Abiotic differences and anthropogenic interference affect ......2.1 Study Sites This study was conducted at two locations along the South Fork Eel River. The low level of interference

CEC Research | https://doi.org/10.21973/N3537J Spring 2019 1/10

Abioticdifferencesandanthropogenicinterferenceaffectfoothillyellow-leggedfrogbreeding

SharonTamir1,AnnaSzymanska2,AmandaCallahan3,

GinaLucas3,JenifferAmezquita4

1UniversityofCalifornia,SantaBarbara,2UniversityofCalifornia,LosAngeles,3UniversityofCalifornia,Riverside,4UniversityofCalifornia,Merced

ABSTRACT

As human presence rapidly introduces novel environmental pressures to nativeecosystems, many species experience population declines. Sensitive taxa such asamphibiansmay be particularly vulnerable to such environmental disturbances.Ranaboylii,thefoothillyellow-leggedfrogandaCaliforniaStateSpeciesofSpecialConcern,servesasamodel forunderstandingtheeffectofanthropogenic interference,suchaschanging climate and disturbed habitats, on reproductive success. In this study, wemeasuredeggmassabundance,abioticcharacteristicsofovipositionmicrohabitats,anddevelopmentalconditionsofeggmassesattwolocationswithdifferentlevelsofhumaninterference along the South Fork Eel River in the pacific northwest of California.Wefoundthatabioticconditionsaffectedeggmassproximitytonearestneighbor,hatching,and predation, whereas the level of human interference affected egg mass size anddesiccation. These findings further confirm the need to identify and protectR. boyliioviposition habitats and be cautious about drasticallymodifying the climate towhichtheyareadapted.

Keywords:anthropogenic,GosnerStagingSystem,oviposition,Ranaboylii,riparian

INTRODUCTION

Anthropogenic interference in riparianecosystemshasaffectedsuccessofresidentspecies. Human disturbance can alter thebiological composition of an environmentthroughtheintroductionofinvasivespeciesor decimation of native species, aswell asthephysicalcompositionofanenvironmentbytheintroductionofconstructionprojectsthat alter the abiotic factors in a region(Kupferberg et al. 2012). Changes in the

biotic and abiotic environment can begauged by native amphibian success,making amphibians possible indicators ofriparian ecosystem health (Welsh andOllivier, 1998). For example, the humanintroduction of the American bullfrog(Lithobates catesbeianus) in freshwaterhabitatshascausedadecline inred-leggedfrog (Rana aurora) larvae viability becauseof predation and competition pressures(Hayes and Jennings 1986). Mitigationefforts, such as attempting to eradicate


American bullfrogs, are being attemptedthroughout California (Kupferberg 1996b).Abioticenvironmental factors,suchas landdevelopment or climate change, are moredifficulttoreverttoapreviousstate.Waterdiversion from U.S. southwestern desertshas caused rampant habitat loss andpopulation decline for several nativeRanidae species (Jennings & Hayes 1994),and climate change-induceddroughtshavereduced breeding sites for the pacificnorthwestern native frog Rana cascadae,the cascades frog, which has nearlydisappearedfromitssouthernmostrangeinCalifornia(Fellers&Drost1993).Elucidatingthe associations between anthropogenicinterference and the physical factors thatplay a role in reproductive behavior iscritical for maintaining native amphibianpopulations.Acandidatespeciesforunderstandingthe

effects of anthropogenic interference onriparian species success is the foothillyellow-leggedfrog,Ranaboylii,aCaliforniaState Species of Special Concern. Thehistoric range of R. boylii once spannedfrom Baja California to Oregon, but hassince been reduced by more than 60%(Hayes et al. 2016). This decline iscorrelated with effects of flow regulation,such as man-made dams, and insufficientprecipitation in the southern half of itsrange (Kupferberg 1996a). R. boylii canreside in a diverse range of freshwaterstreams, from large rivers to small creeks,but require particular conditions foroviposition. Oviposition sites are generallyatcobblebarswithlittlevegetation,shallowwater, and low water velocity (Lind et al.2016). Distance of clutches to shore andambient water temperature vary amongovipositionmicrohabitats, yet temperatureaffectshatchingrateandemergenttadpole

fitness (Catenazzi & Kupferberg 2013).Monitoring egg masses and observingabiotic conditions at oviposition sites canhelp conservationists explore trends in R.boyliiabundanceandrelationshipsbetweenthe environment and developmental rate(Kupferberg1996a,Catenazzi&Kupferberg2013). There are limitations to theseestimates: (1) oviposition occurs fromMarchtoJuneandhatchingoccursbetween5 to 30+ days later, requiring frequentsurveystoobtainanaccuratecountfortheseason, (2) each female only lays one eggmass,andofthateggmassfewerthan10%of the tadpoles survive to adulthood, (3)females reach reproductive maturity atthree years old, so there is a three-yeardelay between a disruption in R. boyliireproduction and its detection, and (4)older females oviposit prior to youngerones and tend to lay larger egg masses(Kupferberg 1996a, Lind et al. 2016). R.boylii oviposition distribution and relativesuccess can help conservationistsunderstand how changes in theenvironment due to anthropogenicinterference affect population abundanceandreproductivebehavior.In this study, we measured R. boylii

abundance and abiotic factors at twoovipositionlocationstogaugehowthelevelof anthropogenic interferencemight affecteggmassdeposition.Forasubsetoftheeggmasses, we measured differences inexternal and internal embryodevelopmentalstageinordertounderstandhow position within an egg mass affectsdevelopmental rate. Differences indevelopment inside and outside the eggmassmay indicate differences in exposuretostressfulconditionsovertime,aswellasinform adaptation mechanisms and futureconservation strategies (Catenazzi &


Kupferberg 2013). We predicted thatreproductive response variables (egg massabundance, distance to nearest neighbor,size, hatching, and developmental stage)would be negatively impacted at locationswith a high level of human interference(BenbowStateRecreationArea,opentothepublic with recent history of construction)compared to those with a low level ofinterference (Angelo Coast Range Reserve,protected coastal conifer and riparianhabitat). Additionally, we predicted bioticresponse variables (predation, desiccation,and scouring) would increase with“harsher” abiotic factors (highertemperatures, greater water velocity, etc.)withineachlocation(Kupferberg1996a).Bycomprehending which factors affectovipositionanddevelopment,wecanbetterunderstandR. boylii reproductive behaviorin an anthropogenic-induced changingenvironment.

METHODS

2.1StudySites

ThisstudywasconductedattwolocationsalongtheSouthForkEelRiver.Thelowlevelof interference site data was collected atAngeloCoast RangeReserve inMendocinoCounty, California (39°45’15.4”N,123°37’53.0”W), a preserved coast coniferandriparianhabitatandpartoftheNaturalReserve System of the University ofCalifornia (Figure 1). The high level ofhuman interference data was collected atBenbowStateRecreationAreainHumboldtCounty, California (40°03’57.8”N,123°47’19.6”W), a publicly-accessiblelocation thatuntil recentlyhadadam thatformedaseasonallake(Figure2).Whenthedamwasremoved,nearbyeggmasseswere

Figure 1. Data collection sites at Angelo CoastRange Reserve. Black dots represent R. boyliiovipositionsitesalongSouthForkEelRiveratwhichabiotic and reproductive response data werecollected.AngeloCoastRangeReserveservedasthelocation with low human interference in this studybecause it is a part of the University of CaliforniaNatural Reserve System and not accessible to thepublic.

Figure 2. Data collection sites at Benbow StateRecreation Area. Black dots represent R. boyliiovipositionsitesalongSouthForkEelRiveratwhichabiotic and reproductive response data werecollected. Benbow State Recreation Area served asthe location with high human interference in thisstudybecauseitisopentothepublicandusedtobea seasonal lake until the damn (located at thedashedrectangle)wasremovedin2016.

relocated.Thedamremovalwascompletedin2016,threeyearspriortodatacollection(Catenazzi 2018). All data was collected inthespringof2019fromMay6to12,duringwhich the weather at both locations was


sunny and ranged from a high of 27°Cduringthedaytoalowof7°Catnight.

2.2AbundanceSurvey

All abundance data was collected usingprotocols and survey sites established byDr. Sarah Kupferberg (Kupferberg 1996a,Kupferberg 1996b, Kupferberg 1997,Kupferberg et al. 2012). Egg massmicrohabitats, conditions, and abundancewere measured by walking along sites inwhichovipositionwasobservedinpreviousyears.

2.3Abiotic,BioticResponse,andReproductiveResponseVariables

In order to test for whether abioticvariables or location-based differences(and, therefore, human interference-baseddifferences) accounted for R. boyliioviposition behavior, egg masses wererandomlychosenwithincobblebarhabitatsateach location (NAngelo=90,NBenbow=45)and abiotic, biotic, and reproductiveresponse variables were recorded. Abioticvariables recorded were water velocity(m/s), water depth (cm), distance fromshore (cm), and water temperature (°C)(Table 1). Biotic variables recorded werepredation (presence or absence),desiccation (measured by the followingscalefromKupferberg(1996a):1-eggmasscompletely exposed to air, 2 - egg masspartially exposed to air, and 3 - egg masscompletely submerged in water), andscouring (measured by the following scalefrom Kupferberg (1996a): 1 - egg masscompletelyremovedfromsubstrate,2-eggmass partially removed, 3 - egg massintact). Reproductive response variablesmeasured were egg mass size (“small” if

less than7cm,“medium” ifbetween7cmand 10 cm, and “large” if greater than 10cm), distance to nearest neighbor (cm),hatching (presence or absence), anddevelopmentalstage.

Table 1. Summary of average abioticmeasurements. A summary of abiotic factorsmeasured at oviposition microhabitats for twolocations with differing human interference alongthe South Fork Eel River. Angelo Coast RangeReserve experiences low levels of humaninterference, and Benbow State Recreation Areaexperienceshigh levelsofhumaninterference.Onlytemperature significantly differed between the twolocations(p<0.0001,F=17.76,NAngelo=90,NBenbow=45).

Developmentalstageoffrogembryoswasassessed using the Gosner Staging Systemfrom1to25(Gosner1960).Developmentalstage recorded was the latest stageobservedontheexterioreggsoftheclutch,withtheexceptionofdatacollectedforthematched pairwise comparison betweeninternal andexternal developmental stage.In order to compare internal and externaldevelopmental stages, the latestdevelopmental stage of the most exterioreggs on the clutch was compared to thelatest developmental stage of eggs severallayerstowardthe interior.Thiscomparisoncould only be conducted with eggs whichwere slightly scoured so as to avoid anyunintendedharm to the clutch. Finally,wecategorized all free-swimming tadpolesaroundtheclutchesasGosnerStage25.


2.4DataAnalysis

All statistical tests were executed usingJMP statistical software version 14. AGeneral Linear Model (GLM) was used todetermine if each reproductive (egg masssize,distancetonearestneighbor,hatching,and developmental stage) and biotic(predation, desiccation, and scouring)response couldbedescribedby anyof theabiotic variables (water velocity, waterdepth, distance from shore, watertemperature) or by level of humaninterference (location). A Pearsoncorrelationwasusedtomodeltheeffectofwater velocity on distance to nearest eggmass. A χ2 test was used to test therelationship between egg mass size andlocation. A logistic regression was used totesttheeffectoftemperatureonpredation.Three models were used to explain theabiotic factors thataffectdesiccation: (1)aone-way ANOVA was used to model theeffect of location, (2) a logistic regressionwas used to model the effect of waterdepth,and(3)alogisticregressionwasusedto model the effect of temperature. Alogistic regression was used to model theeffectof temperatureonhatching.Neitherscouring nor developmental stage yieldeddata that couldbeanalyzedbya statisticalmodel. A GLM model was again used todetermine if abiotic factors differedbetween the two locations (Angelo CoastRange Reserve and Benbow StateRecreation Area). An ANOVA was used tomodel the relationship between locationandwatertemperature.

RESULTS

3.2AbundanceSurvey

We counted 626 egg masses in AngeloCoastRangeReservealonga5.2kmstretchof river (120 egg masses/km). At BenbowState Recreation Area, egg masses totaled532 for a 3.0 km stretch of river (177 eggmasses/km).

3.3Abiotic,BioticResponse,andReproductiveResponseVariables

Reproductive (eggmass size, distance tonearest neighbor, hatching, anddevelopmentalstage)andbiotic(predation,desiccation, and scouring) responsevariableswereaffectedbyabioticfactorsaswellasbylocation.There was a greater egg mass size in

Angelo Coast Range Reserve (the low-interferencelocation)thaninBenbowStateRecreation Area (the high-interferencelocation) (p = 0.037, χ2 = 10.31, NAngelo = 90,NBenbow = 45, Figure 3). There was a positiverelationship between distance to thenearest neighbor and water velocity (p <0.0001,R2=0.16,N=135,Figure4).Therewas a positive relationship betweenwatertemperatureandhatchingeggmasses (p=0.01,F=6.64,NHatching=29,NIntact=106,Figure5). There was no relationship betweendevelopmentalstageandanyoftheabioticvariablesmeasured(p=0.93,F=0.01,N=135).However,wefoundthatexternaleggswere more developed than internal eggswithineggmasses(p=0.003,t=-3.31,N=22,Figure6).


Figure 3. Eggmass size is greater at locationwithlow human interference. Eggmass size ofR. boyliiwas measured by surface area on the followingscale: 1 – small (less than 7 cm), 2 – medium(between 7 cm and 10 cm), and 3 – large (greaterthan 10 cm). Average eggmass sizewas greater atAngelo Coast Range Reserve, the location of lowhuman interference, than at Benbow StateRecreation Area, the location of high humaninterference(p=0.037,χ2=10.31,NAngelo=90,NBenbow=45).Errorbarsrepresentoneunitstandarderror.

Figure4.Distancetonearestneighbordecreasesaswatervelocity increases.AsambientwatervelocityofR.boyliieggmassincreased,distanceofeggmasstonearestproximaleggmassdecreased(p<0.0001,R2 = 0.16, N = 135). This may be due to fewermicrohabitats thatadequatelyprotect theeggmassfromscouring.

Figure 5. Instance of hatching increases withtemperature. Hatching of R. boylii eggs was morecommon in microhabitats with warmer ambienttemperature(p=0.01,F=6.64,NHatching=29,NIntact=106). Hatching may be accelerated by rising watertemperaturesasanadaptationtoavoiddesiccation.Errorbarsrepresentoneunitstandarderror.

Figure 6. Exterior eggs developmore rapidly thaninterioreggs.Developmentalstagewasrecordedonthe most exterior and slightly interior eggs in R.boylii eggmasses using the Gosner Staging Systemfrom 1 to 25. Exterior eggs were more developedthaninteriorones(p=0.003,t=-3.31,N=22).Thisdesynchrony may be due to differing exposure toenvironmental stressors or access to oxygen. Errorbarsrepresentoneunitstandarderror.

We observed that as water temperaturedecreased, predation increased (p = 0.003,χ2=8.87,NPredation=25,NUntouched=110,Figure7).We also found that severity of desiccationincreasedwithwatertemperature(p=0.02,χ2 = 5.10, N = 135), exhibited an inverserelationshipwithwaterdepth(p<0.0001,χ2=41.56,N=135),anddifferedbetween

locations (p<0.0001,F=45.58,NAngelo =90,NBenbow = 45, Figure 8). None of the abioticfactorsmeasuredhadaneffectonscouring(p = 0.10, F = 1.90, N = 135). The onlydifferenceinabioticfactorsbylocationwaswater temperature (p < 0.0001, F = 17.76,NAngelo=90,NBenbow=45,Table1).


Figure 7. Instance of predation decreases withtemperature. Predation was more common in R.boylii egg masses present in microhabitats withcooler ambientwater temperature (p = 0.003, χ2 =8.87,NPredation=25,NUntouched=110).Thismaybedueto predator temperature preferences. Error barsrepresentoneunitstandarderror.

Figure 8. Desiccationwasmore severe at locationwith low human interference. Desiccation of R.boylii egg masses was measured on the followingscale:1)eggmasscompletelyexposedtoair,2)eggmass partially exposed to air, and 3) egg masscompletely submerged in water. Desiccation wasmore commonly observed at Angelo Coast RangeReserve, the location of low human interference,thanatBenbowStateRecreationArea, the locationof high human interference (p < 0.0001, F = 45.58,NAngelo = 90, NBenbow = 45). The reason for thisobservation is unclear and requires furtherinvestigation.Errorbarsrepresentoneunitstandarderror.

DISCUSSION

Overall, we found that both abioticfactors (watervelocity,water temperature,and depth) and the level of human

interference (location) affect thereproductive (egg mass size, distance tonearest neighbor, hatching, anddevelopmental stage) and biotic responsevariables (predation, desiccation, andscouring) measured, and both areimportant for describing the reproductivebehaviorofR.boylii.Contrary to our prediction, egg

masses/km were higher at Benbow StateRecreation Area, the location with highlevels of human interference, than atAngelo Coast Range Reserve, the locationwith low levels of interference. Furtherresearchmustbedonetounderstandwhatthe cause might be, despite greater foottrafficandconstructiondisturbancesatthehigh-interference location thanarepresentatthelow-interferencelocation.Within the range of water velocities

conducive to oviposition, eggmasseswerefound closer together when velocity wasgreater (Figure 4). This may be due tolimitedoviposition spots thatoffer enoughprotection from water flow to avoidscouring.R.boyliipreferanarrowrangeofwater velocities compared to availablecobble bar habitat (Lind et al. 2016) andreturn to the same breeding sites forconsecutive years (Kupferberg 1996a).Further research must be done todetermineifproximitytoanothereggmassaffectstadpolefitnessthrough intraspecificcompetition, and if there is a tradeoffbetween neighbor proximity and chosenmicrohabitat,suchaspredationorscouring.Larger egg masses were found at the

location with low levels of humaninterference (Angelo Coast Range Reserve)thanthelocationwithhighlevelsofhumaninterference (Benbow State RecreationArea)(Figure3).Biggereggmassesarelaidby larger females, and frog sizemaybean


indicator of age and health (Kupferberg1996a), implying that frogs in locations oflower human interference experienceimproved survival. Although Angelo CoastRange Reserve may have better R. boyliisurvival after reaching adulthood, it had agreater instance of egg mass desiccationthan at Benbow State Recreation Area(Figure8).As predicted, the threat of desiccation

increased as water depth decreased andtemperature increased; however, we alsoobserved a difference in desiccation bylocation (Figure 8). Further research mustbeconductedtounderstandwhatthecausemight be, as water recession levels atAngelo Coast Range Reserve have notvariedmuch over the past few years (U.S.Geological Survey 2019). Conversely, therewas no relationship between scouring andabiotic factorsmeasured. It ispossiblethattaking the average velocity over an entiresite was not refined enough to find apattern between scouring and watervelocity. However, scouring of egg massesdepends on factors beyondwater velocity,such as the positioning of the mass onsubstrate and orientation with respect tothestreamflow.Severalofthesameabioticfactors that promote desiccation alsopromoteearlyhatching.Hatchingeggmassesweremorefrequent

in areas with warmer ambient watertemperaturethanincoolerones(Figure5).This finding issupportedbyZweifel (1955),whofoundthatR.boyliibreedpreferablyatthe turn of the season and await thebeginning of the dry, warm season to laytheir eggs. As climatic temperatures rise,appropriatetemperaturesforhatching(andcoincidentally for avoiding desiccation) arereachedearlier in spring,promptingearlierhatching (Kupferberg 1996a, Wheeler and

Welsh 2008). Alternatively, hatching inwarmer waters may also be a defensemechanism against predation. Depredatedeggmasseswerefoundmorecommonly inareas with cooler ambient watertemperature(Figure7).AcommonR.boyliipredator observed at every site was thecommon garter snake, genus Thamnophis,which like R. boylii develops at a quickerrate when temperatures are warmer (Fox1948) and whose development mightsimilarly be affected by climate change.However, newly-born garter snakes moveslower in cooler water (Heckrotte 1967),possibly biasing predatory advances tostatic prey like R. boylii eggs. Althoughoccurance of hatchingwas correlatedwithwater temperature, developmental stagewasnot.A lack of correlation between

developmental stage and the location orthe abiotic variablesmeasured is expectedbecausedevelopmentalstagedependsonacombination of factors including, but notlimited to, environmental stressors(Catenazzi & Kupferberg 2013). The effectof theenvironmentondevelopmental ratewithin the egg mass, however, is notequally distributed. We found that theexternalenvelopeoftheeggmassdevelopsmorequickly than the internalpart (Figure6). Thismaybedue to increasedexposureto stressors, such as temperature, on theexternal eggs of the egg mass. If the eggjelly insulates the interiorof theeggmass,coolingitwithrespecttotheexterior,thenperhaps the interior also experiencesdecreasedoxygenturnover.Forexample,inopisthobranch gastropod egg masses,interioreggs receive lessoxygenthantheirexterior neighbors due to a reduceddiffusion rate which impedes their growth(Cohen&Strathman1996).Themechanism


for this difference in development wouldrequire further investigation in order tounderstandhowinternalandexternalpartsof the eggmass respond to environmentalpressures such as reduced oxygen, light,andpredation.Tomaximizeeffectivenessofconservation

efforts, conservationists must have aholistic understanding of the completerange of factors, abiotic and biotic, thatpotentially characterize or threatenoviposition habitats. Future studies areneeded to evaluate how biotic factors likethe invasive American bullfrog, Lithobatescatesbeianus, affect reproductive success.To better understandwhyR. boylii chooseto mate during the transition betweenseasons, research should be conducted toexplore possible benefits to reproducingwhile water levels are receding, and howclimatechangemightaffectthem.As the global climate shifts and humans

continue to regulate water flow,conservationists must make an effort todescribe the environmental factors criticalto an ideal oviposition habitat.Understanding the reproductive anddevelopmental effects of environmentalchanges can informproactive conservationmeasuressuchasidentifyingandprotectingbreeding areas, because these areaspromotehighfecundityandsurvivalandareintegral to the success of the R. boyliipopulations. These actions, along withcontinued monitoring and programs thatpreserve and restore the hydraulicprocesses of riverine habitats, are neededto improve conditions for this wildlifespecies and function as the last line ofdefense before we lose this charismaticnativeCalifornianspecies.

ACKNOWLEDGMENTS

We deeply appreciate Tim Miller, KrikorAndonian,andAnaMiller-terKuilefortheirsupport and guidance. We would like toespeciallythankDr.SarahJ.Kupferbergforher assistance with R. boylii backgroundinformation, research questiondevelopment, and for sharing abundancedata collected in the South Fork Eel River.This work was conducted in part at theUniversity of California’s Angelo CoastRange Reserve, doi:10.21973/N3R94R, andatBenbowStateRecreationArea.

REFERENCES

Catenazzi, A., & S.J. Kupferberg. 2013. Theimportance of thermal conditions to recruitmentsuccess in stream-breeding frog populationsdistributed across a productivity gradient.BiologicalConservation.168:40–48.

Catenazzi,A.,&S.J.Kupferberg.2018.Consequencesof dam-altered thermal regimes for a riverineherbivore's digestive efficiency, growth andvulnerability topredation.FreshwaterBiology63:1037–1048.

Cohen, C.S., & R.R. Strathmann. 1996. Embryos attheedgeoftolerance:effectsofenvironmentandstructure of egg masses on supply of oxygen toembryos.TheBiologicalBulletin.190:8–15.

Fellers, G.M., & C.A. Drost. 1993. Disappearance ofthe cascades frogRanacascadae at the southernend of its range, California, USA. BiologicalConservation,65:177–181.

Hayes,M.P.,&M.R.Jennings.1986.Declineofranidfrog species in western North America: arebullfrogs (Rana catesbeiana) responsible? JournalofHerpetology20:490–509.

Hayes,M.P.,Wheeler,C.A.,Lind,A.J.,Green,G.A.,&D.C.Macfarlane.2016.Foothillyellow-leggedfrogconservationassessment inCalifornia.Gen. Tech.Rep. PSW-GTR-248. Pacific Southwest ResearchStation,U.S.ForestService,Albany,CA.


Fox,W.1948.Effectoftemperatureondevelopmentof scutellation in the garter snake, Thamnophiselegansatratus.Copeia1948:252–262.

Gosner, K.L. 1960. A simplified table for staginganuran embryos and larvae with notes onidentification.Herpetologica.16:183–190.

Heckrotte, C. 1967. Relations of body temperature,size, and crawling speed of the common gartersnake,Thamnophiss.sirtalis.Copeia.759–763.

Jennings, M., & M. Hayes. 1994. Decline of nativeranid frogs in the desert southwest.Herpetologyof theNorthAmericanDeserts - Proceedingsof aSymposium,SpecialPubs.5:183–211.

Kiesecker, J.M., & A.R. Blaustein. 2010. Effects ofintroduced bullfrogs and smallmouth bass onmicrohabitat use, growth, and survival of nativered-legged frogs (Rana aurora). ConservationBiology.12:776–787.

Kupferberg, S.B., & J.P. Bent. 1996a. Allergic fungalsinusitis in the pediatric population. Archives ofOtolaryngology–Head&NeckSurgery122: 1381–1384.

Kupferberg, S.J. 1996b. Hydrologic andgeomorphic factors affecting conservation of ariver-breeding frog (Rana boylii). Ecologicalapplications.6:1332–1344.

Kupferberg,S.J.1997.Bullfrog(Ranacatesbeiana)invasion of a California river: the role of larvalcompetition.Ecology.78:1736–1751.

Kupferberg, S.J., Lind, A.J., & W.J. Palen. 2009.Pulsedfloweffectsonthefoothillyellow-legged

frog (Rana boylii): population modeling. FinalReport.

Kupferberg,S.J.,Palen,W.J.,Lind,A.J.,Bobzien,S.,Catenazzi, A., Drennan, J.O.E., & M.E. Power.2012. Effects of flow regimes altered by damsonsurvival,populationdeclines,andrange-widelosses of California river-breeding frogs.ConservationBiology26:513–524.

Lind, A.J., Welsh Jr, H.H., & C.A. Wheeler. 2016.Foothill yellow-legged frog (Rana boylii)ovipositionsitechoiceatmultiplespatialscales.JournalofHerpetology50:263–270.

U.S. Geological Survey. 2019, National WaterInformationSystemdataavailableontheWorldWide Web (USGSWater Data for the Nation),accessed May 16, 2019, at URLhttps://waterdata.usgs.gov/nwis/

Welsh Jr., H.H., & L.M. Ollivier. 1998. Streamamphibiansas indicatorsofecosystemstress:acase study from California’s redwoods.EcologicalApplications8:1118–1132.

Wheeler, C.A., & H.H. Welsh Jr. 2008. Matingstrategy and breeding patterns of the foothillyellow-legged frog (Ranaboylii).HerpetologicalConservationandBiology.3:128–142.

Zweifel, R.G. 1955. Ecology, distribution andsystematicsoffrogsofthe"Ranaboylii"Group,by Richard G. Zweifel. University of CaliforniaPress.

Documents

Abiotic differences and anthropogenic interference affect ......2.1 Study Sites This study was conducted at two locations along the South Fork Eel River. The low level of interference