Human-provoked amphibian decline in central Italy and the efficacy of protected areas

Human-provoked amphibian decline in central Italyand the efficacy of protected areas

Manuela DrsquoAmenAC Biancamaria PietrangeliB and Marco A BolognaA

ADepartment of Environmental Biology University of Roma Tre Viale Marconi 446 Rome ItalyBItalian National Institute for Occupational Prevention and Safety Rome ItalyCCorresponding author Email mdamenuniroma3it

AbstractContext Todaymore than32of amphibian species are threatened andmore than43face a steepdecline in numbers

Most species are being affected simultaneously by multiple stressors and habitat protection is often inadequate to preventdeclines

Aims The main goal of the present research was to understand the consequences of alternative human land use inproducing landscape disturbance for amphibians At the same time we also evaluated the effect of changing climaticconditions as additional potential drivers of population decline Another goal was to determine whether and to what extentthe existing nature reserves have been effective in protecting species in recent decades

Methods Weused generalised additivemodels (GAMs) to investigate the association between the state (stabledecline)of amphibian populations in 5 5 km cells in central Italy and proxies of different typology of anthropogenic stressorsclimatic variables and protection measures

Key results We found a significant association between anthropogenic landscape modifications and species declineThis negative relationshipwas revealedwith agricultural predictors for themajority of the species whereas urban fabrics hada slightly smaller impact We found significant associations between amphibian declines and climatic variation particularlythe increasing number of dry days Protected areas protected declines of two species only

Conclusions Our results showed that the status of amphibians in this region warrants greater attention than has beengiven previously The detrimental effect of agricultural practices combined with increasing aridity makes amphibianpopulations particularly susceptible to extinction and the conservation measures applied till now are inadequate for speciesprotection in this region

Implications Our results should stimulate the implementation of environmental policies that focus not only on theprotection of single habitats but also on ensuring the environmental quality of the surrounding landscapes Moreover anadaptive management approach should be applied to take into account future modification of hydrology and climate

Additional keywords amphibian extinction climate change land cover natural reserves

Introduction

Amphibian populations are declining in many areas of the world(Wake and Vredenburg 2008) Since the late 1970s scientistshave reported declines of several species (eg Pounds andCrump1994 Young et al 2001 Ron et al 2003) and an increasingincidence of developmental malformations (eg Blaustein andJohnson 2003 DrsquoAmen et al 2008) Recent studies warn thatmore than 32 of amphibian species are threatened and morethan 43 face a steep decline in numbers (IUCN 2008) Mostdeclining amphibians are being affected simultaneously bymultiple stressors including habitat destruction and alterationintroduction of exotic species climatic changes increasedexposure to ultraviolet-B (UV-B) radiation and an increasedprevalence of diseases (eg Gibbons et al 2000 Kieseckeret al 2001 Davidson et al 2002 Linder et al 2003 Sih et al2004 Randa and Yunger 2006 Davidson and Knapp 2007Brown et al 2008 DrsquoAmen and Bombi 2009)

Of these stressors habitat loss and fragmentation are the mostwidespread factors driving amphibians to extinction (Gardneret al 2007)The constructionof roads housingdevelopments andcommercial strips andagricultural practices candestroywetlandsand alter ecological processes All these anthropogenic processesfragment the landscape reduce wetlands and isolate them fromone another and produce pollution that degrades the water whereamphibians liveandbreedThese factors in turnmaybreakdowncritical metapopulation processes and alter the structure andpersistence of populations (Beebee 1997 Semlitsch 2000)

Another potential factor driving population decline is the shiftof climatic conditions There is increasingly strong evidence thatrecent climate change has affected the biology of numerousspecies worldwide (Alexander and Eischeid 2001 Corn 2005Menzel et al 2006McMenamin et al 2008DrsquoAmen andBombi2009) As most amphibians depend on water availability andhumid environments for breeding and for egg and larval growth

CSIRO PUBLISHING

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CSIRO 2010 101071WR09167 1035-371210070547

they are extremely vulnerable to the effects of reductions inannual precipitation and change in seasonality (Carey andAlexander 2003 Chadwick et al 2006) Moreover the timingof the seasonal activities of hibernation aestivation andreproduction are tightly related to temperature conditions (egReading 1998) Several climatological studies described apositive trend for mean temperature a reduction in the numberofwet days and an increase in precipitation intensity all over Italyduring the last century (eg Brunetti 2004 2006 Toreti andDesiato 2008) These climatic trends occurred mainly in the past50 years and were associated with broad-scale amphibiandeclines (DrsquoAmen and Bombi 2009)

The main goal of the present research was to understand theconsequences of human land-use disturbances for differentamphibian species in a Mediterranean area in central ItalyAnother goal was to assess whether species declines arerelated to the climatic shifts that have occurred in Italy inrecent decades by considering climatic variables that haveinfluenced amphibian persistence (DrsquoAmen and Bombi 2009)A further goal of our analysis was to determine whether and to

what extent the existing protected areas have been effective forspecies protection in recent decades Indeed although protectedecosystem areas inhibit habitat destruction and direct humandisturbance they can be less adequate for protecting speciesfrom other stressors such as chemical pollution and above allclimatic-shift conditions

To achieve these goals we began by examining changes inspecies abundance at the regional scale and then we devised aspatial approach based on the identification of the spatial effectsof environmental alterations in determining the geographicpatterns of declines observed in recent decades (Davidsonet al 2002 DrsquoAmen and Bombi 2009) This analysis isrelevant because no efficient conservation measures can beplanned if there is an incomplete understanding of the causesleading to declines

Materials and methodsSpecies data

We utilised presence data of 10 species of amphibians in Latiumcentral Italy (data source used by Bologna et al 2000) (Fig 1)

Fig 1 Study region with the grey grid indicating amphibian presence cells utilised for statisticalanalyses

548 Wildlife Research M DrsquoAmen et al

This regional-scale dataset was derived from a compilation ofbibliographic records of amphibians and field samplingsspanning form 1970 to 2004 Field data were collected bothopportunistically and through specific field campaigns byhundreds of volunteers within the regional atlas project Thedatabase is composed of 5723 amphibian records accompaniedby ancillary information such as geographical coordinates andthe observation year On the basis of this information all speciesrecords were referred to a 5 km 5 km geographic-gridresolution across the entire region and the amphibian surveyhistory for each grid cell was reconstructed

Environmental data

We measured the percentage of different types of artificial andagricultural land use (Table 1) in each 5-km square based ondigital 1 100 000-scale Corine Land Cover maps 2000 obtainedfrom the National Environmental Information System (SINAnet)of the Institute for Environmental Protection and Research(ISPRA) (data available at httpwwwsinanetapatititprodottimcgissearchterm=gis accessed 13 May 2008) We alsocalculated the percentage of land-use change between 1990and 2000 and we measured the total length of streets in eachcell As proxy of the potential impact of human activity anddensity on amphibian survival we considered a synthetic indexthat measures the human influence on the Earthrsquos land surface(Sanderson et al 2002) The human influence index (HII) definesthe anthropogenic impact through geographic proxies at theglobal scale at a resolution of 1 km 1 km It was producedthrough an overlay of nine global data layers which representthe variation across space of the following four categories offactors presumed to exert an influence on ecosystems populationdensity land transformation accessibility and electrical-power

infrastructure (see Sanderson et al 2002 for a detaileddescription of each dataset) The number of people in a givenarea is frequently cited as a primary cause of declines in speciesand ecosystems (Cincotta and Engelman 2000) with higherhuman densities leading to higher levels of disturbance Land-transformation categorywhich includes layers of global landusebuilt-up centres population settlements streets and railways isconsidered the greatest threat to biological diversity resulting inloss and fragmentation of habitat in many different ecosystems(eg Vitousek 1997) The human-access category compriseslayers of roads major rivers and coastlines All ecosystemscan be affected by the presence of access ways because theseprovide opportunities for several nature-disrupting activitieseg hunting and extraction of resources pollution and wastedisposal (Gucinski et al 2001) Finally because the increase ofthe human influence on ecosystems in the 20th century is fuelledby fossil energy the HII also incorporates a power infrastructureproxy

To explore the potential relationship between climate changeand species declines we used the annual mean of the followingthree variables that describe factors known to influenceamphibian biology (eg Davidson et al 2001 2002 Poundset al 2006 McMenamin et al 2008) number of dry dayscumulate precipitation (mm) and temperature (C) Annualmean values for these parameters were provided by theNational System for the Collection Elaboration and Diffusionof Climatologic Data of Environmental Interest (SCIA)(data available at httpwwwsciasinanetapatitsciawebscia_mappehtml accessed 13May 2008)We downloaded the annualmean values of the considered variables for the 1961ndash2000period and we kriged them in ArcGIS 93 (ESRI IncRedlands CA USA) to produce climatic surfaces representingtheir geographic variation across Latium with 1 km 1 kmpixels From these layers we calculated the shift in the meanvalues between the decades 1961ndash70 and 1991ndash2000 and weresampled these climatic surfaces at a 5 km 5 km resolution bycalculating the mean values per grid cell

Finally we also included in our analyses the percentage ofprotected surface for each cell to estimate the effectiveness of theprotected areas for the conservation of amphibians All areasbelonging to theNatura 2000 network andNational andRegionalNatural Parks were considered (data available at ftpftpscnminambienteitCartografieNatura2000 accessed 3 September2008)

Statistical analyses

To assess amphibian species decline in every occupied gridsquare of the study area we utilised sighting records from theregional database described above Only records with adefinite year of sighting were considered for the calculationswhereas multiple records within the same year were excludedFinally a total of 297 cells were selected for the followinganalyses (the number of presence cells for each species isreported in Table 2) (Fig 1)

Several statistical methods have been developed to infer theprobability of species persistence from museum or atlas records(eg Solow 1993a 1993b McCarthy 1998 Solow and Roberts2003) The basic idea underlying thesemethods is that confidence

Table 1 Predictor abbreviations and descriptions

Predictor abbreviation Description

Urban predictorART Artificial surfacesURB Urban fabricICT Industrial commercial and transport unitsMDC Mine dump and construction sitedSTR Total length of street coverageART VEG Artificial non-agricultural vegetated areas

Agricultural predictorAGR Agricultural areasARA Arable landP CRO Permanent cropsPAS PasturesHET AGR Heterogeneous agricultural land

Land transformation predictorCLC VAR Land-cover change

Human pressure predictorHII Human influence index (ranging from 0= no

human influence to 70 = largest impact)Climatic predictorT VAR Mean annual temperature variationP VAR Cumulate annual precipitation variationDD VAR Annual number of dry days variation

Habitat protection predictorPA Protected areas

Anthropogenic drivers of amphibian decline Wildlife Research 549

in the continued existence of a species is greater the more recentthe sighting (Solow and Roberts 2003) In particular we utilisedthe Solow and Roberts (2003) non-parametric equation basedon the most recent sightings and the end of the observationperiod which makes minimal assumptions about the sightingrate (it assumes that the sighting rate is positive and smooth at theend of the observation period) Indeed because we calculated theprobability of persistence for 10 species in more than 200 gridcells we could not assume a priori a common distribution for thesighting rate The Solow and Roberts (2003) equation generatesthe following P-value for testing the null hypothesis (H0 = thespecies remains extant at the time T (the total number of yearsfrom the first record)) against the alternative hypothesis (H1 = thespecies is extinct)

p frac14 tn tn1

T tn1

where tn is the number of years since the first record to the mostrecent record and tn1 is the number of years from the first recordto the penultimate record SmallP-values suggest that the data areunlikely to occur if the species is still extant and consequentlythe P-value reflects the probability that another sighting willoccur Since this probability depends on variation of speciesabundance we utilised this value to estimate local declines Weassumed that if the probability is lt15 the abundance of thespecies is decreased so much to consider the species decliningin the cell

Using this criterion for each specieswe attributed the categorySTABLE (P015) and DECLINE (P lt 015) at all theoccurrence squares Moreover to rank the species by their rateof local decline for each species we calculated the percentageof DECLINE cells relative to the total number of occupied cells(ie STABLE+DECLINE)

We explored the relationship of species cell status (STABLE(0) DECLINE (1)) to the considered environmental variables byusing generalised additive modelling (GAM) techniques with abinomial probability distribution and a logit linkGAMsare semi-parametric extensions of the traditional linear statistical modelswhere some predictors can be modelled non-parametrically inaddition to linear and polynomial terms for other predictors Theonly underlying assumption made is that the functions areadditive and that the components are smooth The strength ofGAMs is their ability to deal with highly non-linear and non-

monotonic relationships between the response and the set ofexplanatory variables (Hastie and Tibshirani 1986) For eachspecies we first tested all predictors individually in univariateGAMs (also quadratic effect was tested for climatic variables)and we retained as relevant for further analysis only thosewhose regression coefficients were significant at a P-value oflt025 (chi-square test) (Hosmer and Lemeshow 1989) We thenentered all selected predictors in multivariate models in whichsmoother terms were fitted with four and two degrees offreedom By using a stepwise procedure we determined themost parsimonious combination of predictors and the mostappropriate level of the lsquosmootherrsquo terms which produce thelsquobestrsquomodel in terms of the Akaikersquos information criterion (AIC)statistic (Akaike 1974) TheAIC score allows tomeasure thefit ofthe models to the data (on the basis of the likelihood) (Burnhamand Anderson 2002) The relative explanatory power of theretained predictors were then quantified as the change in theAIC score (DAIC) that resulted when each predictor was droppedone by one from the final model the higher the DAIC the higherthe importance of each variable (eg Knapp et al 2003McPherson and Jetz 2007) In all multivariate modelscollinearity among environmental descriptors was avoided bybuilding separate models for those variables strongly associated(r2 gt 06) with other parameters (ie ART is strongly correlatedwith URB (r2 = 094) and STR (r2 = 086) whereas AGR iscorrelated with ARA (r2 = 071)) Among these alternativemodels AIC was again used to select the best-fit model

Results

Our analyses showed a local decline in the Latium region for allthe considered specieswith 23ndash24DECLINEcells The specieshaving the highest rate (4412) of decline is the smooth newt(Lissotriton vulgaris) whereas the Italian tree frog (Hylaintermedia) is declining in the lowest percentage of squares(2373) (Table 2)

Some of the variables considered were not significant inunivariate models or were not retained after stepwiseprocedure in the final model for any species including ARTAGR MDC and all of the quadratic terms of climatic variablesFor all species statistically significant non-linear relationshipswere found between declines and at least one variable(Table 3) Species persistence in the cells was negativelyrelated with a maximum of four predictors (ie the commontoad Bufo bufo the Italian tree frog the smooth newt the greenfrog Pelophylax spp the northern spectacled salamanderSalamandrina perspicillata) The percentage of protected areaswas a significant predictor only for two species (the northernspectacled salamander and the agile frog Rana dalmatina)

Overall the decline of eight species was associated with atleast one agricultural predictor and for six species the declinewas associated with proxies of habitat destruction and alterationas a result of the urban and industrial fabric The predictors ofclimatic variation were retained in the final model of six species(Table 3) A relationship between the HII and amphibian declinewas found for five species (the smooth newt the Italian streamfrog Rana italica the common toad the green frog and theItalian tree frog) On the contrary land-cover change was a

Table 2 Local decline of amphibians in LatiumNumber of stable and decline cells and the rate of local decline

Species No of declinesquares

No of totalsquares

Rate ofdecline ()

Lissotriton vulgaris 45 102 4412Rana italica 31 76 4079Triturus carnifex 33 84 3929Bufo bufo 49 129 3798Salamandrina perspicillata 16 52 3077Bombina pachypus 11 37 2973Bufo viridis complex 9 33 2727Phelophylax spp 36 133 2707Rana dalmatina 9 34 2647Hyla intermedia 14 59 2373


Tab

le3

General

Add

itiveMod

elresultsshow

ingthefina

lmod

elAIC

valuean

dsign

ificant

variab

lesselected

withtheirrelative

impo

rtan

ceDA

ICresults

wheneach

predictorisremoved

from

thefinalm

odelD

AIC

indicateseach

predictorrsquosrelativ

eim

portance

inthemodelD

AIC

ofthemostimportantp

redictor

foreach

speciesisshow

nin

bold

Species

Final-m

odel

|DAIC|

AIC

URB

ICT

STR

ARTVEG

ARA

PCRO

PAS

HETAGR

CLCVAR

HII

TVAR

PVAR

DD

VAR

PA

Lissotrito

nvulgaris

13810

425

193

161

019

Ranaita

lica

8519

589

285

600

Trituruscarnifex

10803

177

641

Bufobu

fo15

942

409

309

309

722

Salamandrinaperspicilla

ta54

14

543

634

481

1335

053

Bom

bina

pachypus

4764

326

144

Bufoviridiscomplex

3413

000

Phelophylax

spp

13524

255

715

1162

1905

Ranada

lmatina

2611

686

1520

654

Hylainterm

edia

4734

366

060

1648

773


significant predictor of declines for only one species (the Italiantree frog) (Table 3)

When considering the urban and agricultural predictorsseparately we can observe a plain divergence among thevariables representing urban and industrial use URB was themost important and it was associated with the decline of fourspecies (the smooth newt the northern spectacled salamanderthe Apennine yellow-bellied toad Bombina pachypus and theItalian tree frog) whereas the others (ICT STR and ART VEG)were significant for one species only (the green toadBufo viridiscomplex the northern spectacled salamander and the green frogrespectively) or not significant at all (MDC) On the contrary allvariables linked to agricultural practices had a comparableimportance except for P CRO which was significant for theItalian crested newt Triturus carnifex only Among climaticvariables one predictor (DD VAR) was associated with thedeclines of five species (the smooth newt the Italian crestednewt the green frog the agile frog and the Italian tree frog)whereas P VAR and T VAR were both significant predictors forthe common toad only (Table 3)

Focusing only on the most important predictors of speciesdecline those pertaining to climate had the highestDAIC for 40of the species (the Italian crested newt the common toad thegreen frog and the agile frog) Urban predictors were the mostsignificant predictors for three species (the smoothnewt thegreentoad and theApennine yellow-bellied toad) TheHIIwas themostimportant predictor for two species (the Italian stream frog andthe Italian tree frog) whereas variables pertaining to the groupof agricultural practices were the most important predictorsfor one species only (the northern spectacled salamander) Thepercentage of protected areas per square and the variation ofland cover never had the highest DAIC score (Table 3)

We graphically combined our results of the species rate ofdecline and of the total number of significant negative predictors(Fig 2) For this visualisation we assumed the threshold of35 reduction in regional distribution for considering aspecies deserving of high conservation interest setting the

x- and y-axes intersect at that point The graphic approachdivides the 10 species into four groups characterised bydifferential categories of risk (Fig 2) Three species (thecommon toad the smooth newt and the Italian stream frog)showed the most critical situation because they are bothaffected by a high number of stressors and their population hasalready been reduced in more than 35 of their regionaldistribution (Fig 2 up-right dial) Conversely on the basis ofthe same parameters the green toad and the Apennine yellow-bellied toad had the mildest condition in this region (Fig 2 low-left dial) More composite situations emerge for the otherspecies Notwithstanding the high rate of decline the Italiancrested newt could be protected because few factors affectpopulation viability (Fig 2 low-right dial) By contrastspecies that currently show lower rates of decline may needmore complex conservation measures because several stressorsaffect their survival (ie the green frog the northern spectacledsalamander Italian tree frog and the agile frog) (Fig 2 up-leftdial)

Discussion

Declining of amphibians in central Italy

Our results show that several amphibian species in the Latiumregion in Italy have suffered recent declines According to ourresults two species are of particular concern because their rate oflocal decline is higher than 40 namely the smooth newt and theItalian stream frog Both species are classified as Least Concernin the IUCN Red List (Temple and Cox 2009) and did notshow a high rate of decline at the national level (DrsquoAmen andBombi 2009) However their decline in Latium deserves highconservation attention because it may signal a more seriousproblem for the speciesrsquo future persistence

The rate of local decline that we calculated for amphibianspecies in the study areas is clearly related to our choice of thestatistical method There are numerous methods that provide aprobabilistic basis for the persistence hypothesis based on

Lissotriton vulgaris

Rana italica

Triturus carnifex

Bufo bufo

Salamandrina perspicillata

Bombina pachypus

Bufo viridis complex

Phelophylax spp

Rana dalmatina

Hyla intermedia

0

1

2

3

4

5

20 22 24 26 28 30 32 34 36 38 40 42 44 46

Rate of decline

Num

ber

of s

igni

fican

t pre

dict

ors

Fig 2 Differential categories of conservation requirement for amphibians in Latium


sighting data (Solow 1993a 1993b Burgman et al 1995McCarthy 1998 Solow and Roberts 2003) Each methodmakes particular assumptions about the sighting recordbecause the performance is sensitive to deviations from theseassumptions the choice of the method should be based on thecharacteristic of the sighting record utilised (Solow and Roberts2003 Rivadeneira et al 2009) In our dataset we cannot a prioridefine a univocal form of the sighting rate for all cells Indeedmany of the local disappearances of amphibians in the studyregionmay occur because of gradual declines as a result of habitatloss fragmentation and degradation On the contrary otherswould take place more rapidly for several causes For instancehuman activities such as wetland drainage for building purposesmay produce an immediate drop in population size Climaticevents such as severe drought in the arid coastal areas can also beresponsible for such rapid declines a total reproductive failure ina single year may cause a severe drop in population size of short-lived species (Stewart 1995) Moreover exposure to amphibianchytridiomycosis or other parasites in high-altitude populationscan produce massive deaths in short periods (eg Bosch et al2007) The non-parametric test that we applied works well whenno information on population stability is known for eachcalculation (Solow and Roberts 2003 Solow 2005) Therobustness of the non-parametric test is expected to come atthe cost of lower power than the correct parametric test despitethis problem the test hasbeenapplied to several groupsof animalsand plants (eg Solow and Roberts 2003 van Der Ree andMcCarthy 2005 Farnsworth and Ogurcak 2006 Duffy et al2009)

Landscape and climate disturbance on amphibians

Our analyses of habitat destruction and alteration asmeasured bydifferent categories of urban and agricultural land use allowed usto draw significant conclusions For all species the amount ofurban and agricultural land use was associated with the observeddeclines and the HII was an important predictor for half of thespecies This supports the notion that human pressure is ofteninconsistent with the environmental requirements of amphibians(Sala et al 2000 Atauri and de Lucio 2001Davidson et al 2002Hazell 2003 Cushman 2006 Gardner et al 2007) Urban areasare inhospitable habitats for amphibians because their naturalhabitats are converted into roads houses and industrial areasEven if wetlands are preserved in urban areas often in parks theyexperience high human use and are excavated and stocked withfish (Delis et al 1996 Knutson et al 1999) The strength ofhabitat-alteration effect varies among species not only accordingto the intensity of the disturbance but also according to intrinsicbiological factors (Davidson et al 2002) The species that wefound strongly associated with surrounding urban land use (thesmooth newt and the northern spectacled salamander) are verysensitive to altered habitats Accordingly Andreone and Luiselli(2000) ranked these species lsquovirtually inadaptable to alteredenvironmentsrsquo basing their classification on these speciesecological constraints and distribution

Interestingly the probability of amphibian stable populationswas significantly reduced by high agricultural surrounding-landcover (80 of the species) Agricultural practices can produce adetrimental effect on amphibians by producing environmental

contaminants (eg Howe et al 1998 Lips 1998Relyea andMills2001 Boone and Semlitsch 2002 Davidson et al 2002) habitatloss and fragmentation Modern farming practices cause majorimpacts including draining and filling ofwetlands conversion ofnatural habitats into intensively managed annual monoculturessoil compaction and disturbance (Bonin et al 1997 Hecnar1997) Our results showed that in the study area not onlypermanent and intensive farming but also more heterogeneousagricultural areas were associated with declines Interestinglyalthough agricultural variables were a contributing factor thestrongest association with declines was shown only for thenorthern spectacled salamander This result suggests thatagricultural practices may act with other stressors even if theyare not a main driver of population declines For instancesublethal exposures of contaminants as a result of water driftfrom cultivated areas might increase the susceptibility ofamphibians to other stressors such as predation UV-Bradiation pathogens or changes in climate (Pounds 2001Relyea and Mills 2001 Relyea 2003) In addition ashypothesised by DrsquoAmen and Bombi (2009) the highpercentage of agricultural land use may exacerbate the effectof range fragmentation driving populations towards extinction

Human density may have a direct impact on populationsrsquosurvival not only by means of urbanisation but also in moresubtle ways such as overexploitation for food pets medicinaland biological supply markets (Stuart et al 2004) This negativeinfluence is consistent also with our results because the intensityof human activities represented by the HII variable was animportant explanatory power for five species particularly forthe Italian stream frog and the Italian tree frog

The spatial pattern of declinewas consistentwith the influenceof climate change for 6 of 10 species The growing number ofdry days which reflects increasing precipitation variability andaridity was the most important factor related to local decline ofamphibians in central Italy Our findings are congruentwith those of other authors both in Central and North America(Pounds et al 1999 McMenamin et al 2008) Some ecologicaltraits can explain the lack of a significant relationship betweendeclines and climatic predictors for the remaining species Thenorthern spectacled salamander and the Italian stream frog arecharacteristic of forested habitats where they breed in oxygenatelow-running stream which are less influenced by precipitationintensity with respect to other typologies of water bodies Thegreen toad is one of the most adaptable amphibians of thePalearctic and is more tolerant to dry conditions than manyother species (Gasc et al 1997) The Apennine yellow-belliedtoad utilises temporary water bodies in multiple distinct periodsof calling and oviposition that alternate with non-reproductiveactivity (Guarino et al 1998) This reproductive plasticityprobably allows Bombina pachypus populations to use thetemporary pools preferred for breeding thus successfullyovercoming climate fluctuations Our results do not necessarilyimply a directmortality caused by climatic stressors Climatemayproduce well documented synergistic effects with diseases suchas fungal infections or with UV-B radiation (Kiesecker et al2001 Simoncelli et al 2005 Kriger and Hero 2007) It isimportant to note that climatic change is expected to intensifyin the coming decades so that the detrimental effect shown in thepresent paper will worsen which will lead to massive range


contractions especially in the south-west of Europe (Arauacutejo et al2006 IPCC 2007) Therefore it will be particularly importantto account for climate-linked threats to species conservationfor planning long-term management programs of amphibianpopulations

Spatial-scale dependency

The causes of decline illustrated in the present paper are specificto the landscape resolution whereas other processes can behighlighted across a different range of scales (Cushman andMcGarigal 2002) This trend is clearly shown when comparingour results with those obtained for the same species at a coarserresolution (10 km 10 km) and at a larger spatial scale (Italy) byDrsquoAmen andBombi (2009) All but one species (the Italian greenfrog) were associated with landscape predictors at both scalesHowever if we consider separately the effect of artificial andagricultural land cover some discrepancies emerge IndeedDrsquoAmen and Bombi (2009) found fewer declines associatedwith agricultural than urban predictors whereas at the regionalscale we observed an opposite trend In particular only twospecies (the smooth newt and the Apennine yellow-bellied toad)were negatively affected by agriculture at both scales of analysesand three species (the smooth newt the northern spectacledsalamander and the green frog) by urban fabric In contrastthe climatic results are generally in agreement with thecountry-scale research because all species identified asinfluenced by climate variations at the regional level were alsoassociated with at least one climatic variable at the national level

This comparison suggests a scale dependence of differentcategories of disturbance The signal obtained by urban-fabricdisturbance emerges mainly at a large-scale analysis because theurbanisation activities completely eliminate suitable habitats foramphibians thus extirpating entire populations On the otherhand agriculture appears to be the main determinant of speciesdeclines at a finer resolution because it acts locally producinghabitat fragmentation and increasing the risk of populationisolation On the contrary climate change is likely to be a keyfactor at a multiple resolutions Since many facets of the biologyand ecology of amphibians are closely related to temperatureand moisture any modification of the climatic factorsmeasured at a different resolution leads to an alteration of thephenology breeding activity and demography for the moresensitive species (Duellman and Trueb 1994 Angilletta et al2002)

Efficacy of protected areas

We discovered a negative association between species declineand abundance of protected areas only for two species It meansthat the current network of nature reserves in Latium has beeninadequate for safeguarding amphibian populations Thisinefficient protection can be due to conservation strategies thatsafeguard single populations and reproduction sites rather thanlandscapes Because quality of habitat near breeding wetlandsis important to most amphibians it is necessary to considerthe surrounding landscape in protection strategies Effortsconcentrated on narrow terrestrial buffers are likely to beinadequate (Herrmann et al 2005) because wetlandfragmentation and water pollution can affect amphibian

populations inhabiting small protected areas Moreover evenin large and pristine reserves other stressors arise as climaticconditions shift An impressive example is the amphibian declineoccurring in Yellowstone National Park (USA) This park is oneof the best-preserved ecosystems on our planet where specieshave been actively protected longer than anywhere else onEarth In Yellowstone climatic change and in particulardroughts have already disrupted the equilibrium of wetlandecosystem leading to massive disappearances of amphibianpopulation (McMenamin et al 2008) Similarly we canhypothesise that growing arid conditions in Latium greatlydamaged wetland system even if well protected from moredirect human stressors

Conclusions

The status of amphibians warrants greater attention than hasbeen given previously Amphibian populations often occur inrelatively small areas and are more susceptible to extinction as aresult of habitat loss or degradation than are most othervertebrates The protection of breeding sites through smallnatural reserves proved to be inefficient Thus successfulconservation-management plans for this element of the biotarequire landscape restoration coupled with effective ecologicalmonitoringOurfindings are in accordancewith the conclusion ofHoulahan et al (2006) in that wetlands cannot be managed inisolation Neighbouring wetlands and neighbouring land useboth need to be taken into account in land-use planning forconservation

Moreover climatic change is causing substantialmodification to the hydrology land characteristics so thatamphibian populations are being damaged by both habitatloss and other climate-associated mechanisms With respect tothe entire national territory the increasing aridity is one of themain problems in the Latium region because it has the mostevident negative trend in total precipitation with a decrease of10 per century on a yearly basis and 20 and 13 per centuryin spring and summer respectively (Brunetti et al 2006) Thisscenario requires an active commitment for minimising theimpacts on amphibian communities First the prevention ofadditional stress can improve the ability of wetlands torespond to climate change Reducing pollution avoidingvegetation removal and protecting wetland biologicaldiversity and integrity are viable activities to maintain andimprove the resiliency of wetland ecosystems so that theycontinue to provide a suitable habitat for amphibians underchanged climatic conditions (Kusler et al 1999) In somecases however these measures may not be enough In viewof the reduction in precipitation an important element in climate-change adaptation is the need to acquire more water-storagecapacity to buffer adverse effects (Bergkamp andOrlando 1999)At the same time the conservation of a network of ponds withdifferent hydroperiods and possibly avoiding fish introductionshould be an important action for amphibian protection inagricultural landscape (Beja and Alcazar 2003) Linked withthis strategy another adaptation plan can be the prevention ofwetland fragmentation Connectivity between ecosystemsallows migration of species to occur in response to climatechange and therefore the maintenance of migration routesconstitutes a wise approach (Hannah et al 2007)


Acknowledgements

The efforts of many people notably staff and student of the Animal EcologyLaboratory (Dipartimento di Biologia Ambientale Roma Tre University)ensured the completion of the Latiumherpetological database and their effortsare gratefully acknowledged The ideas discussed here have greatly benefitedfrom extensive talks with Pierluigi Bombi This study was funded by theItalian Istituto Superiore per la Prevenzione e la Sicurezza del Lavoro ndash

ISPESL

References

Akaike H (1974) A new look at the statistical model identification IEEETransactions on Automatic Control 19 716ndash723 doi101109TAC19741100705

Alexander M A and Eischeid J K (2001) Climate variability in regionsof amphibian declines Conservation Biology 15 930ndash942doi101046j1523-17392001015004930x

Andreone F and Luiselli L (2000) The Italian batrachofauna and itsconservation status a statistical assessment Biological Conservation96 197ndash208 doi101016S0006-3207(00)00070-7

Angilletta M Niewiarowski P H and Navas C A (2002) The evolutionof thermal physiology in ectotherms Journal of Thermal Biology 27249ndash268

Arauacutejo M B Thuiller W and Pearson R G (2006) Climate warmingand the decline of amphibians and reptiles in Europe Journal ofBiogeography 33 1712ndash1728 doi101111j1365-2699200601482x

Atauri J A and de Lucio J V (2001) The role of landscape structurein species richness distribution of birds amphibians reptiles andlepidopterans in Mediterranean landscapes Landscape Ecology 16147ndash159 doi101023A1011115921050

Beebee T J C (1997) Changes in dewpond numbers and amphibiandiversity over 20 years on chalk downland in Sussex EnglandBiological Conservation 81 215ndash219 doi101016S0006-3207(97)00002-5

Beja P and Alcazar R (2003) Conservation of Mediterranean temporaryponds under agricultural intensification an evaluation using amphibiansBiological Conservation 114 317ndash326 doi101016S0006-3207(03)00051-X

BergkampG andOrlando B (Eds) (1999) lsquoWetlands andClimateChangeExploring Collaboration between the Convention on Wetlands and theUnited Nations Framework Convention on Climate Changersquo (IUCN ndash

The World Conservation Union Washington DC)Blaustein A R and Johnson P T J (2003) The complexity of deformed

amphibians Frontiers in Ecology and the Environment 1 87ndash94doi1018901540-9295(2003)001[0087TCODA]20CO2

Bologna M A Capula M and Carpaneto G M (Eds) (2000) lsquoAnfibi eRettili del Laziorsquo (Fratelli Palombi Editori Roma)

Bonin J DesGranges J L Rodrigue J and Ouellet M (1997)Anuran species richness in agricultural landscapes of Quebecforeseeing long term results of road call surveys In lsquoAmphibians inDecline Canadian Studies of a Global Problemrsquo (Ed D M Green)pp 141ndash149 (Society for the StudyofAmphibians andReptiles St LouisMI)

BooneM D and Semlitsch R D (2002) Interactions of an insecticidewithcompetition and pond drying in amphibian communities EcologicalApplications 12 307ndash316 doi1018901051-0761(2002)012[0307IOAIWC]20CO2

Bosch J Carrascal L M Duraacuten L Walker S and Fisher M C (2007)Climate change and outbreaks of amphibian chytridiomycosis in amontane area of Central Spain is there a link Proceedings of theRoyal Society B Biological Sciences 274 253ndash260

BrownGW Bennett A F and Potts JM (2008) Regional faunal declinendash reptile occurrence in fragmented rural landscapes of south-easternAustralia Wildlife Research 35 8ndash18

BrunettiM (2004) Changes in daily precipitation frequency and distributionin Italy over the last 120 years Journal of Geophysical Research 109D05102 doi1010292003JD004296

Brunetti M Maugeri M Monti F and Nanni T (2006) Temperature andprecipitationvariability in Italy in the last twocenturies fromhomogenisedinstrumental time series International Journal of Climatology 26345ndash381 doi101002joc1251

BurgmanM A Grimson R C and Ferson S (1995) Inferring threat fromscientific collections Conservation Biology 9 923ndash928 doi101046j1523-1739199509040923x

Burnham K P and Anderson D R (Eds) (2002) lsquoModel Selection andMultimodel Inferencersquo (Springer New York)

Carey C and Alexander M A (2003) Climate change and amphibiandeclines is there a link Diversity amp Distributions 9 111ndash121doi101046j1472-4642200300011x

Chadwick E A Slater F M and Ormerod S J (2006) Inter- andintraspecific differences in climatically mediated phenological changein coexisting Triturus species Global Change Biology 12 1069ndash1078doi101111j1365-2486200601156x

Cincotta R P andEngelmanR (2000) lsquoNaturersquos PlaceHumanPopulationDensity and the Future of Biological Diversityrsquo (Population ActionInternational Washington DC)

Corn P S (2005) Climate change and amphibians Animal Biodiversityand Conservation 28 59ndash67

Cushman S A (2006) Effects of habitat loss and fragmentation onamphibians a review and prospectus Biological Conservation 128231ndash240 doi101016jbiocon200509031

Cushman S A and McGarigal K (2002) Hierarchical multi-scaledecomposition of speciesndashenvironment relationships LandscapeEcology 17 637ndash646 doi101023A1021571603605

DrsquoAmen M and Bombi P (2009) Global warming and biodiversityclimate-linked decline of Italian amphibians Biological Conservation142 3060ndash3067 doi101016jbiocon200908004

DrsquoAmen M Salvi D Antoccia A Bombi P Bordoni V Chiesa SGibertini G MarinoM Ruzza A Scalici M Tanzarella C VignoliL andBolognaMA (2008) Studio degli effetti delle emissioni naturalidel gas radon su Triturus carnifex (Amphibia Salamandridae) unapproccio multidisciplinare In lsquoHerpetologia sardiniaersquo (Ed C Corti)pp 180ndash183 (Edizioni Belvedere Latina Italy)

Davidson C and Knapp R A (2007) Multiple stressors andamphibian declines dual impacts of pesticides and fish on yellow-legged frogs Ecological Applications 17 587ndash597 doi10189006-0181

Davidson C Shaffer H B and Jennings M R (2001) Declines of theCalifornia red-legged frog climate UV-B habitat and pesticideshypotheses Ecological Applications 11 464ndash479 doi1018901051-0761(2001)011[0464DOTCRL]20CO2

Davidson C Shaffer H B and Jennings M R (2002) Spatial tests ofthe pesticide drift habitat destruction UV-B and climate-changehypotheses for California amphibian declines Conservation Biology16 1588ndash1601 doi101046j1523-1739200201030x

Delis P R Mushinsky H R and McCoy E D (1996) Decline of somewest-central Florida anuran populations in response to habitatdegradation Biodiversity and Conservation 5 1579ndash1595 doi101007BF00052117

Duellman W E and Trueb L (Eds) (1994) lsquoBiology of Amphibiansrsquo(Johns Hopkins University Press Baltimore MD)

Duffy K J Kingston N E Sayers B A Roberts D L and Stout J C(2009) Inferring national and regional declines of rare orchid specieswithprobabilistic models Conservation Biology 23 184ndash195 doi101111j1523-1739200801064x

Farnsworth E J and Ogurcak D E (2006) Biogeography and decline ofrare plants in New England historical evidence and contemporarymonitoring Ecological Applications 16 1327ndash1337 doi1018901051-0761(2006)016[1327BADORP]20CO2


Gardner T A Barlow J and Peres C A (2007) Paradox presumptionand pitfalls in conservation biology the importance of habitat changefor amphibians and reptiles Biological Conservation 138 166ndash179doi101016jbiocon200704017

Gasc J-P Cabela A Crnobrnja-Isailovic J Dolmen D GrossenbacherK Haffner P Lescure J Martens H Martinez Rica J P Maurin HOliveira M E Sofianidou T S Veith M and Zuiderwijk A (Eds)(1997) lsquoAtlas ofAmphibians andReptiles inEuropersquo (SocietasEuropaeaHerpetologica amp Museum National drsquoHistoire Naturelle Paris)

Gibbons J W Scott D E Ryan T J Buhlmann K A Tuberville T DMetts B S Greene J L Mills T Leiden Y Poppy S and WinneC T (2000) The global decline of reptiles deacutejagrave vu amphibiansBioScience 50 653ndash666

Guarino F M Bellini L Mazzarella G and Angelini F (1998)Reproductive activity of Bombina pachypus from southern ItalyItalian Journal of Zoology 65 335ndash342 doi10108011250009809386770

Gucinski H FurnissM J Ziemer R R and BrookesMH (2001) Forestroads a synthesis of scientific information General technical reportPNW-GTR-509 (USDA Forest Service Pacific Northwest ResearchStation Portland OR)

Hannah L Midgley G Andelman S Arauacutejo M Hughes G Martinez-Meyer E Pearson R andWilliams P (2007) Protected area needs in achanging climateFrontiers in Ecology and the Environment 5 131ndash138doi1018901540-9295(2007)5[131PANIAC]20CO2

Hastie T and Tibshirani R (1986) Generalized additive models StatisticalScience 1 297ndash310 doi101214ss1177013604

Hazell D (2003) Frog ecology in modified Australian landscapes a reviewWildlife Research 30 193ndash205 doi101071WR02075

Hecnar S J (1997) Amphibian pond communities in southwesternOntario In lsquoAmphibians in decline Canadian Studies of a GlobalProblemrsquo Herpetological Conservation Number 1 (Ed D M Green)pp 1ndash15 (Society for the Study of Amphibians and Reptiles St LouisMO)

Herrmann H L Babbitt K J Baber M J and Congalton R G (2005)Effects of landscape characteristics on amphibian distribution in aforest-dominated landscape Biological Conservation 123 139ndash149doi101016jbiocon200405025

Hosmer D W and Lemeshow S (Eds) (1989) lsquoApplied LogisticRegressionrsquo (Wiley Interscience New York)

Howe G E Gillis R and Mowbray R C (1998) Effect of chemicalsynergy and larval stage on the toxicity of atrazine and alachlor toamphibian larvae Environmental Toxicology and Chemistry 17519ndash525 doi101002etc5620170324

Intergovernmental Panel on Climate Change (IPCC) (2007) IPCC Fourthassessment reportWorkingGroup1Report lsquoThePhysicalScienceBasisrsquoAvailable at httpwwwipccchipccreportsar4-wg1htm [verifiedNovember 2010]

IUCN (International Union for the Conservation of Nature) (2008) 2008IUCN Red List of Threatened Species Available at httpwwwiucnredlistorg [accessed November 2008]

Kiesecker J M Blaustein A R and Belden L K (2001) Complex causesof amphibian population declines Nature 410 681ndash684 doi10103835070552

Knapp R A Matthews K R Preisler H K and Jellison R (2003)Developing probabilistic models to predict amphibian site occupancy in apatchy landscape Ecological Applications 13 1069ndash1082 doi1018901051-0761(2003)13[1069DPMTPA]20CO2

KnutsonM G Sauer J R Olsen D AMossmanM J Hemesath LMand Lannoo M J (1999) Effects of landscape composition and wetlandfragmentation on frog and toad abundance and species richnessConservation Biology 13 1437ndash1446 doi101046j1523-1739199998445x

Kriger K M and Hero J M (2007) The chytrid fungus Batrachochytriumdendrobatidis is non-randomly distributed across amphibian breedinghabitats Diversity amp Distributions 13 781ndash788 doi101111j1472-4642200700394x

Kusler J Brinson M Niering W Patterson J Burkett V and WillardD (Eds) (1999) lsquoWetlands and Climate Change Scientific Knowledgeand Management Optionsrsquo (Institute for Wetland Science and PublicPolicy Association of Wetland Managers Berne NY)

Linder G Krest S K and Sparling D W (Eds) (2003) lsquoAmphibianDecline an Integrated Analysis of Multiple Stressor Effectsrsquo (Society ofEnvironmental Toxicology and Chemistry Pensacola FL)

Lips K R (1998) Decline of a tropical mountain amphibian faunaConservation Biology 12 106ndash117 doi101046j1523-1739199896359x

McCarthy M A (1998) Identifying declining and threatened species withmuseum data Biological Conservation 83 9ndash17 doi101016S0006-3207(97)00048-7

McMenamin S K Hadly E A andWright C K (2008) Climatic changeand wetland desiccation cause amphibian decline in YellowstoneNational Park Proceedings of the National Academy of Sciences USA105 16 988ndash16 993 doi101073pnas0809090105

McPherson J M and Jetz W (2007) Effects of speciesrsquo ecology on theaccuracy of distribution models Ecography 30 135ndash151

Menzel A Sparks T H Estrella N Koch E Aasa A Ahas R Alm-Kuumlbler K Bissolli P Braslavskaacute O Briede A Chmielewski F MCrepinsek Z Curnel Y Dahl Aring Defila C Donnelly A Filella YJatczak K Maringge F Mestre A Nordli Oslash Pentildeuelas J Pirinen PRemišovaacute V Scheifinger H Striz M Susnik A Van Vliet A JWielgolaski F Zach S and Zust A (2006) European phenologicalresponse to climate change matches the warming patternGlobal ChangeBiology 12 1969ndash1976 doi101111j1365-2486200601193x

Pounds J A (2001) Climate and amphibian declines Nature 410639ndash640

Pounds J A and Crump M L (1994) Amphibian decline and climatedisturbance the case of the golden toad and the harlequin frogConservation Biology 8 72ndash85 doi101046j1523-1739199408010072x

Pounds J A Fogden M P L and Campbell J H (1999) Biologicalresponse to climate change on a tropical mountainNature 398 611ndash615doi10103819297

Pounds J A Bustamante M R Coloma L A Consuegra J A FogdenM P L Foster P N La Marca E Masters K L Merino-Viteri APuschendorf R Ron S R Saacutenchez-Azofeifa A G Still C J andYoung B E (2006) Widespread amphibian extinctions from epidemicdisease driven by global warming Nature 439 161ndash167 doi101038nature04246

Randa L A and Yunger J A (2006) Carnivore occurrence along anurbanndashrural gradient a landscape-level analysis Journal of Mammalogy87 1154ndash1164 doi10164405-MAMM-A-224R21

Reading C J (1998) The effect of winter temperatures on the timing ofbreeding activity in the common toad Bufo bufo Oecologia 117469ndash475 doi101007s004420050682

Relyea R A (2003) Predator cues and pesticides a double dose of dangerfor amphibians Ecological Applications 13 1515ndash1521 doi10189002-5298

Relyea R A and Mills N (2001) Predator-induced stress makesthe pesticide carbaryl more deadly to grey treefrog tadpoles(Hyla versicolor) Proceedings of the National Academy of Sciencesof the United States of America 98 2491ndash2496 doi101073pnas031076198

RivadeneiraMMHuntG andRoyK (2009) The use of sighting recordsto infer species extinctions an evaluation of different methods Ecology90 1291ndash1300 doi10189008-03161


Ron S R Duellman W E Coloma L A and Bustamante M R (2003)Population decline of the jambato toad Atelopus ignescens (AnuraBufonidae) in the Andes of Ecuador Journal of Herpetology 37116ndash126 doi1016700022-1511(2003)037[0116PDOTJT]20CO2

Sala O E Chapin F S I Armesto J J Berlow E Bloomfield J DirzoR Huber-Sanwald E Huenneke L F Jackson R B Kinzig ALeemans R Lodge D M Mooney H A Oesterheld M Poff N LSykes M T Walker B H Walker M and Wall D H (2000) Globalbiodiversity scenarios for the year 2100 Science 287 1770ndash1774

Sanderson E W Jaiteh M Levy M A Redford K H Wannebo A Vand Woolmer G (2002) The human footprint and the last of the wildBioscience 52 891ndash904 doi1016410006-3568(2002)052[0891THFATL]20CO2

Semlitsch R D (2000) Principles for management of aquatic breedingamphibians The Journal of Wildlife Management 64 615ndash631doi1023073802732

Sih A Bell M A and Kerby J L (2004) Two stressors are far deadlierthan oneTrends in EcologyampEvolution 19 274ndash276 doi101016jtree200402010

Simoncelli F Fagotti A DallrsquoOlio R Vagnetti D Pascolini R and DiRosa I (2005) Evidence of Batrachochytrium dendrobatidis infectionin water frogs of the Rana esculenta complex in central Italy EcoHealth2 307ndash312 doi101007s10393-005-8337-8

Solow A R (1993a) Inferring extinction from sighting data Ecology 74962ndash964 doi1023071940821

Solow A R (1993b) Inferring extinction in a declining population Journalof Mathematical Biology 32 79ndash82 doi101007BF00160376

Solow A R (2005) Inferring extinction from a sighting record Mathe-matical Biosciences 195 47ndash55 doi101016jmbs200502001

Solow A R and Roberts D L (2003) A nonparametric test for extinctionbased on a sighting record Ecology 84 1329ndash1332 doi1018900012-9658(2003)084[1329ANTFEB]20CO2

Stewart M M (1995) Climate driven population fluctuations in rain forestfrogs Journal of Herpetology 29 437ndash446 doi1023071564995

Stuart S Chanson J S Cox N A Young B E Rodrigues A S LFishman D L andWaller RW (2004) Status and trends of amphibiandeclines and extinctions worldwide Science 306 1783ndash1786doi101126science1103538

Temple H J and Cox N A (Eds) (2009) lsquoEuropean Red List ofAmphibiansrsquo (Office for Official Publications of the EuropeanCommunities Luxembourg)

Toreti A and Desiato F (2008) Temperature trend over Italy from 1961 to2004 Theoretical and Applied Climatology 91 51ndash58 doi101007s00704-006-0289-6

van Der Ree R and McCarthy M A (2005) Inferring persistence ofindigenous mammals in response to urbanisation Animal Conservation8 309ndash319 doi101017S1367943005002258

Vitousek P M (1997) Human domination of Earthrsquos ecosystems Science277 494ndash499 doi101126science2775325494

Wake D B and Vredenburg V T (2008) Are we in the midst of the sixthmass extinction A view from the world of amphibians Proceedings oftheNationalAcademyof SciencesUSA105 11 466ndash11 473 doi101073pnas0801921105

YoungBE LipsKRReaser JK IbaacutentildeezR SalasAWCedentildeo JRColoma L A Ron S La Marca E Meyer J R Muntildeoz A BolantildeosF Chaves G and Romo D (2001) Population declines and prioritiesfor amphibian conservation in Latin America Conservation Biology 151213ndash1223 doi101046j1523-1739200100218x

Manuscript received 2 December 2009 accepted 16 September 2010


httpwwwpublishcsiroaujournalswr

they are extremely vulnerable to the effects of reductions inannual precipitation and change in seasonality (Carey andAlexander 2003 Chadwick et al 2006) Moreover the timingof the seasonal activities of hibernation aestivation andreproduction are tightly related to temperature conditions (egReading 1998) Several climatological studies described apositive trend for mean temperature a reduction in the numberofwet days and an increase in precipitation intensity all over Italyduring the last century (eg Brunetti 2004 2006 Toreti andDesiato 2008) These climatic trends occurred mainly in the past50 years and were associated with broad-scale amphibiandeclines (DrsquoAmen and Bombi 2009)

The main goal of the present research was to understand theconsequences of human land-use disturbances for differentamphibian species in a Mediterranean area in central ItalyAnother goal was to assess whether species declines arerelated to the climatic shifts that have occurred in Italy inrecent decades by considering climatic variables that haveinfluenced amphibian persistence (DrsquoAmen and Bombi 2009)A further goal of our analysis was to determine whether and to

what extent the existing protected areas have been effective forspecies protection in recent decades Indeed although protectedecosystem areas inhibit habitat destruction and direct humandisturbance they can be less adequate for protecting speciesfrom other stressors such as chemical pollution and above allclimatic-shift conditions

To achieve these goals we began by examining changes inspecies abundance at the regional scale and then we devised aspatial approach based on the identification of the spatial effectsof environmental alterations in determining the geographicpatterns of declines observed in recent decades (Davidsonet al 2002 DrsquoAmen and Bombi 2009) This analysis isrelevant because no efficient conservation measures can beplanned if there is an incomplete understanding of the causesleading to declines

Materials and methodsSpecies data

We utilised presence data of 10 species of amphibians in Latiumcentral Italy (data source used by Bologna et al 2000) (Fig 1)

Fig 1 Study region with the grey grid indicating amphibian presence cells utilised for statisticalanalyses



Environmental data


















p frac14 tn tn1

T tn1





Results






No of totalsquares

Rate ofdecline ()



Tab

le3

General

Add

itiveMod

elresultsshow

ingthefina

lmod

elAIC

valuean

dsign

ificant

variab

lesselected

withtheirrelative

impo

rtan

ceDA

ICresults

wheneach

predictorisremoved

from

thefinalm

odelD

AIC

indicateseach


eim

portance

inthemodelD

AIC

ofthemostimportantp

redictor

foreach

speciesisshow

nin

bold

Species

Final-m

odel

|DAIC|

AIC

URB

ICT

STR

ARTVEG

ARA

PCRO

PAS

HETAGR

CLCVAR

HII

TVAR

PVAR

DD

VAR

PA

Lissotrito

nvulgaris

13810

425

193

161

019

Ranaita

lica

8519

589

285

600

Trituruscarnifex

10803

177

641

Bufobu

fo15

942

409

309

309

722


ta54

14

543

634

481

1335

053

Bom

bina

pachypus

4764

326

144

Bufoviridiscomplex

3413

000

Phelophylax

spp

13524

255

715

1162

1905

Ranada

lmatina

2611

686

1520

654

Hylainterm

edia

4734

366

060

1648

773







Discussion





Rana italica

Triturus carnifex

Bufo bufo


Bombina pachypus


Phelophylax spp

Rana dalmatina

Hyla intermedia

0

1

2

3

4

5

20 22 24 26 28 30 32 34 36 38 40 42 44 46

Rate of decline

Num

ber

of s

igni

fican

t pre

dict

ors


















Conclusions




Acknowledgements


ISPESL

References






























































































Environmental data


















p frac14 tn tn1

T tn1





Results






No of totalsquares

Rate ofdecline ()



Tab

le3

General

Add

itiveMod

elresultsshow

ingthefina

lmod

elAIC

valuean

dsign

ificant

variab

lesselected

withtheirrelative

impo

rtan

ceDA

ICresults

wheneach

predictorisremoved

from

thefinalm

odelD

AIC

indicateseach


eim

portance

inthemodelD

AIC

ofthemostimportantp

redictor

foreach

speciesisshow

nin

bold

Species

Final-m

odel

|DAIC|

AIC

URB

ICT

STR

ARTVEG

ARA

PCRO

PAS

HETAGR

CLCVAR

HII

TVAR

PVAR

DD

VAR

PA

Lissotrito

nvulgaris

13810

425

193

161

019

Ranaita

lica

8519

589

285

600

Trituruscarnifex

10803

177

641

Bufobu

fo15

942

409

309

309

722


ta54

14

543

634

481

1335

053

Bom

bina

pachypus

4764

326

144

Bufoviridiscomplex

3413

000

Phelophylax

spp

13524

255

715

1162

1905

Ranada

lmatina

2611

686

1520

654

Hylainterm

edia

4734

366

060

1648

773







Discussion





Rana italica

Triturus carnifex

Bufo bufo


Bombina pachypus


Phelophylax spp

Rana dalmatina

Hyla intermedia

0

1

2

3

4

5

20 22 24 26 28 30 32 34 36 38 40 42 44 46

Rate of decline

Num

ber

of s

igni

fican

t pre

dict

ors


















Conclusions




Acknowledgements


ISPESL

References






























































































p frac14 tn tn1

T tn1





Results






No of totalsquares

Rate ofdecline ()



Tab

le3

General

Add

itiveMod

elresultsshow

ingthefina

lmod

elAIC

valuean

dsign

ificant

variab

lesselected

withtheirrelative

impo

rtan

ceDA

ICresults

wheneach

predictorisremoved

from

thefinalm

odelD

AIC

indicateseach


eim

portance

inthemodelD

AIC

ofthemostimportantp

redictor

foreach

speciesisshow

nin

bold

Species

Final-m

odel

|DAIC|

AIC

URB

ICT

STR

ARTVEG

ARA

PCRO

PAS

HETAGR

CLCVAR

HII

TVAR

PVAR

DD

VAR

PA

Lissotrito

nvulgaris

13810

425

193

161

019

Ranaita

lica

8519

589

285

600

Trituruscarnifex

10803

177

641

Bufobu

fo15

942

409

309

309

722


ta54

14

543

634

481

1335

053

Bom

bina

pachypus

4764

326

144

Bufoviridiscomplex

3413

000

Phelophylax

spp

13524

255

715

1162

1905

Ranada

lmatina

2611

686

1520

654

Hylainterm

edia

4734

366

060

1648

773







Discussion





Rana italica

Triturus carnifex

Bufo bufo


Bombina pachypus


Phelophylax spp

Rana dalmatina

Hyla intermedia

0

1

2

3

4

5

20 22 24 26 28 30 32 34 36 38 40 42 44 46

Rate of decline

Num

ber

of s

igni

fican

t pre

dict

ors


















Conclusions




Acknowledgements


ISPESL

References





























































































Tab

le3

General

Add

itiveMod

elresultsshow

ingthefina

lmod

elAIC

valuean

dsign

ificant

variab

lesselected

withtheirrelative

impo

rtan

ceDA

ICresults

wheneach

predictorisremoved

from

thefinalm

odelD

AIC

indicateseach


eim

portance

inthemodelD

AIC

ofthemostimportantp

redictor

foreach

speciesisshow

nin

bold

Species

Final-m

odel

|DAIC|

AIC

URB

ICT

STR

ARTVEG

ARA

PCRO

PAS

HETAGR

CLCVAR

HII

TVAR

PVAR

DD

VAR

PA

Lissotrito

nvulgaris

13810

425

193

161

019

Ranaita

lica

8519

589

285

600

Trituruscarnifex

10803

177

641

Bufobu

fo15

942

409

309

309

722


ta54

14

543

634

481

1335

053

Bom

bina

pachypus

4764

326

144

Bufoviridiscomplex

3413

000

Phelophylax

spp

13524

255

715

1162

1905

Ranada

lmatina

2611

686

1520

654

Hylainterm

edia

4734

366

060

1648

773







Discussion





Rana italica

Triturus carnifex

Bufo bufo


Bombina pachypus


Phelophylax spp

Rana dalmatina

Hyla intermedia

0

1

2

3

4

5

20 22 24 26 28 30 32 34 36 38 40 42 44 46

Rate of decline

Num

ber

of s

igni

fican

t pre

dict

ors


















Conclusions




Acknowledgements


ISPESL

References


































































































Discussion





Rana italica

Triturus carnifex

Bufo bufo


Bombina pachypus


Phelophylax spp

Rana dalmatina

Hyla intermedia

0

1

2

3

4

5

20 22 24 26 28 30 32 34 36 38 40 42 44 46

Rate of decline

Num

ber

of s

igni

fican

t pre

dict

ors


















Conclusions




Acknowledgements


ISPESL

References












































































































Conclusions




Acknowledgements


ISPESL

References





























































































Acknowledgements


ISPESL

References





























































































Human-provoked amphibian decline in central Italy and the efficacy of protected areas

Documents

Transcript of Human-provoked amphibian decline in central Italy and the efficacy of protected areas