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Original article

On the role of Posidonia oceanica beach wrack formacroinvertebrates of a Tyrrhenian sandy shore

Isabella Colombinia, Miguel Angel Mateob, Oscar Serranob, Mario Fallacia,Elena Gagnarlia, Laura Serranob, Lorenzo Chelazzia,*aIstituto per lo Studio degli Ecosistemi, CNR, Via Madonna del Piano 10, 50019 Sesto Fiorentino Firenze, ItalybCentro de Estudios Avanzados de Blanes Consejo Superior de Investigaciones Cientıficas, c/ Acces a la Cala St. Francesc,

14, 17300 - Blanes, Girona, Spain

a r t i c l e i n f o

Article history:

Received 2 May 2008

Accepted 17 July 2008

Published online 18 September 2008

Keywords:

Mediterranean sandy beach

Wrack colonisation

Species succession

Abundance

Multi-isotopic analysis

* Corresponding author. Tel.: þ39 055 522591E-mail address: chelazzi@ise.cnr.it (L. Ch

1146-609X/$ – see front matter ª 2008 Elsevidoi:10.1016/j.actao.2008.07.005

a b s t r a c t

The use of Posidonia oceanica beach wrack by macroinvertebrates of the sandy beach at

Burano (Tuscany, Italy) was assessed by following the colonisation dynamics of the wrack

and analysing the stable isotopes ‘scenario’ of the main local carbon and nitrogen sources

and consumers. One-hundred experimental cylinders, filled with P. oceanica wrack, were

placed on the beach and sampled over a 1-month period. Abundance and species richness

of macroinvertebrates in wracks varied through time. Wrack was colonised by crustaceans

almost immediately after deployment of the experimental cylinders. The amphipod Tali-

trus saltator largely dominated the faunal assembly and, together with the isopod Tylos

europaeus, occupied the wracks closer to the sealine. These were followed by dipterans,

staphylinids, pselaphids and tenebrionids that occurred in drier wracks higher up on the

eulittoral. Moisture content of the wrack and sand decreased through space and time. This

was the primary factor explaining the spatial and temporal changes observed in macro-

invertebrate abundance, with species colonising or abandoning wracks according to

thresholds of environmental parameters. Isotopic analysis clearly established the absence

of any direct dietary link between P. oceanica wrack and macroinvertebrates. Terrestrial

food sources were also discarded. Both our experimental data and a literature search

showed that the organic matter from seston as filtered by the sand is the most plausible

carbon and nitrogen source for beach food webs. Even if P. oceanica wrack is not a trophic

source for macroinvertebrates, it is vitally important as a physical structure that provides

detritivorous and predatory species with refuge from environmentally stressful conditions.

ª 2008 Elsevier Masson SAS. All rights reserved.

1. Introduction the carbon synthesised by primary producers may not be

Understanding the functioning of coastal ecosystems needs

an accurate knowledge of materials and energy flow between

compartments (Mateo et al., 2006). An important fraction of

2; fax: þ39 055 5225920.elazzi).er Masson SAS. All rights

exploited locally but, instead, be transported far away to fuel

the food webs of other ecosystems. This is particularly true in

highly dynamic ecosystems such as marine coastal

environments.

reserved.

a c t a o e c o l o g i c a 3 5 ( 2 0 0 9 ) 3 2 – 4 4 33

The sea–land interface is a complex area where terrestrial

and marine ecosystems interact intensely in several ways.

Sandy shores occupy approximately three-quarters of the

shorelines of the world (Bascom, 1980) and are known to have

very little in situ primary production (Inglis, 1989; McLachlan

and Brown, 2006). Marine allochthonous inputs are thus of

primary importance for beaches that receive substantial

carbon and nitrogen inputs from the sea in the form of macro-

and micro-detritus from various origins. Among stranded

macrophytes, seagrasses have an important role in controlling

coastal sedimentary processes (De Falco et al., 2003), in oper-

ating as important nutrient sinks for nearshore communities

(Ochieng and Erftemeijer, 1999; Mateo et al., 2003; McLachlan

and Brown, 2006), in influencing the geomorphology of sandy

shores by attenuating waves, reducing energy to beaches and

protecting from erosion (Hemminga and Nieuwenhuize, 1990),

in acting as refuges and in supporting prey resources that are

the basic element of food webs for vertebrate predators such as

lizards, shorebirds, foxes, coyotes etc. (Polis and Hurd, 1996;

Dugan et al., 2003; Colombini and Chelazzi, 2003).

There is a substantial literature on seagrass meadows of

Posidonia oceanica (L.) Delile, an endemic and dominant species

of the Mediterranean. This mainly focuses on seagrass growth

patterns, fate of production, dynamics of organic deposits,

leaf litter decomposition, carbon cycling and bacterial carbon

of sediments (Cebrian et al., 1997; Mateo et al., 1997; Marba

et al., 2002; Holmer et al., 2004). Recently, some attention has

been given to the quantities and functions of beach-cast

material (Colombini et al., 2000; Dugan et al., 2003; Jaramillo

et al., 2006; Olabarria et al., 2007) and in particular of P. oceanica

of Mediterranean areas (Mateo et al., 2003). The importance of

beach casts, their colonisation by macroinvertebrate species

and subsequent successional patterns was reviewed by

Colombini and Chelazzi (2003). With the exception of Inglis

(1989) and Olabarria et al. (2007), none of the other authors

have used experimentally deployed wrack patches to analyse

the dynamics of the associated fauna but have studied extant

ones. Moreover, information on spatial and temporal vari-

ability of macroinvertebrate fauna associated with the wrack

as affected by several environmental parameters obtained

during the same experiments is very poor. The stable isotopes

approach to analyse the trophic links between carbon sources

and consumers in ecosystems is nowadays a common prac-

tice. It assumes that the isotopic ratio of a certain carbon or

nitrogen source is transferred to its consumers undergoing

a predictable metabolic fractionation. This predictability

allows us to infer the theoretical diet of consumers by cor-

recting for this fractionation. While numerous isotopic studies

have focussed on the trophic pathways of infralittoral

communities associated with seagrass meadows (Vizzini and

Mazzola, 2003; Holmer et al., 2004; Hyndes and Lavery, 2005;

Carlier et al., 2007), those focussing on supralittoral commu-

nities of sandy beaches are quite rare (Adin and Riera, 2003;

Ince et al., 2007). Assessing the potential transference of

energy and matter from marine sub-tidal to supralittoral

zones is important because it can represent the basis for

sustaining the high biomass and diversity observed in sandy

beach ecosystems (Dugan et al., 2003; Ince et al., 2007).

In this paper we examine the possible role of P. oceanica

wrack as provision of shelter and/or as a trophic niche for the

macroinvertebrate fauna of a sandy beach. For this study the

beach adjacent to the Burano Lagoon (Tuscany, Italy) was

selected because of the conspicuous number of behavioural

and ecological studies that have been conducted there on

beach macrofauna (Scapini et al., 1992; Fallaci et al., 1996,

2002, 2003; Aloia et al., 1999; Colombini et al., 2005). The

colonisation dynamics of experimental wrack by the local

fauna was followed in time (33-day experiment) and space

(grid, sand and wrack compartments) as affected by key

environmental factors (moisture, pH, and conductivity).

Possible trophic links between P. oceanica wrack and macro-

invertebrates were assessed using an isotopic approach. Other

possible sources of carbon and nitrogen from both terrestrial

and marine environments were considered as well.

2. Materials and methods

2.1. Sampling site

The study site was located in a 30-km stretch of coast between

the Ansedonia promontory (southern Tuscany, Grosseto

province) and the Fiora River mouth (northern Latium, Viterbo

province). In this area the coast is characterised by

a morphologically homogeneous beach (oriented from north-

west to south-east) and is exposed (exposure rating ¼ 11.5

according to McLachlan, 1980). In front of this stretch of coast

there is a P. oceanica meadow of ca. 30 km2 at a mean depth of

18 m (Bianchi et al., 1993) (Fig. 1). Close to the promontory of

Ansedonia lies a protected area (WWF Italy, Burano Oasis)

where beach access to the public is controlled. For this reason

the study was conducted here and experiments were carried

out in an area far away (42�2305000N, 11�2204000E) from the beach

entrance. At this point the eulittoral zone included the part of

the beach devoid of vegetation, where beach wrack material

was stranded during heavy sea storms. The mean width of

this zone was 15 m, beach slope was 24.5% and its profile

varied according to wave action, sea currents and wind. Mean

grain size was 1.295 F according to the method of Folk and

Ward (1957). The supralittoral zone extended for 10 m across

the beach and formed the foredune with pioneer plants. The

extralittoral zone, characterised by a dune ca. 8 m in height,

was covered by a typical Mediterranean maquis. The area was

characterised by microtidal excursions with a tidal range of

less than 30 cm (Colombini et al., 2003).

During the period of the study the sand was covered with

drift material, mainly of fluvial origins, but also with scattered

P. oceanica detritus (agaegropiles, leaf litter, and rhizomes).

Nevertheless, a well-developed P. oceanica ‘banquette’ did not

occur, although they could occasionally achieve significant

sizes during sea storms (50-cm piles 3 m in width along a 300-

m stretch of coastline).

2.2. Experimental design

The beaches at Feniglia and Tagliata (north-west and south-

east with respect to the Ansedonia promontory) are

commonly loaded with large banquettes of P. oceanica depos-

ited in areas close to the promontory by the dominant south-

eastern currents. On the Feniglia beach about 150 kg of dried P.

Tagliata

Feniglia

Ansedonia

Burano Lagoon

N

Italy

30 m

50 m

Site locationPosidonia oceanica meadow

5 km

42°23’50”N

11°22’40”E

Tyrrhenian Sea

Fig. 1 – Study site near the Burano lagoon, Tuscany, Italy. The dashed lines indicate bathymetric levels.

a c t a o e c o l o g i c a 3 5 ( 2 0 0 9 ) 3 2 – 4 434

oceanica leaf litter was collected from a large wrack banquette

along a homogeneous beach fascia. In the laboratory the

collected material was placed over nets and dried at 25 �C with

circulating air for 2 months in order to exclude all extant

macrofauna.

Field experiments were carried out from 11 May to 13 June

2005 during a period of theoretically stable climatic condi-

tions. Prior to deployment, P. oceanica leaf litter was soaked in

seawater for 6 h to ensure a homogeneous initial degree of

humidity. One-hundred cylinders (50 cm high, 20 cm in

diameter) were made from green plastic net (9-mm mesh size,

big enough for macroinvertebrates to have free access to the

wrack and to prevent P. oceanica leaf litter from falling out).

Half of the cylinders height was buried into the sand letting

the other half stand above the sand surface. These halves

were separated by a net made of the same material as the

cylinders. The half above the sand was filled to the brim with

1273.5 � 31.2 g (mean and SE) fresh weight of P. oceanica leaf

litter. The cylinders were covered with a plastic lid pressed

with a 1-kg sand bag to obtain similar compacted experi-

mental wracks and to prevent the material from being blown

out by the wind. The leaf compartment of the experimental

cylinder will be hereafter referred to as ‘wrack’. The sand

compartment below the wrack will be referred to as ‘below

wrack sand’(BWS).

A grid, consisting of 100 transects separated from each

other by 3 m and laid perpendicularly to the shoreline was

designed. For each transect, beginning at 1 m from the

shoreline, five positions, at 3-m intervals, were determined

over the eulittoral. The grid therefore resulted in 500 positions

and covered a rectangular area of the beach 297 � 12 m. At the

beginning of the experiment, of the 500 possible positions 100

cylinders were placed over the grid, 20 for each of the five

distances from the shoreline. The position of the latter was

determined according to a computer random generated

distribution pattern.

2.3. Sampling procedures

In order to assess species succession after the deposition of

the material, two experimental cylinders plus two control

sand samples for each distance from the sea were collected

between 08:00 and 10:00 am at 1, 2, 3, 4, 5, 8, 13, 19, 26, and 33-

day intervals from the onset of the experiment. A higher

sampling frequency was conducted during the first days of the

experiment because greater microclimatic changes (especially

for moisture contents) were expected in the wrack in this

period (Messana et al., 1977). After the fifth sampling session

a 5–7-day sampling interval was carried out except for day 8

when a sudden heavy rainfall occurred and the experimental

wracks were checked. Controls consisted of sand cores (25 cm

in height, 20 cm in diameter) sampled at a 1-m distance from

each corresponding experimental cylinder parallel to the

shore. Control cores will be hereafter referred to as ‘control

sand’ (CS). All samples (wrack, BWS, and CS) were collected

separately in thermally-sealed plastic bags. All macro-

invertebrates found were immediately extracted using sieves.

For sand samples 1-mm mesh size was used, whereas for

wrack samples leaves were separated with sieves of 4 mm and

specimens remaining in or escaping the mesh were hand

collected. Individuals were sorted and, when possible, taxo-

nomically classified to species level. A sex ratio was deter-

mined for the two Phaleria species. A size–frequency analysis

was applied to check whether the larvae of Phaleria spp. could

be grouped in different classes according to their size (total

length). This was executed by using the probability paper

method (Harding, 1949). Reliability was tested by employing

both chi-squared and G tests ( p < 0.05) (Zar, 1984). Computa-

tion was executed using ANAMOD 1.6 software (Nogueira,

1992).

Wrack samples were immediately weighed after collection.

Sub-samples (ca. 100 g each) of wrack and sand (for BWS and

CS) were collected and stored in the refrigerator prior to

a c t a o e c o l o g i c a 3 5 ( 2 0 0 9 ) 3 2 – 4 4 35

determination of moisture content (%), conductivity (mS/cm)

and pH according to standard methods (Black, 1973). Moisture

was calculated as the difference between wet and dry weight

(before and after drying at 105 �C until constant weight).

Conductivity and pH were measured after stirring a suspen-

sion of 5 g of sample for 15 min in 100 or 25 ml of demineral-

ised water for P. oceanica and sand samples, respectively.

2.4. Isotopic analysis

At the experimental site, five pitfall traps were deployed at 3-

m intervals from the shore to the base of the dune and kept

operative for 24 h to collect individuals that were used for

stable isotope determination for food web analysis. For this

analysis some macroinvertebrates were selected according to

their trophic level (detritivores, predators). Individuals were

kept alive for 24 h to allow evacuation of gut contents and

then were frozen at �20 �C. For amphipods and isopods two

age class were selected. For amphipods the two classes were

chosen according to the number of articles of the second

antennal flagellum: <10 articles (juveniles) and >20 articles

(adults). For isopods the two classes were selected according

to the maximum width of the 4th pereionit:<3 mm (juveniles)

and >5 mm (adults). The intermediate classes were not

selected because the aim was to assess clear differences

between the two age classes. Prior to isotopic analysis the

specimens were dried at 70 �C until constant weight and

stored in a dry, dark environment.

For isotopic analysis freshly deposited P. oceanica was also

collected along the shoreline in front of the experimental area.

Samples of the most abundant vascular plants occurring in

the foredune (Anthemis maritima L., Cakile maritima Scop.,

Crucianella maritima L., Elymus farctus (Viv.) Runem., Otanthus

maritimus (L.) Hoffmanns et Links, Salsola kali L., Sporobolus

pungens (Schreber) Kunt, Medicago marina L.) and in the dune

system (Juniperus oxycedrus L., J. phoenicea L.) adjacent to the

experimental area were collected in order to assess their

possible use as food for the beach community of macro-

invertebrates or if P. oceanica wrack deposits contributed in

some way as humus for dune vegetation.

Each replicate of macroinvertebrates consisted of 4–10

individuals. An aliquot of ca. 0.7 mg of that composite sample

was used for isotopic determination. The elimination of

carbonates by acidification prior to isotopic analysis was

considered only for crustacean species (Mateo et al., 2008;

Serrano et al., 2008). Acidification consisted of the addition of

1-M HCl drop-by-drop and left in acid for 3 h to eliminate

possible traces of carbonates (Nieuwenhuize et al., 1994). Non-

acidified aliquots were used for d15N determination. P. oceanica

leaf was gently scraped to eliminate epiphytes. A ca. 1.5-mg

dry weight (DW) aliquot of P. oceanica leaf litter from a 5-g DW

powdered bulk sample was used. Only green leaf material

from four individuals of each species of dune vascular plants

was used. For each individual 1 g DW leaf material was dried,

milled and from this material 1.2 mg was encapsulated for

isotopic analysis. The intact portion (about 70 g) of all control

sand samples (n ¼ 100) was sieved using a 125-mm sieve to

extract sand organic matter. Prior to sieving at each distance

from the sea shore (1, 4, 7, 10, and 13 m) samples were grouped

into five cumulated samples for each distance so as to obtain

an adequate organic content for the isotope analysis. The

material passing the sieve was acidified as described above.

Around 6 mg of the resulting material were used to obtain the

isotopic ratios of the sand organic matter (SOMb). A mean

beach SOMb was calculated for 1–4 m (SOMb1) and for 7–13 m

(SOMb2) from the sea shore. The first two distances were

separated from the remaining ones because they were under

the major influence of the sea.

Carbon and nitrogen isotopic signatures were measured

from the gasses evolved from sample combustion in a Fin-

nigan Delta S isotope ratio mass spectrometer (Conflo II

interface) at the Scientific–Technical Services of the Univer-

sity of Barcelona. Isotopic values are reported in the d notation

relative to the standards Vienna Pee Dee Belemnite for carbon

and air for nitrogen (dsample ¼ [(Rsample/Rstandard) � 1] � 1000,

R ¼ 13C/12C, or R ¼ 15N/14N). Analytical precision based on the

standard deviation of internal standards (atropine, IAEA CH3,

CH6, CH7, and USGS40 – analytical grade L-glutamic acid, for

carbon, and atropine, IAEA N1, NO3, N2, and USGS40, for

nitrogen) ranged from 0.06 to 0.11& (mean ¼ 0.09&) for

carbon, and from 0.06 to 0.28& (mean ¼ 0.16&) for nitrogen.

2.5. Numerical procedures and statistical analysis

All data were checked for normality (Kolmogorov–Smirnov

test) and for variance homogeneity (Levene’s test) (Zar, 1984).

For experimental cylinders and controls a two-factor

ANOVA was performed to assess differences of species rich-

ness and ln(n þ 1) transformed abundance of macro-

invertebrates in space (five distances) and in time (ten days).

To compare species richness of experimental cylinders with

that of controls a paired-sample t-test was used. Spearman’s

rank correlation was used to test the association between

macroinvertebrate zonation in the experimental wracks and

time. This was obtained considering the day of capture and

distance from the shoreline for each individual.

To identify the spatial and temporal distributions of the 10

most abundant taxa Hotelling’s confidence ellipses (Batsche-

let, 1981) were calculated at a 95% level of probability. To

assess the differences between the distributions of the

selected taxa Hotelling’s two-sample test was used (Batsche-

let, 1981). A one-factor ANOVA was performed to ascertain if

differences were dependent on both spatial and temporal

factors or only on one factor.

The environmental parameters (moisture content,

conductivity and pH) of the different compartments were

correlated with space and time using Spearman’s rank

correlation.

In order to test the relationships between macrofauna and

environmental parameters, a presence–absence approach

was used associated to univariate parametric t-tests. In this

analysis, pairs of data series of the parameters were

compared, one series with values of all samples where at least

one individual was recorded, and another series with values

where no individuals occurred. For macroinvertebrate abun-

dances the statistical requirements of normality and variance

homogeneity were met when the data were ln(n þ 1) trans-

formed and zero counts were eliminated from the data series.

Furthermore, multiple linear regressions were carried out

Table 1 – Total captures of macroinvertebrates in theexperimental cylinders and controls taking into accounttheir distribution across compartments

Experimental cylinders CS Total

Wrack BWS

1 Tylos europaeus 118 22 152 292

2 Talitrus saltator 1574 41 185 1800

3 Aranei 67 10 2 79

4 Diptera 465 0 0 465

5 Staphylinidae 86 0 0 86

6 Brachygluta globulicollis 37 0 0 37

7 Phaleria bimaculata 86 28 3 117

8 Phaleria provincialis 7 3 1 11

9 Phaleria spp. larvae 265 51 34 350

10 Trachyscelis aphodioides 1 16 9 26

11 Formicidae 51 1 0 52

12 Others 85 11 9 105

Total 2842 183 395 3420

BWS, below wrack sand; CS, control sand.

a c t a o e c o l o g i c a 3 5 ( 2 0 0 9 ) 3 2 – 4 436

between most abundant macrofauna species and environ-

mental parameters.

Significant levels of probability were considered when

p < 0.05.

Animal species were separated a priori into two trophic

categories, depending on whether they were considered

‘detritivores’ or ‘predators’ (Caussanel, 1970). In a wide range

of consumer–food pairs, the isotopic content of an animal

has been found on average to be 1& (d13C) and 3.4& (d15N)

higher than that of its food (DeNiro and Epstein, 1978, 1981).

More recent literature reviews (Ponsard and Arditi, 2000; Post,

2002) give similar values so the quoted figures were consid-

ered to be the best available estimates of the means of

enrichment per trophic transfer. Theoretical food sources

were visually assigned to consumers using co-plots of d13C

versus d15N relying on the assumption that isotope signals

change in a predictable manner as they flow along the

trophic web.

For sediment organic matter (SOMp), seston, and epiphytes

(exclusively associated to P. oceanica meadows) values were

drawn from the literature (Vizzini et al., 2002, 2005; Adin and

Riera, 2003; Vizzini and Mazzola, 2003, 2006; Holmer et al.,

2004).

All statistical analyses were performed using STATISTICA

7.1 (STATSOFT, Inc, OK, USA and SPSS (SPSS Inc. Release 6.0)

statistical software packages.

Table 2 – Two-factor analysis of variance for ln(n D 1) transformin the experimental cylinders and in the controls

Experimental cylinders

Abundance Species richness

Time 21.474*** 5.192***

Space 1.900 NS 2.280 NS

Time � space 2.142* 0.979 NS

Residuals

(*p < 0.05; ***p < 0.001; NS, not significant; df, degrees of freedom).

Values represent F ratio

3. Results

3.1. Macroinvertebrate abundance: temporal and spatialpatterns

Adding up the 10 days of sampling, 3420 arthropods were

caught from all compartments (Table 1). From these, 52.6%

were Amphipoda (Talitrus saltator Montagu), 13.6% Diptera

(mainly Thoracochaeta brachystoma Stenhammar) and 8.7%

Isopoda (Tylos europaeus Arcangeli). Of the Coleoptera, the two

tenebrionids of the Phaleria genus (Phaleria bimaculata L., Pha-

leria provincialis Fauvel), and in particular their larvae, were the

most representative species (14.0% of the total). P. bimaculata

was more abundant (n ¼ 117) than its sympatric species

(n ¼ 11) and presumably the majority of the larvae belonged to

the former species. Predatory species, belonging to the

Staphylinidae (e.g. Cafius xantholoma Granvenhorst) and Pse-

laphidae (Brachygluta globulicollis Mulsant and Rey) families,

together with Aranei (mainly Arctosa cinerea Fabricius) and

Formicidae were less abundant.

The distribution of macroinvertebrate abundance among

the three compartments considered (wrack, BWS, and CS)

was very heterogeneous (Table 1). The majority of individ-

uals collected were sampled in the wrack (83.1%), while only

5.4% were in the sand below the wrack. Control samples

yield 11.5% of the total captures. This preference for the

experimental cylinders (wrack and BWS) was general except

for Tylos europaeus and Trachyscelis aphodioides Latreille where

no preferences were recorded (c2 ¼ 0.41 NS, c2 ¼ 1.88 NS,

respectively). In the experimental cylinders the sex ratio of P.

bimaculata was female biased (\/_ ¼ 2.8, c2 ¼ 24.64, p < 0.001)

with females more abundant than males in the first 2 days of

sampling (\/_ day 1 ¼ 4.28, c2 ¼ 13.08, p < 0.001, n ¼ 37; day

2 ¼ 7.6, c2 ¼ 23.81, p < 0.001, n ¼ 43; other days ¼ 0.89,

c2 ¼ 0.03, NS, n ¼ 34). Instead, in the pitfall traps sex ratio

was male biased (\/_: pitfalls ¼ 0.86, c2 ¼ 6.67, p < 0.01,

n ¼ 1215).

The analysis of variance for macroinvertebrate abundance

and species richness showed highly significant differences

through time in the experimental cylinders, whereas no

differences were found in space (Table 2). However a signifi-

cant interaction occurred between space and time only for the

number of individuals. Also in the controls abundance and

species richness showed variations through time and only for

abundance highly significant differences were found among

distances. Paired-sample t-test between species richness of

ed abundance and species richness of macroinvertebrates

Controls

df Abundance Species richness df

9 2.460* 2.741* 9

4 6.483*** 1.375 NS 4

30 1.523 NS 1.090 NS 36

42 50

0

2

4

6

8

10

12

14

16

0 5 10 15 20 25 30 35Day

Distan

ce fro

m sh

orelin

e (m

)

21

34 5

6

7 9

10

11

2

1

Fig. 2 – Hotelling’s confidence ellipse (95%) of mean day of

appearance and across-shore mean zonation of the

different beach macroinvertebrates in the experimental

cylinders (empty ellipses) and controls (shaded ellipses).

The numbers near the ellipses indicate the taxa as

reported in Table 1.

a c t a o e c o l o g i c a 3 5 ( 2 0 0 9 ) 3 2 – 4 4 37

experimental cylinders and that of controls showed higher

values for the former (t ¼ 15.99, p < 0.001, n ¼ 86).

In the experimental cylinders the distance of macro-

invertebrates from the sealine increased throughout the

period of the experiment (rs ¼ 0.617, p < 0.001, n ¼ 3025). In

particular, the analysis of the 10 most abundant taxa through

space and time (Fig. 2) showed that the two crustaceans were

the first species to massively invade the experimental cylin-

ders, showing a mean day of presence (mdp) of 1.40 days and

2.13 days after the beginning of the experiment for T. saltator

and T. europaeus, respectively (Fig. 2). Furthermore, crusta-

ceans had the tendency to occupy the experimental cylinders

closer to the sea with a mean zonation of 1.56 and 2.63 m from

the shoreline for the two species, respectively. Hotelling’s

two-sample test showed highly significant difference between

Table 3 – Hotelling’s two-sample tests and one-factor ANOVA o(n1, capture number of the first taxon; n2, capture number of th

Hotelling’s t

Experimental cylinders

T. europaeus vs. T. saltator 26.775***

Staphylinidae vs. B. globulicollis 0.922 NS

Staphylinidae vs. P. bimaculata 5.780**

P. bimaculata vs. Phaleria spp. larvae 9.546***

P. bimaculata female vs. male 12.265***

P. bimaculata female vs. Phaleria spp. larval stage 1 28.556***

P. bimaculata female vs. Phaleria spp. larval stage 2 7.703***

P. bimaculata female vs. Phaleria spp. larval stage 3 2.270 NS

Phaleria spp. larval stage 1 vs. stage 2 8.303***

Phaleria spp. larval stage 1 vs. stage 3 3.185*

Phaleria spp. larval stage 2 vs. stage 3 0.993 NS

Controls

T. europaeus vs. T. saltator 29.119***

Experimental cylinders vs. controls

T. europaeus 71.870***

T. saltator 764.933***

*p < 0.01, **p < 0.01, ***p < 0.001; NS, not significant.

isopods and amphipods (Table 3) in space and time. Control

samples showed differences between T. saltator and T. euro-

paeus (Fig. 2, Table 3) with a mdp of 16.29 and 12.67 days,

respectively. For T. saltator the results obtained for the

experimental cylinders and CS were different but only from

a temporal point of view, whereas for T. europaeus differences

were both in space and time.

Non-crustacean species colonised experimental cylinders

higher up on the eulittoral with dipterans already appearing

after day 2 (mdp ¼ 2.41 days). Predatory species, such as

staphylinids and B. globulicollis contemporaneously appeared

(mdp ¼ 4.29 and 4.32 days, respectively) (Table 3) after the

dipterans, whereas the most important tenebrionid species

occurred in the wracks after day 5 and 23 (mdp ¼ 5.42 and

23.59 days for P. bimaculata, and T. aphodioides, respectively)

but at a higher distance from the shoreline compared to

predatory species (Fig 2, Table 3). P. bimaculata (Table 3)

showed temporal differences between sex (females

mdp ¼ 3.17, males mdp ¼ 11.73) and with its larvae

(mdp ¼ 8.58), with females differing in mean day of appear-

ance from the first and second larval stage (stage 1

mdp ¼ 10.42, stage 2 mdp ¼ 6.75, stage 3 mdp ¼ 4.88). For-

micidae and Aranei occurred on the experimental cylinders

after day 7 and 11 (mdp ¼ 7.32 and 11.62 days, respectively).

3.2. Environmental parameters

Overall, moisture content in all compartments showed

a decrease both in time and along the sea–land axis and

a significant negative rank correlation occurred in all cases

(Fig. 3). Wrack and BWS moisture decreased from 67 to 14%

and from 2.0 to 0.8%, respectively, during the experimental

period, while in CS the decrease in moisture was from 2.5 to

1.4% for the same period. Wrack material near the seashore

(samples at 1-m distance) was 1.5 times more humid than the

f spatial and temporal distributions of macroinvertebratese second taxon)

est One-factor ANOVA n1 n2

Time Space

14.355*** 49.063*** 140 1615

0.002 NS 1.807 NS 86 37

1.115 NS 9.513 NS 86 114

11.131*** 4.899* 114 316

24.010*** 1.325 NS 84 30

48.941*** 2.388 NS 84 166

13.696*** 0.751 NS 84 133

1.323 NS 3.194 NS 84 17

14.179*** 0.561 NS 166 133

6.336* 0.692 NS 166 17

0.864 NS 1.449 NS 133 17

6.218* 58.101*** 152 185

98.162*** 7.244** 140 152

1529.664*** 0.232 NS 1615 185

Wrack

ba

c d

e f

rs = -0.252p < 0.05

01020304050607080

Mo

istu

re (%

)

rs= -0.817p < 0.001

Below wrack sand

00.5

11.5

22.5

33.5

4

Mo

istu

re (%

)

rs = -0.296p < 0.01

rs= -0.665p < 0.001

Control sand

00.5

11.5

22.5

33.5

14.5

5

0 5 10 15 20 25 30 35Day

Mo

istu

re (%

)

rs= -0.375p < 0.001

0 2 4 6 8 10 12 14Distance from shoreline (m)

rs = -0.565p < 0.001

Fig. 3 – Mean moisture contents with 95% confidence limits are shown in the three compartments (wrack n [ 84, BWS

n [ 86, CS n [ 100) during the course of the experiment and at increasing distance from the shoreline. Spearman’s rank

correlation coefficients and their probability are also reported.

a c t a o e c o l o g i c a 3 5 ( 2 0 0 9 ) 3 2 – 4 438

rest of the material. BWS and CS showed similar decreasing

patterns, from 3.4% of moisture near the shore to 1.4% next to

the dune.

Conductivity decreased significantly in time only for wrack

(rs ¼ �0.348, p < 0.01, n ¼ 84) and in time and space for CS

(time: rs ¼ �0.265, p < 0.01, n ¼ 100; space: rs ¼ �0.581,

p < 0.001, n ¼ 100). There was no significant pattern in

conductivity in BWS.

The pH was lowest in the P. oceanica wrack (7.8 on average)

compared to other compartments. For wrack there was a very

slight decreased (ca. 0.1 units) in time and space (time:

rs ¼ �0.319, p < 0.01, n ¼ 84; space: rs ¼ �0.295, p < 0.01,

n ¼ 84), whereas for CS (ca. 0.2 units) a slight increase was

recorded during the course of the experiment (rs ¼ 0.300,

p < 0.01, n ¼ 100) and from the shoreline to the dune

(rs ¼ 0.275, p < 0.01, n ¼ 100). Instead, no consistent pattern in

time or space was observed in the pH of BWS.

3.3. Relationship between macroinvertebrates andenvironmental parameters

In general, the univariate t-tests (Table 4) showed significantly

higher values in the moisture contents of samples where

macroinvertebrates were present compared to those where

they were absent. Instead, tenebrionid species were present

where moisture contents were lower. Crustacean species

preferentially colonised wrack and sand samples with mois-

ture contents ranging from 50 to 75% and from 2 to 5%,

respectively. P. bimaculata with its larvae, were mainly found

in BWS when moisture contents were lower than 2.5%. Higher

values of conductivity occurred in wrack where T. europaeus

and Diptera were present and in CS where the two crusta-

ceans occurred. For the groups where univariate t-tests were

significant, a mean pH value of 7.85 was found in samples

where individuals were present. In particular, in wrack

samples pH values were higher where taxa were present

compared to where they were absent, while in CS the opposite

occurred.

Multiple regression analysis between macroinvertebrates

and environmental parameters (Table 5) showed that T. sal-

tator had positive correlations with moisture contents in the

experimental cylinders and in controls and a negative one

with conductivity of the wrack. In controls T. europaeus was

more abundant where higher sand moisture contents

occurred, whereas in the experimental cylinders isopods

were negatively correlated with conductivity in the wrack

Table 4 – Univariate t-tests for independent samplescomparing environmental parameters (moisture content,conductivity, pH) with presence or absence ofmacroinvertebrates for the three compartmentsconsidered

Moisture Conductivity pH

Wrack (n ¼ 84)

T. europaeus 4.56*** 2.00* –

T. saltator 5.32*** – 3.54***

Diptera 7.57*** 2.99** 3.66***

Staphylinidae 7.60*** – –

B. globulicollis 4.41*** – 2.52*

P. bimaculata – – 2.51*

T. aphodioides �4.01*** – –

BWS (n ¼ 86)

T. europaeus 4.30*** – –

T. saltator 4.78*** – –

Staphylinidae 2.38* – –

B. globulicollis 3.00** – –

P. bimaculata �2.60* – –

Phaleria spp. Larvae �3.33** – –

T. aphodioides �3.27** – –

CS (n ¼ 100)

T. europaeus 2.48* 3.98*** �3.60***

T. saltator 2.79** 3.74*** �2.63**

t values are positive when means of parameter where taxa were

present were higher than those where they were absent and

negative when means were lower where individuals were present.

Non-significant taxa are not shown and dashes indicate non-

significant differences. For further explanations see Tables 1 and 2.

a c t a o e c o l o g i c a 3 5 ( 2 0 0 9 ) 3 2 – 4 4 39

and positively with pH of the sand. For the tenebrionid

P. bimaculata a positive relationship with moisture contents

of the wrack was found, whereas its larvae were negatively

correlated with sand conductivity of the experimental

cylinders.

3.4. Stable isotopes

The carbon isotopic composition of the macroinvertebrates

captured over the experimental area ranged from �25.6&

measured for the predatory carabid Scarites buparius (Forster)

to �19.0& recorded in the isopod T. europaeus (Table 6).

Table 5 – Multiple linear regressions between ln(n D 1) transfoparameters (moisture, conductivity, pH) of wrack and sand

Wrack

Moisture (%) Conductivity (mS cm�1) Moistu

Experimental cylinders

T. europaeus – �0.424* –

T. saltator 0.078** �0.670* 0.97

P. bimaculata 0.012** – –

Phaleria spp. larvae – – –

Controls

T. europaeus 0.60

T. saltator 1.08

Non-significant taxa and parameters are not shown. Dashes indicate n

Table 2.

Nitrogen isotopic ratios were lowest, 3.4&, in S. buparius and

highest, 11.7&, in the predatory coleopteran Parallelomorphus

laevigatus (Fabricius). The average d13C and d15N values for

macroinvertebrates feeding on detritus (excluding the Tene-

brionidae Pimelia bipunctata Fabricius) were respectively

�20.8 � 0.36& (SE) and 8.3 � 0.4&, while the same average

figures for the four predatory species captured were

�22.7 � 1.1& and 8.2 � 1.8&, respectively.

All sand plants collected in the area presented largely

distinct isotopic signatures from those of macroinvertebrates

(Table 6). With the exception of C. maritima and S. kali, all of

them yielded negative d15N values. Carbon isotopic signatures

in the plants were on average more negative than in the

macroinvertebrates (�25.6 and �21.8&, respectively). The

genus Juniperus presented distinct carbon and nitrogen

isotopic signatures from the rest of the plants. The Cheno-

podiacea S. kali and the Brassicacea C. maritima showed

exceptionally high nitrogen isotopic ratios (around 6&) and

the maximum and the minimum d13C values (�12.2 and

�30.8&, respectively).

P. oceanica leaf was highly enriched in 13C with respect to the

rest of the sample analysed (�12.7& on average). The literature

review on isotopic signatures of SOMp and seston associated

with P. oceanica meadows, and on P. oceanica epiphytes, yielded

d13C and d15N values ranging from �20.6 to �15.9& and from

4.9 to 6.3& (Table 6). While epiphytes and SOMp were enriched

in 13C with respect to the macroinvertebrates (ca. 4–6&), the

average d13C values for seston and macroinvertebrates were

similar. The average d15N for macroinvertebrates was higher

(ca. 3&) than that of seston. The total SOMb was �21.6 and

4.1& for d13C and d15N values, respectively. Furthermore,

proceeding landwards d13C of SOMb significantly decreased

(SOMb ¼ �0.364 � distance � 19.084, R2 ¼ 0.835, p < 0.001,

n ¼ 24).

4. Discussion

This experiment, conducted in the field in semi-natural

conditions, is an attempt to follow species succession and

colonisation of wracks through time keeping fixed patch size,

an important variable influencing macrofaunal abundance. In

rmed abundance without zero counts and environmental

Sand Constant R2 n

re (%) Conductivity (mS cm�1) pH

– 0.803* – 0.325* 28

3* – – – 0.475** 24

– – 0.647** 0.200** 34

�4.016** – 2.546*** 0.102** 69

5*** – – – 0.359*** 36

0*** – – �1.502* 0.590*** 22

on-significant regression coefficients. For further explanations see

Table 6 – Isotopic signatures for the beach-dune macroinvertebrates, plants (green leaves), P. oceanica (leaf litter), beachsand organic matter (SOMb), and literature values for sediment organic matter of P. oceanica beds (SOMp), seston andepiphytes, these last values exclusively associated to P. oceanica meadows

Abbreviation d13C d15N

Mean n SE Mean n SE

Animal species

Arctosa cinerea Arc �20.8 4 0.05 10.1 4 0.03

Geophilus sp. Geo �23.2 4 0.23 7.5 4 0.37

Parallelomorphus laevigatus Par �21.0 3 0.01 11.7 4 0.04

Phaleria bimaculata PhBi �21.6 3 0.13 8.9 4 0.14

Phaleria provincialis PhPr �21.1 4 0.10 9.1 4 0.13

Phaleria spp. (larvae) PhLa �20.7 4 0.19 9.4 4 0.29

Pimelia bipunctata Pim �24.7 4 0.03 4.6 4 0.06

Scarites buparius Sca �25.6 3 0.58 3.4 4 0.18

Talitrus saltator (adult) TalAd �21.9 4 0.17 6.5 5 0.05

Talitrus saltator (juvenile) TalJu �21.2 4 0.07 7.3 5 0.06

Tylos europaeus (adult) TylAd �19.0 4 0.31 8.9 4 0.05

Tylos europaeus (juvenile) TylJu �20.5 4 0.11 8.3 4 0.04

Animal mean �21.8 45 0.55 8.0 50 0.65

Plant species

Anthemis maritima Ant �27.6 4 0.19 �2.6 4 0.15

Cakile maritima Cak �30.8 4 0.17 6.0 4 0.10

Crucianella maritima Cru �29.7 4 0.36 �2.8 4 0.34

Elymus farctus Ely �25.5 4 0.14 �3.8 4 0.08

Juniperus oxycedrus J.ox �22.9 4 0.23 �5.3 4 0.11

Juniperus phoenica J.ph �24.7 4 0.16 �6.4 4 0.12

Medicago marina Med �27.4 4 0.16 �0.8 4 0.06

Otanthus maritimus Ota �27.3 4 0.21 �2.3 4 0.19

Salsola kali Sal �12.2 4 0.12 6.2 4 0.10

Sporobolus pungens Spo �27.9 4 0.23 �3.4 4 0.24

Plant mean �25.6 40 1.66 �1.5 40 1.36

Posidonia oceanic Pos �12.7 9 0.25 4.5 9 0.28

Sand organic matter – beach sand 1– 4 m SOMb1 �19.9 10 0.34 4.5 5 0.53

Sand organic matter – beach sand 7–13 m SOMb2 �22.8 14 0.27 3.8 8 0.26

Sand organic matter – beach sand total SOMb �21.6 24 0.36 4.1 13 0.27

Literature values

Sediment organic matter – P. oceanica SOMp �17.7 54 0.41 5.3 42 0.38

Seston Ses �20.6 8 0.86 4.9 3 0.72

Epiphytes (P. oceanica) Epi �15.9 12 0.48 6.3 12 0.49

a c t a o e c o l o g i c a 3 5 ( 2 0 0 9 ) 3 2 – 4 440

fact, Olabarria et al. (2007), comparing different size patches of

stranded detritus, found significant differences with higher

abundance and species richness in medium and larger

patches compared to smaller ones. In the present study the

initial evenness of patches with no extant macrofauna

permitted an equal starting point in all locations of the grid

irrespective of their position on the beach. The experiment

showed that macroinvertebrates preferred areas with wrack

compared to bare sand and that in the experimental cylinders

abundance decreased through time. Also species richness

changed during the course of the experiment with higher

values in the wracks compared to those of controls.

A main outcome of the study was that as soon as wracks

were deployed they were promptly invaded by early colo-

nisers with higher numbers of crustaceans in wracks closer to

the sea. In particular, the two crustacean species analysed

here colonised wracks differently both in space and in time.

The presence of amphipods and isopods as primary colonisers

has already been reported by many authors (Inglis, 1989;

Marsden, 1991; Colombini et al., 2000; Dugan et al., 2003).

However, in this study crustaceans abandoned the wracks

after the first days, whereas in the controls they were present

throughout the entire study period. Departure of the crusta-

ceans from the wrack can be related to the variations of the

microclimatic conditions of the wracks and in particular to

that of their moisture content. This parameter decreased

significantly both along the sea–land axis and during the

course of the experiment. Our results showed that the

experimental wracks were inhabited by crustaceans when

moisture contents were relatively high. However, when

experimental wracks dried out they became unattractive to

crustaceans but attractive to other species. In this case the

mechanism involved seems to be related to the different

thresholds for certain parameters of the different taxa.

Abundance of crustaceans declined drastically from the

wracks when the minimum threshold for wrack moisture was

reached (below 50%). Furthermore, crustaceans were present

in the wrack and control sand where higher values of

conductivity were found, even if in wrack, within a certain

range (6.2–8.5 mS cm�1), a negative correlation with this

parameter occurred. Moreover for pH, within the species’

thresholds, crustaceans always preferred the same mean

a c t a o e c o l o g i c a 3 5 ( 2 0 0 9 ) 3 2 – 4 4 41

value that occurred among the higher values in wrack and

among the lower ones in control sand, thus confirming the

findings of Colombini et al. (2005). Generally, talitrids are

known to possess great behavioural plasticity being capable of

reducing unfavourable diurnal conditions, such as extreme

temperatures and desiccation, by changing their position both

vertically and horizontally on the beach (Scapini et al., 1992;

Fallaci et al., 2003). So when talitrids experienced unsuitable

microclimatic conditions in the wracks these were abandoned

immediately.

The presence of the dipteran species (T. brachystoma) on the

more landward wracks already after 2 days confirms the

findings of Hodge and Arthur (1997) for other species of British

seaweed flies (Coelopa frigida Fabricius, Coelopa pilipes Haliday,

Thoracochaeta zosterae Stenhammar;) in which all three

dipteran species had arrived on wracks by day 2. Coelopa larvae

generally fed on bacterial populations (Cullen et al., 1987) and

their developmental rate was generally associated with

temperature conditions (Phillips et al., 1995). The same pattern

probably occurred for T. brachystoma in the P. oceanica leaves.

Consequently, the presence of eggs and larvae of dipterans in

the wrack attracted predators, such as staphylinids (C. xan-

tholoma) and pselaphids (B. globulicollis), as was demonstrated

by feeding experiments on C. xantholoma in which a strict

predator–prey relationship occurred (Backlund, 1945).

Tenebrionids (P. bimaculata and its larvae) were mid-

invaders and preferentially occupied experimental wracks

higher up on the eulittoral in relation to their preference for

lower moisture contents in the sand (Aloia et al., 1999;

Colombini et al., 2005). The differences found in the sex ratios

in the experimental wracks compared to the active population

(see pitfall traps) indicated that females were attracted to the

experimental cylinders before males suggesting that wracks,

or sand beneath the wracks, might be used as sites for ovi-

deposition. Another fact supporting this hypothesis was the

appearance of the first larval stage a week after female colo-

nisation. The other larger larval stages invaded the wracks

slightly after adults meaning that wracks could attract pre-

existing larvae and be used as an important nursery ground by

these tenebrionids. The tenebrionid T. aphodioides was defin-

itively a late invader appearing on wracks only in the last

period of the experiment. A process of interspecific facilitation

has been suggested by some authors (Schoenly and Reid, 1987;

Heard, 1994) with late species benefiting from the presence of

the earlier arrival of primary colonists. The presence of early

arrivals modifies the resource qualitatively and makes it more

suitable for later invaders. Another process probably involved

is reciprocal avoidance due to the temporal separation that

reduced levels of interspecific interference at the food source.

In general, the presence of a specific fauna in the wrack is thus

the result of a combination of factors such as species adap-

tation to specific microclimatic conditions of the wracks, and

the need to find an adequate food source benefiting from the

presence of other species (both bacteria and invertebrates) on

the wrack. Changes in the microclimatic conditions of the

wrack suggest that beach deposits might represent an

important but quite transient resource for food and shelter for

resident macroinvertebrates as was also shown for stranded

wracks of beaches in tropical and temperate areas (Colombini

et al., 2000; Colombini and Chelazzi, 2003; Orr et al., 2005).

With the exception of seston and sand organic matter

(SOMb), the rest of the potential sources of organic carbon

considered in this study showed clearly distinct d13C vs. d15N

values from the macroinvertebrate fauna. Accepting the

broadly mean trophic enrichment in d13C of 1& (DeNiro and

Epstein, 1978) and in d15N of 3.4& (DeNiro and Epstein, 1981;

Minagawa and Wada, 1984), the expected mean isotopic ratios

for the preferentially exploited food resource by the non-

predatory macroinvertebrate species would be around �21.8

and 4.9& for d13C and d15N, respectively (Fig. 4). The only

exception was P. bipunctata that presented a theoretical diet of

�23.7 and 1.2&. This species was distributed in a more land-

ward area compared to other scavengers (Fallaci et al., 1997;

Aloia et al., 1999) and thus probably foraged on more terres-

trial resources. Adults and juveniles of T. saltator clearly did

not directly feed on P. oceanica leaves as shown by the isotopic

results, but probably took refuge in wracks in search of shelter

and suitable microclimatic conditions during the day. This

finding is in accordance with the results of Adin and Riera

(2003) that showed that neither dune plants (Agropyrum jun-

ceum, L., Atriplex laciniata L.) nor seagrass (Zostera marina L.)

were used as food sources by T. saltator. These authors sug-

gested that several macroalgal species occurring in the

strandline could contribute to the diet of T. saltator even if this

amphipod preferentially utilised Fucus sp. as main food

source. P. oceanica was the most d13C enriched and this result

was in good agreement with other data reported in the liter-

ature (Vizzini et al., 2002; Carlier et al., 2007). There are several

rationales supporting the theory that seagrasses do not

significantly contribute to the basis of the food web in marine

habitats because they are too C13-enriched compared to

primary consumers (Gacia et al., 2002; Vizzini et al., 2002;

Hyndes and Lavery, 2005) and this seems to occur also for

beach stranded P. oceanica leaves. Tylos europaeus presented

a theoretical diet with values very close to those obtained for

SOMb, especially for juveniles. A similar result was also

obtained for another oniscid, Tylos ponticus Grebnitzky, for

which a marine type of diet (with more algae compared to

seagrass) was suggested by both the isotopic results and the

feeding preference experiments (Dias and Hassall, 2005). Our

findings at Burano strongly suggest that the seston of the

water column is the main organic matter supplier for sandy

beaches with low macroalgae inputs, in particular for the

areas closer to the seashore (Fig. 4). This is supported by the

clear impoverishment of the SOMb in d13C from the seashore

to the dune, probably reflecting the change in the proportion

of organic matter contributed by the seston or by the dune

vegetation. The seston, carried by the water washing the

shore, seems to be retained by the sand that acts as a particle

filter. The isotopic composition of the SOMb1, collected at 1–

4 m from the shoreline, is similar to that of the seston, and the

average isotopic composition of the SOMb, all over the studied

area, matches perfectly with the theoretical diet and range

(see box in Fig. 4) of the detritus feeders considered in this

study assuming a wider range of metabolic increase as gath-

ered from the literature (from 0 to 1& for d13C and from 1 to 5&

for d15N, Minagawa and Wada, 1984; Post, 2002).

The theoretical diets calculated for the predators have

shown that P. laevigatus seems to feed predominantly on

Phaleria spp., the diet of A. cinerea seems based purely on adult

-34 -32 -30 -28 -26 -24 -22 -20 -18 -16 -14 -12 -10-8

-6

-4

-2

0

2

4

6

8

10

12

14

Cak

Par

ArcTylAd

TylJuvTalJuvTalAd

Pos

Sal

Sca

GeoPhBi

PhLa

Pim

PhPr

Cru

Med

OtaAnt

Spo J.ox

J.ph

Ely

SOMp

Epi

Ses

SOMb

C (‰)Depleted Enriched 13

N (‰

)D

ep

leted

E

nrich

ed

15

Fig. 4 – d13C–d15N plot for macroinvertebrates, dune plants (italics), beach sand organic matter (SOMb), and P. oceanica wrack

(Pos) occurring at the beach. Burano The label for macroinvertebrate predators is underlined. Data for sediment organic

matter of P. oceanica beds (SOMp), seston over P. oceanica meadows (Ses), and P. oceanica epiphytes (Epi) have been compiled

from the literature. Diamonds stand for the theoretical diet of the indicated macroinvertebrates (dashed lines) assuming 1

and 3.4& metabolic increase from the diet to the consumer for d13C and d15N, respectively. The big hollow circle represents

the average theoretical diet of all non-predatory macroinvertebrates (except for P. bipunctata). The rectangle represents the

range of the average theoretical diet for the non-predatory macroinvertebrates assuming a wider range of metabolic

increase as gathered from the literature (from 0 to 1& for d13C and from 1 to 5& for d15N). The error bars correspond to the

standard errors of the means. For abbreviations of species see Table 6.

a c t a o e c o l o g i c a 3 5 ( 2 0 0 9 ) 3 2 – 4 442

individuals of T. saltator, Geophilus sp. seems to prey on P.

bipunctata and in the case of S. buparius, no potential prey was

identified. P. laevigatus is a diurnal predator that inhabits the

low eulittoral and during its foraging activity it exploits wrack

deposits of this area where it can easily find Phaleria spp. The

wolf spider A. cinerea is also a diurnal hunter that searches for

its prey on the beach where apparently it can capture large

size talitrids. In other Lycosidae species, such as Pardosa

lapidicina Emerton and Pardosa ramulosa McCook, Morse (1997)

reported direct observations on hunting on newly-molted

amphipods and Page (1997) showed enriched d15N values

relative to their potential amphipod prey. However, wolf

spiders are also known to attack small flies feeding in the low

intertidal and on Collembola (Morse, 1997), so in this case the

isotopic signature might be the result of a mixed diet. The

nocturnal centipede Geophilus sp. that lives under stranded

logs in the high supralittoral, showed P. bipunctata as a theo-

retical prey. However, this result seems quite improbable due

to the different temporal and spatial patterns of the two

species, the tenebrionid being diurnal and distributed in dunal

and retrodunal areas (Fallaci et al., 1997). Direct observations

showed that Geophilus sp. can prey on another tenebrionid

Xanthomus spp. that occupies a trophic niche similar to that of

P. bipunctata. S. buparius, a large carabid species living under

stranded woods at the dune base and on the foredune, prob-

ably hunted macroinvertebrates inhabiting the dune rather

than the beach since the isotopic signal of its theoretical prey

fell in an area with depleted d13C and d15N values.

None of the primary producers analysed (beach-dune

vascular plants) appeared to be potential sources of carbon

and nitrogen for the beach fauna nor did they seem to use

P. oceanica detritus as a nutrient. They presented isotopic

values typical of many terrestrial woody plants with particu-

larly low d15N values (Cloern et al., 2002), characteristic of non-

nitrogen-fixing plants. Noticeable exceptions were the very

high d15N values of C. maritima and S. kali (around 6&), two

known nitrogen-fixing plants (Pakeman and Lee, 1991). The

high d13C of the latter reflects the biochemical features of

photosynthesis being characterised by an NADP-malic

enzyme biochemical type and a C4 photosynthetic metabo-

lism (Olesen, 1974). Similar d13C values (�10.0&) were

obtained for S. kali by Pyankov et al. (2001) when studying the

origin and evolution of C4 photosynthesis in Chenopodiaceae.

5. Conclusion

This study suggests that the spatial and temporal patterns of

both detritivores and predators in the stranded wracks are the

result of a combination of factors. Species succession is

regulated by species adaptation to specific microclimatic

conditions of the wracks, by the need to find an adequate food

a c t a o e c o l o g i c a 3 5 ( 2 0 0 9 ) 3 2 – 4 4 43

source by benefiting from the presence of other species (both

bacteria and macroinvertebrates) on the wrack and by the

need to find an adequate refuge from the stressful environ-

mental conditions.

Furthermore, the study has clearly shown that P. oceanica

wrack is not a dietary source for the macroinvertebrate fauna

of Burano beach, as already shown in the marine habitat, but

it is a physical structure of vital importance for detritivorous

and predatory species as refuge from environmentally

stressful conditions.

This study should be complemented with further research

taking into consideration the effect of wrack size, seasonality

and bacterial presence on the abundance and species richness

of beach macroinvertebrates.

Acknowledgments

The authors are grateful to Guillermo Mendoza, Dani Martin

(Centre of Advanced Studies of Blanes, CEAB, CSIC), and to

Rafa Marce for their help in some statistical aspects of the data

analysis. This study has been supported partially by funds of

a bilateral programme between CNR (Italy) and CSIC (Spain),

and partially by the EU-INCO project WADI (CT2005-15226).

We are also grateful to Fabio Cianchi of the WWF Burano Oasis

for his assistance. The experiments performed for this study

comply with the current laws of Italy.

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