FORCE-FEEDINGTHE COUNTRYSIDE:the impacts of nutrientson birds andother biodiversity

for birdsfor peoplefor ever

Evidence review

FORCE-FEEDINGTHE COUNTRYSIDE:the impacts of nutrients onbirds and other biodiversity

Evidence review

M A MacDonald, J M Densham, R Davis andS Armstrong-Brown

May 2006

This document is a summary of a full scientific review of the evidence:M A MacDonald (2006) The indirect effects of increased nutrient inputs onbirds in the United Kingdom: a review. RSPB.

To receive a copy of the full review document or further copies of thissummary please contact Jim Densham at the RSPB. This summary documentcan be downloaded from www.rspb.org.uk/waterwetlands

Contentspage

Executive summary 1

Introduction 2

Farmland 6

Aquatic habitats 10

Moorland and heathland habitats 12

Case studies 14Loch of StrathbegOuse Washes

Conclusions 15

References 16

Improved grasslandSteve Austin (rspb-images.com)

Acknowledgements

The authors would like toacknowledge the support and helpfuladvice of David Gibbons, GwynWilliams, Ken Smith, Andy Evans,Murray Grant and Will Peach in theproduction of this review

• Increased levels of nutrients are damaging habitats across the UK.Nutrient pollution force-feeds the countryside, altering plant growth rates,changing plant communities and disrupting the food chain for wildlife,including birds.

• Governments must take tougher action to ensure the efficient use andrecycling of nitrogen and phosphorus, and limit losses to theenvironment. The knowledge and technologies exist to achieve this,through capturing and re-using the nutrients present in organic wastes.Now, policies are required to put this knowledge into practice, through amixture of better regulation, incentives and education.

• Without tougher action, the UK will be unable to meet a wide range ofinternational and national commitments to safeguard water quality,reduce the pollution of raw water supplies, and protect wildlife.

• In the UK, twice as much nitrogen and three times as much phosphorusare present in natural systems, compared to before the industrialrevolution1. The sources of this pollution are fertilisers, fossil fuelcombustion and sewage effluent.

• The availability of inorganic fertilisers helped to drive agriculturalintensification in the twentieth century, resulting in widespread changesto crop and grassland management. Those changes boosted yields, butalso damaged farmland wildlife, including birds.

• Red-backed shrike is now extinct in the UK; its decline was largely drivenby management change linked to fertiliser application to grassland. Thisprocess also helped drive corncrake and cirl bunting to the brink ofextinction in the UK; these two species are slowly recovering as a resultof intensive conservation effort.

• Increased nutrient concentrations in aquatic habitats can increase the sizeof populations of some birds, but, almost always damage other parts ofwetland ecosystems, and often compromise the habitat and foodrequirements of specialist birds such as bittern.

• Moorland and heathland habitats are sensitive to increases in nutrientloadings, as a result of atmospheric nitrogen deposition. Many moorlandbirds benefit from a mosaic of heather and grass moorland, but somespecies are known to be sensitive to large-scale loss of heather cover,including red grouse and stonechat. The importance of atmosphericnitrogen deposition to overall losses of heather is probably relatively smallcompared to other processes, such as afforestation and increasedgrazing intensity; but contributes to the overall degradation of thesevulnerable habitats.

1 Millennium Ecosystem Assessment, 2005. Ecosystems and Human Well-being: Synthesis.Island Press, Washington, DC.

Executive summary

1

And

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Hay meadowAndy Hay (rspb-images.com)

This report discusses the impact ofincreased plant nutrient availability onbiodiversity. It summarises a moredetailed review of the evidence forindirect or food-chain effects ofphosphorus and nitrogen on UK birdpopulations2. The excessive use ofnutrients also has wider costs forsociety. Water companies spendmillions of pounds a year removingnutrients from drinking and wastewaters, and the external costs ofindustrial production of nitrogenbased fertilisers, in terms ofgreenhouse gas emissions, areimmense. These issues are notdiscussed further in this report butare important when considering thecosts and benefits of taking action toreduce nutrient pollution.

Nutrients and fertilityThe elements nitrogen andphosphorus are essential for plant

Introduction

2

LapwingAndy Hay (rspb-images.com)

Tidal creek and mudflatsChris Gommersall (rspb-images.com)

Classification of the trophic status of

inland standing waters

Total P (µg/l)

Ultra-oligotrophic <4

Oligotrophic <10

Mesotrophic 10–35

Eutrophic 35–100

Hypertrophic >100

OECD, (Foundation for Water Research,2000).

Forms of pollutant

Nitrate Soluble form of nitrogen used in fertilisers to promote plant growthNO

3but in excess can lead to eutrophication

Phosphate Compound form of phosphorus used in fertilisers and detergents.PO

4Promotes plant growth and can lead to eutrophication

Ammonia Gas which is highly soluble, forming Ammonium (NH4) in water, canNH

3contribute to eutrophication and acid rain

Nitrogen Greenhouse gas produced from fuel combustion.oxides NO

xDeposited on land from the atmosphere and can cause acid rain

Nitrous Powerful greenhouse gas released during the breakdown of organicoxide N

2O matter and fertilisers, and from industrial processes. Deposited on land

from the atmosphere

Human activity is altering the fertilityof the countryside. Industrialisationand agricultural intensification havebeen accompanied by dramaticchanges to the natural cycling ofplant nutrients (specifically nitrogenand phosphorus). There have beenlarge increases in the amounts ofplant nutrients released into theenvironment as pollution, which arecausing long-term threats to thehealth of the earth’s ecosystems,and compromising the quality ofwater supplies across the globe1.Serious effects on many natural andsemi-natural habitats, collectivelyknown as ‘eutrophication’, or ‘over-enrichment’, have been documentedfrom all parts of the world. Thesechanges have been accompanied bydeclines in a wide range of speciesin the United Kingdom, includingsome birds.

• Nitrogen and phosphorus are essential elements for life, and people

use them in a variety of forms everyday to grow crops and drive

industrial processes. However, when they enter the natural

environment in excess they can cause harm by accelerating plant

growth and altering the balance and structure of natural systems.

• The amount of nitrogen and phosphorus entering the environment

has increased dramatically over the last century, with serious effects

on habitats and species.

growth. In compound forms, asnitrates, phosphates, ammonium oroxides of nitrogen they can beabsorbed and used by plants; but insome of these forms, and asgaseous ammonia or nitrous oxide,they can also be transported awayfrom their intended targets. Habitatsreceive a background level ofnutrients derived from naturalprocesses but human activities haveled to greatly increased amountsreaching the environment. Nutrientpollution stimulates plant growth,disadvantaging species that areadapted to low-nutrient conditions,and altering the structure andfunctioning of ecosystems.

Human nutrient useNitrogen can be chemically fixedfrom the atmosphere, and is used inthe manufacture of fertilisers andsome other industrial processes.Phosphorus is mined from mineralreserves in countries such asMorocco. When processed thesenutrients are used in a wide range ofactivities, including agriculture,industrial processes and themanufacture of detergents.Agriculture is a major user ofnutrients; inorganic fertilisers applied

to crops have facilitated largeincreases in yields. Fertilisersaccount for around 60% of thenitrogen used by people, and about80% of all mined phosphate3.Phosphorus also enters agriculturalsystems as a nutrient in animal feed.Phosphate application to land rosesharply from the 1940s, exceeding400,000 tonnes annually by 1950(Figure 1)4. Total nitrogen use beganto rise sharply from the early 1950s,and accelerated in the 1960s. Bothphosphate and nitrogen fertiliser usepeaked in the 1980s and have sincefallen slightly, as a result of set-aside, and moves towards moreefficient fertiliser use.

Outside the agricultural sector,phosphates are used in industrialprocesses and are an ingredient ofmany detergents. Phosphates aidthe action of other detergentingredients. However, when thewashing process is complete thephosphates can enter watercoursesvia sewage treatment works.Recently, efforts have been madeto reduce the phosphorus contentof detergents, including banningtheir use in some Europeancountries.

3

Eutrophication

‘The enrichment of water by

nutrients, stimulating an array

of symptomatic changes

including increased production

of algae and/or higher plants,

which can adversely affect the

diversity of the biological

system, the quality of the

water and the uses to which

the water may be put.’

The Environment Agency

(2000)

Lapwing flock above wet grasslandDavid Kjaer (rspb-images.com)

Dead fishDavid Kjaer (rspb-images.com)

CorncrakeAndy Hay (rspb-images.com)

Natural backgroundlevels 9%

Industry 7%

Detergents 10%

Human andhousehold waste24%

Agriculture 50%

Other 3%Industry 2%Other land, suchas forests andurban areas 4%

Sewagetreatment works32%

Agricultural land 60%

The main sources of nitrates in rivers

in England and Wales in 2003

(source: WRc 2004)

The main sources of phosphorus in

rivers in England and Wales in 1993

(source: Defra 2003)

4

clothes, flushing the toilet anddiscarding waste food, all add to thenutrient loads that appear in sewage.Much effort has gone into attemptsto reduce nutrient loadings in effluentdischarges, with some success; forexample, water company investmentto remove phosphate from sewagedischarges is helping to improve thequality of water in the NorfolkBroads. Detergents have beenidentified as a major source ofphosphorus in Forfar Loch8, inScotland, causing year on year algalblooms in summer, which aresuffocating the loch. A campaignaims to raise awareness of this issueand urge people in Forfar to usephosphate-free detergents.

The burning of fossil fuel releasesnitrogen to the atmosphere, as wellas fixing nitrogen from the air via thecombustion process. Eighty per centof nitric oxide emissions andapproximately 40% of nitrous oxideemissions come from human activity;mostly industry and motor vehicle use9.

Transport of nutrientsNitrogen reaches the environment ina number of forms. Nitrates are

highly soluble and are generally lostto the wider environment throughleaching and run-off. About a third ofthe nitrogen in fertiliser applied in theUK is lost to surface water andgroundwaters10 5. In addition tonitrates, there are numerousgaseous forms of nitrogen. Somenitrogen escapes as inertatmospheric nitrogen, which returnsharmlessly to the air. Some isemitted in as ammonia gas, whichtends to be deposited close to itssource (generally animal manures).Finally, some is converted into andemitted as nitrogen oxides andnitrous oxide; these are powerfulgreenhouse gases and aretransported over large distances inthe atmosphere. Phosphorus occursin fewer forms than nitrogen.Soluble, biologically availablephosphorus is discharged in largequantities from sewage works,particularly where these have limitedtreatment facilities. The majority ofagricultural phosphorus in contrast, isbound to soil particles andtransported in the form of sedimentrun-off. Such sediments can releasetheir phosphorus when they becomephosphorus-saturated or aredisturbed (for example, when lakesediments are perturbed by boattraffic or bottom-feeding fish) or ifthere is a change in water chemistrysuch as pH or salinity.

The scale of nutrient pollutionOn a global scale, human activity hasmore than doubled the fixation ofnitrogen gas from the atmosphereinto forms that can affect theenvironment9 11. Humans have alsotripled the amount of biologicallyavailable phosphorus since theindustrial revolution1.

Nutrients exist within theenvironment at ‘background levels’,

Sources of nutrientsreaching the environmentThe major sources of nutrientpollution are emissions fromagriculture, industry, sewagedischarges (nitrogen and phosphorus)and combustion of fossil fuels inindustry and transport (nitrogen).Sources of nutrient pollution may bedescribed as either ‘point source’,where they come from a fixeddischarge point, (e.g. a sewageworks), or ‘diffuse’, where they arelost from systems operating over awide area (e.g. from some agriculturalfields or atmospheric sources).

Because agriculture uses nutrients asan essential part of the growingcycle, it is a major source of nutrientpollution. Agriculture is estimated toaccount for approximately 70% ofnitrogen and 50% of phosphorusentering water5, of 90% of ammoniaemissions6 (the great majority arisingfrom livestock wastes) and of 64% ofnitrous oxide emissions7.

Domestic sewage and industrialeffluent are major point sources ofnitrogen and phosphorus. Our dailyactivities, including washing, cleaning

Figure 1

Long-term trends in UK fertiliser consumption, with related output changes

illustrated by the yield of wheat grain (sources: Rothamsted, Defra, AIC)

ton

nes

of w

hea

t gra

in –

t/h

a

‘00

0 to

nn

es n

utr

ien

t

potashphosphate

wheat yield

nitrogen

2,000

1,750

1,500

1,250

1,000

750

500

250

0

8.0

6.0

4.0

2.0

0.01910 1920 1930 1940 1950 1960 1970 1980 1990 2000

5

as a result of natural processes suchas rock weathering anddecomposition of organic material.However, in human-altered systems(which effectively comprise thewhole of the UK), nutrient levels haverisen substantially. Both nitrate andphosphate levels in UK rivers showedupward trends from the 1930s and1940s, when records began10. Similartrends have been found for nitrate ingroundwater and in lakes and lochs inthe UK. Recent success in reducingpoint-source pollution have improvedpollution records for some sectors,although levels of nitrogen andphosphorus in aquatic systems havestill risen dramatically, over the longterm. Recent trends show annualnitrogen loads to rivers in Englandand Wales increased from 503kilotonnes in 1983 to 514 kilotonnesin 200312, whereas phosphorusconcentrations showed a downwardtrend at most sites13. UK ammoniaemissions in 2004 were 336kilotonnes, down 12% since 19905

but still much higher than 50 yearsago, because of the increased use ofnitrogen in feeds and fertiliser14. Thelevels of atmospheric nitrous oxidehave also fallen, by 45% between1990 and 20047, largely as a result inreductions in industrial pollution.

There is strong evidence thatnutrients entering the environmentover time have had effects on thevegetation of the UK and elsewhere.Eutrophication is proposed as a majorcause of historical shifts in the floraof the UK, with flower-rich farmlandhabitats having largely disappeared15,and many plant species becominglocally extinct. Plant species andcommunities that are typical of lowfertility (soils or waters) have beenespecially hard hit. Conversely,species with a preference for fertilesites or water bodies were more

successful in the late twentiethcentury than they had been inthe 1950s16.

English Nature has classified 20,733hectares of England’s designatedSites of Special Scientific Interest(SSSI) as being in unfavourablecondition due to water pollution fromagriculture17. This accounts for over7% of England’s SSSI network andincludes some land within RSPBreserves, such as the Ouse Washes(see Case Study, page 14). A recentreview of nutrient pollution in theScottish water environment wascarried out by SEPA18. This reviewidentified 146 rivers and 17 lochswhich show damage from inputs ofnutrients from sewage discharge,diffuse agricultural pollution andother sources. The total length ofrivers affected by eutrophication inScotland is 2,184 km, the equivalentto 8.6% of the river network. Pointsource sewage discharge affects1,544 km and diffuse agriculturalinputs 1,598 km of rivers. Somewater bodies are affected by nutrientinputs from both sources. One sucharea suffering impacts from nutrientpollution is the Loch of StrathbegRSPB reserve, designated a SSSI, aRamsar site and SPA (see CaseStudy on page 14).

Impacts on vegetation have knock-onconsequences for a range of wildlife,which rely on the affected habitatsfor food and shelter. Birds may beaffected by changes to plant andinvertebrate food sources andnesting sites. The studies whichfollow, identify the impacts ofnutrient pollution on three types ofhabitat, and examine theimplications for birds speciesassociated with these.

Water violetPeter Creed

5

6

Farmland covers 75% of the UK andtherefore exerts a great influence onits landscapes and resident wildlife.Agriculture has intensified in manyparts of the UK in the twentiethcentury. In part, this has been madepossible by the availability ofinorganic fertilisers and has led tochanges in the crop and non-crop

vegetation which form the basis ofthe food chain, affectinginvertebrates, and ultimately birdsand other wildlife. For example, therehas been a decline of almost 50% infarmland bird populations since 1970,as indicated by the Farmland BirdIndex (Figure 2). Organic andinorganic fertiliser use affects non-

Farmland

• Agriculture differs from other sectors, as farmland is deliberately

fertilised. Nutrients are essential to plant growth and their presence

is key to achieving good yields. The availability of plentiful inorganic

supplies of nutrient has helped to change the way crops, including

grassland, are grown and managed.

• Problems arise when nutrients cause negative environmental

consequences on farmland, or when unused nutrients are dispersed

from the agricultural system.

• Some organisms are directly affected by the toxicity of nutrients

applied to the land, but the majority of wildlife impacts are indirect.

• Indirect effects of nutrients include:

1. losses of habitat and food resources, associated with the decline

in mixed farming as farms polarise into intensive specialist units;

2. changes in the species richness and vegetation structure of farmed

habitats, resulting in reduced invertebrate food resources; and

3. the replacement of hay with silage production, with a consequent

loss of invertebrate and seed resources, and an increase in

disturbance from cutting and grazing.

Figure 2

UK farmland bird indicator (source: RSPB/BTO/Defra)

Arable field marginRoger Tidman (rspb-images.com)

Cirl buntingMike Lane (rspb-images.com)

Ind

ex (

1970

= 1

00)

Farmland bird indicator

1970 baseline

140

120

100

80

60

40

20

0 1970

2002

1998

1994

1990

1986

1982

1978

1974

7

crop plants and some invertebratesdirectly, and other wildlife indirectly.Some invertebrates, notablyearthworms19 20, may be killed byheavy applications of organic andinorganic fertiliser, due to short termtoxic ammonia concentrations,salinity and desiccation, but mostimpacts on invertebrates are indirectdue to changes in vegetation(Table 1). Birds may be affected byfertiliser use via several indirectmechanisms (Table 2).

The use of fertilisers is only one ofseveral factors that have promotedthe intensification of agriculture;other technological improvementsand policies have also changed theway in which crops and grasslandare produced and managed withsimilar results. It is therefore difficultto disentangle the impact ofnutrients in fertilisers from thosecaused by other aspects ofagricultural intensification. However,in some cases there is strongevidence that increased fertiliser use

Table 1

Summary of direct and indirect effects of fertiliser application on some invertebrate groups

(source: MacDonald, 2006)

Group Effects

Earthworms (Lumbricidae) High levels of organic and inorganic fertilisers toxic, but positive long-term response toorganic fertiliser

Spiders (Araneae) Favoured by processes that increase prey abundance, but affected by intensivemanagement that reduces the suitability of sward architecture

Moths and butterflies (Lepidoptera) Abundance and species richness reduced by loss of host plants and changes tomicroclimate

Beetles (Coleoptera) Specialist species disadvantaged by loss of host plants; some large species unable tocomplete life cycle under intensive management

Craneflies (Diptera: Tipulidae) Favoured by increased organic content and nutritive value of sward (following applicationof organic fertiliser); sensitive to cutting regime

Leafhoppers etc. Favoured by increased nutritive value and primary productivity, but specialists(Hemiptera: Auchenorrhyncha) disadvantaged by loss of plant species; removed by intensive management

True bugs (Hemiptera: Heteroptera) Favoured by increased nutritive value and primary productivity, but specialistsdisadvantaged by loss of plant species; removed by intensive management

Grasshoppers and crickets (Orthoptera) Unsuitable habitat caused by growth of dense grass sward; inability to complete lifecycle due to cutting regime and microclimate

is the major driving force, andchanges in nutrients within farmlandhave affected the plant speciesrichness of fields, vegetationstructure, farm management andthe landscape.

Species richnessThe diversity of plant species in thecountryside is affected by nutrientenrichment. Increased fertiliserapplications generally reduce plantspecies richness or biodiversity in allfarm fields, not just grassland. Plantbiodiversity in farmland may bepositively correlated withinvertebrate species richness, due tothe increased opportunities forspecialist invertebrates19 21. Forexample, in arable field margins ofsouthern England plant diversity islinked to butterfly and predatorybeetle species richness andabundance22. Loss of plant speciesdiversity thus has the potential toreduce invertebrate speciesdiversity. Invertebrate abundance,however, is not necessarily linked to

either plant species richness orinvertebrate species richness.

Vegetation structureFertiliser applications affect cropsward structure by promoting fasterand earlier spring growth, leading totaller, denser swards. In arablefields, this, together with cropbreeding and pesticidedevelopment, has helped to drivethe shift from spring-sown toautumn-sown crops. The resultingreduction in over-winter seedresources has affected seed eatingbirds, such as the yellowhammerand linnet. In grassland, the fasterand earlier growth is generally cutfor silage or intensively grazed,leading to short (although still dense)and homogeneous swards.Invertebrates that eat plants maybenefit from the increased nutrientcontent of fertilised crops and grass,and the increased shoot and rootgrowth resulting from fertiliserapplication. Similarly, winteringgeese, which graze on grass, prefer

8

fertilised fields. Managementrecommendations for theseimportant winter visitors to the UKinclude fertiliser application tograssland and grazing by livestock.

Many indirect effects oninvertebrates are negative. Changesto sward structure probably have thegreatest effects on invertebrateabundance. These effects are mostclearly observed in grassland underintensive grazing and/or cuttingregimes. Invertebrates that areadapted to a specific grass swardstructure will be negatively affectedby fertiliser application andassociated management practices.Grasshoppers and crickets are anexample of this, as their habitatrequirements are poorly met inintensively managed improvedgrassland23. Furthermore, these andother large insects aredisproportionately affected bydisturbance arising from grazing andcutting, as their longer life cyclesand relatively low ability torecolonise mean that they are morelikely to disappear from intensivelymanaged farmland.

Several bird species have sufferedfrom reduced abundance and/oravailability of their invertebrate foodsources. Species reliant on largeinvertebrates, such as cirl buntingand red-backed shrike, are especiallysensitive. The loss of large soildwelling invertebrates is alsosuggested as a major cause ofreduced productivity of breedingwaders in grassland24 25. Birds, suchas snipe, starling and chough, thatfeed on soil invertebrates may beaffected by reduced access to thesefood items in dense swards.

Increased crop growth can alsocontribute to the drying of soil,forcing soil dwelling invertebrates,such as earthworms, deeper intothe soil.

Land managementFertilisers have facilitated changes inland management that have affectedwildlife. These changes areparticularly significant in pastorallandscapes, and include theproduction of silage, which haslargely replaced hay production. Thisshift has had radical effects onvegetation. It has also had highlysignificant effects on farmland birdpopulations, operating via threepathways:1. reduced invertebrate food due to

frequent cutting;2. reduced seed resources as grass

is cut before setting seed; and3. destruction of adults, chicks and

nests.

Early and frequent cutting of grassfor ensiling affects sward structure,and reduces the seed available forfarmland birds, such as theyellowhammer26. Destruction ofadults, chicks and nests duringsilage cutting is a major cause ofreduced productivity in nesting birdssuch as whinchat and corncrake27.Where fertilised grass is not cut, itcan support higher stockingdensities of grazing livestock.Intensive grazing and silage cuttingdirectly remove invertebrates, andintensive grazing can lead toincreased nest trampling in groundnesting species such as skylark28

and lapwing29. These species mayalso suffer higher predation rates inintensively managed fields, eitherbecause taller swards may reduce

their ability to detect predators, orbecause reduced swardheterogeneity decreases nestconcealment.

Farming systemsThe use of inorganic fertilisers hasled to changes in patterns of land-use, by releasing farmers from theneed to include fertility-building leys,with or without grazing, in the croprotation. As a result, there has beena loss of mixed farming and, ingeneral, a polarisation of agriculturetowards arable farming in the southand east, and pastoral farming in thenorth and west of the UK. Birdspecies such as starling, cirl buntingand lapwing that prefer thejuxtaposition of arable fields andpasture have been disadvantaged bythe trend away from of mixedfarming30 31.

99

Mechanism by which fertiliser use may have indirectly affected a bird species1

Species Listing

corncrake red P

lapwing amber C+ P C C C+

snipe amber C C

curlew amber C+ C

redshank amber C+

turtle dove red C-

skylark red P- P C- C C C-

swallow amber C

yellow wagtail amber C+ C C

whinchat green C C+

red-backed shrike red C+

chough amber C+

starling red C+ C

tree sparrow red C C-

linnet red C-

yellowhammer red C C- C

cirl bunting red P C- C+

reed bunting red C C- C

corn bunting red C C- C C

1 P = proven (eg by recovery or experimental study), P- = proven, but fertiliser use is secondary to other causes of mechanism,C = correlation, C+ = strong correlation, C- = correlation, but fertiliser use is secondary to other causes of mechanism

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Figure 3

Flow diagram illustrating the expected mechanisms for indirect effects of nutrient inputs on birds in farmland

Decreasedstructural suitability

for nesting birds

Fewer foodresources forvertebrates

Increased nestdestruction

Fewer seedfood resources

Higherstocking

ratesEarlier/more

frequentharvesting

Broad-leaved plantsout-competed

Increased crop/grass growth

and yield

Lowerinvertebrate

diversity

Red

ucti

on

in

sw

ard

su

itab

ilit

y f

or

gro

un

d

nesti

ng

bir

ds

Table 2

Summary of suggested ways in which application of fertilisers has indirectly affected farmland birds in

the United Kingdom (source: MacDonald, 2006)

Lower plantdiversity

Aquatic habitats

• Nutrients dissolved in water or attached to sediment reach aquatic

habitats and can change plant growth patterns in delicate

ecosystems, such as shallow lakes and reedbeds.

• Moderate increases in nutrients may promote an increased supply of

plant food for invertebrates and birds in some circumstances, for

example around sewage outfalls in estuaries and in some river systems.

• However, at higher nutrient levels, the changes to ecosystem

functions resulting from eutrophication are detrimental.

• Aquatic birds can be adversely affected by: changes in the abundance

and species composition of swimming and bottom dwelling

invertebrates; changes in the abundance, size, and species

composition of available fish prey; and reductions in habitat quality

as a result of accelerated succession or changes in vegetation structure.

The food-chain effects ofeutrophication can be complex andhighly localised in aquatic systems.Hence, changes in bird populationsare not always downwards and somebird species may benefit from amoderate increase in nutrients whilstothers can be extremely sensitive toeven small changes. Increases innutrient concentrations may bebeneficial to birds up to a point, butafter this, radical changes occur tothe habitat on which they rely forfood and nesting sites.

Open freshwaterShallow freshwater lakes areespecially susceptible toeutrophication. They tend to exist ineither a clear-water state dominatedby plants, or a phytoplankton-dominated, turbid-water state32 33.Lakes can shift between the statesrelatively suddenly, with switchingtriggered by a variety of processes,including changes in fish communityand physical disturbance ofvegetation. Importantly, the likelihoodof switching is strongly influenced by

Lake at Wood of Cree,

RSPB reservePaul Collin (rspb-images.com)

BitternAndy Hay (rspb-images.com)

Table 3

The effects of nutrient increases on birds using aquatic habitats (source: MacDonald, 2006)

Group Response Typical species

Dabbling plant and Increase initially as aquatic plant growth Mute swan, coot, wigeon, pintailinvertebrate-feeding waterfowl increases but ultimate decline due to loss of

food resources at high nutrient levelsDiving bottom-feeders (fresh waters) Increase initially but ultimate decline due to loss of Goldeneye, pochard, tufted duck, scoters

food resources and reduced water transparencyDiving bottom-feeders Increase due to greater food availability resulting Scaup, goldeneye(coastal waters) from modest nutrient increasePursuit divers (oligotrophic lakes) Decline due to reduced water transparency and Red-throated diver, black-throated diver

changes to fish size distributionPursuit divers (mesotrophic lakes) Possible increase due to increased Goosander, red-breasted merganser,

prey abundance great-crested grebeReedbed specialists Decline due to loss of reed, increased rate of Bittern, other possibilities include bearded

succession and reduced food resources tit and water railShorebirds (waders and wildfowl) Increase due to greater food availability, Oystercatcher, dunlin, grey plover, knot,

except where macroalgal mats are persistent; redshank (and other waders), winteringspecialist feeders may decline geese; shelduck (decline)

Gulls Increase due to greater food availability Common gull, great black-backed gull

10

11

Reedbed habitatsReedswamp vegetation has declinedacross areas of western and centralEurope38 but despite there beingsome coincidence between reeddecline and eutrophication, no causeand effect has been proven. In theNorfolk Broads, a relationship hasbeen found between nitrateconcentrations in water and thedecline of a particular floating form ofreed, known as hover39.Eutrophication may affect birdsreliant on reedbed by acceleratingthe succession of the plantcommunities and by reducing theamount of open water present. Thered-listed bittern is especiallyadapted to reedbeds, and may beaffected by reduced food supply asone of its major food items in Britainis rudd, which performs poorly ineutrophic conditions40 41.

Upland freshwater lakesIn the absence of human activitiescausing inputs of nutrients, uplandlakes in the UK are mostly low innutrients, and support limited butspecialised plant life. Because of this,these lakes can be particularlysusceptible to small increases innutrient loadings. For example, fishcommunities in upland lakes can bealtered by nutrient pollution byencouraging the growth of fewer butlarger individuals.

Estuaries and coastal watersEstuaries and coastal waters aregenerally better flushed through withwater than freshwater lakes so theeffects of eutrophication aregenerally less persistent. However,where eutrophication occurs ittypically leads to a decline in plantcommunities such as seagrass andeelgrass beds, and their replacementby algal mats and phytoplanktonblooms42 43. In intertidal mudflats, the

nutrient levels, but both states arebuffered against this switching to acertain extent, so that a clear-waterstate can persist at high nutrientlevels, and a turbid-water state, onceestablished, may persist afternutrient levels are reduced.

Invertebrate communities infreshwater are sensitive to nutrientinputs. Bivalve molluscs areespecially sensitive to eutrophicconditions, whilst others, such asannelid worms are more tolerant.Eutrophication of shallow lakes, inEngland and elsewhere, leads to areduction of fish diversity, with roachand bream becoming dominant atthe expense of perch, rudd andtench34. Eutrophic conditions alsochange the invertebrates living at thebottom of water bodies, leading to aloss of sensitive species and foodsupply for birds, such as pochard,which dive from the surface to feedon them35. Nutrient enrichment mayalso alter the size class of fish prey,reducing the abundance of suitablysmall-sized individual fish. Fishfavoured by eutrophic conditions mayalso compete with birds for food; thishas been suggested as a cause ofthe decline of tufted duck in LoughNeagh36 37. Large zooplankton, such aswater fleas, favour a clear-waterstate, because submerged plants(which rely on clear water) providethem with shelter from predatoryfish31. In freshwater lakes, a shift instable states to non-clear waterresults in a decline in food plants forherbivorous and omnivorouswaterfowl.

Under certain conditions, extremeeutrophication can lead to hugeincreases in plant growth whichstarve water of oxygen. These anoxicconditions can kill both invertebratesand fish in an affected stretch of water.

presence of algal mats forcesinvertebrates closer to the surface ofthe mud to evade the oxygendepleted conditions caused by thealgal growth. This provides a short-term flush of food for otherorganisms, including birds but if themats persist, invertebrateabundance may decline severely andthe food supply will be reduced inthe long term44.

In coastal areas small aquaticcrustaceans such as the mud shrimpand polychaetes like ragworm aretolerant of eutrophic conditions andcan provide abundant foodresources to shorebirds. In tidalareas, shorebirds benefit fromhuman influenced nutrient inputs,although birds with specialised preyrequirements or foraging habits,such as shelduck, may not45.Immediately adjacent to pointsources of nutrient pollution, such assewage outflows, invertebratenumbers are reduced by theextreme conditions but in thesurrounding areas they can be muchhigher46. However, the invertebratecommunities are very different incomposition from those found innaturally low-nutrient waters. Wheresewage outfalls are removed, orwhere treatment is implemented,invertebrate biomass usually falls,although the diversity of speciesincreases and more closelyresembles that found in naturalconditions. Historically, birdpopulations have risen in estuarieswhere sewage inputs haveincreased. Diving ducks are anexample of a group of birds thathave benefited from the increasedfood supplies around sewageoutfalls, and their numbers havebeen shown to decline whereoutfalls have been removed or bettertreatment installed44.

12

Upland moor and lowland heath,dominated by heather, are naturallynutrient-poor habitats that aresensitive to increases in inputs.Fertilisers are not generally applieddirectly to these habitats. Instead,increases in nutrient loading are theresult of atmospheric nitrogendeposition. This source of nitrogenhas increased enormously over thepast century, despite somereductions over the past twodecades.

VegetationThere has been a decline in theextent of heather cover in bothupland moorland and lowland heathin the United Kingdom in recentyears. In England and Wales, theland area covered by heather fellfrom 631,400 to 509,800 hectaresbetween 1947 and 198047. InScotland, heather cover declinedby 23% (over 300 000 ha) in theperiod 1947–198848. Causes of thedecline include overgrazing(leading to invasion of grasses),afforestation (the cause of over halfthe heather loss in Scotland),conversion to farmland, andsuccession to scrub.

Atmospheric deposition of nitrogenincreases the nitrogen content ofheather leaves and decreases theroot:shoot ratio. This changeincreases the plant’s sensitivity todesiccation, and dieback can occur,especially during winter droughts.The heather beetle feeds exclusivelyon heather and this increasednitrogen content of heather foliageincreases heather beetle larvalgrowth49. It is therefore suggestedthat nitrogen deposition increasesthe probability of beetle outbreaks50.Dieback resulting from heatherbeetle attacks or desiccation maycause disturbance to heathersufficient for grasses to invade andboth of these mechanisms may beincreased by nitrogen deposition.Disturbance of heather by grazinganimals has further effects on thecover of heather and grass onmoorland, independent of the effectsof nutrient inputs51. Between the1970s and 1990s grazing intensityincreased in many upland areas andhas been a major cause of transitionfrom heather to grass moorland.Increased nitrogen deposition mayhave facilitated increased grazingintensity by improving the forage

12

Heathland

Heath tiger beetle

Hen harrierAndy Hay (rspb-images.com)

• Upland moor and lowland heath habitats are naturally low in

nutrients and are therefore sensitive to atmospheric nitrogen deposition.

• Heather (Calluna vulgaris) is sensitive to increased nitrogen

availability, and increased nutrient loads can favour grasses; although

generally some form of disturbance is required to cause moorland to

shift from heather to grass dominance. The most common reason for

this is increased grazing intensity, which is not necessarily related to

nitrogen deposition.

• Some upland bird species, including red grouse and stonechat, are

particularly sensitive to heather loss. It is possible that such species

are adversely affected by the impacts of atmospheric nutrient deposition.

• Many moorland bird species benefit from a mixture of grass- and

heather-dominated moorland. The effects of heather loss on these

species will depend on the initial heather cover and spatial

configuration, with most species only likely to be detrimentally

affected by heather loss if it occurs over large areas.

Moorland and heathlandhabitats

13

Table 4

Predicted effects of loss of heather cover to moorland birds (source: MacDonald, 2006)

Species Category1 Sensitivity Likely reaction to loss of heather cover

Red grouse Confined to heather moorland high loss of heather food resource; loss of nesting habitatBlack grouse Major breeding habitat moderate increased predation and loss of food resourceHen harrier Breed mainly on moorland moderate loss of nesting habitat and prey itemsGolden eagle Feeding habitat moderate loss of nesting habitat and prey itemsMerlin Breed mainly on moorland moderate loss of nesting habitat and prey itemsGolden plover Breed mainly on moorland low strong effects unlikelySnipe Locally important breeding habitat low strong effects unlikelyCurlew Major breeding habitat low strong effects unlikelySkylark Major breeding habitat low probable benefit from increase in grass coverMeadow pipit Major breeding habitat moderate loss of appropriate mosaic of habitatsWhinchat Major breeding habitat low probable benefit from increase in bracken coverStonechat Major breeding habitat high loss of nesting sites and appropriate mosaic of habitatsWheatear Locally important breeding habitat low probable benefit from increase in bracken or grass coverRing ouzel Major breeding habitat moderate loss of nesting habitat and appropriate mosaic of habitatsTwite Locally important breeding habitat moderate loss of nesting habitat

1 Use of heather moorland as described by Thompson et al. (1995).

quality of moorland (throughincreased nitrogen content of foliageand increased grass cover), althoughsuch increases in grazing intensitywere driven primarily by other factors(such as agricultural fundingmechanisms). The scale of thecontribution of nitrogen deposition tothis process is difficult to determine.These mechanisms for changing thecomposition of heather are alsosuggested as causes for the loss oflowland heath in western Europe.However, lack of management is alsoimplicated, with succession to scruband the cessation of burning beingthe main factors52 53.

BirdsIn upland moorland, the shift fromheather to grass moorland, due toprocesses already described, is likelyto be the most important effect ofnitrogen deposition on birds. Arecent study54, which examineddetailed relationships between birdabundance and vegetationcharacteristics, found that severalspecies appear to use non-heather

components of moorland, or requirea mosaic of grass and heather cover.Based upon this and other moorlandbird studies, there is sufficientevidence to estimate sensitivity toheather loss for fifteen species. Twospecies (red grouse and stonechat)are considered sensitive to heatherloss, because they are stronglyassociated with mature heathercover for breeding and foraging. Sixspecies (curlew, snipe, golden plover,skylark, whinchat and wheatear) areclassed as having low sensitivity toheather loss. Indeed, some of thesespecies are likely to benefit from theconversion of heather moorland toeither grass or bracken, while forothers the structure of moorlandvegetation, rather than its floristiccomposition, appears to be moreimportant in determining theirabundance. A further seven species(black grouse, hen harrier, merlin,golden eagle, meadow pipit, ringouzel and twite) are classed asmoderately sensitive to heather loss.These species require a mosaic ofheather and grass cover, and the

effects of heather loss on birds willdepend on the extent of initialheather cover and its spatialdistribution. Most moorland birds arenot favoured by continuous heathercover, and are only likely to bedetrimentally affected where heatherloss occurs across relatively largeareas. Nitrogen deposition maycontribute to such losses, but theirmain drivers remain processes suchas afforestation and intensivegrazing. Furthermore, populations ofsome moorland birds may currentlybe determined by processes otherthan availability of habitat, such ashuman persecution55.

Whilst the plant communities oflowland heathland have undoubtedlysuffered from eutrophication, birdsare not a good indicator ofenvironmental health for this habitat.Few bird species specialise in thishabitat, and their populations areprobably more affected by processesother than eutrophication.

13

14

Case studies

Impacts of nutrient pollution on RSPB nature reserves

Loch of StrathbegThe Loch of Strathbeg is a 915 ha wetland reserve in north east Scotland. Ithas a range of biodiversity and geological features which have beenrecognised as important for wildlife at the international, national and locallevels and has been designated as Site of Special Scientific Interest (SSSI), aRamsar site and a Special Protection Area (SPA). It has been designated forbreeding sandwich terns and its internationally important winteringpopulations of wildfowl, such as whooper swan, pink footed geese and teal.The loch and the surrounding areas of wet grassland, fens and driergrasslands support in excess of 20,000 waterfowl, including large numbersof breeding and wintering wildfowl and waders. There are also a wide rangeof plant communities supporting a number of uncommon species, such ascreeping spearwort and slender-leaved pondweed.

According to Scottish Natural Heritage, a number of the conservationfeatures at the Loch of Strathbeg are not currently in favourable condition.Many of these features depend directly or indirectly on the water quality ofthe loch and a burn feeding into the loch. Heavy siltation and increasinglevels of nitrogen and phosphorus from agriculture are causing majorproblems in the loch, which is experiencing change in vegetation structurefrom macrophyte dominance to dominance by epiphytic algae. Thesechanges in plant composition are having indirect impacts on key conservationfeatures, including grazing wildfowl, coots and dabbling ducks.

Ouse WashesAn area of internationally important wetland, the Ouse Washes SSSI formsthe largest example of washland in Britain. Designated as a SpecialProtection Area (SPA), the Ouse Washes attract nationally and internationallyimportant numbers of waterfowl in winter, whilst in the summer they providebreeding habitat for waders such as snipe and black-tailed godwit. The site isalso a Special Area of Conservation (SAC) for spined loach and a Ramsar sitefor a range of wetland features. The RSPB manages just under 1,450hectares of wet grassland, ditch and fen habitats at Ouse Washes.

Large areas of the SSSI, however, are affected by a combination of prolongedsummer flooding and a combination of diffuse and point source pollution,resulting in 86% of the SSSI being classified as in unfavourable condition(982 hectares of which is on the RSPB’s reserve).

In particular, inputs of nutrients have gradually eroded the quality of aquaticplant communities in the rivers and ditches, which were once some of themost diverse in Britain56. The high nutrient loadings have considerablyincreased mat forming duckweed communities in the ditches. The nutrientinputs are also affecting the quality of the wet grassland habitats which are akey feature of the Washes, a Biodiversity Action Plan (BAP) priority habitat,and support important numbers of breeding wading birds such as snipe,lapwing and redshank.

Pink footed geese at

Loch of Strathbeg reserveChris Gommersall (rspb-images.com)

Cattle at the

Ouse Washes reserveAndy Hay (rspb-images.com)

15

Conclusions

ReedbedMatt Self (rspb-images.com)

15

• Increased levels of nutrients are adversely affecting natural and semi-natural habitats in the UK, reducing the diversity of plants andinvertebrates found in our countryside.

• Strong causal links exist, in a number of cases, between nutrient pollutionand knock-on effects on the food chain of wildlife, including birds. Inseveral other cases, insufficient evidence exists to demonstrate this causallink at present, but there is a clear case for further research.

• Nitrogen and phosphorus in chemical fertilisers have helped to change theway crops, including grassland, are grown and managed. This in turn hasreduced the variety of non-crop plant species in farmland, reducedinvertebrate and seed resources for some birds, and increased thepotential for disturbance by farm operations.

• Red-backed shrike is now extinct in the UK; its decline largely driven byfertiliser application to grassland. This process also helped drive corncrakeand cirl bunting to the brink of extinction in the UK; these two species areslowly recovering as a result of intensive conservation effort.

• Nutrient pollution affects delicate aquatic ecosystems such as lakes, lochsand reedbeds. Whilst eutrophication may favour birds in somecircumstances, in others it adversely affects the availability of suitableinvertebrate and fish prey for habitat specialists such as bittern.

• Moorland and heathland habitats are naturally low in nutrients andsensitive to external nutrient inputs. While nitrogen deposition is not themajor cause of the shift away from heather to grasses and othervegetation, it can exacerbate the effects of disturbance such as grazing.This can have knock-on consequences for birds such as the red grouse,which are adapted to heather dominated habitats.

• Knowledge and technologies exist to improve nutrient management in allsectors. Government needs to develop the right mix of policies to putthese skills into practice, including better regulation, incentives and advice.

16

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17

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a healthy environment for birds and wildlife,

helping to create a better world for us all.

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