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produces a range of beach morphodynamic types,

varying from reflective (narrow and steep) to dissipative

beaches (wide and flat), as sand becomes finer and

waves and tides larger (Short1999). Species richness,

total abundance, and biomass of the resident biota

increase from reflective to dissipative beaches, and

biological interactions (e.g., competition, predation) areovershadowed by physical factors on reflective beaches,

but become more influential on dissipative beaches

(Defeo and McLachlan2005; Schlacher et al.2008).

The analysis of the food web structure and trophic

relationships in sandy beach ecosystems has become a

growing area of research (Colombini et al. 2011).

Sandy beach food webs are mainly based on marine

resources, such as phytoplankton, wrack (stranded

algae and sea grasses), and carrion (McLachlan and

Brown 2006). These sources support a macroscopic

food web comprising mainly of scavengers and depositfeeders as primary consumers, while carnivorous

fishes and polychaetes are consumers, which in turn

may be preyed upon by birds (Heymans and McLach-

lan1996; Lercari et al.2010; Bergamino et al.2011).

Recent studies have attempted to elucidate trophic

pathways on sandy beach ecosystems, pointing out that

trophic pathways and food web complexity can be

strongly linked to morphodynamic factors which

influence the occurrence and abundance of phyto-

plankton (Lercari et al.2010; Bergamino et al.2011).

Moreover, recent findings suggest that the intertidalfauna is mainly supported by marine resource inputs

(Paetzold et al.2008; Colombini et al.2011). Despite

these advances, information describing the food web

structure as such and key network properties that

determine food web dynamics on sandy beaches

remains scarce (but see Lercari et al.2010).

Food webs describe feeding relationships between

taxa within ecosystems with structural patterns in the

arrangement of feeding links (Camacho et al. 2002;

Dunne et al.2002; Pimm2002). Understanding these

patterns is a key aspect of food web ecology, beingcrucial for the description of ecosystem functioning

and important for the understanding of the biological

processes that underlie community organization

(Cohen et al. 1990; May 2006). For this reason,

certain topological properties have been studied to

discern food web patterns, including the proportion of

predators and prey, and the number of trophic links

(e.g., Dunne et al. 2004; Stouffer et al. 2005; Romanuk

et al. 2006; Sanchez-Carmona et al. 2012). Previous

work suggests that connectance and the number of

species are important factors in the structure of food

webs in different ecosystems (Vermaat et al. 2009), as

well as being a measure of the robustness of food webs

to species loss (Dunne et al.2002).

In the present study, we analyzed the structure ofsandy beach food webs and determined major struc-

tural properties of the food web to evaluate their

ecological implications for the functioning of sandy

beach ecosystems. To this end, binary food webs were

used, considering number of species and links per

species, for two sandy beaches with contrasting

morphodynamics. A total of 17 food web properties

were calculated and then examined with published

food web models of other ecosystems to identify

drivers of food web structure.

Methods

Study area

We analyzed the network structure of two exposed

microtidal sandy beaches (tidal range =0.5 m) with

contrasting morphodynamics located on the Uru-

guayan Atlantic coast: Arachania (reflective) and

Barra del Chuy (dissipative) (Fig.1). The former is

narrow (width approximately 40 m) and containscoarse sediments (mean grain size =0.56 mm) and

a steep slope (7.80 %), whereas the dissipative beach

is wider (width approximately 70 m), consisting of

fine sands (mean grain size =0.20 mm) with a gentle

slope (3.53 %). Among all Uruguayan beaches, this

dissipative beach represents the highest macrofauna

richness, abundance, and biomass, whereas the reflec-

tive beach presents relatively low macrofauna species

richness (Lercari and Defeo 2006). A full character-

ization of the main properties of both beaches is

provided in Defeo et al. (1992,1997) and Gomez andDefeo (1999).

Data collection and food web construction

The food web structures for these sandy beaches were

previously analyzed by Lercari et al. (2010) using the

ECOPATH II mass balance model software (Polovina,

1984; Christensen and Walters 2004). Both models

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considered all main species identified in the ecosys-

tems. The dissipative beach model included 20 trophic

groups and the reflective beach model integrated 9

trophic groups, including benthic invertebrate species

as groups, as well as 1 fish group, 1 bird group, 1

plankton group, and 1 detritus group (Table1).

Functional feeding groups were used to group fishes

and birds species according to similar feeding and

habitat characteristics. For the macroinvertebratespecies, the following sample design was followed

on both beaches: three transects perpendicular to the

shoreline and spaced 8 m apart, with sampling units

(SUs) on each transect every 4 m beginning at the base

of the dunes to the lower limit of the swash zone. At

each SU, a sheet metal cylinder (27 cm in diameter)

was used to remove the sediment up to a depth of

40 cm. Each SU was sieved through a 0.5 mm mesh,

and the organisms retained were fixed in 5 % buffered

formalin (see Defeo et al.2001for details). The origin

of the trophic links information was extracted frompublished information, qualitative records, and stable

isotope analysis determined for some of the consum-

ers. Detailed explanations on the data source for diet

composition of the trophic groups are provided in

Lercari et al. (2010).

Binary networks were constructed to represent the

food web for each sandy beach using Network3D

Software (Williams 2010), developed for previous

food web studies (e.g., Williams and Martinez 2000,

2008; Williams et al. 2002). Input data were set in a

two-column format: a consumers number appears in

the first column, and one of its resources numbers

appears in the second column.

Food web properties and data analyses

We analyzed seventeen food web properties that

describe species and link characteristics, as well asfood chain properties (see Table2for definitions). In

binary food webs, the most accurate trophic level

estimation is called the mean short weighted trophic

level (TL) which is the mean of shortest TL and prey-

averaged TL (Williams and Martinez 2004). For

definitions of the terms used to describe food web

properties, here please refer to Table2.

In order to investigate the sandy beach food webs in

a global context, we considered 10 of the food webs

described by Dunne et al. (2004). We included two

terrestrial systems: the Coachella Valley Desertlocated in California, USA (166370W, 33540N;

area =*740 km2; number of trophic species =29;

Polis1991) and the Caribbean island of St. Martin in

the northern Lesser Antilles (18040N, 63030W;

number of trophic species =42; Goldwasser and

Roughgarden1993); one marine system: the upwell-

ing Benguela current ecosystem (2750S, 1130E;

number of trophic species =29; Yodzis1998); three

freshwater lakes and pond webs: Bridge brook Lake,

SouthAmerica

Uruguay

Brazil

South Atlantic Ocean

Arachania

Barra del Chuy

Argentina

Fig. 1 Map of Uruguay

showing the two sandy

beaches analyzed in this

study: Barra del Chuy and

Arachania indicated by a

black circle. Map produced

using SimpleMappr

(Shorthouse2010)

Aquat Ecol (2013) 47:253261 255

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Upstate New York, USA (4420N, 74W; number of

trophic species = 25; Havens, 1992), Little Rock

Lake located in northern Wisconsin, USA (4560N8940W; number of trophic species = 92; Martinez

1991), Skipwith Pond in the North Yorkshire, England

(53400N, 0590W; number of trophic species =25;

Warren 1989); and three estuary webs: Chesapeake

Bay in Eastern USA (36500 to 39400N; number of

trophic species =31; Baird and Ulanowicz1989), St.

Marks Estuary located in Florida, USA (30060N,

84110W; number of trophic species = 48; Christian

and Luczkovich1999), Ythan Estuary in NE Scotland

(1570W, 57200N; number of trophic species =83;

Hall and Raffaelli1991).

Since most of the food web characteristics are

correlated (Vermaat et al. 2009), we used principal

components analysis (PCA) to account for the covari-

ance structure of the food web metrics. In this way, we

reduce data dimensionality revealing the similaritiesbetween individual samples and the relationship

between the measured properties. To this end, the R

package for multivariate analysis FactoMineR (Hus-

son et al. 2011) was used. The number of retained

dimensions in the PCA was determined by taking into

account the percentage of variance explained by these,

considering 75 % as a reference. Since we consider

each single beach a unique ecosystem with dynamic

properties, statistical comparison in the food web

properties is not possible.

Results

The dissipative and the reflective beach showed

differences in several structural properties of the food

web (Table2). The mean trophic level and the

maximum trophic level were higher in the dissipative

beach (2.27 and 3.34, respectively) than in the

reflective (2.13 and 3.25, respectively). Both food

webs presented a high trophic similarity with a

predominance of intermediate trophic level species(85 % in the dissipative beach and 67 % in the

reflective beach). The dissipative beach presented

higher links per species (2.95) than the reflective

beach (2.11), but the reflective beach showed a higher

connectance (0.23) than the dissipative beach (0.15).

Moreover, the percentage of omnivorous species was

50 % in the dissipative beach and 55 % in the

reflective beach. Functional groups from the dissipa-

tive beach showed higher standard deviation of

vulnerability and generality (1.06 and 1.03, respec-

tively) than those from the reflective beach (0.76 and0.90, respectively). This result indicated that in the

dissipative beach system, a trophic species presented

greater variability in the number of prey organisms

and the number of predators than in the reflective

beach system.

As a result of the PCA, only 2 dimensions were

retained, explaining 75.27 % of the variance. Figure 2

shows sandy beaches (dissipative and reflective) and

Bridge Brook Lakegrouped together. Theseecosystems,

Table 1 Functional groups considered for the food web

models of the dissipative beach (Barra del Chuy) and the

reflective beach (Arachania), located in the Atlantic coast of

Uruguay

Dissipative beach Reflective beach

Birds Fishes

Fishes Polychaeta

Polychaeta Hemipodia californiensis

Hemipodia californiensis Amphipoda

Euzonus (Thoracophelia)

furcifera

Atlantorchestoidea

brasiliensis

Spio (Microspio) gaucha Isopoda

Carabide Excirolana braziliensis

Gastropoda Decapoda

Olivancillaria auricularia Emerita brasiliensis

Olivella formicacorsii Bivalvia

Buccinanops duartei Donax hanleyanus

Bivalvia Zooplankton

Amarilladesma mactroides Phytoplankton

Donax hanleyanus Detritus

Amphipoda

Atlantorchestoidea

brasiliensis

Phoxocephalopsis sp.

Isopoda

Chiriscus giambiagiae

Excirolana braziliensis

Excirolana armata

Decapoda

Emerita brasiliensis

Zooplankton

Phytoplankton

Detritus

256 Aquat Ecol (2013) 47:253261

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together with Ythan Estuary, exhibited an important

contribution to the construction of Dimension 2

(Table3). Dimension 2 was mainly determined by the

number of trophic species, links per species, mean food

chain length, fraction of basal species, and the trophic

similarity (Table4). In this sense, these variables were

possibly responsible for the cluster formed by the

beaches and the lake systems studied, and the isolated

position of Ythan Estuary.

Similarly, Dimension 1 contained some ecosystems

that particularly contributed to its construction

(Coachella Desert; Skipwith Pond; Ythan Estuary;

Chesapeake Bay; Table3). Connectance, fraction of

intermediate species, fraction of species that are

cannibalistic, fraction of top species, and normalized

standard deviation of vulnerability (number of con-

sumers per taxon) were the main variables that

determined Dimension 1 (Table4), being responsible

for the groups described in relation to this dimension.

Skipwith Pond and Coachella Desert formed a sepa-

rate group (Fig.2).

Discussion

Our analysis revealed that the dissipative and the

reflective beaches presented differences in the struc-

tural properties of the food web. The reflective beach

had higher degree of connectance and proportion of

omnivorous species, but lower trophic levels, lower

number of trophic species, links per species, and

proportion of intermediate trophic species than the

Table 2 Food web properties of the two contrasting sandy

beaches: dissipative and reflective

Food web

properties

Dissipative Reflective Definition

Trophic

species (S)

20 9 Number of trophic

species

Links/Species

(L/S)

2.95 2.11 Number of all

trophic links in

the web

(L) divided by S

Connectance

(C)

0.15 0.23 Proportion of all

possible links

that are realized

(L/S2)

Percentage of

top predators

(%Top)

5 11 Species with prey

but no predators

Percentage of

intermediatespecies

(%Int)

85 67 Species with both

prey andpredators

Percentage of

basal species

(%Bas)

10 22 Species with

predators but no

prey

Percentage of

herbivores

(%Her)

40 22 Species which are

strictly herbivore

Generality

standard

deviation

(GenSD)

1.03 0.9 Number of

resources per

taxon normalized

Vulnerabilitystandard

deviation

(VulSD)

1.06 0.76 Number of consumers per

taxon normalized

Link Standard

deviation

(LinkSD)

0.6 0.42 Number of links

per taxon

normalized

Percentage of

omnivores

(%Omn)

50 55 Taxa that feed on

taxa at different

trophic levels

Maximum

trophic

similarity

(MaxSim)

0.81 0.79 Number of

predators and

prey shared in

common dividedby the pairs total

number of

predators and

prey

Percentage of

cannibals

(%Can)

5 11 Taxa that feed on

their own taxa

Trophic level

(TL)

2.27 2.13 Short weighted

trophic level

Table 2 continued

Food web

properties

Dissipative Reflective Definition

Maximum

trophic level

(MaxTL)

3.34 3.25 Maximum short

weighted trophic

level

Chain length

(ChaLen)

2.15 2 Mean food chain

length, averaged

over all species

Characteristic

path length

(Path)

1.79 1.55 The mean shortest

food chain length

between species

pairs

The description of the food web properties was taken from

Williams and Martinez (2000) and Dunne (2009)

Aquat Ecol (2013) 47:253261 257

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dissipative beach. Moreover, consumers in the dissi-

pative beach seem to have more generalized diets than

consumers in the reflective beach. These results are in

accordance with a previous, more detailed, food web

study for these sandy beaches (Lercari et al. 2010). Itshould be noted that trophic species aggregation has

strong influence on the measurement of %top and

basal species (Martinez1991). This fact could explain

the over-estimation of these parameters on sandy

beaches since many taxonomic species in our model

were basal resources and top predators.

Our analyses are based on a high-resolution

description following grouping strategy using indi-

vidual species and trophic link information based on

Lercari et al.2010. In this sense, our results provided a

robust comparison of the food web properties between

the sandy beaches analyzed here.

Sandy beach food webs are dominated by interme-

diate trophic level species, such as filter and deposit

feeders, being food webs characterized by low chain

length (Heymans and McLachlan1996; Lercari et al.2010; Colombini et al. 2011). Previous food webs

studied on sandy beaches revealed that the maximum

trophic levels range from 3.82 with 16 compartments

(Heymans and McLachlan, 1996) to 3.14 with 20

compartments (Lercari et al. 2010). Including the dune

system, the maximum trophic levels of the top

predators in the beach-dune system were 3.51 with

51 compartments (Colombini et al. 2011). On dissi-

pative beaches, the presence of a productive surf zone

with diatom accumulation provides large amounts of

food available for filter feeders and could explain thehigh trophic similarity with the dominance of inter-

mediate trophic species (Defeo and McLachlan2005).

On reflective beaches, the harsh swash environment

with dynamic and turbulent swashes, and where waves

break directly on the steep beach face, may exclude

organisms without active and rapid burrowing abilities

at low and medium beach levels (Defeo et al. 2001;

Incera et al. 2006). Moreover, it has been suggested

that reflective beaches are more stable and safer

environments for the development of supralittoral

species due to the lower risk of immersion and beingwashed away (Defeo and Gomez2005). Supralittoral

species include mostly primary consumers and sec-

ondary consumers (Colombini et al. 2011) such as

insects and talitrid amphipods.

Our study showed that number of species, links per

species, trophic similarity, and characteristics path

length are the major aspects influencing the food web

structure on sandy beaches. When contrasted with

published information for other food webs, the

proportion of intermediate species on the reflective

beach showed similar values to Mediterranean streams(66 %), while the dissipative beach was close to lake

systems (range 6886 %) (Dunne et al. 2004; San-

chez-Carmona et al. 2012). These values were lower

than those observed in marine systems (range 9295),

but higher than for streams (2227 %) and slightly

higher than in estuarine systems (5669 %) (Dunne

et al. 2004). In our food webs, benthic invertebrates

were mainly scavengers and detritivorous. Moreover,

in both sandy beaches, the production is poorly

-4 -2 0 2 4 6

-3

-2

-1

0

1

2

3

4

Principal component 1 (44.48%)

Principalcom

ponent2(30.7

9%)

Ythan Estuary

Bridge Brook Lake

SkipwithPond

Cheasapeak Bay

CoachellaDesert

St. Martins Islands

ReflectiveSandy Beach

DissipativeSandy Beach

Fig. 2 Principal component analysis for aquatic and terrestrial

ecosystems considering the food web properties described in

Table2. Percentage values represent the proportion of the

variance explained by each principal component

Table 3 Contribution percentages of aquatic and terrestrial

ecosystems to the dimensions considered in the principal

component analysis

Ecosystems Contributions

Dimension 1 Dimension 2

Skipwith Pond 19.44 2.24

Bridge Brook Lake 0.73 13.74

Chesapeake Bay 12.82 0.21

Ythan Estuary 23.38 32.55

Coachella Desert 41.61 10.35St Martin Island 1.74 2.31

Dissipative sandy beach 0.23 13.45

Reflective sandy beach 0.05 25.16

Values in bold indicate contributions higher than 10 %

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consumed (4 % on the dissipative 6 % on the reflec-

tive), and most of the biomass flows are directed to

exportations and detritus (Lercari et al. 2010). This

suggests that weak interaction effects of primary

consumers on resources are the most frequent inter-

action in these food webs. Moreover, donor control

dynamics are expected, in which the rate of detrital

input is thought to be a major factor influencing the

interactions within the macrobenthic community(Pimm 2002). This pattern can enhance the stability

of these food webs, in the sense that the system

recovers faster after a disturbance, by dampening

fluctuations of populations densities (May 1973;

McCann et al. 1998; Neutel et al. 2002; Montoya

and Sole,2003).

We found that the connectance values calculated

for sandy beaches were relatively high compared with

previous works that analyzed 16 food webs and

reported a range of 0.030.32 (Dunne et al. 2002,

2004). The connectance value for the dissipative beachwas close to the Bridge Brook Lake (0.17) and the

value for the reflective beach to marine systems (range

of 0.220.24). However, our connectance results were

lower than those of a terrestrial system (the Coachella

Valley, 0.31), and lake/pond (0.32) food webs, while

they were higher than Mediterranean streams (range

0.090.14) and estuarine webs (0.040.1) (Dunne

et al.2004; Sanchez-Carmona et al.2012). It has been

suggested that connectance may increase food web

robustness to species extinction and ecosystem stabil-

ity, and that this effect is more important than diversity

(Dunne et al.2002,2004; Fussman and Heber 2002;

Kondoh2003). In this case, robustness of a food web

refers to the propensity for networks to fragment and is

defined in terms of the number of secondary extinc-

tions that result from primary species loss. Moreover,previous work reported that connectance is a good

predictor of omnivory and that more omnivorous links

increase ecosystem stability (Fussman and Heber

2002). In our results, the reflective beach showed a

smaller number of species but higher connectance and

omnivory, which could result in a greater robustness to

species loss (i.e., less secondary extinction occur) than

the dissipative beach which showed intermediate level

of connectance and lower levels of omnivory. In spite

of this, our results showed that sandy beach food webs

present low mean path length on both beaches (1.79 onthe dissipative and 1.55 on the reflective beach),

suggesting that species are highly interconnected

within the ecosystems. This fact has important

ecological implications, suggesting that change in

diversity, by the loss of species (e.g., caused by habitat

loss) or the introduction of new species, can be

propagated through the ecosystem, thereby affecting

the ecosystem structure (Williams et al.2002). These

results open a new question on sandy beach ecology

concerning the effects of biodiversity loss on the food

web structure.In summary, our results show new potential effects

of food web interaction patterns in community struc-

ture and dynamic on sandy beaches. This has impor-

tant consequences for conservation issues. The

understanding of species interactions allows predict-

ing the response of ecosystem function to changes in

structural aspects such as the effects of invasive

species and local extinction. Our food web analysis

suggested that species and link characteristics, such as

trophic similarity, number of species, and links per

species, play a critical role structuring the food webson sandy beach ecosystems. Moreover, the predom-

inance of weak trophic interactions of primary

consumers and the relatively high connectance could

enhance the stability of these ecosystems and act

together with the strong physical forces in structuring

populations and communities. Although sandy beach

populations are mainly controlled by physical factors,

the effects of interaction patterns on the community

structure and stability remain open. We think that for

Table 4 Contribution percentages of food web properties to

the dimensions considered in the principal component analysis

Variables Contributions

Dimension 1 Dimension 2

S 4.74 17.68

L/S 4.62 16.27

C 17.18 0.26

%Top 11.59 6.36

%Int 14.69 0.16

%Bas 1.43 10.80

GenSD 5.72 0.07

VulSD 11.92 2.52

%Omn 8.30 8.12

MaxSim 2.89 15.18

%Can 14.92 2.12

Path 2.00 20.46

Values in bold indicate contributions higher than 10 %

Aquat Ecol (2013) 47:253261 259

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future works on sandy beaches, an important aspect to

analyze would be the stability of the population

dynamics against species loss by considering the role

of several structural factors of the networks (e.g.,

Dunne et al.2002). The higher degree of connectance

and omnivory in the reflective beach could enhance

the stability and robustness of the food web. Incomparison with the dissipative beach, the food web

may be more fragile to the loss of species with a

greater magnitude of secondary extinctions. This

could be tested by building different configurations

of both food webs simulating the sequential local

extinction of the groups and then comparing the

stability/robustness indicators.

Acknowledgments We thank Omar Defeo (Facultad deCiencias, UNDECIMAR, Uruguay) for his mentorship and

friendship through the years. This work was supported by

SANDISA IMWEBU grants (L.B). We thank Katherina Schoo

and Sydney Moyo for the language editing. We are also grateful

to Piet Spaak and an anonymous referee for helpful comments in

the manuscript. DL thanks PEDECIBA and ANII. L.B. thanks

Jesus Orozco (Rhodes University, South Africa) for his

transmission of knowledgeand encouragement in a friendly way.

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