lable at ScienceDirect

Acta Oecologica 37 (2011) 422e432

Contents lists avai

Acta Oecologica

journal homepage: www.elsevier .com/locate/actoec

Original article

Food webs of a sandy beach macroinvertebrate community using stableisotopes analysis

Isabella Colombini a, Mauro Brilli b, Mario Fallaci a, Elena Gagnarli a, Lorenzo Chelazzi a,*a Istituto per lo Studio degli Ecosistemi, CNR, Via Madonna del Piano 10, 50019 Sesto Fiorentino, Florence, Italyb Istituto di Geologia Ambientale e Geoingegneria, CNR, Via Salaria km 29.300, B.O. 10, 00016 Monterotondo Stazione, Rome, Italy

a r t i c l e i n f o

Article history:Received 4 March 2010Accepted 20 May 2011Available online 20 June 2011

Keywords:Mediterranean coastal ecosystemTerrestrial macroinvertebratesFood websSource partitioningStable isotopes

* Corresponding author. Tel.: þ39 055 2288297; faE-mail address: chelazzi@ise.cnr.it (L. Chelazzi).

1146-609X/$ e see front matter � 2011 Elsevier Masdoi:10.1016/j.actao.2011.05.010

a b s t r a c t

The study examines the food webs of macroinvertebrates along a gradient from the sandy shore to a duneslack in the retrodune. The study was conducted at the Maremma Regional Park in an area subjected tobeach progradation. Transects with pitfall traps were set perpendicular to the sea to capture macro-invertebrates, whereas vegetation biomass was evaluated using quadrats. Marine allochthonous materialwas also examined. Stable isotopes of d13C and d15N were analysed both in plants and macroinvertebratesof marine and terrestrial origins. Hierarchical cluster analysis was used to group species with similarvalues.Multi-sourcemixingmodelswere used to analyse the contribution of carbon ofmarine origin to thediets, to calculate trophic levels and to estimate the diets of certain species. The results indicate a decreasein the contribution of marine carbon in the diets of terrestrial macroinvertebrates along the seaeland axis.

� 2011 Elsevier Masson SAS. All rights reserved.

1. Introduction

Food web dynamics in near-shore terrestrial habitat arecommonly influenced by flows of energy and biomass from the sea.The availability of marine resources is often associated to changesin distribution, abundances or growth of populations at almostevery trophic level including herbivores, scavengers, intermediateand top predators of invertebrate and vertebrate species (Polis andHurd, 1995, 1996a,b; Rose and Polis, 1998; Colombini and Chelazzi,2003; Dugan et al., 2003; Barrett et al., 2005; Marczak et al., 2007).These allochthonous inputs can change food webs in recipienthabitats through arrays of interactions affecting food web stabilityaccording to which trophic position subsidies enter a food web(Huxel et al., 2002; Anderson and Polis, 2004) or affecting themagnitude of a species response to subsidies (Polis et al., 1997).Along the coastal ecotone the majority of studies have focused ondonor habitats of high productivity subsidizing very unproductiverecipient habitats and much work was carried out on desert islandsin the Gulf of California or along the hyper-arid Peruvian coastlinesjuxtaposed with very productive ocean waters (Polis and Hurd,1996a; Stapp and Polis, 2003; Wait et al., 2005; Catenazzi andDonnelly, 2007a). In another recent paper on marine-terrestrialresource flows Paetzold et al. (2008) analysed a forest island,where terrestrial primary productivity was comparable to that

x: þ39 055 2288299.

son SAS. All rights reserved.

found in the surrounding marine ecosystem. The study concludedthat marine subsidies in the form of stranded wrack were lessimportant for recipient terrestrial consumers and were mainlyconfined to intertidal specialist consumers and mobile consumersthat opportunistically forage in intertidal habitats.

Sandy beaches have very little in situ primary production(McLachlan and Brown, 2006) and stranding of shore drift(detached seagrass, macroalgae and carrion) represents the mainconduit ofmarine subsidies to the terrestrial environment (Koepckeand Koepcke, 1952; Kirkman and Kendrick, 1997; Colombini andChelazzi, 2003). These accumulations support the food chainstarting from primary consumers, mainly scavengers and detri-tivores (Inglis, 1989), which attract predators, such as carnivorousbeetles, spiders and scorpions (Anderson and Polis, 1998) and inturn may be preyed upon by vertebrate species, such as lizards,birds and rodents (Polis and Hurd, 1996b; Polis et al., 1997; Castillaet al., 2008).

In the last few years there has been a growing interest inelucidating trophic pathways of sandy beach ecosystems with theuse of stable isotopes of carbon and nitrogen. This technique takesinto account assimilated food and may be used to assess thenumber of trophic levels a system supports (Hesslein et al., 1991).Recently, Schlacher and Connolly (2009) documented how sandybeach consumers of intertidal areas could be linked to terrestrialcarbon delivered by river plumes whereas Bergamino et al. (2011)elucidated how morphodynamic factors could explain the con-trasting differences in food web structure. Some studies on sandybeaches (Barrett et al., 2005; Catenazzi and Donnelly, 2007a)

I. Colombini et al. / Acta Oecologica 37 (2011) 422e432 423

identified how marine subsidies contribute to support lizard pop-ulations, while others showed that marine macrophytes areintrinsically linked to the food web of terrestrial beach inverte-brates (Adin and Riera, 2003; Ince et al., 2007; Catenazzi andDonnelly, 2007a,b; Paetzold et al., 2008). However, all thesestudies have analysed invertebrates directly associated to thewrackdeposits but very little is known about the trophic pathway ofarthropod communities inhabiting the beach-dune system and towhat extent inland terrestrial arthropods derive energy frommarine subsidies. Ince et al. (2007) hinted that both marine andterrestrial-derived vegetation entered the food web of amphipodsand dipteran flies but in this case only few dune plant species andmarine macrophytes were analysed. Another tentative approach ofanalysing both plant and invertebrate species of a beach-duneecosystem was made by Colombini et al. (2009) but again onlya few species had been considered.

At our study site Colombini et al. (2006) had previouslyevidenced a very dynamic environment with higher invertebratediversity values than adjacent areas and the presence of differenthabitats (beach, dune, dune slack) in a small spatial scale (150m). Inthe present study we examined the terrestrial macroinvertebratecommunity along a gradient from the shore to a dune slack withsalt marsh characteristics. Our aim was to assess trophic pathwaysof the most abundant macroinvertebrates using stable isotoperatios of carbon (d13C) and nitrogen (d15N) and to evaluate therelative contribution of marine vs. terrestrial sources of energy forconsumers. Trophic levels of major guilds were also calculated.Furthermore, our major question was: to what degree do majorguilds of the most abundant terrestrial arthropods derive energyfrom marine inputs in the form of stranded shore wrack and howfar do marine resources penetrate the beach-dune system?

2. Materials and methods

2.1. Study site

The study was carried out on a sandy beach and associated dunesystem6 km south of theOmbrone river (42�37052.80 0 N,11�04042.300

E) in theMaremma Regional Park (Grosseto, Italy) (Fig.1). This beachwas highly instable because of a severe erosion near the rivermouthand a pronounced accretion in its southern section (Colombini et al.,

Fig. 1. Geographic location of the study site with a line transect showing the differentareas according to the vegetation cover.

2006). Consequently beach width increased and dune heightsdecreased proceeding southwards from the rivermouth.Weworkedon an exposed beach (Marques et al., 2003) with a wide, flat aphytaleu- and supralittoral (40 m in width), a low dune (1.10 m in height)covered by halo-psammophilous vegetation and a dune slack, a lowlying depression between the first and second dune belt charac-terised by a typical salt marsh vegetation and flooded by the seaduring severe winter storms.

2.2. Sampling procedures

Seasonal sampling was carried in four months (October 2006,January, April, July 2007). Two transects, at a 25 m distance, wereset perpendicularly to the shoreline and proceeded landwardsfor 150 m to the backdune up to the pinewood vegetation. Thetransects consisted of pitfall cross traps set at a 5 m interval thatcaptured macroinvertebrates freely moving at the surface. Faunasamples were collected, counted and identified to species level.

We sampled above-ground vegetation in the different seasonsby clipping and removing vegetation in quadrats (50 � 50 cm)located externally from the two transects at 1 m (October), 2 m(January), 3 m (April) and 4 m (July) distance from the pitfall traps.Plants were identified to species level and weighed after ovendrying at 70 �C until constant weight. Mean plant biomass,expressed in kg m�2, was calculated pooling data from quadratssampled from 35 m to 90 m (dune) and from 95 m to 150 m (wetdune slack).

Beach wracks was mainly composed of rhizomes of the marineangiosperm Cymodocea nodosa due to the presence of a conspic-uous seagrass meadow at 4e10m of depth in front of the study area(Bianchi et al., 1993). Deposits of Posidonia oceanica and/or red,brown and greenmacroalgaewere, instead, sporadic or quite scarceall year long. To determine seagrass deposits monthly samples weretaken along 5 transects set perpendicular to the shoreline andalways in the same spots. These consisted of strips of sand (2 m inwidth and at a 10 m interval) ranging from the sealine limits to thefirst pioneer plants (about 40 m inland) within which seagrass wascollected at the sand surface andweighed after oven drying at 70 �Cuntil constant weight.

2.3. Collection and preparation for stable isotope analysis

During autumn 2006 the majority of terrestrial macro-invertebrate species was collected from the pitfall traps for stableisotope ratios determination. To obtain a rich inventory of the mostabundant (n > 10) or most representative species inhabitingthe study site, in the successive seasons more samples were takento include species with different life cycles. Furthermore, otherspecies were collected from the vegetation using hand nets or byactive search. For crustacean species the isotopic ratios of bothadults and juveniles were determined. For amphipods the twoclasses were chosen according to the number of articles of thesecond antennal flagellum (juveniles < 10 articles and adults > 20articles), whereas for isopods according to the maximum width ofthe 4th pereionit (juveniles < 3 mm and adults > 5 mm). Weexcluded the intermediate classes because the aim was to assessclear differences in the diets between adults and juveniles. Onlyfor some insect species (Eurynebria complanata, Parallelomorphuslaevigatus, Phytosus nigriventris, Isidus moreli, Pimelia bipunctata,Phaleria provincialis) both the preimaginal and adult stages wereexamined because both occurred in the samples. In other cases onlythe larval stage was analysed because adults were never found(Acanthaclisis baetica) or never identified (Diptera gen. sp.). Threeintertidal species (the mollusc Donax trunculus, the polychaetaOphelia radiata and the isopod Eurydice affinis) were sampled to

I. Colombini et al. / Acta Oecologica 37 (2011) 422e432424

assess the possibility of marine components entering the terrestrialfood web. These three species were chosen because they were themost abundant intertidal species in this section of the beach(Chaouti et al., 2006). Only soft tissues were used. All individualswere kept alive for 24 h to allow evacuation of gut contents andthen were frozen at �20 �C.

Among the resident vertebrate species we sampled the Italianwall lizard (Podarcis sicula) and the lesser white-toothed shrew(Crocidura suaveolens) with pitfall traps. After using ice spray asa local anaesthetic the tail apex (5 mm) of five lizards was clippedand frozen at �20 �C. Lizards were released after medication withantibiotics. Shrews were captured and fur samples were taken toavoid sacrificing animals. All samples were then oven dried at 70 �Cuntil constant weight and stored.

Samples of the most abundant vegetation of the dune and of thedune slack were taken to assess the terrestrial source of primaryproductivity that entered the foodweb. Leaves from five individualsof each species of vascular plants were used for isotopic analysis.Plants, such as Sporobolus pungens and Inula crithmoides, witha wide distribution pattern along the sea-dune transects weresampled in two places, on the dune and in the dune slack (wherea higher soil conductivity occurred, unpublished data) and indi-viduals were pooled in two groups according to their distance fromthe sea.

We sampled fresh leaves of stranded marine seagrasses(C. nodosa, P. oceanica) and thalli of macroalgae (Ulva lactuca, redand brown algae). To eliminate epiphytes from seagrasses leaveswere gently scraped.

Seston was collected superficially in the surf zone witha plancton net (mesh size 200 mm), running parallel to the shore ata distance of about 50 m from the shoreline, whereas diatoms weregathered stranded on the beach as foam deposits. All material wasimmediately frozen.

Surface sediment samples (up to 10 cm in depth) were collectedat 10 m, 30 m, 50 m, 70 m, 90 m, 110 m, 130 m, 150 m from theshoreline. The sand was dried and sieved with an automatic shakerusing 63 mm sieves to separate sand grains from most of thesediment organic matter (SOM).

Faeces of cattle, fallow deers and sea gulls were also sampled toassess other sources of organic matter. During winter season theareawas heavily used by cattle, whereas during nocturnal hours thesite was a feeding ground for fallow deers. The beach was used asoccasional sleeping grounds by several hundred sea gulls.

Prior to isotopic analysis all samples were dried at 70 �C untilconstant weight and stored in a dry, dark environment.

For each macroinvertebrate and plant species, 5 individuals(where possible) were separately ground with mortar and pestleand two replicates were made from each individual. For isotopicdetermination an aliquot of ca. 0.3 mg were used for animal andseston, 1 mg for plant and algae and 3e4 mg for SOM samples. Weeliminated carbonates by acidification prior to isotopic analysis formarine macrophytes and animals, intertidal crustacean species andSOM (Mateo et al., 2008; Serrano et al., 2008). Acidification con-sisted of the addition of 1-M HCl drop-by-drop and left in acid for3 h to eliminate possible traces of carbonates (Carabel et al., 2006).Non-acidified aliquots were used for d15N determination. Subsam-ples were then individually oxidised in a Carlo Erba 1110 elementalanalyser (Carlo Erba Instruments, Milan, Italy) coupled to a FinniganDelta Plus mass spectrometer. Isotope ratios were expressed usingthe standard delta notation (d13C, d15N) in per mil (&) differencesfrom a standard: dsample ¼ [(Rsample/Rstandard) � 1] � 1000,R ¼ 13C/12C, or R ¼ 15N/14N. The d values reflected the ratio of heavyand light isotopes in the samples comparedwith standard referencematerials, namely Vienna PeeDee Belemnite (PDB) carbonate andatmospheric air nitrogen.

2.4. Data analysis

A mean zonation was calculated for spontaneously active indi-viduals of each macroinvertebrate species considered. This wasobtained by calculating the distance in metres from the sealinelimit (0 m) of each individual found in the different pitfall traps ofthe two line transects. For plant species the mean zonation wascalculated on a presence/absence basis. To detect how d13C andd15N values changed according to their distance from the seaa regression analysis was performed between the isotopic signa-tures of macroinvertebrates or plants and their mean zonation.

A hierarchical cluster analysis using Ward’s method and theEuclidean distance was accomplished on stable isotopic carbon andnitrogen ratio values of plants, macroinvertebrates and allochthonousitems in order to identify groups. For each group the mean values ofd13C and d15Nwere assessed and aHotelling’s confidence ellipse of thetwo means (Batschelet, 1981) was calculated at a 95% level of proba-bility. A mean zonation was calculated for each group and a one-wayanalysis of variance, followed by a Tukey HSD test, was performed.

To estimate how far inlandmarine-derived elements enter in thefood web the proportion of marine diet calculated for each specieswas plotted against their mean zonation pattern. The proportion ofeach primary source was calculated with the source-partitioningmixing model (Phillips and Gregg, 2003; Phillips et al., 2005)using IsoSource software (www.epa.gov/wed/pages/models.htm).In our study five sources were chosen and the following system ofmass balance equations were solved to determine the proportions(fA, fB, fC, fD, fE) of source isotopic signatures (dA, dB, dC, dD, dE) whichcoincide with the observed signature for the mixture (dM):

dM ¼ fAdA þ fBdB þ fCdC þ fDdD þ fEdE

1 ¼ fA þ fB þ fC þ fD þ fE

Three basal sources were chosen for marine-derived elements:seagull faeces, marine seagrasses (calculating a mean value of theisotopic signature of C. nodosa and P. oceanica) and other marineorganisms (using a mean value for algae and marine macro-invertebrates), whereas for terrestrial primary producers two basalsources were used: terrestrial plants (calculating amean value of allspecies) and sediment organic matter (calculating a mean value).

As d15N values provide an indication of the trophic position ofa consumer, the following formula (Lubetkin and Simenstad, 2004)was used to estimate the trophic enrichment and level of eachmacroinvertebrate species.

For trophic enrichment

1 ¼ f1 þ f2 þ f3 þ f4 þ f5

a ¼ Ct � ðf1t1 þ f2t2 þ f3t3 þ f4t4 þ f5t5Þwhere a is the trophic enrichment, Ct is the tracer value (d13C ord15N) of the species, t1s are the tracer values of each food source andf1s are the fractions that t1s are the tracer values each potentialfoods contribute to the consumer’s diet.

For trophic level

L ¼ f1L1 þ f2L2 þ f3L3 þ f4L4 þ f5L5 þ 1

where f1s are the fractions each food contributes to the consumer’sdiet, the L1s are the trophic levels of those foods and L is the trophiclevel of the species of interest.

Basal sourceswere: seagull faeces (assumed trophic position, a.t.p.,L1 ¼ 4), marine seagrasses (a.t.p. L2 ¼ 1), marine organisms (includingalgae, marine invertebrates and seston, a.t.p. L3 ¼ 1.4), terrestrialplants (a.t.p. L4 ¼ 1) and sediment organic matter (a.t.p. L5 ¼ 1).

I. Colombini et al. / Acta Oecologica 37 (2011) 422e432 425

To identify the relative contribution of each food sources to thegroups of species obtained with cluster analysis multi-source mix-ing models (Phillips and Gregg, 2003) were used. Basal resources ofconsumers were selected according to trophic guilds, field obser-vations and to their distance from the sea. For predators (a model)both terrestrial and marine macroinvertebrates were identifiedas basal sources using cluster analysis. For primary consumers(b model) sources were: seagrasses, algae and plants; whereas forscavenger species (g model) sources were: plants, seagrasses,stranded marine organisms & seagull faeces and SOM & terrestrialvertebrate faeces. These were then corrected for discriminatingfactors of 0.39& for d13C and of 3.4& for d15N (Post, 2002).

3. Results

3.1. Energy sources of the ecosystem

Stranding of the seagrass C. nodosa represented the mainconduit of marine subsidies. During the sampling period beach

Table 1Mean isotopic signatures of plants, two vertebrate species and other itemswith standard enumbers (n) and mean zonations or actual distances (m ¼metres from the shoreline). a ¼

Species P d13C d15N n m

Mean S.E. Mean S.E.

PlantsCupressaceaeJuniperus oxycedrus 3 �28.3 0.2 �5.9 0.6 5 102

AmaryllidaceaePancratium maritimum 3 �29.7 0.2 �2.8 0.4 5 70

PoaceaeAmmophila arenaria 2 �28.0 0.4 �1.7 0.4 5 63Elymus farctus 3 �28.0 0.5 �3.0 0.5 5 64Erianthus ravennae 1 �13.2 0.1 �2.8 0.3 5 137Sporobolus pungens 1 �14.4 0.3 0.2 0.5 5 45Sporobolus pungens 1 �14.0 0.3 �4.1 0.5 5 123

CyperaceaeSchoenus nigricans 2 �29.0 0.5 �1.3 0.4 5 122

JuncaceaeJuncus acutus (stem) 2 �26.1 0.3 �1.0 1.0 5 122Juncus acutus (leaf) 3 �27.3 0.6 �4.4 0.3 5 122

AmaranthaceaeSalicornia fruticosa 2 �26.6 0.3 0.6 0.4 5 123Salsola kali 1 �13.7 0.1 0.7 0.9 5 55

CaryophyllaceaeSilene colorata 3 �29.4 0.3 �2.8 0.4 5 78

PlumbaginaceaeLimonium etruscum 2 �28.8 0.4 1.2 0.5 5 106

EuphorbiaceaeEuphorbia paralias 3 �27.5 0.4 �2.8 0.5 5 57Euphorbia peplis 1 �14.1 0.2 �4.3 0.6 5 60

FabaceaeMedicago litoralis 3 �29.6 0.3 �2.9 0.1 5 85Ononis variegata 3 �30.3 0.2 �3.0 0.2 5 75

BrassicaceaeCakile maritima 2 �30.7 0.5 1.1 0.6 5 40

EricaceaeErica multiflora 3 �27.4 0.4 �8.3 0.2 5 145

GentianaceaeBlackstonia perfoliata 3 �27.8 0.3 �3.2 0.2 5 107

PlantaginaceaePlantago coronopus 3 �30.7 0.5 �3.0 0.6 5 123

ApiaceaeEchinophora spinosa 3 �28.6 0.4 �4.9 0.3 5 50Pseudorlaya pumila 2 �30.0 0.2 �1.2 0.4 5 72

AsteraceaeAnthemis maritima 3 �32.7 0.4 �6.1 0.5 5 68Dittrichia viscosa 2 �29.7 0.4 �1.3 0.2 5 125Helichrysum stoechas 3 �29.4 0.4 �3.3 0.6 5 85Inula crithmoides 2 �28.8 0.2 �1.2 0.3 5 50Inula crithmoides 3 �27.1 0.9 �3.9 0.3 5 125Xanthium italicum 2 �27.0 0.5 �2.0 0.3 5 62

stranding of C. nodosa was not constant through time (Kolmogor-oveSmirnov test: Z ¼ 1.871 P < 0.01) and reached its highest levelin February and March (0.12 and 0.13 dw kg m�2). An overall valueof 0.452 dw kg m�2 y�1 was calculated for seagrass stranding ina one year period of time.

A total of 40 species of terrestrial plants were identified. Thesewere represented by pioneer plants occurring in the foredune andin the dune (Table 1). Between 35 m and 90 m, a mean plantbiomass of 0.21 dw kg m�2 was calculated during the entiresampling period. In the dune slack, between 95 and 150 m, a valueof 0.98 dw kg m�2 was obtained.

3.2. Stable isotope analysis

Among terrestrial plants (Table 1) d13C values rangedfrom �32.7& (Anthemis maritima) to �13.2& (Erianthus ravennae),whereas d15N values from �8.3& (Erica multiflora) to 1.2& (Limo-nium etruscum). Among the terrestrial macroinvertebrates (Table 2)Tachyporus sp. and the larva P. nigriventris had the lowest (�28.1&)

rrors (S.E.). Groups (P) found with cluster analysis are reported together with sampleassociated toM. remyi, s ¼ stranded, i¼ intertidal, sz ¼ surf zone, nl ¼ not localised.

Species d13C d15N n m

Mean S.E. Mean S.E.

OthersBacillariophyceae gen. sp. �20.2 0.3 4.5 0.2 5 sPhaeophyceae gen. sp. �20.8 0.7 3.2 0.2 5 sUlvophyceaeUlva lactuca �19.7 0.5 7.0 1.2 4 s

Rhodophyta gen. sp. �20.8 1.2 3.5 0.2 5 sCymodoceaceaeCymodocea nodosa �10.2 0.2 3.4 0.6 5 s

PosidoniaceaePosidonia oceanica �12.9 0.6 0.4 0.4 5 s

DonacidaeDonax trunculus �21.1 0.1 4.8 0.3 5 i

OpheliidaeOphelia radiata �17.0 0.1 8.0 0.1 5 i

CirolanidaeEurydice affinis �18.4 0.2 7.7 0.1 5 i

VertebratesLacertidaePodarcis sicula �22.7 0.7 3.4 0.9 4 112

LaridaeLarus cachinnans faeces �19.0 0.7 16.6 2.9 5 nl

SoricidaeCrocidura suaveolens �23.6 0.2 2.8 1.3 5 90

CervidaeDama dama faeces �32.3 0.1 1.2 0.6 5 nl

BovidaeBos taurus faeces �27.4 1.2 0.9 0.3 5 nl

Seston �20.6 0.3 4.5 0.2 5 szWood debris �27.5 0.1 0.2 0.1 5 sStranded wood (a) �27.8 0.2 �1.6 0.7 5 sSOM �28.3 0.4 1.7 0.3 5 10SOM �26.7 0.2 1.8 0.5 5 30SOM �26.9 0.2 1.1 0.5 5 50SOM �27.3 0.2 0.2 0.3 5 70SOM �27.3 0.2 2.1 0.1 5 90SOM �26.0 0.1 1.7 0.1 5 110SOM �25.1 0.2 1.3 0.2 5 130SOM �27.4 0.1 0.3 0.1 5 150

Table 2Mean isotopic signatures of terrestrial macroinvertebrates with standard errors (S.E.). Groups (A) found with cluster analysis are reported together with sample numbers (n)and mean zonations (m ¼ metres from the shoreline). (a) ¼ on L. etruscum, (b) ¼ on S. nigricans.

Species A d13C d15N n m Species A d13C d15N n m

Mean S.E. Mean S.E. Mean S.E. Mean S.E.

Hygromiidae StaphylinidaeTrochoidea trochoides (a) 3 �25.7 0.6 1.2 0.5 5 106 Quedius sp. 3 �26.7 0.6 3.5 0.2 4 122T. trochoides (b) 4 �25.8 0.5 �1.4 0.2 5 122 Mycetoporus sp. 2 �23.0 0.4 11.7 0.5 3 20

Helicidae Tachyporus sp. 2 �28.1 0.4 7.8 1.0 5 20Eobania vermiculata 3 �25.0 0.4 1.7 1.1 5 25 Phytosus nigriventris 1 �16.5 0.5 7.6 0.3 5 11

Phalangiidae Phytosus nigriventris L. 1 �6.5 0.1 7.4 0.2 5 11Phalangium opilio 3 �25.2 0.6 1.6 0.8 4 116 Atheta sp. 1 1 �22.5 0.7 12.4 0.6 5 23

Pseudoscorpionida gen. sp. 2 �20.6 0.3 3.8 0.5 4 73 Atheta sp. 2 2 �11.7 0.5 9.7 0.4 3 12Lycosidae Atheta sp. 3 2 �25.2 1.5 7.5 0.6 5 25Arctosa cinerea 2 �21.6 0.8 7.1 1.0 5 51 GeotrupidaeArctosa perita 2 �22.6 1.4 4.1 0.6 4 88 Thorectes intermedius 3 �25.6 0.5 4.0 0.4 4 88

Thomisidae Cetonidae gen. sp. L. 3 �25.4 0.9 4.2 0.8 3 40Thomisus onustus 2 �24.6 0.2 5.3 0.3 5 122 Elateridae

Tylidae Isidus moreli 2 �22.5 0.7 5.1 0.6 5 31Tylos europaeus ad. 2 �20.5 0.6 7.6 0.2 5 14 Isidus moreli L. 1 �17.3 1.8 6.2 0.4 5 32Tylos europaeus juv. 2 �21.9 0.5 6.5 0.2 5 6 Buprestidae

Porcellionidae Acmaeodera quadrifasciata 4 �23.1 0.2 �3.8 0.5 5 75Agabiformius obtusus 2 �23.4 0.2 2.3 0.5 5 79 Coccinellidae

Talitridae Adalia decempunctata 2 �26.5 0.3 6.4 1.9 5 122Macarorchestia remyi 2 �20.7 0.6 2.7 0.5 5 30 OedemeridaeOrchestia gammarellus ad. 4 �24.7 0.3 �1.1 0.1 5 124 Oedemera flavipes 4 �22.9 0.3 �3.7 0.6 5 75Orchestia gammarellus juv. 4 �25.1 0.2 �1.0 0.2 5 123 Stenostoma rostratum 2 �23.3 0.9 1.6 0.4 5 75Talitrus saltator ad. 2 �22.8 0.4 5.6 0.2 5 8 AnthicidaeTalitrus saltator juv. 2 �22.0 0.4 6.6 0.2 5 3 Cyclodinus constrictus 2 �26.3 0.7 7.5 1.1 5 122

Geophilidae TenebrionidaeGeophilus sp. 2 �22.4 0.4 7.2 0.4 5 42 Tentyria grossa 3 �26.1 0.1 2.8 0.2 5 84

Collembola gen. sp. 4 �26.1 0.2 �1.9 0.2 2 113 Stenosis brenthoides 3 �25.5 0.1 3.4 0.5 5 81Machilidae gen. sp. 4 �24.7 0.0 �5.3 0.2 5 106 Pimelia bipunctata 2 �25.9 0.2 5.6 0.6 5 64Blattellidae Pimelia bipunctata L. 3 �24.5 0.5 3.3 0.6 2 60Loboptera decipiens 4 �26.6 0.2 �1.1 0.4 5 92 Gonocephalum pusillum 3 �25.6 0.3 2.5 0.3 5 97

Rhinotermitidae Trachyscelis aphodioides 1 �9.8 0.2 5.0 0.4 5 24Reticulitermes lucifugus 3 �24.4 0.1 0.9 0.2 5 60 Phaleria provincialis 1 �16.7 1.4 6.8 0.5 5 18

Acrididae Phaleria provincialis L. 1 �15.0 1.2 6.9 0.3 5 21Oedipoda caerulescens 2 �20.0 1.6 1.2 0.3 5 45 Halammobia pellucida 2 �24.3 0.7 5.5 0.3 5 47Aiolopus strepens 3 �25.2 1.2 3.3 0.1 3 90 Xanthomus pellucidus 2 �22.8 1.0 3.0 0.3 5 42

Labiduridae Bruchidae gen. sp. 4 �26.5 0.2 �5.1 0.5 4 27Labidura riparia 3 �24.9 0.5 4.0 0.7 5 107 Curculionidae

Miridae Mesites pallidipennis 3 �25.2 0.2 0.4 0.3 5 25Lygus pratensis 2 �25.5 0.7 6.1 0.8 5 73 Myrmeleontidae

Lygaeidae Acanthaclisis baetica L. 2 �26.2 0.8 6.8 1.0 4 56Beosus maritimus 3 �25.1 0.3 2.5 0.4 5 106 Ascalaphidae

Carabidae Libelloides coccajus 3 �25.8 0.3 2.8 0.2 5 125Cicindela campestris 3 �25.7 0.3 1.8 0.4 4 127 Sepsidae gen. sp. 3 �27.0 0.3 3.0 0.5 4 99Cylindera trisignata 2 �22.1 0.7 6.4 0.4 5 0 Heleomyzidae gen. sp. 2 �23.4 0.9 8.0 0.9 4 18Calomera littoralis 3 �24.8 0.4 2.6 0.4 5 100 Drosophilidae gen. sp. 2 �24.2 0.7 14.1 0.7 5 40Eurynebria complanata 2 �21.4 0.3 9.7 0.1 4 23 Diptera gen. sp. L. 1 �9.3 0.3 10.0 0.7 5 20Eurynebria complanata L. 2 �20.1 0.2 6.6 0.0 1 16 BraconidaeScarites buparius 2 �22.5 2.0 3.6 0.6 4 35 Apanteles sp. 3 �25.8 0.2 2.4 0.9 5 29Parallelomorphus laevigatus 2 �21.7 0.7 10.9 0.2 4 5 ScoliidaeParallelomorphus laevigatus L. 1 �17.3 1.1 8.4 0.5 5 7 Scolia sexmaculata 3 �24.7 0.6 3.1 0.8 5 106Licinus sp. 4 �24.5 0.3 �1.9 0.5 4 123 Mutillidae

Histeridae Smicromyrme viduata 3 �24.8 0.4 3.3 1.1 5 73Hypocaccus dimidiatus 1 �13.8 0.8 9.7 0.2 5 2 Formicidae gen. sp. 3 �26.2 0.2 0.3 0.3 5 75

PompilidaePompilus cinereus 2 �21.3 0.9 9.7 0.5 5 30

I. Colombini et al. / Acta Oecologica 37 (2011) 422e432426

and highest (�6.5&) 13C values, respectively, while the silverfishMachilidae gen. sp. and the larvae of the dipteran Drosophilidaegen. sp. were the species with the most depleted (�5.3&) andenriched (14.1&) 15N values, respectively.

For each plant and animal species a mean zonation was calcu-lated (Tables 1 and 2) and for animal species this was plottedagainst its mean d13C and d15N values (Fig. 2). In this ecosystemthere was a significant decrease in the isotopic signatures of themacroinvertebrate population when proceeding towards land(d13C ¼ �0.062 � distance � 18.967, R2 ¼ 0.348. P < 0.0001;d15N ¼ �0.063 � distance þ 8.184, R2 ¼ 0.425, P < 0.0001). Thesame analysis applied to the plant community did not show

significant correlations between plants’ distances from the sea andtheir isotopic signatures. However, in the case of S. pungens and ofI. crithmoides, C4 and C3 plants with a wide seaeland distributionpattern, the stable isotopes of d15N measured closer to the sea werehigher than those obtained for inland areas (F test: for d15N ofS. pungens (45 m) vs. S. pungens (123 m) df ¼ 1.18 F ¼ 82.726P < 0.001; for d15N of I. crithmoides (50 m) vs. I. crithmoides (125 m)df ¼ 1.18 F ¼ 61.702 P < 0.001).

Hierarchical cluster analysis at a dissimilarity level of 50%resulted in plants being pooled into three groups (P1, P2 and P3),and macroinvertebrates being pooled into four groups (A1, A2, A3and A4) (Tables 1 and 2, Fig. 3). Cluster analysis clearly segregated

-10

-5

0

5

10

15

0 10 20 30 40 50 60 70 80 90 100 110 120 130 140 150

d15N

(‰

)

-35

-30

-25

-20

-15

-10

-5

0

d13C

(‰)

y = -0.0634x + 8.1836R2 = 0.425P < 0.0001

y = -0.0617x – 18.967R2 = 0.348P < 0.0001

msea land

Fig. 2. Simple regression analysis between mean zonation patterns (in metres) ofmacroinvertebrate species and mean d13C (square symbols) and d15N (circle symbols)values. Regression equations and probability levels (P) are also shown.

I. Colombini et al. / Acta Oecologica 37 (2011) 422e432 427

C4 plants (P1) with higher d13C, such as E. ravennae, S. pungens,Salsola kali and Euphorbia peplis, from the rest of the C3 plants. TheC3 plants were then grouped in two different clusters on the base ofthe d15N.

The four macroinvertebrate groups (A1, A2, A3 and A4) differedin the isotopic signatures of both d13C and d15N in all cases exceptfor A3 vs. A4 for d13C and A1 vs. A2 for d15N.

The analysis of the spatial distribution patterns along theseaeland axis of the macroinvertebrate species belonging to thefour groups obtained with cluster analysis showed different meanzonations. A1 group pooled species strictly related to the eulittoralarea of the beach (mean zonationwith standard error 16.6� 2.8m),such as adults and larvae of the tenebrionid P. provincialis and of thestaphylinid P. Nigriventris. Instead, A2 group had amean zonation of43.5 � 6.0 m and pooled both beach and foredune species. Adultsand juveniles of crustaceans species of beach areas (Tylos euro-paeus, Talitrus saltator, Macarorchestia remyi), and tenebrionids ofthe dune (Halammobia pellucida and P. bipunctata) were pooledtogether with spiders (Arctosa cinerea, Arctosa perita) and coleop-teran carabids (Cylindera trisignata, P. laevigatus, E. complanata). A3group pooled species inhabiting the backdune (mean zonation86.6 � 6.0 m), such as molluscs (Eobania vermiculata, Trochoidea

-35 -30 -25 -20 -15 -10 -5

d13C (‰)

-10

-5

0

5

10

15

20

d15N

(‰

)

P 1 P 2

P 3

A 1A 2

A 3

A 4

Fig. 3. Stable isotopes of d13C and d15N (with standard errors) relative to terrestrialplant and macroinvertebrate species analysed with hierarchical cluster analysis. Forplant species three groups are indicated (P1 empty triangles, P2 empty circles, P3empty squares), whereas for macroinvertebrates four groups are shown (A1 fulltriangles, A2 full circles, A3 full squares, A4 inverted full triangles). Hotelling’s confi-dence ellipses at a 95% level of probability are also shown for plants (dashed lineellipses) and macroinvertebrates (continuous line ellipses).

trochoides), earwigs (Labidura riparia), coleopteran carabids(Cicindela campestris, Calomera littoralis) and tenebrionds (Tentyriagrossa). Finally, A4 group (mean zonation 107.5 � 6.3 m) pooledspecies inhabiting the dune slack, such as amphipods (Orchestiagammarellus), springtails, silverfish and oedemerids (Oedemeraflavipes). Differences among the mean zonation values (ANOVAdf ¼ 3.72 F ¼ 26.098 P < 0.001) of the macroinvertebrate groupswere significant in four cases when comparing beach groups (A1 orA2) with the more terrestrial groups (A3 or A4) (Tukey testsP < 0.05) but not when comparisons were made within groups(between A1 and A2 groups or between A3 and A4 groups).

Lizards and shrews did not differ in the isotopic signature of d13Cand d15N (df ¼ 1.15 for d13C F ¼ 2.623 NS, for d15N F ¼ 0.647 NS) andhad a similar mean zonation pattern (T test t ¼ 0.77 df ¼ 8 NS).

The analysis of the isotopic signatures of marine algae, sestonand marine macroinvertebrates presented d13C values varyingfrom �21.1 to �17.0& and d15N from 3.5 to 8.0& (Table 1, Fig. 4).Seagrasses had higher d13C values than C4 plants. Gull faeces hadthe highest d15N values. d13C values of SOM were more depletedcompared to items of marine origins and varied from �28.3to �25.1&. A mean value with standard error of �26.9 � 0.3& wasobtained when all points were pooled and this did not differ(df ¼ 1.36 F ¼ 0.081 NS) from the overall mean value of the plants(�26.3 � 1.1&). On the other hand d15N values of SOM had a meanvalue of 1.3 � 0.2& and was significantly different (df ¼ 1.36 ford15N F ¼ 23.787 P < 0.001) from that of the plants (�2.6 � 0.4&).Faeces of fallow deer and cattle differed significantly in d13C valuesbut not in d15N values (df ¼ 1.17 for d13C F ¼ 40.862 P < 0.001; ford15N F ¼ 0.249 NS). Faeces of cattle had d13C similar to that of duneplants (df ¼ 1.37 for d13C F ¼ 0.655 NS).

The proportion of marine items in diets was estimated formacroinvertebrate species (Table 3). Only for the A1 group theproportion of marine food items was higher than that of terrestrialorigin. In all other groups the opposite occurred. When theproportion of marine items was correlated with the spatial distri-bution pattern of the different species a significant decrease wasobtain proceeding landwards (Fig. 5).

The trophic enrichment for carbon calculated for each speciesvaried from 0.07 to 0.59 with a mean of 0.39, whereas that fornitrogen varied from 3.17 to 3.74 with a mean of 3.45 (Table 3).Trophic levels calculated for macroinvertebrates of beach-duneecosystems showed three trophic levels. The trophic levels of theA1 group corresponded to primary consumers (tenebrionids and

1 Bacillariophyceae gen. sp. 2 Phaeophyceae gen. sp. 3 U. lactuca 4 Rhodophyta gen. sp. 5 C. nodosa 6 P. oceanica

-35 -30 -25 -20 -15 -10 -5

-10

-5

0

5

10

15

20

6

5

15

3

2 4

1

19 11 12

10

7 13

9 8

16 17

18 14

23

20 2122

7 D. trunculus 8 O. radiata 9 E. affinis10 L. cachinnans faeces 11 D. dama faeces 12 B. taurus faeces

13 Seston 14 Wood debris 15 Stranded wood 16 SOM 10 m 17 SOM 30 m 18 SOM 50 m

d15N

(‰

)

d13C (‰)

19 SOM 70 m 20 SOM 90 m 21 SOM 110 m 22 SOM 130 m 23 SOM 150 m

Fig. 4. Stable isotopes of d13C and d15N (with standard errors) of marine allochthonousinputs of algae, seston, marine plants and organisms, sediment organic matter (SOM),wood debris and faeces of birds and vertebrate herbivores.

Table 3Proportion of terrestrial vs. marine food items entering the trophic web of macroinvertebrates and two vertebrate species. Trophic levels (TL) were obtained with multi-sourcemixing model based on five basal resources (seagull faeces, marine seagrasses, marine organisms, terrestrial plants and sediment organic matter). DC and DN ¼ indicate thediscrimination factors that were calculated.

Beach-dune species Land Sea DC DN TL Dune slack species Land Sea DC DN TL

A1 A3Isidus moreli L. 0.27 0.73 0.21 3.33 2.28 Tentyria grossa 1.00 0.00 0.48 3.52 2.00Phaleria provincialis L. 0.16 0.84 0.12 3.38 2.33 Trochoidea trochoides 0.98 0.02 0.38 3.49 2.00Phaleria provincialis ad. 0.20 0.80 0.09 3.34 2.35 Cicindela campestris 0.96 0.04 0.54 3.52 2.03Phytosus nigriventris 0.15 0.85 0.13 3.29 2.51 Apanteles sp. 0.98 0.02 0.53 3.47 2.03Parallelomorphus laevigatus L. 0.16 0.84 0.07 3.17 2.70 Libelloides coccajus 0.96 0.04 0.37 3.45 2.04Hypocaccus dimidiatus 0 1 0.19 3.35 2.90 Eobania vermiculata 0.92 0.08 0.42 3.43 2.04

Phalangium opilio 0.93 0.07 0.36 3.43 2.04A2 Gonocephalum pusillum 0.95 0.05 0.41 3.40 2.07Stenostoma rostratum 0.83 0.17 0.41 3.40 2.00 Thorectes intermedius 0.94 0.06 0.57 3.55 2.07Macarorchestia remyi 0.64 0.36 0.38 3.47 2.01 Stenosis brenthoides 0.94 0.06 0.56 3.57 2.07Agabiformis obtusus 0.80 0.20 0.35 3.49 2.05 Aiolopus strepens 0.91 0.09 0.52 3.53 2.11Xanthomus pellucidus 0.74 0.26 0.44 3.55 2.08 Beosus maritimus 0.90 0.10 0.45 3.44 2.11Pseudoscorpida gen. sp. 0.58 0.42 0.36 3.59 2.09 Calomera littoralis 0.98 0.02 0.48 3.49 2.11Scarites buparius 0.70 0.30 0.35 3.55 2.12 Scolia sexmaculata 0.87 0.13 0.57 3.61 2.12Arctosa perita 0.69 0.31 0.43 3.58 2.17 Smicromyrme viduata 0.87 0.13 0.49 3.53 2.15Pimelia bipunctata 0.93 0.07 0.41 3.38 2.19 Labidura riparia 0.87 0.13 0.46 3.52 2.15Thomisus onustus 0.82 0.18 0.57 3.52 2.22 Pimelia bipunctata 0.84 0.16 0.44 3.50 2.15Isidus moreli 0.64 0.36 0.49 3.74 2.22Halammobia pellucida 0.78 0.22 0.56 3.39 2.29 VertebratesLygus pratensis 0.88 0.12 0.42 3.39 2.31 Crocidura suaveolens 0.79 0.21 0.36 3.52 2.09Talitrus saltator ad. 0.63 0.37 0.42 3.47 2.32 Podarcis sicula 0.72 0.28 0.37 3.65 2.09Eurynebria complanata L. 0.40 0.60 0.25 3.48 2.37Cylindera trisignata 0.53 0.47 0.30 3.48 2.41Tylos europaeus juv. 0.52 0.48 0.39 3.48 2.41Talitrus saltator juv. 0.52 0.48 0.33 3.45 2.44Arctosa cinerea 0.47 0.53 0.32 3.33 2.51Tylos europaeus ad. 0.35 0.65 0.19 3.28 2.56Geophilus sp. 0.55 0.45 0.41 3.32 2.59Heleomyzidae gen. sp. 0.66 0.34 0.59 3.37 2.75Pompilus cinereus 0.41 0.59 0.41 3.37 3.03Eurynebria complanata 0.41 0.59 0.35 3.32 3.04Parallelomorphus laevigatus 0.43 0.57 0.47 3.24 3.33Mycetoporus sp. 0.55 0.45 0.30 3.50 3.35Atheta sp. 1 0.49 0.37 0.37 3.48 3.51

y = 0.488e-0,009x

R² = 0.503

0

0.1

0.2

0.3

0.4

0.5

0.6

0.7

0.8

0.9

1

0 10 20 30 40 50 60 70 80 90 100 110 120 130 140 150

m

Prop

ortio

n of

mar

ine

food

sou

rces

P < 0.001

dnalaes

Fig. 5. Proportion of marine food sources present in the diet of different macro-invertebrate species calculated with the multi-source mixing model (see Table 3) andplotted against their mean zonation (in metres). An exponential regression equation isreported together with the coefficient of determination and its probability.

I. Colombini et al. / Acta Oecologica 37 (2011) 422e432428

elaterids, TL 2.28e2.35) and to those of predator species (staphy-linids, carabids, and histerids, TL 2.51e2.90). Instead, the A2 groupincluded primary consumers, such as some amphipods, tenebrio-nids, oedemerids, and scavengers, such as other amphipods,isopods, tenebrionids (TL 2.00e2.44). Predators, such as staphyli-nids, hymenopterans, carabids or dipterans feeding on carrion, hadTL 2.51e3.35, whereas top predators, such as Atheta sp. 1, had TL3.51. On the other hand in the dune slack macroinvertebrates of theA3 group showed only one trophic levels (TL 2.00e2.15), andincluded a variety of species belonging to different trophic guilds(primary consumers, scavengers and predators). The speciesbelonging to the A4 group were excluded from the multi-sourcemixing model because their C and N values lied out of the rangeof the basal sources that were included in the model.

Differences were found when analysing the isotopic signaturesof different age classes (Fig. 6). For insect species larvae had higherd13C values compared to adults and had lower or equal d15N in allcases except for the larvae of I. moreli (df ¼ 1.18 for d13C F ¼ 15.651P < 0.01, for d15N F ¼ 5.030 P < 0.05). Instead, for crustaceansjuveniles of T. saltator and T. europaeus showed the same isotopicsignatures (Fig. 6) and had similar proportions of food sources intheir diet (Table 4), but were enriched and depleted, respectively, inboth 13C and 15N compared to adults (T. saltator df ¼ 1.17 for d13CF¼ 4.355 NS, for d15N F¼ 19.361 P< 0.001; T. europaeus df¼ 1.14 ford13C F ¼ 7.797 P < 0.05, for d15N F ¼ 18.083 P < 0.01). In the case ofO. gammarellus no significant differences occurred in the isotopicsignatures of the two age classes (df¼ 1.17 for d13C F ¼ 1.636 NS, ford15N F¼ 0.205 NS) suggesting a common terrestrial diet (Fig. 3) anda similar zonation pattern (Table 2) (df ¼ 833 t ¼ 0.80 NS).

For certain macroinvertebrate species three different types ofmulti-source mixing models were selected according to the trophicguilds of the different species (Table 4). Predator species of beach-dune areas included carabids, spiders and hymenopterans. Adultsand larvae of the carabid E. complanata were found feeding onsimilar prey sources but exploited them in different ways (Table 4).Instead, the larvae of P. laevigatus, another carabid of the beacharea, mainly fed on more marine species when compared to thelarva of E. complanata. As for the other carabids, C. trisignata and

-30 -25 -20 -15 -10 -5

-2

3

8

13

1

1 3

3

2

4

4

5

5

6 6

7

7

8

8

9 9

1 T. europaeus 2 O. gammarellus 3 T. saltator

4 E. complanata 5 P. laevigatus 6 P. nigriventris

7 I. moreli 8 P. bipunctata 9 P. provincialis

d13C (‰)

d15N

(‰

)

2

Fig. 6. Stable isotopes of d13C and d15N of adults (full circles) and juveniles or larvae(empty circles) of crustacean (1e3) and insect species (4e9) are shown together withstandard errors.

Table 4Medium values of five food sources obtained with multi-source mixing models calculconsidered (a model: a ¼ A1, b ¼ A2, c ¼ A3, d ¼ A4, e ¼ marine macroinvertebrates; b ma ¼ P1, b ¼ P2 & P3, c ¼ C. nodosa & P. oceanica, d ¼ marine organisms & seagull faeces,

Beach-dune species A1 Parallelomorphus laevigatus laevigatus L.Isidus moreli L.Phaleria provincialisPhaleria provincialis L.

A2 Arctosa cinereaArctosa peritaThomisus onustusTylos europaeus ad.Tylos europaeus juv.Agabiformius obtususMacarorchestia remyiTalitrus saltator ad.Talitrus saltator juv.Geophilus sp.Oedipoda caerulescensCylindera trisignataEurynebria complanataEurynebria complanata L.Scarites bupariusIsidus moreliPimelia bipunctataHalammobia pellucidaXanthomus pellucidusPompilus cinereus

Dune slack species A3 Trochoidea trochoidesEobania vermiculataReticulitermes lucifugusAiolopus strepensLabidura ripariaBeosus maritimusCalomera littoralisThorectes intermediusStenosis brenthoidesPimelia bipunctata L.Gonocephalum pusillumMesites pallidipennisSepsidae gen. sp.Scolia sexmaculataSmicromyrme viduataFormicidae gen. sp.

VertebratesPodarcis siculaCrocidura suaveolens

I. Colombini et al. / Acta Oecologica 37 (2011) 422e432 429

Scarites buparius, these species definitively showed more terrestrialhabits. Of the two spider species A. cinerea exploited both marineand terrestrials sources compared to A. perita that preferredmore terrestrial trophic sources. The hymenopteran Pompilus cin-ereus showed a very similar food source partitioning to that ofE. complanata.

In the tenebrionid P. provincialis both adults and larvae feed onthe same food sources, but larvae consumed more marine foodsthan adults (Table 4). In the tenebrionid P. bipunctata adults andlarvae mainly fed on plant species. The click beetle I. moreli showedadults and larvae feeding on the same food sources (b model) butwith different proportions of the food items entering into the diets.In fact, while larvae mainly fed on marine plants and algae, adultsfed on stranded algae and terrestrial plants. For crustaceans speciesthe same considerations can be applied. T. saltator and T. europaeusboth fed on SOM with faeces and marine allochthonous inputs(Table 4) with adults and juveniles of T. europaeus and juveniles ofT. saltator with higher proportions of marine allochthonous inputsin their diet.

Predators of the A3 group mainly fed on species of the A4 groupfollowed by those of the A3 group. Primary consumers, instead,

ated for selected macroinvertebrates. Food sources vary according to the speciesodel: a ¼ P1, b ¼ P2, c ¼ C. nodosa & P. oceanica, d ¼ stranded algae, e ¼ P3; g model:e ¼ SOM & terrestrial vertebrate faeces).

Model Trophic source

a b c d e

a 0.59 0.04 0.06 0.22 0.09b 0.13 0.13 0.49 0.18 0.07g 0.10 0.03 0.36 0.46 0.05g 0.04 0.13 0.05 0.50 0.28

a 0.13 0.17 0.26 0.22 0.22a 0.11 0.06 0.08 0.62 0.13a 0.01 0.05 0.73 0.19 0.02g 0.05 0.09 0.07 0.64 0.15g 0.05 0.14 0.06 0.47 0.28b 0.12 0.34 0.12 0.13 0.29b 0.21 0.23 0.20 0.13 0.23g 0.05 0.17 0.07 0.33 0.38g 0.04 0.13 0.05 0.50 0.28a 0.08 0.24 0.39 0.13 0.16b 0.48 0.08 0.06 0.03 0.35a 0.11 0.17 0.25 0.29 0.18a 0.09 0.71 0.04 0.01 0.15a 0.32 0.07 0.09 0.37 0.15a 0.14 0.04 0.05 0.69 0.08b 0.03 0.25 0.04 0.56 0.12g 0.91 0.02 0.00 0.01 0.06g 0.02 0.11 0.03 0.26 0.58b 0.10 0.36 0.13 0.20 0.21a 0.10 0.68 0.05 0.02 0.15

b 0.07 0.25 0.06 0.08 0.54b 0.08 0.32 0.07 0.10 0.43b 0.15 0.13 0.09 0.05 0.58b 0.02 0.59 0.03 0.24 0.12b 0.01 0.58 0.01 0.34 0.06b 0.05 0.52 0.06 0.15 0.22a 0.00 0.01 0.33 0.66 0.00b 0.00 0.68 0.00 0.31 0.01b 0.17 0.20 0.11 0.07 0.44g 0.21 0.63 0.04 0.08 0.04g 0.06 0.61 0.05 0.07 0.20b 0.14 0.08 0.06 0.03 0.69g 0.01 0.46 0.01 0.04 0.48a 0.00 0.02 0.39 0.58 0.01a 0.00 0.01 0.46 0.53 0.00b 0.08 0.10 0.05 0.03 0.74

a 0.13 0.04 0.05 0.71 0.07a 0.05 0.05 0.07 0.75 0.08

I. Colombini et al. / Acta Oecologica 37 (2011) 422e432430

mainly consumed C3 plants. Generally marine allochthonous itemswere rarely incorporated into the diets of the A3 group.

For the two vertebrate species (P. sicula and C. suaveolens) thea model was applied. The results indicate that shrews had slightlyhigher proportions of species belonging to the A4 group in theirdiet as compare to lizards (Table 4), whereas the latter tended toincorporate more species belonging to the A1 group.

4. Discussion

The beach-dune system at the study site received a substantialquantity of marine subsidies, mainly consisting in C. nodosa, thatwere irregularly deposited on the eulittoral throughout the year.The marine biomass that annually reached the beach was twice thesize of the autochthonous plant biomass present in the area. Thiswas mainly due to the presence of a conspicuous seagrass bedin the shallow waters in front of the study site but also to theparticular instability of this section of the coast. In fact, thecontinuous evolution of the beach’s state, with high wind velocitiesassociated to a rapid beach progradation, prevented the formationof a stable and densely vegetated dune (Hesp, 1989). Also thepresence of Ammophila arenaria plants, which grow rapidly,colonising seaward beach surfaces by rhizome growth and initiallyforming relatively low dune heights but wide dune widths(Rodriguez-Echeverria et al., 2008), was another factor influencingthe system. At the study site plants were continuously experiencingsand burial because of the active dune system thus plant biomasswas lower than in other more stable areas of the beach. Biomass ofthe above-ground vegetation of the dune slack was definitivelyhigher than that of the adjacent foredune but lower than that ofother dune slacks that have reached the climax stage. McLachlanet al. (1987) in Algoa Bay, South Africa, reported an above-groundmean dry weight biomass of about 69 g m�2 in the vegetated zoneof the slack, whereas Berendse et al. (1998) on Terschelling islandshowed that in a 5-year-old plot of a dune slack the living above-ground dry weight biomass was only 150 g m�2 but that in the76-year-old plot it increased to 1344 g m�2. The slack at the studysite showed a dry weight biomass of 980 g m�2 indicating that thedune slack still had not reached its climax as it was continuouslyundergoing changes due to the dynamism of the system. This duneslack was flooded by sea water during winter storms but alsoreceived surface run-offs from the Uccellina hills backing up thearea. During the summer the water table dropped approximately1 m below the soil surface (unpublished data) and the basophilouspioneer vegetation, represented by Schoenus nigricans and Juncusacutus and adapted to low nutrient availability (Grootjans et al.,1997; Sykora et al., 2004), was in its middle colonization phase.

Due to the complexity of the abiotic conditions of the entireecosystem, the number of plant species was quite high evenconsidering that the study areawas spatially restricted (150 m) andincluded a large non-vegetated area (eu- and supralittoral). Thepresence of three talitrid species, two of which inhabiting beachareas (T. saltator and M. remyi) and the other living in the duneslacks (O. gammarellus), was a peculiar characteristic of the system.O. gammarellus, a typical salt marsh species (Sprung and Machado,2000), probably originated from a population of the Ombrone riverthat had reached the area through channels built artificially andhad colonised the dune slacks. The survival of this species wasguaranteed by frequent flooding of the area and by the presence ofJ. acutus hummocks in which the species took refuge during theday, especially during dry periods (personal observations). Otherimportant species on the beach were the coleopteran staphylinids(P. nigriventris) and the tenebrionids (P. provincialis) that wereintrinsically tied to the wrack debris (Colombini et al., 2000, 2009).On the dune and dune slack areas species abundance was quite low

including that of O. gammarellus. In these two areas other species,such as spiders of the Arctosa genus, were found dominant togetherwith predator carabids.

The significant difference that appeared in the isotopic signa-tures of plants with C3 and C4 photosynthetic pathways was clearlydemonstrated by the results. C4 plants (P1 group and seagrasses)more enriched in 13C compared to the C3 plants (P2 and P3 groups)were thus provided with an important adaptive mechanism tosurvive in hot environments (Bjorkman et al., 1974) with low soilfertility (Brown,1978). The intraspecific differences of d13C and d15Noccurring in a C3 plant (I. crithmoides) and of d15N in a C4 plant(S. pungens) can be explained considering that the plants weresampled in areas with different soil conductivity values (Colombiniet al., 2009). It has been shown that elevated levels of N availabilitycan lead to increased rates of N-cycling and that this increase inturn results in 15N enrichment of the soil pool. Plants accessing tothis soil pool can then become relatively 15N-enriched over time(Dawson et al., 2002) and plants lying at different positions withina site can show differences. This can explain the differencesbetween the P2 and P3 groups, with P3 showing species that haveprevalently more terrestrial characteristics (Juniperus oxycedrus,E. multiflora, etc.) and P2 that pools species prevalently adapted tomarine water submersion (Cakile maritima, S. nigricans, J. acutus,L. etruscum, Dittrichia viscosa, Xantium italicum). Furthermore, Guyet al. (1980) demonstrated that C3 plants of inland saline wetlandsshowed salinity-induced changes in d13C values due to a shift in thebalance between the relative activities of the two primary enzymesof CO2 fixation.

Differently from what occurred in the plants there wasa decrease in the stable isotopic signatures of the terrestrial mac-roinvertebrate species when proceeding towards land. The decreasein d13C values indicated that the influence of marine subsides in thefood web decrease at increasing distance from the sea. This was alsoconfirmed by the results obtained with the mixing model based onthe five food sources. A similar result was obtained by Paetzold et al.(2008) that showed the relatively low contribution of marine-derived resources to the diet of terrestrial arthropod consumers ofa productive temperate island. Analysing the spatial distribution(along the seaeland axis) of the macroinvertebrate species thatmake up the four groups pointed out by cluster analysis, it appearedclear that these groups included eu- and supralittoral species(A1 and A2 groups) on the one hand and extralittoral species (A3and A4 groups) on the other. Furthermore, the A1 group derivedcarbon from marine sources as it had a stable isotope ratio moreenriched in 13C compared to the other groups. Instead, A2 groupderived carbon from both marine and terrestrial sources in an equalway or prevalently from terrestrial food items. As shown by the twotrophic levels that were obtained, the species belonging to the A1group were mainly primary and secondary consumers, the latterforaging on preys found within the stranded wracks. A2 group wasmore heterogeneous and exhibited species belonging to trophicguilds grouped into three trophic levels. Primary consumers(herbivores feeding on vascular plants of marine and terrestrialhabitats), scavengers, predators and top predators mainly belongedto the beach and to the seaward face of the dune. However, othermore mobile species (fliers or spiders) occupied the landward faceof the dune. A3 group pooled species inhabiting the backdune andshowed only one trophic level, which included a variety of speciesbelonging to different trophic guilds (primary consumers, scaven-gers and predators). The fact that some predator species of the A2and A3 groups occupied lower trophic levels can be an indicationthat these predators belonged to different trophic chains. The A4group included species feeding on pollen and others soil arthropods(collembolans, amphipods andmud snails), which eat items such asmonocellular algae, bacteria and fungi (Schmidt et al., 2004;

I. Colombini et al. / Acta Oecologica 37 (2011) 422e432 431

Chahartaghi et al., 2005), for which isotopic signatures were notevaluated. These species probably belonged to different food chainsto which predators of the A3 group belonged.

The application of the multi-source mixing model allowed anoverview of the different food web typologies that are obtained inthe different areas of the ecosystem. These differences were notonly found between species belonging to the same feeding guildbut also between adults and juveniles or larvae of crustaceans andinsect species. As stated by McLachlan (1991) food competitionis generally a rare phenomenon in sandy beach ecosystems. Thepresent work indicated that trophic competition could be limitedthanks to a spatial subdivision of species (spiders of the same genuswith different mean zonation patterns and different feeding habits)or to differences in the activity patterns of surface species (diurnaland nocturnal) but also thanks to different metabolic needs ofdifferent age classes.

Marine allochthonous inputs weremainly exploited for the dietsof scavengers or predators feeding on scavengers of the A1 group,and showed that marine-derived sources entered the food chainonly at this level. This result fits inwell with the results of Andersonand Polis (2004) in which species feeding on basal resources werelikely to respond strongly to subsidies entering at the base of thefood web. In contrast, taxa at higher trophic levels could consumeprey from multiple food web compartments and could showa reduced response to subsidies affecting only one compartment.

The absence of differences in the isotopic signature of d13C andd15N between lizards and shrews suggested similar trophic nicheseven if they had different activity patterns, one being diurnal andthe other nocturnal. Both lizards and shrews showed a low trophiclevel even if theywere secondary consumers. Differently fromwhatwas reported for insular populations of lizards (Barrett et al., 2005)and rodents (Stapp and Polis, 2003), in our case both vertebrateswere not subsidized by marine-derived sources. This was alsoshown by the multi-source mixing model in which more than 70%of the diet was of terrestrial origin. This difference was also pointedout by Barrett et al. (2005) when lizards of coastal populations werecompared with those of unsubsidized inland populations.

The results of the study show that in the case of donor habitats ofhigh productivity subsidizing areas of high productivity the impor-tance of beach wracks was limited to beach areas. This result iscomparable to that of Paetzold et al. (2008) inwhichhighly productivemarine resource inputs were less important for recipient terrestrialconsumers of productive temperate islands andweremainly confinedto intertidal specialist consumers. However, consumer responses tospatial subsidies cannot be explained only by differences in produc-tivity among adjacent systems (Marczak et al., 2007) but appear to bemodified by other factors, such as type of inputs, biotic characteristicsof the recipient consumers for spatial subsidies, and size and physicalcharacteristics of donor and recipient habitats (Baxter et al., 2005;Marczak et al., 2007; Paetzold et al., 2008).

In conclusion this study is the first to focus food web structure ofbeach/dune assemblages and to show that allochthonous marine-derived material mainly subsidizes macroinvertebrates species ofthe eulittoral and contributes very little to the food chains of moreterrestrial species. The complexity of the areas backing up the beachand the presence of a dune slack rich in plant species probablywere sufficient to provide autochthonous resources to both macro-invertebrates and vertebrates inhabiting the area. Species living onthebeachdune hadaccess to both allochthonous andautochthonousresources entering food webs at various trophic levels and thiscompartmentalization probably stabilised the food webs. Moreinformation is needed to understand howdifferent age classes of thesame species might be able to use different areas of the ecosystemaccording to theirmetabolic needs or howmosses, lichens, algae andbacteria species might be an important missing link to the picture.

Acknowledgements

The study was supported partially by funds of the ItalianNational Council of Research (CNR) and partially by the Europeanproject WADI (INCO-CT-2005-015226). We also would like to thankthe Maremma Regional Park and the Azienda Regionale Agricola ofAlberese.

References

Adin, R., Riera, P., 2003. Preferential food source utilization among stranded mac-roalgae by Talitrus saltator (Amphipoda, Talitridae): a stable isotopes study inthe northern coast of Brittany (France). Estuar. Coast. Shelf Sci. 56, 91e98.

Anderson, W.B., Polis, G.A., 1998. Marine subsidies of island communities in the Gulfof California: evidence from stable carbon and nitrogen isotopes. Oikos 81,75e80.

Anderson, W.B., Polis, G.A., 2004. Allochthonous nutrient and food inputs: conse-quences for temporal stability. In: Polis, G.A., Power, M.E., Huxel, G.R. (Eds.),Food Webs at the Landscape Level. University of Chicago Press, Chicago, Illinois,pp. 82e95.

Barrett, K., Anderson, W.B., Wait, A., Grismer, L.L., Polis, G.A., Rose, M.D., 2005.Marine subsidies alter the diet and abundance of insular and coastal lizardpopulations. Oikos 109, 145e153.

Batschelet, E., 1981. Circular Statistic in Biology. Academic Press, London, UK.Baxter, C.V., Fausch, K.D., Saunders, W.C., 2005. Tangled webs: reciprocal flows of

invertebrate prey link streams and riparian zone. Freshwat. Biol. 50, 201e220.Bergamino, L., Lecari, D., Defeo, O., 2011. Food web structure of sandy beaches:

temporal and spatial variation using stable isotope analysis. Estuar. Coast. ShelfSci. 91, 536e543.

Berendse, F., Lammerts, E.J., Olff, H., 1998. Soil organic matter accumulation and itsimplications for nitrogen mineralization and plant species composition duringsuccession in coastal dune slacks. Plant Ecol. 137, 71e78.

Bianchi, C.N., Cinelli, F., Morri, C., 1993. La carta bionomica dei Mari Toscani. RegioneToscana, Italy.

Bjorkman, O., Mahall, B., Nobs, M., Ward, W., Nicholson, F., Mooney, H., 1974. Ananalysis of the temperature dependence of growth under controlled conditions.In: McGough, S.A. (Ed.), Carnegie Institution of Washington, Yearbook 73. J.D.Lucas Printing Co, Baltimore, Maryland, pp. 757e767.

Brown, R.H., 1978. A difference in N use efficiency in C3 and C4 plants and itsimplications in adaptation and evolution. Crop Sci. 18, 93e98.

Carabel, S., Godìnez-Domìnguez, E., Verìsimo, P., Fernàndez, L., Freire, J., 2006. Anassessment of sample processing methods for stable isotope analyses of marinefood webs. J. Exp. Mar. Biol. Ecol. 336, 254e261.

Castilla, A.M., Vanhooydonck, B., Catenazzi, A., 2008. Feeding behaviour of theColumbretes lizard Podarcis atrata in relation to Isopoda (Crustaceae) species:Ligia italica and Armadillo officinalis. Belg. J. Zool. 138, 146e148.

Catenazzi, A., Donnelly, M.A., 2007a. The Ulva connection: marine algae subsidizeterrestrial predators in coastal Peru. Oikos 116, 75e86.

Catenazzi, A., Donnelly, M.A., 2007b. Role of supratidal invertebrates in the decom-position of beach-cast green algae Ulva sp. Mar. Ecol. Prog. Ser. 349, 32e42.

Chahartaghi, M., Langel, R., Scheu, S., Ruess, L., 2005. Feeding guilds in Collembolabased on nitrogen stable isotope ratios. Soil Biol. Biochem. 37, 1718e1725.

Chaouti, A., Colombini, I., Fallaci, M., Gagnarli, E., Scapini, F., Chelazzi, L., Bayed, A.,2006. Réponse du macrozoobenthos aux déversements de la rivière Ombronesur la plage sableuse du parc regional de la Maremma (Toscane, Italie). In: TheMediterranean Coastal Areas from Watershed to the Sea: Interactions andChanges MEDCORE Project International Conference Florence 10e14 November2005, pp. 275e295.

Colombini, I., Aloia, A., Fallaci, M., Pezzoli, G., Chelazzi, L., 2000. Temporal andspatial use of stranded wrack by the macrofauna of a tropical sandy beach. Mar.Biol. 136, 531e541.

Colombini, I., Chaouti, A., Fallaci, M., Gagnarli, E., Scapini, F., Bayed, A., Chelazzi, L.,2006. Effect of freshwater river discharge on terrestrial arthropods in Atlanticand Mediterranean sandy shores. In: Scapini, F. (Ed.), The MediterraneanCoastal Areas from Watershed to the Sea: Interactions and Changes. FirenzeUniversity Press, Florence, Italy, pp. 233e261.

Colombini, I., Chelazzi, L., 2003. Influence of marine allochthonous input of sandybeach communities. Oceanogr. Mar. Biol. Annu. Rev. 41, 115e159.

Colombini, I., Mateo, M.A., Serrano, O., Fallaci, M., Gagnarli, E., Serrano, L.,Chelazzi, L., 2009. On the role of Posidonia oceanica beach wrack for macro-invertebrates of a Tyrrhenian sandy shore. Acta Oecol. 35, 32e44.

Dawson, T.E., Mambelli, S., Plamboeck, A.H., Templer, P.H., Tu, K.P., 2002. Stableisotopes in plant ecology. Annu. Rev. Ecol. Syst. 33, 507e559.

Dugan, J.E., Hubbard, D.M., McCrary, M.D., Pierson, M.O., 2003. The response of mac-rofauna communities and shorebirds to macrophyte wrack subsidies on exposedsandy beaches of Southern California. Estuar. Coast. Shelf Sci. 58S, 25e40.

Grootjans, A.P., van den Ende, E.P., Walsweer, A.F., 1997. The role of microbial matsduring primary succession in calcareous dune slacks: an experimentalapproach. J. Coast. Conserv. 3, 95e102.

Guy, R.D., Reid, D.M., Krouse, H.R., 1980. Shifts in carbon isotope ratios of two C3halophytes under natural and artificial conditions. Oecologia 44, 241e247.

I. Colombini et al. / Acta Oecologica 37 (2011) 422e432432

Hesp, P., 1989. A review of biological and geomorphological processes involved in theinitiationanddevelopmentof incipient foredunes. Proc.R.Soc.Edinb.96B,181e201.

Hesslein, R.H., Capel, M.J., Fox, D.E., 1991. Stable isotopes of sulphur, carbon, andnitrogen as indicators of trophic level and fish migration in the Lower Mack-enzie River Basin, Canada. Can. J. Fish. Aquat. Sci. 48, 2258e2265.

Huxel, G.R., McCann, K., Polis, G.A., 2002. Effects of partitioning allochthonous andautocthonous resources on food web stability. Ecol. Res. 17, 419e432.

Ince, R., Hyndes, G., Lavery, P.S., Vanderklift, M.A., 2007. Marine macrophytesdirectly enhance abundance of sandy beach fauna through provision of foodand habitat. Estuar. Coast. Shelf Sci. 74, 77e86.

Inglis, G., 1989. The colonisation and degradation of stranded Macrocystis pyrifera(L.) C. Ag. by the macrofauna of a New Zealand sandy beach. J. Exp. Mar. Biol.Ecol. 125, 203e217.

Kirkman, H., Kendrick, G.A., 1997. Ecological significance and commercial harvestingof drifting and beach-cast macro-algae and seagrasses in Australia: a review.J. Appl. Phycol. 9, 311e326.

Koepcke, H.W., Koepcke, M., 1952. Sobre el proceso de transformacion de la materiaorganica en playas arenosas del Peru. Publ. Mus. Hist. Nat. Ser. A 8, 1e25.

Lubetkin, S.C., Simenstad, C.A., 2004. Multi-source mixing models to quantify foodweb sources and pathways. J. Appl. Ecol. 41, 996e1008.

Marczak, L.B., Thompson, R.M., Richardson, J.S., 2007. Meta-analysis: trophic level,habitat, and productivity shape the food web effects of resource subsidies.Ecology 88, 140e148.

Marques, J.C., Gonçalves, S.C., Pardal, M.A., Chelazzi, L., Colombini, I., Fallaci, M.,Bouslama, M.F., ElGtari, M., Charfi-Cheikhrouha, F., Scapini, F., 2003. Compar-ison of Talitrus saltator (Amphipoda, Talitridae) biology, dynamics andsecondary production in Atlantic (Portugal) and Mediterranean (Italy andTunisia) populations. Estuar. Coast. Shelf Sci. 58S, 127e148.

Mateo, M.A., Serrano, O., Serrano, L., Michener, R.H., 2008. Effects of sample prep-aration on stable isotope ratios of carbon and nitrogen in marine invertebrates:implications for food web studies using stable isotopes. Oecologia 157, 105e115.

McLachlan, A., 1991. Ecology of coastal dune fauna. J. Arid Environ. 21, 229e243.McLachlan, A., Ascaray, C., du Toit, P., 1987. Sand movement, vegetation succession

and biomass spectrum in a coastal dune slack in Algoa Bay, South Africa. J. AridEnviron. 12, 9e25.

McLachlan, A., Brown, A., 2006. The Ecology of Sandy Shores, second ed. AcademicPress, London, UK.

Paetzold, A., Lee, M., Post, D.M., 2008. Marine resource flows to terrestrial arthropodpredators on a temperate island: the role of subsidies between systems ofsimilar productivity. Oecologia 157, 653e659.

Phillips, D.L., Gregg, J.W., 2003. Source partitioning using stable isotopes: copingwith too many sources. Oecologia 136, 261e269.

Phillips, D.L., Newsome, S.D., Gregg, J.W., 2005. Combining sources in stable isotopemixing models: alternative methods. Oecologia 144, 520e527.

Polis, G.A., Hurd, S.D., 1995. Extraordinarily high spider densities on islands: flow ofenergy from the marine to terrestrial food webs and the absence of predation.Proc. Natl. Acad. Sci. U.S.A. 92, 4382e4386.

Polis, G.A., Hurd, S.D., 1996a. Linking marine terrestrial food webs: allochthonousinput from the ocean supports high secondary productivity on small islandsand coastal land communities. Am. Nat. 147, 396e423.

Polis, G.A., Hurd, S.D., 1996b. Allochthonous input across habitats, sub-sidised consumers and apparent trophic cascades: examples from theocean-land interface. In: Polis, G.A., Winemiller, K.O. (Eds.), Food Webs:Integration of Patterns and Dynamics. Chapman and Hall, London, UK,pp. 275e285.

Polis, G.A., Anderson, W.B., Holt, R.D., 1997. Towards an integration of landscape andfood web ecology: the dynamics of spatially subsidised food webs. Annu. Rev.Ecol. Syst. 28, 289e316.

Post, D.M., 2002. Using stable isotopes to estimate trophic position: models,methods and assumptions. Ecology 83, 703e718.

Rodriguez-Echeverria, S., Hol, W.H.G., Frietas, H., Eason, W.R., Cook, R., 2008.Arbuscular mycorrhizal fungi of Ammophila arenaria (L.) Link: spore abundanceand root colonisation in six locations of the European coast. Eur. J. Soil Biol. 44,30e36.

Rose, M.D., Polis, G.A., 1998. The distribution and abundance of coyotes: the effectsof allochthonous food subsidies from the sea. Ecology 79, 998e1007.

Schlacher, T.A., Connolly, R.M., 2009. Land-ocean coupling of carbon and nitrogenfluxes on sandy beaches. Ecosystems 12, 311e321.

Schmidt, O., Curry, J.P., Dyckmans, J., Rota, E., Scrimgeour, C.M., 2004. Dual stableisotope analysis (d13C and d15N) of soil invertebrates and their food sources.Pedobiologia 48, 171e180.

Serrano, O., Serrano, L., Mateo, M.A., Colombini, I., Chelazzi, L., Gagnarli, E.,Fallaci, M., 2008. Acid washing effect on elemental and isotopic composition ofwhole beach arthropods: implications for food web studies using stableisotopes. Acta Oecol. 34, 89e96.

Sprung, M., Machado, M., 2000. Distinct life histories of peracarid crustaceans in RiaFormosa salt marsh (S. Portugal). Wetlands Ecol. Manage. 8, 105e115.

Stapp, P., Polis, G.A., 2003. Marine resources subsidize insular rodent populations inthe Gulf of California, Mexico. Oecologia 134, 496e504.

Sykora, K.V., van den Bogert, J.C.J.M., Berendse, F., 2004. Changes in soil and vege-tation during dune slack succession. J. Veg. Sci. 15, 209e218.

Wait, D.A., Aubrey, D.P., Anderson, W.B., 2005. Seabird guano influences on desertislands: soil chemistry and herbaceous species richness and productivity. J. AridEnviron. 60, 681e695.