of years, by in Europe~“,ll, the meres are not naturally identifying their akinetes preserved in the eutrophic systems, they have merely been sediments of Lake Cosciaz in the Na Jazach eutrophic for a long time - probably hunlake district of central Poland. Akinetes are dreds of years. resting stages produced by blue-green algae: because of their resistant cell wall, Phosphorus sources they preserve well in lake sediment@. AklnAs it was difficult to identify a contemetes are, in fact, produced by only a few porary source to account for the high P blue-green algal species, but the fossil concentrations in some of the seepage record of these important contributors to lakes, Moss et al.3 concluded that some the phytoplankton can be extended by use of the meres are probably naturally euof the pigment record7. trophic, with the local bedrockas the most By present-day standards, Gosciaz likely P source. While there must be a natuwould have been considered eutrophic ral background contribution to the nufrom the 15th century onwards, but im- trient budget, such an assumption may portantly its sediment record indicates that underestimate the role of 1000 years of culit is a cultural, not a naturally eutrophic, tural disturbance and the build-up of an lake. Aphu~izo~e~o~and A~a~ena had internal P pool. It is also a reflection of the been present in Gosciaz at low abundances commonly held belief that soils have a for some time, but underwent a substan- near-infinite ability to retain P. There is, tial increase in abundance from about however, increasing evidence that mod1000.~ - an increase that is highly corre- ern agriculture is beginning to saturate lated with the expansion of agriculture in soils with nutrients, substantially alter the catchment as recorded by the pollen soil properties, as well as increasing soil record. Van Geel ef ~1.~ interpret this in- erosion and, hence, nutrient 10~~~2~1:~ - so crease in nitrogen-fixing blue-greens as much so, that winter rainfall can remove a trend towards nitrogen limitation, as a considerable amounts of P from the result of the substantial P loading to the surrounding farmland and transfer it into lake from the medieval period onwards, a the aquatic systems. For these seepage situation clearly similar to that occurring lakes, the internal P load is probably supin the deeper Shropshire-Cheshire meres plemented by nutrient transfer during the todaya. winter months when the soils are waterlogged.
Naturally eutrophic lakes: reality, myth or myopia? ake eutrophication is creeping back Lcourse, onto the environmental agenda. Of the problem has never ceased to exist - it has merely been overshadowed in the past 15 years or so by acid precipitation and, recently, by concerns about climatic warming. High nutrient loadings to lakes and the resultant increased productivity, however, still cost the water supply industry considerable sums of money’. Highly productive systems also tend to have reduced amenity value: few people seem to like swimming in bluegreen algal blooms, and that is without consideration of the health risks associated with algal toxins: even if the owner survives the dog might not (15 dogs died after swimming in a ~~crocys~~sbloom in Rutland Water, UK)*. The toxic blue-green scares of the 1980s were important in refocusing attention on lake eutrophication. Reduced biotic diversity is also of concern to conservation and nature management agencies. The process-response of lake eutropht cation is reasonably well understood, and has been for some time, following the re search initiatives of the 1960s and 1970s. Lake eutrophication has generally been perceived as a cultural or anthropogenic phenomenon: the currently high nutrient loadings to lakes today are the result of man’s activities in the catchment, or so it is assumed. Given this history of eutrophication research, and the global scale of cultural impacts on both terrestrial and aquatic ecosystems, it is surprising, in the 199Os,to run into the concept of natural eutrophic lakes, described in a new paper by Moss, McGowan and Carvalhos. Examples of lakes with high phosphorus concentrations in relatively pristine catchments do existe, and tend to be associated with local bedrock rich in phosphorus (P). Pristine, however, is not the word one would choose to describe the landscape in which the ShropshireCheshire meres of central England are Iocated. The meres are a collection of 60 or so lakes that lie in a cultural landscape of intense agricultural activity. The mean total phosphorus (TP) concentrations of these lakes range between 50 and 15OO~gl-1 (Ref. 3): they are clearly eutrophic and some of them are assumed to be naturally eutrophics. Many of the deeper lakes are also nitrogen-limited, and there is a strong top-down (grazing) control of ph~oplan~on crops in the shallower lakes, where mean TP concentrations TREE
vol.
10,
no.
4 April
1995
Blue-green folklore
The presence of blue-greens in the Shropshire-Cheshire meres is assumed (in part) to be natural because of its ap pearance in folklore (‘breaking of the meres’*) dating back to the Middle Ages. The Gosciaz sediment record clearly illustrates that such records of blue-green blooms are true but are merely part of the cultural heritage of the area. They are a reflection of the impact of early agricul-
M~~erne~t implications There is more than an abstract, ecological issue at stake here - conservation and restoration cost money. The longterm and presumed natural state of some eutrophic lakes contrasts with the cultural record preserved in their sediments and leads to the question of nature management, conservation and lake restoration ol eutrophic lakes. If the lakes are naturally
0 1995. Elsevier
Science
Ltd
137
NEWS
&
COMMENT-
eutrophic, they can safely be left alone the cheapest and preferred option for some agencies. If they have been disturbed over long timescales, the leave-alone option is also a realistic one: achieving the halcyon status that existed before deforestation and development of medieval agriculture is clearly not feasible. The inertia of the internal P load combined with contemporary nutrient loadings maintains lakes in their current eutrophic state. Besides that, the dominant communities of 2000 or more years ago have, in all probability, disappeared long ago; as a result, inocula to form the basis of natural restoration may not be available. On a slightly shorter timescale, however, there is the problem of restoration goals. It is in these instances that a temporal perspective is important for defining background conditions - ‘natural’ background TP concentrations for restoration projects, using sediment records14 and nutrient transfer functions15 or other hindcasting method+.
wider view of the top-down, bottom-up debate in limnology; similarly, a lengthening of the temporal perspective can be useful in defining natural and cultural. These two contrasting papers3*5 illustrate the importance of longer-term temporal perspectives, both for understanding the contemporary status of a lake (or any other ecosystem for that matter) and its management. For most lowland eutrophic lakes in northwest Europe, ‘natural’ should probably be used with extreme caution: ‘cultural’ is likely to be more apposite. The sediment record in lakes provides an easy means of testing assumptions about the current status of a lake (i.e. natural versus culturaP4), by use of microfossils such as akinete@, pigments7 and nutrient transfer functionsl5. There is, then, a clear need for combining a variety of different ap proaches and including a longer temporal perspective to assist in the understanding of contemporary systems. Sometimes at least, the past can be the key to the present.
Temporal myopia The reluctance to accept that many of these presently eutrophic systems have actually been in a similar condition for hundreds of years is, in part, a reflection of the myopia of contemporary ecologists. It is only recently that the importance of long-term temporal perspectives has been acknowledged. Moss et al.3 argued for a
Acknowledgements I am grateful to Suzanne McGowan for help with the blue-green algae toxins literature and to John Birks and Bas van Gee1for their comments.
12
N. John Anderson
15
Geobotany Thoravej
16
Division, Danish Geological Survey, 8, DK 2400 Copenhagen NV, Denmark
Genetic conflicts and parasitism
I
t has been argued that the interaction between a parasite and its host can lead to an ‘arms race’ between them, in which adaptations in each of the protagonists are successively neutralized by counteradaptations in the other. There are analogies between such an interaction and that between different DNA lineages existing within the same cell. Some such ‘genomic conflicts’ have been demonstrated. For example, geneticists have described systems showing meiotic drive, such as the mouse t-locus and Segregation Distorter systems in Drosophila. Here, individuals heterozygous for the ‘driving’ allele pass it on to much more than 50% of the offspring. This is despite the driving allele having a low homozygous fitness. More recently, it has been discovered that transposable genetic elements increase their abundance through transposition, and rarely, if ever, confer any benefits on their hosts, thus stimulating another genomic conflict. 138
0 1995, Elsevier
Science
Ltd
There is thus a spectrum of genetic conflicts, running from those between different DNA sequences in the same cell to those between parasite species and their hosts. Could all share similar underlying explanations? Exploring the parallels between these diverse systems was one of the goals of a recent European Science Foundation Workshop on genetic conflicts and parasitism. The meeting was organized by researchers at the Laboratoire de dynamique du genome et evolution, and the Institut d’ecologie, at the Parisian Universities VII and VI, respectively. The meeting, held in Paris in October 1994, was attended by around 40 scientists from 11 countries. One of the best examples of genomic conflicts is generated by cytoplasmic male sterility mutations in hermaphrodite plants. As organelle DNAs pass solely through the ovules, a mutation in an organelle genome that caused male sterility
References 1
Sutcliffe, D.W. and Jones, J.G., eds (1992) Eutrophication: WaterSupply,
Research
and Application
to
Freshwater Biological
Association Codd, GA. and Beattie, K.A. (1991) PALS Microbial. Digest 8,82-86 3 Moss, B., McGowan, S. and Carvalho, L. (1994) Limnot. Oceanogr. 39, 1020-1029 4 Murphy, T.P., Hall, K.J. and Yesaki, I. (1983) 2
Limnol. 5
Oceanogr
2958-69
van Geel, B., Mur, L.R., Ralska-Jasiewiczowa,M. and Goslar, T. (1994) Reu. falaeobot. Palynol. 83,97-105
Livingstone, D. (1984) in Lake Sediments and Environmental History (Haworth, E.Y. and Lund, J.W.G.,eds), pp. 191-202, Leicester University Press 7 Swain, E.B. (1985) Freshw. Biol. 15, 6
53-75 8
Reynolds, C.S.(1971) FieldStud.
3,
409-432 9 10 11
13 14
Beales, P.W. (1980) New Phytot. 85, 133-161 Fritz, S.C.(1989) J. Ecol. 77, 182-202 Gaillard, M-J. et al. (1991) .t Paleolimnol. 6, 51-81 Krug, A. (1993) Hydrobiologia 251, 285-296 Sharpley, A.N. et al. (1994) J. Enuiron. Qua/. 23, 437-451 Anderson, N.J. (1993) Trends Ecol. Euol. 8, 356-361 Bennion, H. (1994) Hydrobiotogia 275/276, 391-410 Heathwaite, A.L. (1994) J. Hydrol. 159, 395-421
but an increase in female fertility could spread through the organelle population. The resulting high frequency of female plants in the population would strongly favour nuclear genes restoring male fertility. It is therefore unsurprising that systems of cytoplasmic male sterility and nuclear restorer genes have been observed in many plant species. The molecular causes of cytoplasmic male sterility are very variable, consisting usually of the formation of chimaeric genes in mitochondrial DNAs, as was described by P. SaumitouLaprade (University of Lille, France). MitochondriaI DNA variants will be subject to selection at different levels, and different models for the process were described by B. Godelle and B. Albert (respectively from the University of Paris XI, and the University of Orsay, France). A hymenopteran example of cytoplasmic sex ratio distorters was also discussed by J. Breewer (University of Amsterdam, The Netherlands). One unexpected discovery (described here by E. Zouros, University of Crete, lraklion, Greece) is that the mussel Mytilus has two different lineages of mitochondrial TREE
vol.
IO,
RO. 4 April
1995