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Rice Fields and Waterbirds in the Mediterranean Region andthe Middle EastAuthor(s): Violetta LongoniSource: Waterbirds, 33(sp1):83-96. 2010.Published By: The Waterbird SocietyDOI: http://dx.doi.org/10.1675/063.033.s106URL: http://www.bioone.org/doi/full/10.1675/063.033.s106

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83

Rice Fields and Waterbirds in the Mediterranean Regionand the Middle East

VIOLETTA LONGONI

Department of Animal Biology, University of Pavia, P.za Botta 9, 27100 Pavia, Italy

E-mail: violetta.longoni@unipv.it

Abstract.—In southern Europe, rice (Oryza sativa) is one of the most important agricultural crops. Relationshipsbetween rice fields and bird occurrence are well studied for some taxa while quantitative data are lacking for other,more secretive, species. Rice cultivation may be important in the conservation of some threatened birds; for exam-ple, agricultural flooded areas in northwestern Italy support 25% of the Italian population of Eurasian Bittern (Bo-taurus stellaris) although variation in farming techniques affect the suitability of fields for birds. Agriculturalpractices that benefit birds include avoiding intermittent flooding or dry cultivation, maintaining stubble duringwinter, allowing some weed patches to persist inside fields and along ditches and conserving natural vegetation inrice field landscapes. Additionally, biological and alternative cultivation methods seem to provide better environ-mental conditions compared to traditional methods. To promote environmental and conservation values of ricefields, BirdLife International coordinates a project throughout Europe for expanding environmentally-friendly ricecultivation. In some regions, rice fields are the only habitat available for wetland birds due to the scarcity or poorquality of natural wetlands. Despite interest in African and Middle Eastern birds and the geographical proximity ofthese areas to Europe, knowledge of birds and rice fields there is extremely limited. The fact that these regions arelocated along some of the most important migration routes in the Old World suggests that their rice fields may beused by large numbers of waterbirds. Received 7 February 2008, accepted 8 September 2009.

Key words.—agriculture, Ardeidae, avifauna, Mediterranean, Middle East, rice fields, waterbirds, wetlands.

Waterbirds 33 (Special Publication 1): 83-96, 2010

In Europe, the countries where climaticcharacteristics allow important rice (Oryzasativa) cultivation are those bordering theMediterranean Sea. Here, rice fields are con-centrated in the largest European alluvialplain as well as in the largest river deltas andestuaries. Central Europe also has small ar-eas of rice cultivation. Currently, Europeanrice cultivation covers about 400,000 ha(FAOSTAT 2007) and accounts for 0.3% oftotal world rice production (Fasola and Ruiz1997). In the last decade, production haschanged little in most European countries(Ferrero 2007), with the exception of thosewhere rice accounts for only a few thousandhectares, where the cultivated area has mark-edly decreased (e.g. Romania, Hungary) ordisappeared (Albania) (FAOSTAT 2007).

Italy is Europe’s most important rice pro-ducer, with approximately 224,000 ha of rice(Table 1). There, cultivation is concentratedin the northwestern portion of the Po RiverPlain, where a complex hydro-geologicalstructure, composed of hundreds of foun-tainheads, facilitates the flooding of fields.The Po River Delta, although a smaller area,

also hosts many paddy fields. Spain, with theExtremadura and Andalucía paddy areas, isEurope’s second largest rice producer, withjust under 120,000 ha. Less extensive cultiva-

Table 1. Rice field distribution in Mediterranean coun-tries, Central Europe and the Middle East. (Source:FAOSTAT 2007.)

Country Area (ha)

Mediterranean countriesEgypt 680,000Italy 224,000Spain 117,000Turkey 80,000Portugal 25,000Greece 24,000France 18,000

Central EuropeRussian Federation 145,000Ukraine 18,000Hungary 2,800Romania 1,200

Middle EastIran 500,000Iraq 129,000

TOTAL 1,964,000

84 WATERBIRDS

tion exist in the southwestern Iberian penin-sula, both within the Doñana and Albuferade Valencia regions of Spain, and in the Te-jo, Sado and Mondego valleys of central Por-tugal. Rice is also cultivated in the Tessaloni-ky area of Greece and in the Rhone Delta(Camargue) in France. In both these areas,the high salt loads of the deltaic environ-ment generally do not allow for any othercrops to be cultivated. Turkey and Egypt arethe two non-European Mediterranean riceproducers, the latter being the most impor-tant in the region with an average of 680,000ha of paddies (Table 1).

Considerable land reclamation for hu-man exploitation occurred in Europe in theearly 20th century. Agricultural conversionand urbanization have caused the loss of 80-90% of natural wetlands (Finlayson et al.1992), which are especially vulnerable due tothe fertility of wetland soils and easy access towater for irrigation (Pain and Dixon 1997).The remaining natural marshes and lagoonsare restricted to peripheral areas on the mar-gins of the agricultural zones, usually unsuit-able for farming. In many cases, their ecolog-ical value is severely jeopardized by pollu-tion, human disturbance and introducedspecies, often resulting in birds using alter-native habitats such as rice fields. Almost30% of European waterbird species have anunfavorable conservation status (Tucker andEvans 1997; BirdLife International 2004).

The only two rice-growing countries inthe Middle East, Iran and Iraq, have 500,000and 129,000 ha of rice fields, respectively. Inthese countries, wetlands historically havebeen better preserved than in Europe, andnumerous large Important Bird Areas (IBA),dominated by the presence of flooded ormarshy areas, still survive.

The cropping cycle in Europe begins inApril with field flooding, which immediatelyprecedes or follows sowing. The water keepsseeds at an optimal temperature until germi-nation, which occurs 20-30 d later. Water lev-els fluctuate in order to allow agriculturaloperations such as spreading of pesticidesand fertilizers, or because of dry weather.Rice reaches its maximum height in Augustand is then harvested, after fields have been

drained, in September or October. Thecropping cycle is delayed by one month inthe Middle East, with sowing in May-Juneand harvesting in October-November(FAOSTAT 2007). Stubble is frequentlyburned and/or buried. Flooding during thenon-cropping season (Elphick et al. 2010)varies among countries, depending on hy-drological conditions; it is common in theEbro Delta in Spain and rather frequent inFrance, but it is extremely rare in Italy.

The ecological conditions under whichrice is cultivated are rather variable. In Italyand central Europe the climate of rice-pro-ducing areas is temperate-continental, withcold winters, warm summers, and most rain-fall occurring during spring and autumn. Inother countries the climate is Mediterra-nean, with dry and warm summers and mildwinters. Rice is primarily grown on fine-tex-tured, poorly drained soils that are not verysuitable for other crops, often in coastal ar-eas where soils are saline (e.g. the Camar-gue, Ebro Delta).

Birds can benefit from rice fields by ex-ploiting them for some of their biologicalneeds (Pierluissi 2010; Stafford et al. 2010).Rice field use by waterbirds has been studiedin depth in several regions, including Italy,France and the Iberian Peninsula, where ex-tensive literature on the topic exists; morelimited information is available for othercountries, such as Greece, while literature islargely lacking for Central Europe, the Mid-dle East and North Africa (Table 2). Even forcountries with extensive literature, manybird taxa have been largely neglected withmost publications concentrating on herons.Several important variables, such as waterdepth or the conditions on dikes, have alsoreceived little study.

Waterbird use of rice fields throughoutthe year is usually the main way that thefields’ adequacy as a substitute for naturalwetlands has been assessed (Richardson andTaylor 2003), with studies of food availabilityand intake rate providing information onforaging habitat quality. This review exam-ines the literature on the occurrence of birdsin southern European rice fields, includingthe effects of the presence of rice fields on

RICE AND BIRDS AROUND THE MEDITERRANEAN 85

Table 2. Waterbird species occurring in rice fields in Mediterranean Europe. Data were obtained from referencescited in this paper, personal observation, and personal communications. No information is included from countriesin Central Europe or the Middle East. Non-waterbird species and vagrants are excluded. Breed = uses fields duringthe breeding period; Nest = places nests in fields; Migr = uses fields during migration; Winter = uses fields in winter.SPEC = Species of European Conservation Concern: 1 implies globally threatened; 2 implies unfavorable conser-vation status in Europe and global population concentrated in Europe; 3 implies unfavorable conservation status inEurope but global population concentrated elsewhere. IUCN = International Union for Nature Conservation RedList Category: NT = Near Threatened.

Species Breed Nest Migr Winter SPEC IUCN

Little Grebe Tachybaptus ruficollis x x xGreat Cormorant Phalacrocorax carbo x xEurasian Bittern Botaurus stellaris x x x x 3Little Bittern Ixobrychus minutus x x 3Black-crowned Night Heron Nycticorax nycticorax x x x 3Squacco Heron Ardeola ralloides x x 3Western Cattle Egret Bubulcus ibis x x xLittle Egret Egretta garzetta x x xWestern Great Egret Ardea alba x x xGrey Heron Ardea cinerea x x xPurple Heron Ardea purpurea x x 3White Stork Ciconia ciconia x x x 2Glossy Ibis Plegadis falcinellus x x x 3Eurasian Spoonbill Platalea leucorodia x x 2Greater Flamingo Phoenicopterus roseus x x x 3Graylag Goose Anser anser xEurasian Wigeon Anas penelope x xGadwall Anas strepera 3Eurasian Teal Anas creccaNorthern Pintail Anas acuta 3Northern Shoveler Anas clypeata 3Mallard Anas platyrhynchos x x x xCommon Shelduck Tadorna tadorna x x xRed-crested Pochard Netta rufina x x xCommon Pochard Aythya ferina 2Water Rail Rallus aquaticus x xSpotted Crake Porzana porzana x xCommon Moorhen Gallinula chloropus x x x xEurasian Coot Fulica atra x x xCommon Crane Grus grus x 2Black-winged Stilt Himantopus himantopus x x xPied Avocet Recurvirostra avosetta x xEuropean Golden Plover Pluvialis apricaria x xGrey Plover Pluvialis squatarola xNorthern Lapwing Vanellus vanellus x x x x 2Little Ringed Plover Charadrius dubius xCommon Ringed Plover Charadrius hiaticula xKentish Plover Charadrius alexandrinus 3Red Knot Calidris canutus x 3Curlew Sandpiper Calidris ferruginea xSanderling Calidris albaLittle Stint Calidris minuta xTemminck’s Stint Calidris temminckiiDunlin Calidris alpina x 3Ruddy Turnstone Arenaria interpres xBroad-billed Sandpiper Limicola falcinellus x 3Ruff Philomachus pugnax x 2Jack Snipe Lymnocryptes minimus x 3Common Snipe Gallinago gallinago x x 3Eurasian Woodcock Scolopax rusticola x 3Bar-tailed Godwit Limosa lapponica x

86 WATERBIRDS

bird biology, studies of waterbird feedinghabits and food availability in paddies, the ef-fect of rice field flooding or drying, theknown influence of chemical products, andhow rice field characteristics influence Euro-pean birds. The discussion is divided intocropping and inter-cropping seasons, as pro-posed by Mañosa i Rifé (1997).

CROPPING SEASON

Several European authors have evaluatedavian use of rice fields by searching for corre-lations between population parameters andthe surface of soil covered by rice; however,quantitative data have only been collectedfor European heron populations. In majorEuropean rice growing areas, rice fields arewidespread and offer valuable foraginggrounds with suitable nesting sites inter-spersed (Prosper and Hafner 1996; Fasolaand Ruiz 1997; Kazantzidis et al. 1997). Rice

fields have been suggested as the most im-portant habitat in Mediterranean Europe forforaging herons (Fasola et al. 1996), thebirds for which use of rice field for foragingincreases most significantly during thebreeding season (Fasola and Ruiz 1996). Fa-sola et al. (1996) estimated that the birds in50-100% of Mediterranean heronries de-pend on rice fields as foraging sites duringthe breeding season. Similarly, 40% of theEurasian Bittern (Botaurus stellaris) popula-tion in Italy is completely dependent on theexistence of flooded paddies (Longoni et al.2007; V. Longoni, unpublished data).

Size and distribution of heronries arepositively correlated with the surface areaunder rice cultivation in the surroundinglandscape (Fasola and Alieri 1992). In thebreeding range of Italian herons, highernesting densities are reached where ricefields dominate the landscape (Fasola 1983).The proportion of land within 1.5 and 10 km

Black-tailed Godwit Limosa limosa x x x 2 NTWhimbrel Numenius phaeopus xEurasian Curlew Numenius arquata x x 2 NTSpotted Redshank Tringa erythorpus x 3Common Redshank Tringa totanus x 2Common Greenshank Tringa nebularia xMarsh Sandpiper Tringa stagnatilisGreen Sandpiper Tringa ochropus xWood Sandpiper Tringa glareola x 3Common Sandpiper Actitis hypoleucos x 3Black-headed Gull Chroicocephalus ridibundus x x x xLittle Gull Hydrocoloeus minutus x x 3Audouin’s Gull Ichthyaetus audouinii x x 1 NTMediterranean Gull Ichthyaetus melanocephalus x xMew Gull Larus canus x x 2European Herring Gull Larus argentatus xYellow-legged Gull Larus michahellis x x xLesser Black-backed Gull Larus fuscus x xCommon Tern Sterna hirundo x x xLittle Tern Sternula albifrons x x 3Gull-billed Tern Gelochelidon nilotica x x 3Black Tern Chlidonias niger x x 3White-winged Tern Chlidonias leucopterus x x x

Table 2. (Continued) Waterbird species occurring in rice fields in Mediterranean Europe. Data were obtained fromreferences cited in this paper, personal observation, and personal communications. No information is includedfrom countries in Central Europe or the Middle East. Non-waterbird species and vagrants are excluded. Breed =uses fields during the breeding period; Nest = places nests in fields; Migr = uses fields during migration; Winter =uses fields in winter. SPEC = Species of European Conservation Concern: 1 implies globally threatened; 2 impliesunfavorable conservation status in Europe and global population concentrated in Europe; 3 implies unfavorableconservation status in Europe but global population concentrated elsewhere. IUCN = International Union for Na-ture Conservation Red List Category: NT = Near Threatened.

Species Breed Nest Migr Winter SPEC IUCN

RICE AND BIRDS AROUND THE MEDITERRANEAN 87

of nesting sites that is used for rice produc-tion is positively correlated with the numberof tree-nesting herons (Hafner and Fasola1997; Parejo and Sanchéz-Guzmán 1999;Tourenq et al. 2000, 2004) and influencesthe probability that an isolated reedbed, orthe paddies themselves, are colonized byEurasian Bitterns (Bogliani et al. 2001; V.Longoni, unpublished data). In contrast,Squacco Heron (Ardeola ralloides) brood sizesdecline with increasing rice cultivation,probably because this sensitive species ismore dependent on natural, unaltered wet-lands than other herons (Hafner et al. 2001).Western Cattle Egret (Bubulcus ibis) is a moreopportunistic species that rapidly colonizedEurope starting in the 1960s, with the firstnests in the Camargue in 1967 (Tourenq etal. 2004). This generalist egret is thought tobenefit greatly from the presence of ricefields (Tourenq et al. 2004). Other herons,such as Little Egret (Egretta garzetta) and Pur-ple Heron (Ardea purpurea) exploit naturalwetlands more than their availability wouldsuggest (Campos and Lekuona 2001; Lom-bardini et al. 2001; Tourenq et al. 2001a), butare intermediate in their use of rice fields.

Since Mediterranean countries are char-acterized by dry summers and wet winters,feeding areas for birds may become greatlylimited during dry years, thus promotingrice field use (Tourenq et al. 2001b, 2004).With the exception of sensitive species, likethe Purple Heron, rice field use by herons isproportional to rice field availability in mostof Europe. An exception is the Camargue/Rhone Delta where rice fields are used lessthan expected given their availability (Fasolaet al. 1996). This area, however, has morenatural wetlands than other major rice grow-ing areas in southern Europe, allowingwaterbirds to remain in their natural habitatwhere sufficient resources are available. InSpain, Purple Herons increasingly forage inpaddies as the season advances and theirfood requirement for chicks grows (Camposand Lekuona 2001). Prey availability in pad-dies peaks at this time, which also representsthe peak of breeding success for Black-crowned Night Herons (Nycticorax nycticorax)and Little Egrets in Italy (Fasola 1998).

Development of rice field communitiesfollows the hydrologic cycle (González-Solíset al. 1996). Bird prey items differ markedlybetween geographical areas in Europe, bothin terms of abundance and prey species (Fa-sola et al. 1996). Most studies of heron dietsare based on food regurgitated by chicks ordirect observation of hunting adults (Ker-sten et al. 1991; Fasola 1994; Fasola et al.1996). These data could underestimate rap-idly digested prey items, such as annelidsand amphibian larvae, or small prey whichare swallowed quickly (Fasola et al. 1981).Prey availability has been assessed by towingnets through the water in several analyses(Fasola et al. 1981, 1996; Gonzáles-Solís et al.1996), but fast swimmers have been greatlyunderestimated since they can easily escapefrom traps (Gonzáles-Solís et al. 1996).

Generally, waterbird prey in rice fieldsduring summer consist of benthic and sur-face-dwelling invertebrates and aquatic ver-tebrates (Stafford et al. 2010). The mainfoods are tadpoles, adult frogs, crustaceansand fish (Fasola et al. 1981, 1993; Oro et al.1996), but species of the Annelida, Isopoda,Coleoptera (especially Hydrophilidae andDytiscidae), Odonata, Lepidoptera andDiptera are also eaten, while reptiles, mam-mals and birds are taken infrequently (Faso-la 1994; Oro et al. 1996; Dies et al. 2005). Thelarvae of mosquitoes, chironomids and oth-er invertebrates are important in the diet ofducklings (Fasola and Ruiz 1996; Lawler andDritz 2005). These insects benefit from somewinter agricultural practices such as bury-ing—rather than burning—straw and winterflooding (Lawler and Dritz 2005).

Until the 1980s, the only crustacean thathad been reported in the diets of herons us-ing rice fields in Europe was the HorseshoeShrimp (Triops cancriformis) (Fasola et al.1981). However, the introduced Red SwampCrayfish (Procambarus clarkia), native toNorth America, has rapidly become wide-spread in Spain, Portugal, France Italy andsome islands (Correia 2002; Souty-Grosset etal. 2006; Cruz and Rebelo 2007). It is nowthe most abundant crustacean in Europeanrice fields, except in Greece. In southernSpain, the Red Swamp Crayfish is now the

88 WATERBIRDS

primary food of Gull-billed Terns (Gelocheli-don nilotica) (Dies et al. 2005) and is thoughtto be a cause of population increase inGlossy Ibis (Plegadis falcinellus), althoughspecific studies have not found a strong cor-relation (Macias et al. 2004). These crayfishare also an important food item for breedingAudouin’s Gulls (Ichthyaetus audouinii) in theEbro Delta (Oro et al. 2006).

Fish are captured frequently in Italy andSpain, but in France they are often excludedfrom rice fields during the process of pump-ing water from channels to fields. In naturalwetlands, fish that perform aquatic surfacerespiration are easily caught by Little Egrets(Kersten et al. 1991), suggesting that a hypo-oxygenated environment, such as that foundin flooded fields (Mañosa i Rifé 1997; Ferre-ro 2007), favors waterbirds feeding on aquat-ic organisms.

Western Cattle Egrets appear to havehigher food intake in rice fields than in nat-ural habitats (Fasola et al. 1996), but this re-sult could relate to the generalist habits ofthe species, which generally uses terrestrialhabitats more than other herons (Fasola andRuiz 1996; Parejo and Sánchez-Guzmán1999; Tourenq et al. 2001b, 2004), makingrice paddy foraging possible throughout theagricultural cycle. In contrast, paddies arethe second choice for many more specialistbirds. Gull-billed Terns in eastern Spain feedmostly in rice paddies (Dies et al. 2005) andAudouin’s Gulls increase their use of ricefields during periods when offshore trawlingis banned and discarded fish are unavailable(Oro et al. 1996). Gull and tern abundancecorrelates with the surface area covered bywater, including the extent of rice cultivation(Fasola et al. 1983). In northwestern Italy,successful pairs of captive-bred White Storks(Ciconia ciconia) forage mostly in rice fieldsin the vicinity of their nest sites, with birdstravelling up to several km to feed (V. Longo-ni, personal observation).

Rice fields are intensively used by Carri-on Crows (Corvus corone), which can adverse-ly affect the reproductive success of otherspecies nesting nearby, by feeding on theireggs or chicks. Crows mostly depredate thenests of Northern Lapwing (Vanellus vanel-

lus), Common Moorhen (Gallinula chloro-pus), Mallards (Anas platyrhynchos), and tree-nesting herons, but also other less commonspecies.

To a lesser extent, rice fields are used asnesting sites (Fasola and Ruiz 1997; Mañosai Rifé 1997; Czech and Parson 2002; Pierluis-si 2010). Within rice fields nesting is restrict-ed to those species that build floating orbanked nests (e.g. Common Moorhen, Eur-asian Bittern, Black Tern Chlidonias niger,White-winged Tern Chlidonias leucopterus,Pied Avocet Recurvirostra avosetta). Amongthem, Eurasian Coot (Fulica atra) and Black-winged Stilt (Himantopus himantopus) are thetwo commonest species that build bankednests in early spring in flooded fields. Otherspecies place nests in the vegetation of irriga-tion canals (Little Bittern Ixobrychus minutus)or on dykes (Northern Lapwing and Black-tailed Godwit Limosa limosa) (Fasola andRuiz 1997; Mañosa i Rifé 1997).

NON-CROPPING SEASON

In autumn, after harvest, the landscapechanges dramatically; in just a few weeks, ex-tensive wetland areas are transformed intodrylands. Seedbeds are frequently preparedby ploughing fields to a depth of about 20cm right after harvest (Ferrero 2007). Fieldscan then be re-flooded or left dry dependingon the farming practice. Rice fields are usedless by birds in winter, when paddies dry out,prey availability decreases, and suitability forwaterbirds diminishes. In the Ebro Delta,paddies are traditionally kept wet until lateDecember for hunting; in France, this hap-pens in 5-10% of cases (Tourenq et al. 2001b)to attract waterfowl for hunting. Winterflooding is very uncommon in most otherEuropean countries (Fasola and Ruiz 1997;Mañosa i Rifé 1997).

In the Ebro Delta, numbers of winteringwaterfowl are affected by the area of floodedpaddy fields, which, with the Albufera, Doña-na and Camargue, represent the main win-tering areas in the Western Palearctic forducks (Sánchez-Guzmán et al. 2007; Rendónet al. 2008). Northern Shovelers (Anas clypea-ta), Eurasian Teals (Anas crecca), Northern

RICE AND BIRDS AROUND THE MEDITERRANEAN 89

Pintails (Anas acuta), Mallards, Red-crestedPochards (Netta rufina) and Gadwalls (Anasstrepera) all occur in these areas, as do manyEurasian Coots (Llorente et al.1986; Rendónet al. 2008). While some swimming species(e.g. Eurasian Coot, Eurasian Teal) requirethe presence of water, others (e.g. Mallard,Common Moorhen) will also feed on fallenrice seeds in drier conditions (Fasola andRuiz 1996; Czech and Parson 2002).

In Iberia, rice fields support large popu-lations of wintering and migrating shore-birds. As many as 40 species of shorebirdshave been recorded in the Ebro Delta andtheir abundance was strongly dependent onflooded rice fields (Martínez-Vilalta 1985).Wintering waders favor flooded rice fields,which are the only alternative foraging habi-tat when high tides make littoral zones unus-able (Martínez-Vilalta 1985; Barbosa 1996).Dunlins (Calidris alpina), Little Stints (Calid-ris minuta), Common Snipes (Gallinago galli-nago) and Northern Lapwings all frequentpaddies during migration, and rice fieldsand are among the most important stopoversites for Black-tailed Godwits (Lourenço andPiersma 2008).

In most areas, herons are the most visibleusers of rice field during winter. Winteringmigrant Black-crowned Night Herons andWestern Cattle Egrets join resident individu-als in Italy and Spain, most likely due to theprey offered by paddies (Fasola and Alieri1992; Martínez et al. 1992; Fasola and Ruiz1996; Dies et al. 2003). Paddies also providecrucial habitat for wintering White Storks,which use rice fields intensively during win-ter (Rendón et al. 2008). The Ebro Delta andthe Albufera de Valencia region are reportedto be important areas for wintering LittleEgrets. Black-crowned Night Herons areprobably able to perform early nesting at-tempts due to the winter abundance of RedSwamp Crayfish in rice fields (Martínez et al.1992).

Although winter use is greatest in flood-ed fields, unflooded fields are also used bysome species. Ploughing tractors are usuallyfollowed by mixed groups of Western CattleEgrets, Little Egrets, Grey Herons (Ardea ci-nerea), Black-headed Gulls (Chroicocephalus

ridibundus) and Yellow-legged Gulls (Larusmichahellis) searching for small mammalsand invertebrates exposed by the plough.Non-inundated fields can also offer a vari-able amount of wasted seed dropped duringharvesting, which are eaten by ducks, Com-mon Moorhens and Black-tailed Godwits(Czech and Parson 2002; Lourenço andPiersma 2008), as well as passerines. Plough-ing and flooding harvested fields increasesavailability of kernels to waterbirds, probablybecause these practices reduce predation byrodents and passerines (Lourenço and Piers-ma 2008). The introduction of stripper-header harvesters could represent a deleteri-ous harvesting technique due to the reducedamount of rice that remains on the soil (Mill-er and Wylie 1996), but the technique canprovide cover for birds (Elphick et al. 2010).Habitat provided by straw left over after thestripping of rice plants attracts winteringEurasian Bitterns and rails (V. Longoni, per-sonal observation), as it resembles a reedbedand has enhanced invertebrate richness(Lawler and Dritz 2005). Straw manage-ment, therefore, has different consequenceson different types of wading birds (Fasolaand Ruiz 1996; Elphick and Oring 1998;Czech and Parsons 2002).

Waterbirds are not the only species thatoccur in rice fields during winter. Sparrows,finches and buntings feed on scattered rice,birds of prey forage on small mammals andbirds, while crows and starlings feed oppor-tunistically. Western Marsh Harriers (Circusaeruginosus) and Common Buzzards (Buteobuteo) are often seen hunting in rice fieldsboth in winter and in the growing season(Boano and Tofolli 2002; Carpegna et al.2003). Western Barn Owls (Tyto alba) alsouse rice fields throughout the year (Agueroand Poleo 2000), although their presence isseverely limited by the lack of suitable nest-ing sites.

EFFECT OF FLOODING

Rice fields are kept flooded throughoutmost of the cultivation cycle, mainly to pro-tect plants from low temperatures, avoid rap-id temperature variations and limit weed

90 WATERBIRDS

growth. The water level varies over the grow-ing season; it is kept at 5-7 cm during the firststages of growth to promote rice growth androot anchorage, and at 10-15 cm after ricetillering, mainly to avoid pollen sterility ef-fects caused by low temperatures duringcrop flowering. Throughout the cultivationseason, water is usually drained away two tothree times to improve crop rooting or allowfertilization and herbicide spraying. Finally,about 20-30 d prior to harvesting, rice fieldsare completely drained to facilitate harvest-ing operations (Ferrero 2007).

Flooding during alternate seasons gener-ates discontinuous environmental condi-tions in these agricultural areas, changingecological, physical and chemical factors infields, with severe consequences for the suit-ability of this habitat for birds, particularlyregarding food availability. The water regimein rice fields in Europe is the opposite of thatfor natural wetlands, which are flooded inwinter and dry in summer. Birds using ricefields can thus find favorable wet conditionswhen natural wetlands are dry. For numer-ous species of shorebird, the period whenfields are inundated, but before rice plantshave sprouted, coincides with migration.

The start of flooding has immediate con-sequences for bird biology. In l’Albufera deValencia, Black-crowned Night Herons andSquacco Herons start breeding with theflooding of fields in late spring (Prosper andHafner 1996). Black-crowned Night Heronsalso abandon early nesting attempts in Janu-ary and February when, in March and April,fields are dried out and food availability de-clines. While Spanish paddies are dried outin March and April, in Italy, Greece and mostother countries, fields begin to be flooded atthat time, attracting migrating Ruffs (Philo-machus pugnax), Dunlins, Wood Sandpipers(Tringa glareola) and Spotted Redshanks(Tringa erythropus), with many other waderspecies also occurring (Pena 1985; Fasolaand Ruiz 1996; Czech and Parson 2002). InPortugal and Spain, between late Decemberand early March, Black-tailed Godwits forageon spilled rice grain in flooded rice fieldsmore than in dry fields (Sánchez-Guzmán etal. 2007; Lourenço and Piersma 2008). In

the Camargue, Greater Flamingos (Phoeni-copterus roseus) feed in rice fields, in flocks ofup to 50 individuals, as soon as fields areflooded, causing severe damage to youngrice plants (Tourenq et al. 2001c).

Water depth in paddies probably plays animportant role in attracting birds but it hasnot been extensively evaluated, unlike inother parts of the world (e.g. in California,Elphick and Oring 1998, 2003). In Spain,depth has been considered, with the resultthat wintering waders were most likely to usepaddies with a water depth of less than 8 cm(Martínez-Vilalta 1985). Until recently, a fewpuddles, which provided shelter for aquaticorganisms, usually persisted in rice fieldseven during dry periods, due to the presenceof small hollows and dips. However, the in-troduction of laser-levelling, which flattensfields to create significant water savings, hasled to the elimination of aquatic organisms.Experimental fields, with artificial pondsthat can host aquatic organisms during dryphases, show higher abundance and diversi-ty than conventional fields (E. Riservato andG. Bogliani, unpublished data).

Overall, when compared with other fac-tors characterizing field management, theamount of water appears to be the main fac-tor affecting the distribution of many species(Lourenço and Piersma 2009). That thepresence of water, rather than rice itself, isthe most important parameter for bird biol-ogy, is suggested by the fact that the totalnumber of breeding herons is correlatedwith irrigated cultivation—not necessarilyrice—development in Extremadura (Parejoand Sánchez-Guzmán 1999).

USE OF CHEMICAL PRODUCTS

Rice cultivation involves huge amountsof chemical products being released into thesoil and water (Parsons et al. 2010). In theEbro Delta, where water recharge is continu-ous and agricultural waters drain into la-goons and the sea, the release of chemicalsubstances is a serious problem (Mañosa etal. 2001). Some information on this topic isalso available for the Axios Delta in Greece(Papadopoulou-Mourkidou et al. 2004), but

RICE AND BIRDS AROUND THE MEDITERRANEAN 91

none for other Mediterranean countries. Al-though these substances break down in ashort time, they have a strong impact on ricefield ecosystems, with repercussions for birds(Ibáñez et al. 2010). Organic techniques,more favorable to biodiversity (Pain and Dix-on 1997), account for only a small percent-age of the total rice acreage. Use of insecti-cides to control pests directly affects animalcommunities, but algaecides, fungicides,herbicides and fertilizers also alter foodchains, with significant secondary repercus-sions for animal communities. Mesléard et al.(2005), for example, found that organically-farmed fields host higher abundances of Co-leoptera, Odonata and Amphibia, eaten byherons. Tourenq et al. (2003) also foundmore waterbirds feeding in organic fieldsthan in conventional fields.

Chemical control of Horseshoe Shrimp,a major prey item for herons (Hafner et al.1982, 1986; Fasola et al. 1996), has been per-formed regularly since the 1980s, drasticallyreducing its presence in wetlands. Horse-shoe Shrimp declines in the Camargue, dueto use of the pesticides parathion and lin-dane, are presumed to have caused LittleEgrets to forage less in rice fields (Hafner etal. 1986). Use of fipronil to control chirono-mid larvae is also a widespread agronomicpractice. In reality the pesticide has failed todecrease chironomid abundance, but it hasled to a severe decrease of other inverte-brates, reducing the availability of prey tobirds (Mesléard et al. 2005). Chemicals couldalso affect bird reproduction through con-tamination of eggs (Ruiz et al. 1992). Al-though chemicals mostly impact bird popu-lations by reducing food resources, direct ef-fects are also reported. The drastic reduc-tion in the population of Purple Herons inSpain in the 1960s apparently derived fromthe abuse of agricultural pesticides (DelHoyo et al. 1996), while the Little Egret pop-ulation is also reported to have suffered dueto these chemicals (Hafner et al. 1986).

Waterfowl hunting causes variable levelsof lead poisoning in water bodies (Figuerolaet al. 2005). The degree of lead concentra-tion in rice-field soils is not well known, al-though this information would be of interest

both for animal and human health, sincemany rice-field areas are used for hunting.Rates of shot ingestion by birds are high inregions exposed to intensive hunting activity(Figuerola et al. 2005), meaning that water-fowl could be exposed to lead poisoning andin turn become a danger for humans that eatthem.

RICE FIELD CHARACTERISTICS

Approximately 70% of European rice-growing areas are planted with differentjaponica varieties of rice, and the remainderwith indica varieties (Ferrero 2007). Thesevarieties can differ substantially in plantheight and density, which can have varyingimpacts on birds. Rice varieties with tallerand less dense vegetation seem to host morenesting birds, such as Common Moorhensand Mallards, and foraging birds, such asegrets, Little Bitterns and rails (V. Longoni,personal observation), compared to thosewith shorter, denser vegetation, where move-ment may be hampered, prey is less visibleand accessible, and appropriate cover is re-duced. Accordingly, Eurasian Bitterns bothfeed and nest in fields with taller rice plants,and, in early summer, prefer to feed in fieldswith taller marsh plants such as Phragmitesaustralis to provide cover (Longoni et al.2007).

Vegetation at field margins and alongditches drastically changes the appearanceof the habitat, and the presence of hedgesand reduced paddy size can affect species oc-currence (e.g. it reduces the risk of flamingoincursion, Tourenq et al. 2001c). Rice-fieldbanks covered by low herbaceous vegetationare attractive for nesting Northern Lap-wings, which recently became a commonbreeding bird in this habitat in northern Ita-ly, and Mallards.

The nature of rice agriculture in Europealso changes significantly when rice is grownon dry soil. Dry-soil rice cultivation is rare inEurope (Mesléard 1994; Fasola et al. 1996),and concentrated in northwestern Italy,where it accounts for 30% of rice cultivation(Fasola and Ruiz 1996). Dry-soil rice cultiva-tion saves water, which can be costly in some

92 WATERBIRDS

areas, facilitates the operation of machineryand chemical applications, and has other ad-vantages to farmers when it can be imple-mented effectively. Unfortunately, the lowsuitability of this habitat for wildlife results ina dramatic loss of biodiversity and a strongreduction in the presence of birds (Mesléard1994; Czech and Parson 2002). Heronscould be particularly affected by the conver-sion of flooded to dry rice agriculture, in adirect and proportional relationship, withpotentially catastrophic results for their pop-ulations should flooded fields no longer beavailable as feeding grounds during thebreeding season (Fasola et al. 1996; Fasolaand Ruiz 1997; Mañosa i Rife 1997; Czechand Parson 2002). Conversion to dry fieldsdoes not seem likely in Egypt, where watersavings are offset by the high yields achievedby continuous inundation, and where farm-ers often refuse to dry paddies, even for lim-ited periods. In Egypt, however, drying is lessessential because rice cultivation is still al-most completely conducted by hand (A. Ba-suni, personal communication).

VALUE OF RICE FIELDS

During autumn and winter, when the ab-sence of water in rice fields dramatically re-duces their suitability for birds, naturalmarshes have a greater bird abundance, spe-cies richness and number of exclusive spe-cies (Tourenq et al. 2001b; Czech and Parson2002). In early spring, when migrants (most-ly shorebirds) and breeders (mostly gullsand herons) arrive, fields are flooded, butnot yet covered by vegetation, and act likemud-flats (Oro et al. 1996; Fasola and Ruiz1997; Tourenq et al. 2001b; Dies et al. 2005).Once fields are covered with vegetation, few-er species can benefit from them (Mañosa iRife 1997; Tourenq et al. 2001b); herons, andmost other birds that feed in rice fields atthis time, need natural habitats such aswoodland patches in order to nest. At thistime, use of natural marshes is greater thanexpected from their availability relative torice paddies in the same area (Campos andLekuona 2001; Tourenq et al. 2001a). Ricefields, on the other hand, are used in pro-

portion to their availability only when natu-ral wetlands are scarce or unavailable (Bar-bosa 1996; Fasola et al. 1996; Tourenq et al.2001a, b). Rice fields are used by Dunlinswhen tidal areas are unavailable for forag-ing, and are thus an important secondaryfood source (Barbosa 1996). Little Egrets, inspite of their extensive use of rice paddies,prefer freshwater marshes when available, inthe Camargue (Hafner et al. 1982) and theAxios Delta (Kazantzidis and Goutner 1996).Rice fields are not high value habitat forthose species that preferentially feed on fish-es or saltwater aquatic animals; for example,Purple Herons in Spain prefer rivers to ricefields (Campos and Lekuona 2001) and ricepaddies are a secondary habitat for Au-douin’s Gulls (Oro 1995; Oro et al. 1996).Eurasian Spoonbills (Platalea leucorodia) arerare in areas dominated by rice cultivation(Fasola and Ruiz 1997), and the birds thatbreed in the Po and Ebro Deltas do not for-age in rice fields (Aguilera et al. 1996; M. Fa-sola, personal communication). Moreover, ittakes more time for birds foraging in ricefields to obtain the same biomass and energyintake as they would achieve by feeding inrivers (Campos and Lekuona 2001), due todifferences in prey size and energy content(Kazantzidis and Goutner 1996; Campos andLekuona 2001). Flooded fields, however,could attract more birds in dry years, whennatural wetlands suffer from scant rainfall(Tourenq et al. 2001b, 2004).

As in other parts of the world (Chan et al.2007), European rice fields are valuable sub-stitutes for disappearing natural wetlandsonly for certain species, and they offer a con-tribution, but not a substitution, in maintain-ing waterbird diversity. The presence of pad-dies in Europe ensures the presence ofhealthy heron populations, and sustains theregional persistence of waterbird speciessuch as Common Moorhen, Eurasian Coot,Black-winged Stilt, Eurasian Bittern andWhite Storks, which otherwise would be lesscommon or even absent. From this point ofview, rice fields could be considered as abuffer habitat able to mitigate the loss of nat-ural wetlands (Weber et al. 1999). In Extrem-adura, Spain, rice fields host an important

RICE AND BIRDS AROUND THE MEDITERRANEAN 93

fraction of migrant populations of birds ofinternational concern. For example, 19% ofthe migrant Common Cranes (Grus grus) inthe East Atlantic Flyway use rice fields asstopover habitat (Sánchez-Guzmán et al.2007) and Portuguese fields are importantfor migrant Black-tailed Godwits (Kuiper etal. 2006; Lourenço and Piersma 2008).

By managing flooding regimes and cattlegrazing in abandoned rice fields, it is possi-ble to advantage both biodiversity and pasto-ral activity (Mesléard et al. 1995). Given eco-logical differences in climate and soil withinthe Mediterranean region, however, furtherstudies of this type are warranted in areasoutside the Camargue. The deterioration ofnatural wetlands in Europe makes rice fieldmanagement a priority for waterbird conser-vation. While reconversion from paddies tonatural marshes, although theoretically pos-sible and fruitful (Mesléard 1994; Mesléardet al. 1995; Comin et al. 2001), is an unrealis-tic proposal on a large scale, management ofrice fields to better enhance biodiversity maybe possible. Because not all crops providethe same value for wildlife, conversion of ricefields to the cultivation of other cerealswould likely be harmful to waterbirds. Al-though the main factors that are detrimental(high levels of chemical use, repeated dryphases during summer, conversion to drycultivation, stubble burning) or favorable(maintenance of water throughout the grow-ing cycle, winter flooding, vegetation alongfield margins) to waterbirds are known,more research on the details of field man-agement would be valuable. Previous worksuggests that a mosaic of different manage-ment options, providing different ecologicalconditions within the agricultural landscape,represents a good choice for bird conserva-tion (Lourenço and Piersma 2009). Themaintenance, management, enlargementand creation of natural wetlands inter-spersed among rice fields could also benefitEuropean waterbirds.

MIDDLE EAST RICE FIELDS

Information on waterbird use of ricefields in the Middle East is completely lack-

ing in the international scientific literature,and the subject is neglected in regional jour-nals (A. Khaleghizadeh, personal communi-cation). Nonetheless, these areas are un-doubtedly of great interest for bird conserva-tion. Iran and Iraq both have extensive natu-ral wetlands, and the region straddles theEastern and Western Palaearctic and lies onan important migratory route for Eurasianbreeding birds. Censuses conducted by theIran Department of the Environment for theInternational Waterbirds Census, have docu-mented a rich wetland avifauna in theFeredonkenar Ramsar site in northern Iran.The site includes, and is surrounded by, ricefields, which are presumably used by water-birds. The Siberian Crane (Grus leucogera-nus) is a critically-endangered bird with ahigh conservation value (BirdLife Interna-tional 2007; IUCN 2008) and small numbersoccur in Feredonkenar every winter, forag-ing in rice fields when hunting disturbancein the natural wetlands is high (A. Kha-leghizadeh and R. Ayé, personal communi-cation). Large numbers of shorebirds pre-sumably also occur, because thousands arereported to be hunted annually. Many birdsspecies, such as Northern Lapwing, LittleGull (Hydrocoloeus minutus), Whiskered Tern(Chlidonias hybrida), Western Barn Owl, Eu-ropean Bee-eater (Merops apiaster), Blue-cheeked Bee-eater (Merops persicus), BarnSwallow (Hirundo rustica) and Rook (Corvusfrugilegus), have been observed in rice pad-dies, including species of conservation con-cern (e.g. Corn Crake Crex crex; A. Ashoori,A. Khaleghizadeh and B. Nezami, personalcommunication). No formal monitoring ofthe rice field avifauna has ever been con-ducted in this region, however, and the sta-tus of waterbirds and their occurrence inrice fields is almost entirely unknown.

ACKNOWLEDGMENTS

Information from the Middle East was difficult to ob-tain. I am indebted primarily to A. Khaleghizadeh (Or-nithology Laboratory, Agricultural Zoology ResearchDep., Iranian Research Institute for Plant Protection, Te-hran, Iran) for providing information and contacts, andto A. Ashoori and B. Nezami for allowing access to fieldnotes on rice fields. Information on Siberian Cranescame from R. Ayé. Data on Iranian IWC were provided

94 WATERBIRDS

by M. E. Sehhatisabet (Kerman Provincial Office of theDepartment of the Environment, Kerman, Iran). G.Conca and D. Segagni compiled a comprehensive list ofwaterbirds occurring in northern Italian rice fields; A.Green, J. C. Cirera and C. Ibáñez Martí provided infor-mation on the Doñana and Ebro regions in Spain. Final-ly, I thank P. Lourenço for improving the paper.

LITERATURE CITED

Aguero, D. A. and Y. Poleo. 2000. Predator potential ofBarn Owl (Tyto alba) on rat populations in ricecrops. Investigacion Agricola 5: 5.

Aguilera, E. 1996. Food and feeding sites of the Eur-asian Spoonbill (Platalea leucorodia) in southernSpain. Colonial Waterbirds 19: 159-166.

Barbosa, A. 1996. Foraging habitat use in a Mediterra-nean estuary by Dunlin, Calidris alpina. Journal ofCoastal Research 12: 996-999.

BirdLife International. 2004. Birds in Europe: Popula-tion Estimates, Trends and Conservation Status.BirdLife Conservation Series No. 12. BirdLife Inter-national, Cambridge, UK.

BirdLife International. 2007. World Bird Database: theSite for Bird Conservation. Version 2.1. BirdLife In-ternational, Cambridge, UK. http://www.birdlife.org, accessed 8 October 2007

Boano, G. and R. Toffoli. 2002. A line transect surveyof wintering raptors in the western Po plain ofnorthern Italy. Journal of Raptor Research 36: 128-135.

Bogliani, G., C. Mazzoli, G. Alessandria, L. Bontardelli,F. Carpegna, M. Della Toffola, A. Ramponi and E. Vi-go. 2001. Scelta dell’habitat del tarabuso Botaurusstellaris nidificante nell’area delle risaie. Avocetta 25:19.

Campos, F. and J. M. Lekuona. 2001. Are rice fields asuitable foraging habitat for Purple Herons duringthe breeding season? Waterbirds 24: 450-452.

Carpegna, F., G. Alessandria and M. Della Toffola. 2003.Note on the wintering of the Marsh Harrier Circusaeruginosus in the paddy fields of Vercelli. Avocetta27: 30.

Chan, S.-F., L. L. Severinghaus and C.-K. Lee. 2007. Theeffect of rice field fragmentation on wintering water-birds at the landscape level. Journal of Ornithology148: 333-342.

Comin, F. A., J. A. Romero, O. Hernandez and M. Me-nendez. 2001. Restoration of wetlands from aban-doned rice fields for nutrient removal, andbiological community and landscape diversity. Res-toration Ecology 9: 201-208.

Correia, A. M. 2002. Niche breadth and trophic diversi-ty: feeding behaviour of the Red Swamp Crayfish(Procambarus clarkii) towards environmental avail-ability of aquatic macroinvertebrates in a rice field(Portugal). Acta Oecologica 23: 421-429.

Cruz, M. J. and R. Rebelo. 2007. Colonization of fresh-water habitats by an introduced crayfish, Procambarusclarkii, in Southwest Iberian Peninsula. Hydrobiolo-gia 575: 191-201.

Czech, H. A. and K. C. Parsons. 2002. Agricultural wet-lands and waterbirds: a review. Waterbirds 25 (Spe-cial Publication 2): 56-65.

Del Hoyo, J., A. Ellyot and J. Sargatal (Eds.). 1996.Handbook of the Birds of the World I. Lynx Edi-cions, Barcelona, Spain.

Dies, J. I., N. Ramon and J. Prosper. 2003. Winter breed-ing by Black-crowned Night Heron in eastern Spain.Waterbirds 26: 379-382.

Dies, J. I., J. Marin and C. Perez. 2005. Diet of nestingGull-billed Terns in eastern Spain. Waterbirds 28:106-109.

Elphick, C. S. and L. W. Oring. 1998. Winter manage-ment of Californian rice fields for waterbirds. Jour-nal of Applied Ecology 35: 95-108.

Elphick, C. S. and L. W. Oring. 2003. Conservation im-plications of flooding rice fields on winter waterbirdcommunities. Agriculture, Ecosystems and Environ-ment 94: 17-29.

Elphick, C. S., O. Taft and P. Lourenço. 2010. Manage-ment of rice fields for birds during the non-growingseason. Waterbirds 33 (Special Publication 1): 181-192.

FAOSTAT. 2007. Food and Agriculture Organisation(FAO). FAOSTAT 2007. http://faostat.fao.org, ac-cessed 26 October 2007.

Fasola, M. 1983. Nesting populations of herons in Italydepending on feeding habitats. Bollettino di Zoolo-gia 50: 21-24.

Fasola, M. 1994. Opportunistic use of foraging resourc-es by heron communities in southern Europe. Ecog-raphy 17: 113-123.

Fasola, M. and R. Alieri. 1992. Conservation of heronryArdeidae sites in north Italian agricultural land-scapes. Biological Conservation 62: 219-228.

Fasola, M. and X. Ruiz. 1996. The value of rice fields assubstitutes for natural wetlands for waterbirds in theMediterranean region. Colonial Waterbirds 19 (Spe-cial Publication 1): 122-128.

Fasola, M. and X. Ruiz. 1997. Rice farming and water-birds: integrated management in an artificial land-scape. Pages 210-235 in Farming and Birds in Europe:The Common Agricultural Policy and its Implicationsfor Bird Conservation (D. J. Pain and M. W. Pienkows-ki, Eds.). Academic Press, London, UK.

Fasola, M., P. Galeotti, G. Bogliani and P. Nardi. 1981.Food of Night Heron (Nycticorax nycticorax) and Lit-tle Egret (Egretta garzetta) feeding in rice fields. Riv-ista Italiana di Ornitologia 51: 97-112.

Fasola, M., V. Gouter and J. Walmsley. 1983. Compara-tive breeding biology of the gulls and terns in thefour main deltas of the northern Mediterranean.Pages 11-123 in Status and Conservation of Seabirds(J. S. Aguilar, X. Monbaillu and A. Paterson, Eds.).SEO, Madrid, Spain.

Fasola, M., P. Rosa and L. Canova. 1993. The diets ofSquacco Herons, Little Egrets, Night, Purple andGray Herons in their Italian breeding ranges. RevueD’Ecologie-La Terre Et La Vie 48: 35-47.

Fasola, M., L. Canova and N. Saino. 1996. Rice fieldssupport a large portion of herons breeding in theMediterranean region. Colonial Waterbirds 19 (Spe-cial Publication 1): 129-134.

Ferrero, A. 2007. Rice scenario in the European Union.Cahiers d’études et de recherches francophones,Agriculture 16: 272-277.

Figuerola, J., R. Mateo, A. J. Green, J. Y. Mondain-Mon-val, H. Lefranc and G. Mentaberre. 2005. Grit selec-tion in waterfowl and how it determines exposure toingested lead shot in Mediterranean wetlands. Envi-ronmental Conservation 32: 226-234.

Finlayson, C., G. Hollis and T. J. Davis. 1992. ManagingMediterranean Wetlands and Their Birds. Interna-tional Waterfowl and Wetland Research Bureau,Slimbridge, UK.

RICE AND BIRDS AROUND THE MEDITERRANEAN 95

González-Solís, J., X. Bernadi and X. Ruiz. 1996. Season-al variation of waterbird prey in the Ebro Delta ricefields. Colonial Waterbirds 19: 135-142.

Hafner, H. and M. Fasola. 1997. Long-term monitoringand conservation of herons in France and Italy. Co-lonial Waterbirds 20: 298-305.

Hafner, H., V. Boy and G. Gory. 1982. Feeding methods,flock size and feeding success in the Little EgretEgretta garzetta and the Squacco Heron Ardeola ral-loides in Camargue, southern France. Ardea 70: 45-54.

Hafner, H., P. J. Dugan and V. Boy. 1986. Use of artificialand natural wetlands as feeding sites by Little Egrets(Egretta garzetta) in the Camargue, southern France.Colonial Waterbirds 9: 149-154.

Hafner, H., R. E. Bennetts and Y. Kayser. 2001. Changesin clutch size, brood size and numbers of nestingSquacco Herons Ardeola ralloides over a 32-year peri-od in the Camargue, southern France. Ibis 143: 11-16.

Ibáñez, C., A. Curcó, X. Riera, I. Ripoll and C. Sánchez.2010. Influence on birds of rice field managementpractices during the growing season: a review and anexperiment. Waterbirds 33 (Special Publication 1):167-180.

IUCN 2008. IUCN Red List of Threatened Species.www.iucnredlist.org, accessed 12 September 2008.

Kazantzidis, S. and V. Goutner. 1996. Foraging ecologyand conservation of feeding habitats of Little Egrets(Egretta garzetta) in the Axios River Delta, Mace-donia, Greece. Colonial Waterbirds 19: 115-121.

Kazantzidis, S., V. Goutner, M. Pyrovetsi and A. Sinis.1997. Comparative nest site selection and breedingsuccess in 2 sympatric Ardeids, Black-crownedNight-Heron (Nycticorax nycticorax) and Little Egret(Egretta garzetta) in the Aries Delta, Macedonia,Greece. Colonial Waterbirds 20: 505-517.

Kersten, M., R. H. Britton, P. J. Dugan and H. Hafner.1991. Flock feeding and food-intake in Little Egrets- the effects of prey distribution and behaviour. Jour-nal of Animal Ecology 60: 241-252.

Kuiper, D. P., E. Wymenga, J. Van Der Kamp and D.Tanger. 2006. Wintering areas and spring migrationof the Black-tailed Godwit. Bottlenecks and protec-tion along the migration route. A&W-rapport 820.Altenburg and Wymenga, ecologisch onderzoek,Veenwounden, Netherlands.

Lawler, S. P. and D. A. Dritz. 2005. Straw and winterflooding benefit mosquitoes and other insects in arice agroecosystem. Ecological Applications 15:2052-2059.

Llorente, G. A., X. Ruiz and J. Serra-Cobo. 1986. Autum-nal feeding of Red-crested Pochard Netta rufina inthe Ebro Delta Spain. Vie et Milieu 36: 97-108.

Lombardini, K., R. E. Bennetts and C. Tourenq. 2001.Foraging success and foraging habitat use by CattleEgrets and Little Egrets in the Camargue, France.Condor 103: 38-44.

Longoni, V., D. Rubolini and G. Bogliani. 2007. Delayedreproduction among Great Bitterns Botaurus stellarisbreeding in ricefields. Bird Study 54: 275-279.

Lourenço, P. and T. Piersma. 2008. Stopover ecology ofBlack-tailed Godwits Limosa limosa limosa in Portu-guese rice fields: a guide on where to feed in winter.Bird Study 55: 194-202.

Lourenço, P. M. and T. Piersma. 2009. Waterbird densi-ties in South European rice fields as a function ofrice management. Ibis 151: 196-199.

Macias, M., A. J. Green and M. I. Sanchez. 2004. The dietof the Glossy Ibis during the breeding season inDoñana, southwest Spain. Waterbirds 27: 234-239.

Mañosa, S., R. Mateo and R. Guitart. 2001. A review of theeffects of agricultural and industrial contaminationon the Ebro delta biota and wildlife. EnvironmentalMonitoring and Assessment 71: 187-205.

Mañosa i Rifé, S. 1997. A review of rice farming and water-bird conservation in the three western Mediterra-nean areas, the Camargue, the Ebro Delta and theNorth-western Po Plain. Station Biologique Tour deValat, Arles, France.

Martínez, C., X. Ruiz and L. Jover. 1992. Alimentacíon delos Pollos de Martinete (Nycticorax nycticorax) en elDelta del Ebro. Ardeola 39: 25-34.

Martínez-Vilalta, A. 1985. Wintering waders in the EbroDelta. Wader Study Group Bulletin 43: 25-28.

Mesléard, F. 1994. Agricultural abandonment in a wet-land area: abandoned ricefields in the Camargue,France - can they be of value for conservation? Envi-ronmental Conservation 21: 354-357.

Mesléard, F., P. Grillas and L. T. Ham. 1995. Restorationof seasonally-flooded marshes in abandoned rice-fields in the Camargue (southern France) - prelimi-nary results on vegetation and use by ducks.Ecological Engineering 5: 95-106.

Mesléard, F., S. Garnero, N. Beck and E. Rosecchi. 2005.Uselessness and indirect negative effects of an insecti-cide on rice field invertebrates. Comptes Rendus Bi-ologies 328: 955-962.

Miller, M. R. and G. D. Wylie. 1996. Preliminary estimateof rice present in strip-harvested fields in the Sacra-mento Valley, California. California Fish and Game82: 187-191.

Oro, D. 1995. The influence of commercial fisheries indaily activity of Audouin’s Gull Larus audouinii in theEbro Delta, NE Spain. Ornis Fennica 72: 154-158.

Oro, D., X. Genovart, X. Ruiz, J. Jiménez and J. Garcia-Gans. 1996. Differences in diet, population size andreproductive performance between two colonies ofAudouin’s Gull Larus audouinii affected by a trawlingmoratorium. Journal of Avian Biology 27: 245-251.

Pain, D. J. and J. Dixon. 1997. Why farming and birds inEurope? Pages 1-24 in Farming and Birds in Europe.The Common Agricultural Policy and Its Implica-tions for Bird Conservation (D. J. Pain and M. W. Pi-enkowski, Eds.). Academic Press, London, UK.

Papadopoulou-Mourkidou E., D. G. Karpouzas, J. Patsias,A. Kotopoulou, A. Milothridou, K. Kintzikoglou andP. Vlachou. 2004. The potential of pesticides to con-taminate the groundwater resources of the Axios riv-er basin. Part II. Monitoring study in the south part ofthe basin. Science of the Total Environment 321: 147-164.

Parejo, D. and J. M. Sánchez-Guzmán. 1999. Effects of ag-ricultural development on colonial ardeid popula-tions in southwestern Spain. Waterbirds 22: 302-306.

Parsons, K. C., P. Mineau and R. B. Renfrew. 2010. Effectsof pesticide use in rice fields on birds. Waterbirds 33(Special Publication 1): 193-218.

Pena A. 1985. Composição e dinâmica anual da avifaunado Paul do Trejoito (Benavente). Boletim da So-cidade Portuguesa de Ciências Naturais 22: 5-19.

Pierluissi, S. 2010. Breeding waterbirds in rice fields: aglobal review. Waterbirds 33 (Special Publication 1):123-132.

Prosper, J. and H. Hafner. 1996. Breeding aspects of thecolonial ardeidae in the Albufera de Valencia, Spain:

96 WATERBIRDS

population changes, phenology and reproductivesuccess of the three most abundant species. ColonialWaterbirds 19: 98-107.

Rendón, M. A., A. J. Green, E. Aguilera and P. Almaraz.2008. Status, distribution and long-term changes inthe waterbird community wintering in Doñana,south-west Spain. Biological Conservation 141: 1371-1388.

Richardson, A. J. and I. R. Taylor. 2003. Are rice fields insoutheastern Australia an adequate substitute for nat-ural wetlands as foraging areas for egrets? Waterbirds26: 353-363.

Ruiz, X., J. Petriz and L. Jover. 1992. PCB and DDT con-tamination of heron eggs in the Ebro Delta, Spain.IWRB Special Publication 20: 115-117.

Sánchez-Guzmán, J. M., R. Morán, J. A. Masero, C. Corba-cho, E. Costillo, A. Villegas and F. Santiago-Quesada.2007. Identifying new buffer areas for conservingwaterbirds in the Mediterranean basin: the impor-tance of the rice fields in Extremadura, Spain. Biodi-versity and Conservation 16: 3333-3344.

Souty-Grosset, C., D. Holdic, P. Noel, J. Reynolds and P.Haffner. 2006. Atlas of Crayfish in Europe. MusèumNational d’Histoire Naturelle, Paris, France.

Stafford, J. D., R. M. Kaminski and K. J. Reinecke. 2010.Avian foods, foraging, and habitat conservation inworld rice fields. Waterbirds 33 (Special Publication1): 133-150.

Tourenq, C., R. E. Bennetts, N. Sadoul, F. Mesleard, Y.Kayser and H. Hafner. 2000. Long-term populationand colony patterns of four species of tree-nesting

herons in the Camargue, South France. Waterbirds23: 236-245.

Tourenq, C., C. Barbraud, N. Sadoul, A. Sandoz, K. Lom-bardini, Y. Kayser and J.-L. Martin. 2001a. Does forag-ing habitat quality affect reproductive performancein the Little Egret, Egretta garzetta? Animal Biodiversityand Conservation 24: 107-116.

Tourenq, C., R. E. Bennets, H. Kowalski, E. Vialet, J.-L.Lucchesi, Y. Kayser and P. Isenmann. 2001b. Are rice-fields a good alternative to natural marshes for water-bird communities in the Camargue, southernFrance? Biological Conservation 100: 335-343.

Tourenq, C., S. Aulagnier, L. Durieux, S. Lek, F.Mesléard, A. Johnson and J.-L. Martin. 2001c. Identi-fying rice fields at risk from damage by the GreaterFlamingo. Journal of Applied Ecology 38: 170-179.

Tourenq, C., N. Sadoul, N. Beck, F. Mesléard and J.-L.Martin. 2003. Effects of cropping practices on the useof rice fields by waterbirds in the Camargue, France.Agriculture Ecosystems & Environment 95: 543-549.

Tourenq, C, S. Benhamou, N. Sadoul, A. Sandoz, F.Mesléard, J.-L. Martin and H. Hafner. 2004. Spatial re-lationships between tree-nesting heron colonies andrice fields in the Camargue, France. Auk 121: 192-202.

Tucker, G. M. and M. I. Evans. 1997. Habitats for Birds inEurope: A Conservation Strategy for the Wider Envi-ronment. BirdLife International, Cambridge, UK.

Weber, T. P., A. I. Houston and B. J. Ens. 1999. Conse-quences of habitat loss at migratory stopover sites: atheoretical investigation. Journal of Avian Biology 30:416-426.