Rubega& Robinson:Salinization and shorebirds

Water salinization and shorebirds:emerging issues

MargaretA. Rubegaand Julie A. Robinson

Rubega,M. A., & Robinson,J. A. 1996.Water salinization and shorebirds:Emerging issues. International Wader Studies 9: 45-54.

Salinityfrom agricultural drainwater, surface flow and subsurfaceflow is a problemin at leastsome inlandwetlands in everywestern state in the UnitedStates. Water salinization is a particularly insidiousthreat to waterbirdpopulations because wetland quality ma, y not visiblydecline until the problemis advanced.In thispaper we review1) evidencethat salinizationis an important managementproblem in inlandwetlands, 2) meansavailable to shorebirdsto copewith ,3) mechanismsby whichthe costsof salinizationare likely to reduceshorebird reproductive success, and 4) how salinizationmodifies structure and diversityof ecosystems.Finally, 5) we discuss emergingmanagement concerns with respectto reducingor eliminatingsalinization effects on shorebirdpopulations. MargaretA. Rubega,Department of Environmental and Resource Science/186, University of Nevada, Reno, 1000Valley Rd., Reno, NV 89512,USA JulieA. Robinson,Ecology, Evolution and Conservation Biology Program/186, University of Nevada, Reno, 1000Valley Rd., Reno, NV 89512,USA •Currentaddress: Department of Biology,University of Houston, Houston, TX 77204-5513,USA

Introduction seleniumand other heavy metals,concentrated throughsoil leachingand water recycling(Ohlendorf et al. 1986, 1989). Bioaccumulation of these toxicants The art and scienceof habitatmanagement revolves resultedin low hatchabilityof eggs,and dramatic around the control and enhancement of habitat malformations(Hoffman et al. 1988)and subsequent quality (cf.Reed 1995). A managementplan for death of thosechicks that did hatch (Ohlendorf et al. shorebirdsadvocates manipulating controllable 1989). In otherwords, although Kesterson received a habitatfactors in orderto providethe best habitat greatdeal of use,it was habitatof very low quality. quality possiblefor shorebirds(Helmers 1992). The Kesterson has since been filled with uncontaminated working definitionof habitatquality currently seems soilin orderto displacebreeding to wetlandsof to be "that which resultsin the greatestnumber of betterhabitat quality, and habitatmanagers are birds" (e.g.,Merendino et al. 1992),or, more rare135 monitoringpotential bioaccumulation through the "that which resultsin the greatestdiversity of new terrestrialfood chain (Wu et al. 1995). species"(e.g.,Boshoff & Piper1992). Although these There is an equally dangerous,potentially much may be meaningfulmanagement goals on shorttime morewidespread, mechanism of wetland water scales,for conservationpurposes only thoseaspects qualityreduction: water salinization.Water of habitatquality thathelp maintaindiverse salinizationis a particularlyinsidious threat to populationsover largetime scalesare of significance waterbirdpopulations because wetland quality may (Karr 1993;Suter 1993;Noss & Murphy 1995). not visiblydecline until the problemis advanced. Numbersof birdspresent, or evenbreeding, in a Salinizationmay resultin reducedreproduction wetland on shorttime scalesare notnecessarily throughchick mortality, while reducedvigor indicesof the contributionof habitatquality to the ci•k...... ;•,•.•lCittru ...;,t.vv lUt dehydrationmay increasemortality maintenanceof populations.For instance, because at all life stages.In this paper we review 1) evidence so muchwetland habitathas been destroyed (Frayer that salinizationis an important management et al. 1989;Dahl 1990),shorebirds may breedin large problemin inland wetlands,2) meansavailable to numbersin wetlandsof very poor quality. One very shorebirdsto copewith salinity,3) mechanismsby dramaticexample of thisphenomenon was which the costsof salinizationare likely to reduce KestersonNational Wildlife Refuge,in the San shorebirdreproductive success, and 4) how JoaquinValley of California.Kesterson was a salinizationmodifies structure and diversityof wetland suppliedwith irrigationdrainwater from ecosystems.Finally, 5) we discusspossible the WestlandsWater District. Largenumbers of managementtechniques for reducingor eliminating wading birdsbred at Kesterson,and the projectwas salinizationeffects on shorebirdpopulations. This viewed initially as a habitat-replacementsuccess. paperis notpresented as a definitivediscussion of Nonetheless,these birds failed to reproduce the cure for wetland water salinization. Our goals, successfully(Williams et al. 1989)because drainwater rather,are to identifythe problem,and generate supplyingthe wetlandwas contaminatedwith interestin the processof definingsolutions.

45 International Wader Studies 9:45-54

Why is salinization a problem in and virtually all of the Middle East(Waisel 1972; inland wetlands? Figure1). In North America,salinity from agriculturaldrainwater, surface flow and subsurface flow is a problemin at leastsome inland wetlandsin Normally, the term salinityis taken to mean the every westernstate in the U.S. (U.S. Fish and Wildlife concentration of . However, the ion Service1992) (Figure 2). Salinizationis particularly compositionof salty water varieswidely, and in acutein the GreatBasin, and in partsof California, inland wetlands(the focusof thispaper) salinity is Arizona,New Mexicoand Texas, where growing actuallya measureof the total concentrationof a humanpopulations and agriculturecompete for number of different ions. The exact combination of limited water, and where most wetlands are ionsand mineralsin water dependslargely on local downstreamfrom urban and agriculturalusers (E1- soilcomposition and hydrologyof surfaceand Ashry& Gibbons1988). Increasingly,solutions to groundwater. theseconflicts involve multiple use and reuseof In arid lands, where salinization is most common, water,resulting in increasedsalinity of water at soilsnaturally containvariable amountsof sodium, agriculturalsites, and subsequently, at terminal potassium,and other mineral salts,but also wetlands.Salinization is alreadya problemat many magnesium,carbonate, bicarbonate, sulfate, boron, of the world'smost important shorebird sites. Sites fluoride, arsenic, and selenium. Hence, in arid lands, declaredof hemisphericor internationalimportance wetlandsand otherbodies of water arefrequently to shorebirdsby the WesternHemisphere Shorebird naturallysalty (and significantlyalkaline) as a Reserve Network in the Great Basin include Mono functionof the processesof runoffand evaporation Lake, Great and Stillwater/Carson Lake over geologictime. For instance,Mono Lake in (WHSRN 1992) andall havesuffered significant California and the in Utah (two degreesof salinization(Patten et al. 1987;Woolf 1993; significantsites for shorebirds;Oring & Reed,this Lico 1992). (Unfortunately,although reserve volume) are both natural saline lakes. For the designationby theWestern Hemisphere Shorebird purposesof this discussion,we will usethe term ReserveNetwork (WHSRN) draws much-needed salinizationto meananthropogenically-caused increases in attentionto sitesof importanceto shorebirds,it watersalinity (defined very broadly as increases in providesno concretemeans of protection, conductivityofa particularwetland or bodyof water, particularlyagainst the gradual degradationof water withoutrestriction to any particular ion composition) on quality.) relativelyshort time scales, even in caseswhere some In the arid Americanwest, many factorstend to degreeof salinity was present naturally. In considering increasethe salinityof inlandwetlands. Increased largerspatial scales, we alsowill usethe term to urban use of riverine waters decreases the amount imply the decreasein relativeavailability of fresh and qualityof water availablefor terminalwetlands. water in a landscape. Effectsof suchdecreases are twofold: 1) some Globally,salinization is commoneverywhere wetlandsdry up, reducingfreshwater and the total agricultureis conductedon arid lands,e.g. north numberof wetlandsavailable in the landscape,and Africa, southern and western Asia, central Australia, 2) remainingwetlands become more shallow and

Figure1. Globaldistribution of salt-affectedsoils (and hence water), and areas with thepotential for waterand soilsalinity problems(adapted from American Society of Civil Engineers1990).

46 Rubega& Robinson:Sahnlzation and shorebirds

Potentialfor salinizationproblems • High • Medium • Low

Figure2. Areasin the conterminousUnited States with the potentialfor waterand soilsalinity problems (adapted from AmericanSociety of Civil Engineers1990; note that coverage for NorthAmerica differs from Figure 1 becauseof differingdefinitions of risk). moresaline through evaporative concentration. For Ettinger1964). City sewagereuse can lead to example,water diversionsof easternSierra Nevada groundwatersalinization (Bagley 1967). snowmelt by the city of LosAngeles have, over the Agriculturalmultiple-use, and enforcementof last century,caused Owens Lake to disappear irrigationconservation programs, also decreases the completely,and Mono Laketo dropmore than 40 qualityof water in inlandwetlands. Federal verticalfeet while triplingin salinity(Patten et al. 1987). Bothof thesenaturally-occurring saline lakes legislationdesigned to end water disputesover the NewlandsIrrigation Project of westernNevada and wereformerly ringed with freshwaterwetlands, northeasternCalifornia (Public Law 101-618,1990), which no longerexist at Owens,and are reduced enoughat Mono to havevirtually eliminatedthe reallocatedwater away from the projectto protect hundreds of thousands of ducks once found there endangeredfish at PyramidLake. Legislationalso (Stateof California 1994a). mandatedmore efficientwater useby the irrigation district. However,spillage reduction associated with Public desire for recreational water in an arid more efficientirrigation operations would double landscapeencourages freshwater impoundments, concentrationsof saltsand heavymetals in surface preventingfreshwater inflow into alreadysaline and subsurfaceflows reachingStillwater National wetlands. For example,a controversialproposal to WildlifeRefuge and nearby shallow wetlands (U.S. separateFarmington Bay from the GreatSalt would Dept. Interior 1988). eliminatefreshwater flows into that part of the lake, replacingmesosaline emergent wetlands with a Much attentionhas rightly beenpaid to the the freshwaterreservoir designed to provide drinking dramaticeffects of heavy metal bioaccumulationon water as well as recreational income for Salt Lake wetlandbirds (e.g.,Hothem & Ohlendorf1989; City suburbs(Woolf 1993). If thisplan were Scheuhammer1991; Skorupa & Ohlendorf1991); implemented,200 km 2 of emergentwetland would muchless has been directed at the consequencesof be lostunder the reservoiritself, while hypersaline salt concentration on these . Salinization is lake waters would become even more saline because more likely to be ubiquitous,and is liable to be a of reducedfreshwater input. Diversionsof this kind problemeverywhere toxicants are accumulatedby are likely to exacerbateconcentration of ionsby leachingand runoff. In contrast,there is a huge evaporation.As the shrinks,the literatureon salinizationeffects on plants,extending surface-to-volumeratio increases,accelerating the to worldwide effortsto producesalt-tolerant hybrids rate of evaporation.In mostcases, surface-to-volume for agriculture.In someparts of the world, these ratiosare alreadyhigh becauseof the initial effortsare directedat making salt water irrigation shallowness of most inland wetlands. Also, urban possible(National Research Council 1990). The water reuse,such as the useof "grey"water for eventual effect of such activities on terminal wateringlawns and decorativeplantings, can wetlandsin arid landsand their populations increasesalinity by 325mg/1/cycle (Bunch& would be extreme.

47 Internatwnal Wader Studies 9 45-54

Table 1. Mean relativesalt gland masses for shorebirds.

Species Massof Classification¾ Source bothglands Conditionsat (in g/g timeof sampling bodymass)

GreenSandpiper 0.01 Freshwater Staaland1967 Tringaochropus Wood Sandpiper 0.02 Freshwater Staaland1967 T. glareola CommonSnipe 0.02 Freshwater Staaland1967 Gallinagogallinago Great Golden Plover 0.03 Freshwater Staaland 1967 Pluvialisapricaria Bar-tailedGodwit 0.05 Marine,except Staaland1967 Limosalapponica duringbreeding Dunlin 0.08 Marine,except Staaland1967 Calidrisalpina duringbreeding Little Stint 0.08 Marine, except Staaland1967 C. minuta duringbreeding Sanderling 0.11 Marine,except Staaland1967 C. alba duringbreeding Red Knot 0.12 Marine,except Staaland1967 C. canutus duringbreeding 0.15 Wild caught Piersma1994 (estimatedfrom graph) coastally 0.05 Captive, freshwater Piersma1994 (estimatedfrom graph) acclimated Common Sandpiper 0.06 Adults- freshwater Staaland1967 Actitishypoleucos and marine 0.08 Chicks-caught at Staaland1967 freshwater RingedPlover 0.07 Freshwaterand marine Staaland1967 Charadrius hiaticula AmericanAvocet 0.04 Collectedat Mahoney& Jeh11985 Recurvirostraamericana hypersalinelakes Wilson'sPhalarope 0.04 Collectedat Mahoney& Jeh11985 Phalaropustricolor hypersalinelakes •Classificationsare those used by Staaland(1967). For all othersources, conditions under which the samples were collected are given.

How does salinity affect shorebird 1960; Schmidt-Nielsen et al. 1957; Schmidt-Nielsen & populations? Fange1958; Schmidt-Nielsen & Sladen1958; Schmidt-Nielsen& Kim 1964)were first to correctly assessthe salt-excreting function of thegland. Direct effects- osmoregulationand maintenance of The aviansalt gland functions in osmoregulationby respondingto increasesin plasmaosmolality and Birds, like other vertebrates, filter solutes, such as volume.Excretion by thegland is controlledthrough salts,out of their bloodstreamby meansof kidneys. thecentral nervous system, with osmolalityand Although the formationof uric acid is lesswater- pressurereceptors in the heart and elsewhere.When consumptivethan the formationof urea,avian glandsare active they secrete a fluid containingNaC1 kidneysare lesseffective at concentratingsolutes that is hyperosmoticto plasma. This secretion than are mammalian kidneys (Schmidt-Nielsen1970; is directed via ducts to the nasal cavities; fluid Skadhauge1981). When drinkingsalty water, birds emergesfrom thenares where it drips,or is forcibly cannotmaintain water balancethrough renal shaken,off thebeak (seeHolmes & Phillips1985 for excretionalone (Willoughby & Peaker1979). review of the secretionprocess). The mechanismby Becausecellular metabolism depends on sufficient whichsalt is concentratedin saltgland secretions has quantitiesof water, and nerve and musclefunction beenmuch studied (see Skadhauge 1981; Holmes & on ion ratioswith narrow marginsof variability, Phillips1985 for reviews). In brief, it involvesactive dehydrationaffects every system in thebody. transportof Na+ and C1-ions across cell membranes, Extremedehydration can lead rapidly to death. and is thus an energy-consumptiveprocess. In the struggleto maintainwater balance,birds have Saltgland function in birdsis tightlycorrelated with in their arsenalpaired supraorbital,or nasal,salt salinehabitats and salty diets. Saltglands are large glands.It hasbeen recognized since 1667 (Comelin; andfully functionalin birdsusing marine habitats seeTechnau 1936 as cited in Cooch1964) that the (especiallythose eating invertebrates that are isotonic enlargementof theseglands was associatedwith with surroundingseawater) while thegland is small saline habitats (Heinroth & Heinroth, 1926-1928; and dormant in most terrestrial and freshwater birds Schildmacher,1932; both as cited in Cooch1964). (summarizedin Holmeset al. 1961).In manyspecies, Schmidt-Nielsonand colleagues(Schmidt-Nielsen activityand developmentof the glandcan be

48 Rubega& Robinson:Sahnization and shorebirds stimulatedby continuousexposure to salinewater prey that arehypotonic to hypersalinelake water, (Table 1 summarizes all available shorebird data). theseprey are still (relativeto freshwater)salty (about 50% ). This is liable to be more of a Althoughwe know that marinebirds possess salt problemin hypersalinesystems than in thosethat are glandscompetent to maintainwater balance, the lesssalinized. Indeed, although Mahoney & Jehl pictureis lessclear for shorebirdsand otherwading (1985)found no differencesin saltgland sizes among birds,especially for thosebreeding at or migrating birdsat differentlakes, mean relative salt gland size throughinland wetlands. First,we have less was 0.04,equivalent to the low end of Staaland's informationabout and saltgland (1967)data for strictlymarine birds. In addition, functionin shorebirdsthan in otherspecies. Of the theirdata show that both avocetsand phalaropesare 155 citationsin Holmes& Phillips' (1985)review, maintainingblood serum osmolalities up to 200 only one (Staaland1968) refers to shorebirds. mOsm/kgbelow those of theirprey at MonoLake. Second, the data that exist for shorebirds are Boththese species and othershorebirds [Red-necked equivocalwith respectto whethersalt glands in Phalaropes(Phalaropus lobatus), Western Sandpipers shorebirds,if stimulated,allow acclimationto salty (Calidrismauri), Least Sandpipers (C. minutilla)]at habitats.Few publishedstudies examine salt gland Mono Laketravel regularly to freshwater sources function in shorebirds. Staaland(1967, 1968) aroundthe lakeshore and inland, where they can be examined14 Europeanshorebird species and seenvigorously bathing and drinking. The concludedon the basisof small gland size and importanceof accessto freshwaterat Mono Lake is experimentalsalt-loading that severalspecies (Green attestedto by the hugeflocks (up to 20,000birds at a Sandpiper,Common Snipe, and WoodSandpiper) time)visiting Rush Creek, a majorfreshwater inflow are poorly adaptedto excreteexcess salt (Staaland on the southshore of the lake,bathing, drinking, and 1968). However, theseexperiments were conducted departingagain, all within the spaceof 2 hours(M. with freshlycaught birds, and sooffer no Rubega,pers. obs.). Furthermore,the lakesat which informationabout the possibleability of the species Mahoneyand Jehl collected data ranged from studiedto acclimateover time throughsalt gland oligosalineLake Abert [saltyenough to containbrine enlargement.Piersma (1994) found that captiveRed Knots that were acclimated to fleshwater had much shrimp(Artemia monica) and flies (Ephydra hians),along with other,less salt-tolerant prey)] to reducedrelative (mass-specific)salt glandssizes hypersalineGreat Salt Lake (saltyenough to contain comparedto wild-caughtRed Knots,indicating nothingbut brine shrimpand brine flies),but did not atrophyof the glandswhen saltstress was removed. includea fleshwaterlake. Theymay have found no It is possiblethat a few speciesof shorebirdsmay differencesin saltgland size among lakes because have no saltglands at all: Maclean(1977) reported theywere lookingat enlargedglands at all lakes. that he was unableto locatesalt glands in a single specimenof Red-kneedDotterel (Charadrius cinctus). Indirect effects - costs of behavioral avoidance Other investigatorsdid not examinesalt glands of salt loading directly,but examinedthe abilityof shorebirdsto acclimateto saltydrinking water in captivity. The mostobvious way for shorebirdsto avoid salty Purdue& Haines(1977) found that Snowy Plovers wetlandsis to makeuse of sitesthat are relatively (Charadrius alexandrinus), Killdeer ( C. vociferus),and flesh. However, if Great Basin wetlands suffer SemipalmatedSandpipers (Calidris pusilla) had salinizationon largespatial scales, such freshwater limited abilities to acclimate. Tolerance of acclimated sites will become fewer and farther between, and SnowyPlovers and SemipalmatedSandpipers increasinginvestments in time and energytraveling extendedto 0.3 M (50% water). Theysuggested betweenwetlands will be requiredin orderto locate that SnowyPlovers maintain water balance on their them. Forbreeding shorebirds, such searches may saltplain breeding grounds by not consumingsalt alsorepresent a furthercost in reductionof time and water, eatinginsects with high freshwatercontents, energyavailable for breeding. Furthermore,as and throughwater-conserving thermoregulatory fleshwater wetlands become more scarce,some birds behaviors,such as standing in poolsduring hot will haveno choicebut to settle,for somelength of weather.Klassen & Ens(1990) showed that captive time, in salinized ones. freshwater-acclimatedRed Knots were capable of As we havealready noted, saline systems are often acclimatingback to seawater. highly productive. The importanceof that Mahoney& Jehl(1985) examined stomach content observationfor shorebirdsis attestedto by the fact andblood plasma osmolality, as well assalt glands that large(but not very diverse)populations of and suggestedthat Wilson'sPhalaropes and breedingand migratory shorebirds are alreadyfound AmericanAvocets avoided swallowing salt water by at the mostsaline lakes in the GreatBasin (e.g., Neel strainingtheir prey. Thisraised the possibility that & Henry, this volume). However, in all thesecases the needfor saltgland competence (and hence freshwaterinflows are availablenearby, and shorebirds are known to use them. Use of freshwater freshwaterin managedwetlands) might be obviated in somespecies by behavioraland mechanicalmeans in thesecases is not exclusivelyfor drinking; of salt avoidance. However, shorebirds able to avoid shorebirdsvisiting fleshwater sources at Mono Lake swallowingsalt water would still eventuallyneed to bathevigorously (M. Rubega,pers. obs.). Because obtainwater with low osmolality,either from preyor the waterproofingof waterbirdfeathers depends on the interaction of feather structure with surface elsewhere,to balancewater lost evaporatively or throughexcretion of nitrogenouswastes. tensionin water (Rijke1970), and surfacetension decreaseswith increasingsolutes (Streeter & Wylie Althoughavocets at MonoLake [one of Mahoney& 1979), probablyincreases feather Jehl's(1985) study sites] are consuming invertebrate wetting. Wet plumagecan increase

49 International Wader Studies 9:45-54

thermoregulatorycosts significantly. [Although significant.Neither research group investigated the summerdaytime temperatures in the GreatBasin are mechanismsthrough which saltloading impaired high, considerthe factthat nighttimetemperatures growth in the treatmentsin which mortalitywas not may fall by morethan 30ø F (17.2ø C), wind is complete.It seemsapparent, however, that salt frequent,and birds are defendingrelatively high core glandsin ducksare not sufficiently competent in the temperatures.]Alternatively, feather wetting may youngestage classes to maintainwater balance. leadto theneed to preenmore frequently, for longer Furthermore,sublethal growth affects which might periodsof time,reducing time and energyavailable influencesurvival to fledgingand beyondare a for other activities,such as foraging. significantconcern. Bildsteinand his colleagues(Johnston & Bildstein How will salinization affect shorebird 1990;DeSanto 1992;Bildstein 1993) showed that nestlingWhite Ibises(Eudocimus albus) fail to gain reproduction? massand becamedehydrated on high-saltdiets, eventhough they exhibited hypertrophy of salt In light of the increasingthreat of salinizationof glands,and eventhough adults tolerate high-salt inland wetlands,the relativepaucity of direct diets. Presentlywe lackequivilant information on informationabout the ability of shorebirdsto juvenilesof any speciesof shorebird. maintainwater balanceis troubling. From the point of view of thosemanaging wetlands for breeding shorebirds, the absolute absence of information on How does salinization affect the abilitiesof hatchlingshorebirds to do so is a ecosystems? genuinethreat to shorebirdpopulations. In general, birds are mostvulnerable during the chicklife stage Dependingon how saltythey are,inland saline (Lack 1954;Wunderle 1991). Chicksare small in size, wetlandsmay supportfew or no fish,thus the havehigh metabolicrates (and hencehigher water predominantvertebrates are aquaticbirds. Thoseare turnoverrates than adults,as well as a greater generallyinvertebrate specialists, or generalists percentageof body massas water) and are capableof subsistingon invertebrates.In general, undergoingrapid physicaland associatedbehavioral increasingsalinity is associatedwith decreasing development.Even precocial species are relatively speciesrichness at all trophiclevels, although the immobilein comparisonto adults,which can readily strengthof thiseffect appears to vary with thescale fly periodicallyto freshwatersites, or deserta of measurement(Williams et al. 1990). At Mono salinizedwetland altogether.Reductions of surface Lake,only two speciesof invertebratesare available tensionin salinewater may causefeather wetting (M. asprey, but thoseare extremelyabundant. This Rubega,pers. obs.). Theresulting heat loss may be a effectis thoughtto be due to the heightened particularlyserious problem for the youngestage productivityof salinewaters, and the exclusionof classesof chicksbecause most species are not fully salt-intolerantcompetitors (Patten et al. 1987). endothermicat hatch (Cramp & Simmons1982). Loweredavian diversity at hypersalinizedsystems, Also, althoughadults may be able to straintheir prey suchas Mono Lake,probably results from exclusion from saltwater and thus reduceintake of saltywater, of speciesfor whichheavy salt loads present an chicksmay lack the bill structuresnecessary to do so intractablewater balance problem (e.g., ducks; see until latein development.It is importantto notethat State of California 1994a). Also, those invertebrates adult shorebirds are not infallible in their choice of remainingin a salinizedwetland are likely to be breedinghabitat. The high mortalityand morbidity (Kirschner 1979), and, therefore,to ratesof offspringat KestersonNWR (which,in have relativelyhigh saltcontents (e.g., Phillips et al. additionto high concentrationsof selenium,contains 1978),exacerbating the needfor freshwateramong highly salinizedwater) attestto this fact. shorebirdsfeeding in salinesystems. At Mono Lake, The few previousstudies of salttolerance in other the knownbreeding shorebird population consists of groupsof hatchlingwaterbirds indicate that salinity only fourspecies (Snowy Plover, Killdeer, American is likely to be a seriousproblem for hatchlings.In a Avocet,and Common Snipe ) (Winkleret al. 1977),all surveyof 39 speciesof Australianwaterbirds, of whomare found near freshwater seeps and Goodsell (1990) showed that 90% of all brood use of springs,with only anothertwo species(Red-necked 67 wetlands was in waters with in the fresh and Wilson'sphalaropes) maintaining significant to brackishrange. Ducklingsof severalspecies that migratorypopulations (Patten et al. 1987). All these breedin freshor brackishwater failed to gain weight speciesare eithermarine or coastalin distribution normallywhen exposedto saltwaterrearing regimes, duringpart of theiryear, or haveknown historical and mortalitywas high in ducklingsless than three associationswith inlandsaline systems. We can daysold (Elliset al. 1963;Swanson et al. 1984;Barnes reasonablyexpect similar patterns of species & Nudds 1991). Ellis et al. (1963) concludedthat persistenceamong breeding Great Basin shorebirds ducklingsalt glandsdo not becomefunctional until 6 at salinized wetlands as salinization worsens. daysof age,but thisobservation is temperedby the Salinizationaffects invertebrates, and •ence factthat theirexperiments were initiated with 4 day shorebirds,in lessobvious ways aswell. Salinization old ducklings.Swanson et al. (1984)and Barnes& leadsto the eliminationof salt-intolerantemergent Nudds (1991)presented more complete experiments vegetationthat would provide habitat for some conductedwith groupsof ducklingsof sevenspecies invertebrates(Wolheim & Lovvorn,1995), altering exposedfrom hatchor 48 hoursof age,respectively, the invertebratecommunity, as well as reducing to four saltwaterregimes. In both cases,interspecific invertebratevariety overall. This reductionin prey variability in growth reductionand mortalitywere speciesrichness has serious implications other than

50 Rubega& Robinson:Sahnlzatlon and shorebirds the exclusionof shorebirdsthat are specialistson one 1992)?Does one measuresalinity once a year,or preytype or another.For growing chicks, lack of repeatedly?How manywetlands represent the area prey choicesmay impairgrowth and development of concernfor the shorebirdpopulation of interest? throughthe absenceof importanttrace nutrients. What strategiesare advisablewhen managersonly controla smallpart of the areaof interest?For what Althoughsalt-tolerant prey may become salinityranges should we managewetlands? spectacularlyabundant in hypersalinesystems, abundancealone is not a measureof diet quality. For We do not have the answersto thesequestions. example,Rubega & Inouye(1994) showed that adult Where little informationabout salinity heterogeneity Red-neckedPhalaropes at Mono Lakeare incapable exists,effective long-term monitoring likely will of survivingon a diet consistingonly of brine dependon intensiveinitial samplingto determine shrimp,the more salttolerant of the two prey species where and how often to monitor. In an ideal world, presentthere (Herbst 1981; Dana & Lenz1986). For managerswould eliminatesources of salinization,or Red-neckedPhalaropes, the entireprey base at Mono Lake consistsof a singleinvertebrate species, the Table 2. Classificationof typesof water (wetlands)with brine fly, and that fly would eventuallyhave been respectto salinity.Modified from Cowardin et al. (1979). eliminatedby salinityincreases had diversionsfrom the Mono Basinnot recentlybeen curtailed (State of Conductivity(S/cm) Classification California1994b). Thus,salinity-induced reductions in preyspecies richness, per se, may not necessarily > 60,000 Hypersaline 45,000 - 60,000 Eusaline threatenshorebird populations, but the qualityand 30,000- 45,000 Polysaline compositionof theprey base after salinization will 8,000 - 30,000 Mesosaline likely limit compositionof shorebirdcommunities. 800 - 8,000 Oligosaline Thiswill be particularlytrue when prey qualityis < 800 Fresh low, and the costsof avoidingsalt-loading (or seekingout freshwaterto balanceit) arehigh. dilute salinizedwater with largevolumes of . In mostreal cases,the feasiblemanagement approachfor shorebirdslikely will dependlargely on Managementof salinized wetlands the timed provisionof limited freshwaterinflows to selected salinized wetlands. No data exist that Waterand wildlife managerslack the information would help us to predicta criticalsalinity level (e.g., necessaryto bestuse available saline and freshwater the level at which individual fitnessis reduced) even to its greatestbenefit to wildlife. For example,Public for a singlespecies, even if fine-scalesalinity control Law 101-618mandates purchases of water rightsto were possible.Indeed Hurlbert (1991)pointed out maintain wildlife habitat at Stillwater NWR (seeNeel that the shapeof the curvedefining the functional & Henry,this volume), but theU.S. Fish & Wildlife relationshipbetween salinity and the healthof Servicelacks information necessary to determinethe populationsis a moreimportant and realistic appropriatetemporal and spatialscale on which to managementtool. Susceptibilityto salinitymay vary make freshwaterinfusions (and hencepurchases) in widely amongspecies, although current evidence order to make the wetland useful to wildlife (U.S. suggestsvariation among hatchlings may be low. Fish and Wildlife Service1992). Until recently, Settingtarget salinities depends not only on a better virtually all surfaceand subsurfacewater reaching biologicalunderstanding of how effectsaccrue in StillwaterNational Wildlife Refugehad alreadybeen particularspecies, but alsoupon policy decisions usedfor irrigation,and that water commonly aboutacceptable effects on speciesrichness and at exceededFederal "beneficial use" criteria for salinity (Lico 1992), as well as other toxicants. the populationlevel. As a matterof maintaining populationsof breedingshorebirds over long time Little is known abouthow to appropriatelymanage scales,we believethat managementof wetland salinewetlands for shorebirds.As a consequence salinizationand freshwaterinflows depends on wetland managers,whether they realizeit or not, are measuring,and reducing,costs to chicks. This conductingexperiments (Elphick, this volume). conjectureis supportedby the factthat productionof Theseexperiments, if carefullyplanned, can provide Avocet(Recurvirostra avocetta) chicks improved (and valuable information about how to make best use of has beenmaintained) in constructedlagoons at limited freshwater. Toward this end, we discuss HavergateIsland, in England,following sluicing below how to measuresalinity, characterize what with fresherwater (Hill 1989)to reducesalinity. constitutes"acceptable" levels of salinity,and discuss Unfortunately,this techniquerequires the movement issuesof temporaland spatialscale in the relevant of largevolumes of water througha wetland system, measures(Robinson & Warnock,this volume) and is not availableto managersoverseeing terminal wetlands where fresh water is limited. Developing targetsalinities Temporal and spatial scalesof interest Measuringwetland salinity is relativelysimple (see Table2), althoughdetermining the temporaland The amountof freshwater needed,and the temporal spatialscale on which to do somay not be and spatialscales at which it will needto be applied straightforward.Does one measure salinity in a is currentlyunknown. As we have alreadypointed singlelocation in eachwetland of interestin orderto out, chicksare liableto suffergreater effects of generatea salinityindex, or in multiplelocations in wetlandwater salinitythan are adults, and to be order to characterizethe degreeof salinity more limited in their ability to maintainwater heterogeneity(e.g., net-function interpolation, Wu balance in a saline environment. Movements

51 Internatzonal Wader Stu&es 9:45-54

between, or within, wetlands to locate and use markedbirds, and effort directed at establishing freshwaterfor drinkingand bathingwill be more baselinetime-budgets. Finally, measures of salt difficult for chicksthan for adults, and may be glandsize and activityfrom individualsmay provide energeticallymore costly. If energeticcosts of goodindices to salinization,especially in conjunction movementare high, growth may be impaired,with with growthrate data. Measuresof saltgland size subsequenteffects on timeto fledging,and hence requiresacrifice of representativeindividuals from pre- andpost-fledging survival. Also, the the populationof interest,as thereis presentlyno distributionof preyas a functionof salinitymay way to estimatesalt gland sizein a living bird. influencethe needto movewithin and among Again,this may not be acceptablefor threatenedor wetlands,and hencethe growthand survivalof endangeredspecies. Until moredata are available chicks.Finally, movements over long distances are for shorebirds,Staaland's (1967, 1968) data are the liable to increaselosses to predators. standardfor comparisonto determinewhat constitutesenlarged (i.e., salt affected) salt glands. In Therefore,on largespatial scales, maintaining live animals,frequent head shakingaccompanied by relativelysmall freshwater inflows close together in fluid spraysor "a runnynose" (dripping bill) are also multiplesalinized wetlands (or in largewetlands) positiveindicators of secretingsalt glands. may amelioratepopulation effects of saltstress more effectivelythan one high-volume, isolated freshwater At thepopulation level, monitoring chick mortality inflow in a singlewetland. The inversemay be true and movementin the landscapein relationto salinity if a singlewetland can provide, e.g., enough suitable will beparticulary important. Comparing nestingsites for the wholepopulation. Because reproductionat salinizedvs. non-salinizedwetlands adults are more mobile and less vulnerable than is criticalfor settingtarget salinities. Ideally, field chicks,wetlands sufficiently fresh to allow good observationsof growthrates, pre-fledging mortality, chickgrowth and survivalalso should provide and time-to-fledgingcan be combinedto infer direct acceptableadult habitat. If costsof salinization and indirecteffects of salinizationon reproduction. accumulateprimarily through direct osmoregulatory Unfortunately,collecting these data is labor- routes(i.e., dehydration), then the needfor intensive,and interpretationcan be complicatedby freshwaterinflows may be eliminatedor reduced sitedifferences unrelated to salinity(e.g., disturbance, post-fledging,when chicks become more mobile and predation,or otherfeatures of water quality). (presumably)have functioning salt glands. Othermethods of populationmonitoring might be usedas suitable surrogates for detailedobservations Biomonitoringof avian populationsin inland of reproductivesuccess. Measuring use of saline wetlands freshwatersources in a salinizedlandscape, for instance,can be accomplishedby simplecensuses. Toprovide data for management,salinity and Whencombined with salinitymonitoring, and an biologicalmonitoring must be coupled.As we have appropriatesampling design (Elphick, this volume), pointedout, simplycounting numbers of birds counts of birds at fresh and salinized wetlands can presentis not sufficient.Until we havemore information about the effects of salinization on provean informativemonitoring technique. This sortof monitoringis likely to be importantfor shorebirdpopulations, biomonitoring is necessaryto understandinglandscape-level effects of salinization, assessthe successof managementtreatments. Over and henceunderstanding how to managea single time,naturally, our goalsshould be to identify wetland,or a groupof wetlands,in relationto the biomonitoringschemes that are simple, non-labor spatialarrangement of freshwaterwetlands. intensive,and cost-effective.Initially, intensive monitoringwill haveto be doneon individuals, The informationvalue of countsin a sampling populations(reproductive and migratory), and designcan be verifiedwith intensiveshort-term ecosystems. studiesof marked individuals. Data on the timing and extentof movementsof shorebirds(and their At the individual level, it is essential to monitor the broods)among fresh and salinized wetlands would growth,behavior and physiological responses of revealhow individual-,population-, and landscape- chicksbeing raised in salinizedwetlands. Growth. level factors interact in salinized environments. This ratesprovide us with a precise,objective measure of sublethal effectsof salinization, and relate (as informationcould then be usedto revisesampling schemesfor improvedmonitoring efficiency. discussedabove) to time-to-fledging,and pre- and post-fledgingsurvival. However,translation of At theecosystem level, it hasbeen shown by other growthrate da•a into salinity standards requires authors(in muchgreater detail than is possiblehere, controldata, i.e., comparable data from chicksraised e.g.,Patten et al. 1982; Aladin & Potts1992) that in non-salinizedwetlands. Unfortunately, salinizationalters ecosystems by altering acquisitionof growthrate data is labor-intensive,and invertebratecommunities (Williams et al. 1990;U.S. involvesdisturbance at a level that may not be Fish & Wildlife Service 1992; Wolheim & Lovvorn acceptableif dealingwith endangeredor threatened 1995).Salinization affects species composition and species.For thesereasons, monitoring of behavior populationdensities (e.g., Dana & Len•z1986) may prove a more feasiblelong-term means of throughdirect physiological effects (e.g. Herbst monitoring. With enoughbaseline information, 1981),effects on plant communities(Waisel 1972; shiftsin behavior(e.g., shift in time spentpreening at Aladin & Potts 1992),and hencehabitat structure theexpense of other'behaviors, marked increases or (Wolheim& Lovvorn1995). Periodicsampling of decreasesin drinkingbehaviors, etc.) may havegreat invertebrateand plant communitiesto monitorthe value ashands-off indicators of salinityeffects on presenceof salt-tolerantinsects and/or halophytic chicks. This method (at leastinitially) requires plants,especially when coupled with avianspecies

52 Rubega& Robinson:Sahmzatlon and shorebirds richnessestimates, could provide an index of Cooch,F. G. 1964.A preliminarystudy of the survivalvalue salinizationuseful to managers. of a functionalsalt gland in prairieAnatidae. Auk 81: 380-393. Cowardin, L. M., Carter, V., Golet, F. C., & LaRoe, E. T. 1979. Conclusion Classificationofwetlands and deepwater habitats of the United States. U.S. Fish and Wildlife Service, Office of BiologicalServices, Washington, D.C. Detailedmanagement recommendations will not be Cramp,S. & Simmons,K. E. L. (eds).1982. The birds of the possibleuntil moredata are availableabout the costs westernPalearctic, Vol. III. OxfordUniversity Press, to shorebirdsof living in salineenvironments. Oxford. Nonetheless,we believeit is clearthat widespread Dahl, T. E. 1990. Wetlands: Losses in the United States 1780's to 1980's. U.S. Fish and Wildlife Service, salinizationof inland wetlandswill have negative Washington,D.C. effects.Wetland managers can bestprotect shorebirds Dana,G. L., & Lenz,P. H. 1986.Effects of increasingsalinity by beingaware of the problem,recognizing that on an Artemiapopulation from Mono Lake, California. managementefforts in the absenceof informationare Oecologia68: 428-436. experiments,and conductingthem (or collaborating De Santo,T. L. 1992.Physiological and ecologicalfactors with researchers)in a scientificallyrigorous manner influencingprey selectionin coastallybreeding White so as to provide criticaldata. Finall.• managersof Ibises(Eudocimus albus). Unpubl. Ph.D. diss., inland wetlandscan protect shorebird populations Universityof Georgia,Athens. by doing anythingpossible to securefreshwater for EI-Ashry,M. T. & Gibbons,D.C. 1988.The Westin profile. wetlandswith breedingshorebirds. In: M. T. EI-Ashryand D.C. Gibbons(eds.), Water and aridlands of the western United States, pp. 1-19. CambridgeUniversity Press, United Kingdom. Ellis, R. A., Goertemiller, Jr., C. C., DeLellis, R. A., & Acknowledgements Kablotsky,Y. H. 1963.The effect of a saltwater regime on thedevelopment of the saltglands of domestic We thank C. S. Elphick,D. Delehanty,L. W. Oring,J. ducklings.Develop. Biol. 8: 286-308. M. Reed,J. Skoropa,and N. Warnockfor comments Frayer,W. E., Peters,D. D., & Pywell,H. R. 1989.Wetlands that improved the manuscript.JAR was supported of the CaliforniaCentral Valley: Status and trends,1939 during the writing of this manuscriptby the B & B to mid-1980's.U.S. Fish& WildlifeService, Region 1, Portland,Oregon. and JayDow, Sr.Wetlands, the NationalAudubon Goodsell, J. T. 1990. Distribution of waterbird broods SocietyGeorge Whittell Nevada Environmental relativeto wetlandsalinity and pH in south-western Fund, NSF DEB-9196050to L. W. Oring, DEB-942256 Australia. Aust. Wildl. Res. 17: 219-229. to L. W. Oring and JAR,an NSF GraduateFellowship Helmers,D. L. 1992.Shorebird management manual. Western to JAR, and USDA Hatch Grants via the Nevada HemisphereShorebird Reserve Network, Manomet, AgriculturalExperiment Station to L. W. Oring. Massachusetts. MAR was supportedin part by U.S. Departmentof Herbst,D. B. 1981.Ecological physiology of the larval brine AgricultureCSRS 95-37101-2026 to L. W. Oring and fly, Ephydrahians, an alkalinesalt-lake inhabiting MAR, and by the Departmentof the Interior,U.S. Ephydrid. Unpubl.M.Sc. thesis, Oregon State GeologicalSurvey, through the Nevada Water University,Corvallis. Institute. The contentsof this publicationdo not Hill, D. A. 1989.Manipulating water habitats to optimise waderand wildfowl populations.In: G. P.Buckley necessarilyreflect the viewsand policiesof the (ed.),Biological habitat reconstruction, pp. 328-343. Departmentof the Interior,nor doesmention of trade Belhaven Press, London. namesor commercialproducts constitute their Hoffman, D. J., Ohlendorf, H. M., & Aldrich, T. W. 1988. endorsementby the United StatesGovernment. Seleniumteratogenesis in naturalpopulations of aquaticbirds in centralCalifornia. Arch. Environ. Contain. Toxicol. 17: 519-525. References Holmes,W. N., & Phillips,J. G. 1985.The aviansalt gland. Biol. Rev. 60: 213-256. Holmes,W. N., Butler,D. G., & Phillips,J. G. 1961. Aladin, N. V., & Potts,T. W. 1992.Changes in Aral Sea ecosystemduring the period 1960-1990. Hydrobiologia Observationson the effectof maintainingGlaucous- 237: 67-79. wingedGulls (Larus glaucescens) on fresh water and sea AmericanSociety of Civil Engineers.1990. Agricultural water for longperiods. J. Endocrin.23: 53-61. Hothem, R. L., & Ohlendorf, H. M. 1989. Contaminants in salinityassessment and management.K. K. Tanji(ed.), ASCE manualsand reports on engineering practice No. 71. foodsof aquaticbirds at KestersonReservoir, California, 1985. Arch. Environ. Contam. Tox. 18: 773-786. Bagley,J. M. 1967.The salinityproblem in reuseof water. In: J.L. Gardnerand L. E. Meyers(eds.), Water supplies Hurlbert, S. H. 1991.Salinity thresholds, lake size and for arid regions.Contribution No. 10 of the Committee history:A critiqueof the NAS and CORI reportson Mono Lake. Bull. So. Cal. Acad. Sci. 90: 41-57. on Desert and Arid Zones Research, AAAS and the University of Arizona. Johnston,J. W., & Bildstein,K. L. 1990.Dietary salt as a Barnes, G. G., & Nudds, T. D. 1991. Salt tolerance in physiologicalconstraint in White Ibis breedingin an AmericanBlack Ducks, Mallards, and their F-1 hybrids. estuary.Phys. Zool. 63: 190-207. Auk 108:89-98 Karr,J. R. 1993.Defining and assessingecological integrity: Bildstein, K. L. 1993. White Ibis: Wetlandwanderer. Beyondwater quality. Environ. Toxicol. Chem. 12: 1521- 1531. SmithsonianInstitution Press, Washington, D.C. Boshoff,A. E, & Piper,S. E. 1992.Temporal and spatial Kirschner, L. B. 1979. Control mechanisms in crustaceans variationin communityindices of waterbirdsat a and fishes.In: R. Gilles (ed.),Mechanisms of coastalwetland, Southern Cape Province. S. Afr. J. osmoregulationin animals: Maintenance of cell volume, pp. Wildl. Res. 22: 17-25. 157-222.Wiley, Inc., New York. Bunch,R. L., & Ettinger,M. B. 1964.Water quality Klaasen,M., & Ens,B. J. 1990. Is saltstress a problemfor depreciationby municipaluse. J. WaterPollut. Cont. waderswintering on the BancD'Arguin, Mauritania? Fed. 36: 1411-1414. Ardea 78: 67-74.

53 International Wader Studies 9:45-54

Lack,D. 1954.Natural regulation of numbers. Schmidt-Nielson,K., J6rgensen,C. B., & Osaki,H. 1957. Clarendon Press, Oxford. Secretionof hypertonicsolutions in marine birds. Fed. Lico,M. S. 1992.Detailed study of irrigationdrainage in and Proc. 16: 113-114. nearwildlife management areas, west-central Nevada, 1987- Skadhauge,E. 1981.Osmoregulation in birds. Springer- 90. PartA. USGSWater ResourcesInvestigations Verlag,Berlin. Report92-4024A, Carson City, Nevada. Skorupa,J., & Ohlendorf,H. M. 1991.Contaminants in Maclean,G. L. 1977.Comparative notes on Black-fronted drainagewater and avian risk thresholds.In: A. Dinar and Red-kneed dotterels. Emu 77: 199-207. and D. Zilberman(eds.), The economics and management Mahoney,S. A., & Jehl,Jr., J. R. 1985.Adaptations of ofwater and drainage in agriculture,pp. 345-368.Kluwer migratoryshorebirds to highly salineand alkaline Academic Publishers,Norwell, Massachusetts. lakes:Wilson's Phalarope and AmericanAvocet. Condor Staaland,H. 1967.Anatomical and physiological 87: 520-527. adaptationsof thenasal glands in Charadriiformes Merendino,M. T., Dennis,D. G., & Ankney,C. D. 1992. birds. Comp.Biochem. Physiol. 23: 933-944. Mallard harvestdata: An indexof wetlandquality for Staaland, H. 1968. Excretion of salt in waders Charadrii breedingwaterfowl. Wildl.Soc. Bull. 20: 171-175. afteracute salt loads. Nytt MagazinZool. 3: 25-28. National ResearchCouncil (U.S.) Panel on Saline State of California Water Resources Control Board. 1994a. Agriculturein DevelopingCountries. 1990. Saline Finalenvironmental impact report,for the review of theMono agriculture:Salt-tolerant plants for developingcountries. Basinwater rights of theCity of Los Angeles. California Reportof a panelof the Boardon Scienceand State Water ResourcesControl Board, Division of Water Technologyfor InternationalDevelopment, Office of Rights,Sacramento. International Affairs, National ResearchCouncil. State of California Water Resources Control Board. 1994b. NationalAcademy Press, Washington, D.C. Decisionand order amending water right licenses to establish Noss,R. E, & Murphy,D. D. 1995.Species and habitat are ,fisheryprotection flows in streamstributary to Mono Lake inseparable.Conserv. Biol. 9: 229-231. andto protect public trust resources at Mono Lake and in the Ohlendorf, H. M., Hoffman, D. J., Saiki, M. K., & Aldrich, T. Mono Lake Basin. California State Water Resources W. 1986.Embryonic mortality and abnormalitiesof Control Board, Sacramento. aquaticbirds: Apparent impacts of seleniumfrom Streeter,V. L., & Wylie, E. B. 1979.Fluid mechanics, 7th ed. irrigationdrainwater. Sci.Total Environ. 52: 49-63. McGraw-Hill, New York. Ohlendorf, H. M., Hothem, R. L., & Welsh, D. 1989. Nest Suter,G. W. 1993.A critiqueof ecosystemhealth concepts success,cause-specific nest failure, and hatchabilityof and indexes. Environ. Toxicol. Chem. 12: 1533-1539. aquaticbirds at selenium-contaminatedKesterson Swanson,G. A., Adomatis, V. A., Lee, F. R., Serie,J. R., & Reservoir and a reference site. Condor 91: 787-796. Shoesmith,J. A. 1984.Limnological conditions Patten,D., Conte,F. P.,Cooper, W. E., Dracup,J., Dreiss, S., influencingduckling use of salinelakes in south-central Harper,K., Hunt, Jr.,G. L., Kilham, P.,Klieforth, H. E., NorthDakota. J. WildlifeManage. 48: 340-349. Melack,J. M., & Temple,S. A. 1987.The Mono Basin U.S. Departmentof theInterior, Office of theSecretary. 1988. ecosystem:Effects of changing lake Level. Report by the NewlandsProject, Nevada-California operating criteria and Mono BasinEcosystem Study Committee, National proceduresrecord of decision. Washington, D.C. ResearchCouncil, National Academy Press, U. S. Fish and Wildlife Service,Division of Environmental Washington,D.C. Contaminants.1992. An overviewof irrigation drainwater Phillips,J. E., Bradley,T. J.,& Maddrell,S. H. P. 1978. techniques,impacts on fish and wildlife resources, and Mechanismsof ionicand osmoticregulation in saline- managementoptions. Washington, D.C. water mosquitolarvae. In: K. Schmidt-Nielsen,L. Bolis, Waisel,Y. 1972. Biologyofhalophytes. Academic Press, New and S.H. P.Maddrell (eds.),Comparative physiology: York. Water,ions and fluid mechanics,pp. 151-171.Cambridge WHSRN. 1992.Western Hemisphere Shorebird Reserve UniversityPress, United Kingdom. Network Newsletter, Vol. 5, No. 1. Piersma,T. 1994.Close to the edge:Energetic bottlenecks Williams, M. L., Hothem, R. L., & Ohlendorf, H. M. 1989. and the evolutionof migratorypathways in Knots. Recruitment failure in American Avocets and Black- Unpubl. Ph.D diss. UitgeverijHet OpenBoek, Den neckedStilts nesting at KestersonReservoir, California, Burg,Texel, The Netherlands. 1984-1985. Condor 91: 797-802. Purdue, J. R., & Haines, H. 1977. Salt water toleranceand Williams,W. D., Boulton,A. J.,& Taaffe,R. G. 1990.Salinity water turnoverin the Snowy Plover. Auk 94: 248-255. asa determinantof saltlake fauna:A questionof scale. Reed,J. M. 1995.Ecosystem management and an avian Hydrobiologia197: 257-266. habitat dilemma. Wild. Soc. Bull. 23: 453-457. Willoughby,E. J.,& Peaker,M. 1979.Birds. In: G. M. O. Rijke,A.M. 1970.Wettability and phylogenetic Maloiy(ed.), Comparative physiology ofosmoregulation in developmentof featherstructure in waterbirds. J.Exp. animals,Vol. 2, pp. 1-55.Academic Press, London. Biol. 52: 469-479. Winkler,D. W., Weigen,C. P.,Engstrom, E B., & Burch,S. E. Rubega,M. A., & Inouye, C. 1994.Prey switchingin red- 1977.Ornithology. In: D. W. Winkler(ed.), An ecological neckedphalaropes Phalaropus lobatus: Feeding studyof Mono Lake, California, pp. 88-113.Institute of limitations,the functionalresponse and water EcologyPublication No. 12.University of California, managementat Mono Lake, California,U.S. A. Biol. Davis. Conserv. 70: 205-210. Wolheim,W. M., & Lovvorn,J. R. 1995.Salinity effects on Scheuhammer, A.M. 1991. Effects of acidification on the macroinvertebrateassemblages and waterbirdfood availabilityof toxicmetals and calciumto wild birds websin shallowlakes of theWyoming High Plains. and . Environ. Poll. 71: 329-375. Hydrobiologia310: 207-223. Schmidt-Nielsen,K. 1960.The salt-secretinggland of WooIf,J. 1993. Davis county plugged drains, flooded shore marine birds. Circulation 21: 955-967. birds'nests. SaltLake Tribune, 26 July 1993:A1, B2. Schmidt-Nielsen,K. 1970.Animal physiology, 3rd ed. Wu, J.1992. Detecting spatial patterns: The net-function Prentice-Hall,Englewood Cliffs, New Jersey. interpolation.Coenoses 7: 137-143. Schmidt-Nielsen,K., & Fange,R. 1958.The functionof the Wu, L., Chen,J., Tanji, K. K., & Banuelos,G. S. 1995. salt gland in the Brown Pelican. Auk 75:282-289. Distributionand biomagnificationof seleniumin a Schmidt-Nielsen,K., & Sladen,W. J. L. 1958.Nasal salt restoredupland grassland contaminated by selenium secretionin the Humboldt Penguin. Nature181: 1217- from agriculturaldrain water. Env.Toxic. Chem. 14: 733- 1218. 742. Schmidt-Nielsen, K., & Kim, Y. T. 1964. The effect of salt Wunderle,J. M., Jr.1991. Age specificforaging proficiency intakeon the sizeand functionof the salt glandof in birds. In: D. M. Power(ed.), Current ornithology, Vol. ducks. Auk 81: 160-172. 8, pp. 273-324.Plenum Press, New York.

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