Mar Biol (2016) 163:65
DOI 10.1007/s00227-016-2835-9
ORIGINAL PAPER
Size‑dependent predation of the mesopredator Marthasterias
glacialis (L.) (Asteroidea)
P. Gianguzza1 · F. Di Trapani1   · C. Bonaviri1 · D. Agnetta2 · S. Vizzini1 ·
F. Badalamenti2 
Received: 20 July 2015 / Accepted: 2 February 2016
© Springer-Verlag Berlin Heidelberg 2016
Abstract  Asteroids are largely recognized as important
predators in all of the world’s oceans and for this reason, they
play a crucial role in shaping the structure and functioning of
benthic ecosystems. The spiny starfish Marthasterias glacia-
lis is generally considered a voracious predator of molluscs,
in particular bivalves. Using field observations and carbon
(δ13C) and nitrogen (δ15N) stable isotopes, we explored
possible changes in diet in relation to size of M. glacialis.
Data were collected at Ustica Island (Southern Tyrrhenian
Sea) from June 2008 to June 2010. M. glacialis showed a
size shift in feeding preferences due to different use of food
items: bivalves, Columbella rustica, Euthria cornea and Tro-
choidea were strongly selected by small starfish whereas the
larger ones preferred Arbacia lixula and Paracentrotus livi-
dus. The clear picture that emerged is that large M. glacialis
is able to control sea urchin populations and indirectly Medi-
terranean rocky reef ecosystems.
Introduction
Marine ecologists have largely emphasized the key role
of starfish predation as a structuring force in benthic eco-
systems (Paine 1974; Gaymer et al. 2004; Gaymer and
Responsible Editor: M.G. Chapman.
Reviewed by G. Fanelli and an undisclosed expert.
* F. Di Trapani
fraditrapani@iol.it
1
Dipartimento di Scienze della Terra e del Mare, Università di
Palermo, CoNISMa, Via Archirafi 18, Palermo, Italy
2
CNR – Istituto per l’Ambiente Marino Costiero, Via G. Da
Verrazzano 17, Castellammare del Golfo, TP, Italy
Himmelman 2008; Estes et al. 2011). In the 1970s, Paine
developed the concept of keystone species using Pisas-
ter ochraceus (Brandt, 1835), whose predatory activity
strongly affected the intertidal biodiversity of the North
Western Pacific benthic communities. Other studies on
starfishes, such as Acanthaster planci (Linnaeus, 1758)
and Pycnopodia helianthoides (Brandt, 1835), have been
seminal in revealing the importance of starfish predation in
structuring Indo-Pacific coral reefs (Pratchett 2005, 2007)
and Pacific mussels’ communities, respectively (Duggins
1983; Freeman 2006).
The spiny starfish Marthasterias glacialis (Linnaeus,
1758) inhabits the eastern Atlantic from Iceland to the
Azores (Guillou 1996), as well as the Mediterranean Sea
(Savy 1987) and South Africa (Penney and Griffiths 1984;
Pérez-Portela et al. 2010). Its depth range varies from
extreme shallow water to about 200 m depth and occurs
on both sheltered muddy sites and exposed rocky bottoms
(Tuya and Duarte 2012). Previous studies have shown that
M. glacialis is a generalist feeder, capable of exploiting a
wide range of slow moving or sessile prey items such as the
saddle oyster Anomia ephippium (Linnaeus, 1758) (Ebling
et al. 1966), the king scallop Pecten maximus (Linnaeus,
1758) (Magnesen and Redmond 2012), the black mussel
Choromytilus meridionalis (Krauss, 1848) (Penney and
Griffiths 1984), the venus clam Venus verrucosa (Linnaeus,
1758) (Guler and Lok 2015), the abalone Haliotis tubercu-
lata (Linnaeus, 1758) (Forster 1962), the algae Audinella
floridula (Frid 1992), the sea urchins Paracentrotus livi-
dus (Lamarck, 1816), Arbacia lixula (Linnaeus, 1758) and
Echinus esculentus (Linnaeus, 1758) (Penney and Griffiths
1984; Dance and Savy 1987).
Fanelli et al. (1999) hypothesized a keystone role for
M. glacialis in the Mediterranean Sea, where the species
would be capable of controlling both P. lividus and A.
13
 65   Page 2 of 11
lixula populations whose grazing may exert a paramount
role in the transition from macroalgal beds to coralline
barrens (Bulleri et al. 1999, 2002; Gianguzza et al. 2006,
2010; Bonaviri et al. 2011).
However, speculations regarding the keystone role of M.
glacialis have generated controversies. In part this is rooted
in the fact that, although recent indirect evidence sug-
gests for M. glacialis an ecological role in controlling sea
urchin populations (Bonaviri et al. 2009; Di Trapani et al.
2009; Gianguzza et al. 2009a, b; O’Sullivan and Emmer-
son 2011), in many places this predator shows a diet mainly
composed by bivalves (Guidetti 2004) and only seabreams
have been reported to effectively control sea urchin popula-
tions (Sala and Zabala 1996; Guidetti 2006).
In the marine protected area (MPA) of Ustica Island, the
ban of extractive human activities has not been sufficient
to restore Diplodus spp. populations (La Mesa and Vacchi
1999; Bonaviri et al. 2009), whereas population of M. gla-
cialis has significantly grown in density and size (Gianguzza
et al. 2009a, b). Noteworthy, in the barren rocky substrates of
Ustica Island MPA, large starfish have been often observed
preying upon P. lividus and A. lixula (Gianguzza et al.
2009a), pointing out how the raise of a mesopredator such as
M. glacialis might contribute to control the populations of P.
lividus and A. lixula where large fish predators lack (Prugh
et al. 2009). Furthermore, a tethering experiment revealed
a high predation rate on sea urchins by large M. glacialis
(Bonaviri et al. 2009), and recently, Galasso et al. (2015)
based only on in situ observations suggested a size-depend-
ent shift in the diet of M. glacialis: bivalves are preferred
prey items of small starfish and sea urchins of large ones.
Thus, the rationale is that the diet of M. glacialis is subject
to considerable changes, according to size, and consequently,
speculations regarding its keystone role in controlling sea
urchin populations need to consider the effects of size.
The overarching aim of the present study was to better
define the feeding habits of small and large M. glacialis in
the barren ground of Ustica Island MPA, thereby contribut-
ing to information about the species life history. The first part
of the study reports on fieldwork carried out to describe the
feeding habits of M. glacialis at different sizes. Later, in the
second part of the study, field observations and stable isotope
analysis were combined to test the hypothesis of a differ-
ent prey selection by size, with larger M. glacialis feeding
chiefly on sea urchins, while smaller ones on bivalves.
Materials and methods
Study area
The study was carried out at Ustica Island, the protruding
part of an extinct volcano located in the southern Tyrrhenian
13
Mar Biol (2016) 163:65
SICILY
MEDITERRANEAN SEA
Zone B
Zone A
N
C1
Zone C
C2
38°42’20” N
1 Km 10°43’43” E
Fig. 1  Map of Ustica Island MPA showing the study area (the take
zone C) and the study sites C1 and C2
Sea (Western Mediterranean, 38°42′20″N–10°43′43″E),
60 km north of the Sicilian coast (Fig. 1). Its base lies at
about 2000 m depth, and it is composed mainly of alka-
line basalts and sedimentary rocks (Milazzo et al. 2000).
The MPA, created in 1986, encompasses a total area of
16.000 ha and contains three zones with different degrees
of protection. The no-take zone (zone A) covers 65 ha
along the western part of the island, while the general
reserve (zone B) and the take zone (zone C) share the
remaining area equally (Fig. 1). According to the institu-
tive decree of the MPA, only research activities are author-
ized in the no-take zone A, whereas recreational activi-
ties, such as SCUBA diving, boat anchoring, swimming
and angling, are strictly prohibited. Recreational activities
in either the B or the C zones are subject to agreement of
the Ustica Town Council (the MPA management body)
(Gianguzza et al. 2006). Fieldwork was carried out in the
southern zone of Ustica Island within the take zone C of
the MPA, at a depth of about 1–5 m (Fig. 1). This zone
was chosen mainly for the density values of M. glacialis
(4 ± 0.5 individuals/250 m2) that should facilitate the study
of the diet of the species (Bonaviri et al. 2009; Gianguzza
et al. 2009a, b; Gianguzza et al. 2010). The sea floor in the
area is characterized by a steep rocky cliff down to about
30–40 m depth. Some terraces are found in the shallow part
of the cliff. The whole area is characterized by high struc-
tural complexity where crustose algae are interspersed with
patches of Cystoseira spp. (mainly Cystoseira brachicarpa
Mar Biol (2016) 163:65 Page 3 of 11  65
var. balearica [Sauvageau Giaccone, 1992] and Cystoseira
compressa [Gerloff and Nizamuddin, 1975] forming a
binary landscape (Gianguzza et al. 2010).
Data collection
As many other starfish, M. glacialis is a non-visual preda-
tor that detects prey from waterborne odors and captures
them using tube feet and arms assuming the characteristic
humped-up feeding position to digest the prey by everting
the stomach. To study the starfish feeding habits, 25 belt
transects, 50 × 5 m (250 m2), were placed at a mean depth
of 5 m parallel to the coast at each of two sites, randomly
chosen within the take zone of the MPA (C1 and C2, Fig. 1).
Two randomly chosen transects per site were then explored
by scuba divers bimonthly between June 2008 and June
2010 during good weather only. All the starfish encountered
were lifted and turned upside down to record whether they
were feeding or not. Due to cryptic behavior of M. glacialis,
crevices and holes were carefully inspected while diving.
When present, prey were identified to the lowest possible
taxonomic level and measured with a Vernier caliper to the
nearest mm [total shell length for molluscs (including her-
mit crabs) and test diameter without spines for sea urchin].
Arm height (AH) of all encountered starfish was meas-
ured underwater with a Vernier caliper to the nearest
0.1 mm. AH data were successively transformed into total
length (TL) as the maximum tip-to-tip diameter according
to the regression reported in Gianguzza et al. (2015). TL
data were then organized in the following 9 size classes:
I (≤17 cm), II (17.1–20 cm), III (20.1–22 cm), IV (22.1–
25 cm), V (25.1–27 cm), VI (27.1–29 cm), VII (29.1–
32 cm), VIII (32.1–34 cm) and IX (>34 cm).
Unfortunately and unpredictably, not enough star-
fish were collected per each size class in each sampling
period, in particular during the second year of survey. For
this reason, data on prey eaten recorded during the whole
period were pooled and analyzed according to the single
factor size class with the 9 fixed levels reported above but
expressed as TL.
To determine prey preferences of M. glacialis, the abun-
dance of potential preys was evaluated at both sites via
underwater visual censuses in two different times (Sum-
mer 2009 and 2010). On the basis of preliminary obser-
vations and literature scrutiny (Kitching and Thain 1983;
Dance and Savy 1987; Milazzo et al. 2000; Guidetti 2004;
Tuya and Duarte 2012), the following taxa were selected:
sea urchins (P. lividus, A. lixula, Sphaerechinus granula-
ris [Lamarck, 1816]), starfish (Ophidiaster ophidianus
[Lamarck, 1816], Coscinasterias tenuispina [Lamarck,
1816]), ophiuroid (Ophioderma spp.), molluscs (Hexaplex
trunculus [Linnaeus, 1758], Cerithium vulgatum [Bru-
guière, 1792], Patella caerulea [Linnaeus, 1758], Conus
spp., Stramonita haemastoma [Linnaeus, 1767], Colum-
bella rustica [Linnaeus, 1758], Euthria cornea (Linnaeus,
1758), Trochoidea and Luria lurida [Linnaeus, 1758]),
bivalves (Arca noae [Linnaeus, 1758] and Barbatia bar-
bata [Linnaeus, 1758]) and anemones (Anemonia viridis
[Forskål, 1775] and Aiptasia spp.). Care was taken for
those species with cryptic behavior.
Different sampling surface areas were used to measure
the abundance of potential M. glacialis prey, based on their
relative spatial distribution and size. To determine the abun-
dance of starfish, larger molluscs and anemones three belt
transects (50 × 5 m) randomly placed in each site were con-
sidered; ten quadrats (1 × 1 m) were randomly placed in the
above-mentioned transects to assess the density of P. lividus
and A. lixula. Further ten quadrats (0.2 × 0.2 m) were then
randomly placed in the same transects to evaluate abun-
dance of C. vulgatum, C. rustica and Trochoidea. Only indi-
viduals >1 cm total length were considered in the counts.
Finally, densities of all preys were standardized to m2.
Spatial and temporal prey availability was tested by a
PERMANOVA with two random factors: time (two lev-
els) and site (with 2 levels, C1 and C2) and run by Primer
v6 & Permanova+ (Clarke and Gorley 2006). Because no
significant differences were detected for factors time (PER-
MANOVA P(MC) = 0.16, F1,1  = 2.78) and site (PER-
MANOVA P(MC) = 0.48, F1,1 = 1.07), data on prey avail-
ability were pooled.
Analysis of the diet
A cluster analysis was performed on the Bray–Curtis simi-
larity resemblance matrix calculated on the arcsine-trans-
formed prey items data of the 9 TL size classes a priori
identified to select homogeneous size group for the analy-
sis of the diet. After applying the SIMPROF test (Clarke
et al. 2008), the analysis distinguished two sizes of M.
glacialis designated as ‘small’ (TL  ≤ 27 cm) and ‘large’
(TL > 27 cm) (Fig. 2). According to the result of the clus-
ter analysis, the diet was then analyzed for the two sizes
independently.
The index of vacuity (V %) (Berg 1979; Chintiroglou
and Koukouras 1991; Bacha and Amara 2012) was used
to describe the feeding activity of this species. V % was
calculated as the percentage of not feeding individual by
the equation V % = TE × 100, where E is the number of
not feeding individuals and T is the total number of indi-
viduals. Vacuity values range from 0 to 20 (edacious spe-
cies), 20–40 (relatively edacious species), 40–60 (moderate
feeder), 60–80 (relatively abstemious) and 80–100 (abste-
mious) (Valinassab et al. 2011; Bacha and Amara 2012).
The importance of each prey to the diet of M. glacia-
lis was evaluated using the following indices: frequency of
occurrence (Fi %) (Hyslop 1980), Ivlev’s electivity index
13
 65   Page 4 of 11
20
40
Similarity
60
80
100
25.1-27
<17
17.1-20
20.1-22
22.1-25
>34
≤17
Fig. 2  Cluster analysis on Bray–Curtis similarity matrix of arcsine-
transformed prey item data of M. glacialis. Samples include the 9 size
classes chosen a priori (from ≤17 to >34 cm TL)
(Ei) (Ivlev 1961), Levin’s standardized index (Bi) (Krebs
1989) and simplified niche overlap Morisita’s index (Cik)
(Labropoulou and Eleftheriou 1997). Frequency of occur-
rence, defined as the number of individuals consuming a
prey item divided by the total number of feeding individu-
als, was calculated as Fi % = SSi × 100 where Si is the num-
ber of individuals feeding on food species ‘i’ and S is the
total number of feeding individuals (Hyslop 1980). Ivlev’s
index measures the utilization of prey species in relation to
their abundance or availability in the environment. It was
calculated as Ei = rrii +n
−ni
i
where Ei is the electivity of the
prey species ‘i’ in the diet of a predator, ri is the percentage
of species ‘i’ in diet, and ni is the percentage of species ‘i’
in the environment (Ivlev 1961). Ei ranges from −1 to 1;
positive values show selection, while negative show avoid-
ance. Tendency to zero is instead indicative of a consump-
tion of the prey according to its abundance in the envi-
ronment. Levin’s index was used to  investigate  on niche
1 glacialis, E. cornea, C. vulgatum and C. tubularis and Tro-
breadth and calculated as Bi =
n−1
1989), where Bi is the breadth niche of the predator species
‘i,’ n is the number of prey ‘j’ on the species ‘i’ diet, and
pij is the relative frequency of ‘j’ prey on ‘i’ diet. Bi ranges
from 0 to 1; low values (<0.6) indicate a diet dominated
by few prey items (specialist predator), while higher values
(>0.6) are indicative of a generalist diet (Labropoulou and
Eleftheriou 1997, Abitia-Cardenas et al. 1999). Morisita’s
index was used to measure possible
 trophic niche overlap,
2 j pij pkj
and it was evaluated by Cik =  p2 + p2 , where Cik is the
j ij
niche breadth overlap of the species ‘i’ and ‘k,’ pij is the
relative frequency of ‘j’ prey on ‘i’ diet, and pkj is the rela-
tive frequency of ‘j’ prey on ‘k’ diet. Index ranges from 0 to
1; values close to 1 are indicative of trophic niche overlap,
generally considered significant when over 0.6 (Labropou-
lou and Eleftheriou 1997).
13
Mar Biol (2016) 163:65
Finally, the contribution of each prey to the average dis-
similarity was calculated using the similarity percentages
procedure (SIMPER) in Primer v6 & Permanova+ (Clarke
and Gorley 2006). A regression analysis between starfish
total length and prey length was performed.
Stable isotopes analysis (SIA)
The feeding habits of M. glacialis were also investigated
through stable isotope analysis (δ13C and δ15N), spe-
cifically to test whether isotopic signatures were size-
27.1-29
29.1-32
32.1-34
dependent. Samples of M. glacialis and potential prey
were collected in summer 2010 and stored at −18 °C until
laboratory analysis. Given that asteroids have a remarkable
capacity for arm regeneration (Lawrence 1992; Lawrence
and Larrain 1994), we collected only part of an arm of
M. glacialis as a replicate. In this way, we minimized the
potential ecological impacts associated with removal of
starfish from local population. Five different individuals of
M. glacialis per size (small and large) and site (C1 and C2)
were amputated. Arms were dissected in the laboratory in
order to exclude pieces of gonad or pyloric caeca. The fol-
lowing potential prey of M. glacialis were hand-collected
by SCUBA divers for stable isotope analysis: sea urchin
(A. lixula, n  = 10 and P. lividus, n  = 10), molluscs (C.
rustica, n = 2, C. vulgatum, n = 4, E. cornea, n = 7, H.
trunculus, n = 10, P. coerulea, n = 6, Trochoidea, n = 2),
bivalves (A. noae, n = 7 and B. barbata, n = 7) and her-
mit crab (Calcinus tubularis [Linnaeus, 1767], n  = 10).
The foot muscle of A. noae, B. barbata, P. coerulea, H.
trunculus and the lantern muscle of both sea urchin spe-
cies (Tomas et al. 2006) were analyzed. The whole soft
body was used for small prey (<2 cm) such as E. cornea,
C. vulgatum and C. tubularis and Trochoidea. All samples
were dried at 60 °C (48 h) and ground to a fine powder. M.
1 −1 (Krebs
2
j pij choidea were treated separately for δ15N and δ13C. Prior
δ13C analyses, samples were acidified with drop-by-drop
2 N HCl to remove carbonates. C and N stable isotopes
were analyzed by a continuous-flow isotope-ratio mass
spectrometer (Thermo Delta Plus XP) coupled to an ele-
mental analyzer CHN (Thermo EA 11112). Experimental
precision, based on the standard deviation of replicates
of the internal standard, was 0.2 ‰. Isotope ratios were
expressed relative to PeeDee Belemnite (PDB) standard
for carbon and to N2 in air for nitrogen. Ratios were cal-
j kj culated by equation from the literature (Peterson and Fry
1987).
Trophic relationships among starfish and prey were
visualized via a trophodynamic plot. A two-way PER-
MANOVA of Bray–Curtis similarity of untransformed
δ13C and δ15N data was performed to test for size effects
on isotopic signatures (δ13C and δ15N) of M. glacialis. The
Mar Biol (2016) 163:65 Page 5 of 11  65

analysis included two factors: size (fixed, with two levels,
‘small’ [TL < 27 cm] and ‘large’ [TL  ≥ 27 cm]) and site
(random and orthogonal, with 2 levels, C1 and C2) and
was run by Primer v6 & Permanova+ (Clarke and Gorley
2006).
A cluster analysis was performed on the Bray–Curtis
similarity resemblance matrix calculated on the square root
transformed δ13C–δ15N data of the collected prey to iden-
tify homogeneous sources of food to be used in a mixing
model. The following 7 food sources were identified after
applying the SIMPROF test (Clarke et al. 2008): (1) C.
rustica, P. coeroulea and Trochoidea referred to as ben-
thic herbivores (BH); (2) A. noae and B. barbata, referred
to as filter feeders (FF); (3) C. tubularis and C. vulgatum
referred to as macro-grazers (MG); (4) A. lixula; (5) E. cor-
nea; (6) H. trunculus; (7) P. lividus. Percentage contribu-
tion of the food sources identified to the diet of M. glacia-
lis was estimated by a Bayesian mixing model approach,
using the software package SIAR in R (Parnell et al. 2010;
R Development Core Team 2010). Mixing models for small
and large M. glacialis were carried out with pooled sites,
since δ13C and δ15N of M. glacialis did not vary signifi-
cantly between sites (see results).
Since no species-specific trophic enrichment fac-
tor (TEF) was available for M. glacialis in the literature,
we selected TEF on estimates for invertebrate consumers
by McCutchan et al. (2003) (0.3 ± 0.14 ‰ for δ13C and
1.4  ± 0.20 ‰ for δ15N). We selected these fractionation
values on the basis that starfish samples were analyzed
by an arm without gonad and pyloric caeca (as a ‘whole’
organism without gonads and guts), and diet was mainly
composed of invertebrates, i.e., low protein content prey
sensu McCutchan et al. (2003).
Results
Analysis of the diet through field observations
Overall, 241 individuals of M. glacialis were found during
the study, 118 of which were feeding on 12 different benthic
prey items. The vacuity index (V %) was relatively low for
both sizes (41.9 and 48.1 %, respectively, small and large),
indicating a status of moderate feeder for M. glacialis.
The diet composition varied with body size (Table 1).
Bivalves, A. noae and B. barbata, were the most frequent
(Fi % = 49.37) prey in the diet of small M. glacialis, while
the sea urchins P. lividus and A. lixula (Fi % = 51.28 and
28.21 %, respectively) are those of the large ones. Other
prey were gastropods such as H. trunculus, C. vulga-
tum and P. caerulea, characterized by low Fi % values
(Table 1).
The electivity index differed between small and large
individuals of M. glacialis (Table 1). In particular, results
showed that A. noae, B. barbata, E. cornea, C. rustica (all
with Ei  = 0.99) and Trochoidea (Ei  = 0.98) were strongly
selected by small M. glacialis individuals, while C. vulgatum
(Ei = −0.89) and A. lixula (Ei = −0.46) were avoided. The
sea urchin P. lividus (Ei  = 0.25) resulted weakly selected.
In contrast, large M. glacialis fed selectively on sea urchins.
P. lividus (Ei  = 0.89) was better selected than A. lixula
(Ei = 0.61). No selection (Ei = 0) was recorded for C. vulga-
tum, E. cornea, P. caerulea, C. rustica and Trochoidea.
The Levin’s index resulted low for both sizes (Bi = 0.29
and Bi  = 0.43, respectively, for small and large M. gla-
cialis), indicating a specialist diet dominated by few prey
items (Labropoulou and Eleftheriou 1997; Abitia-Cardenas
et al. 1999). The dietary overlap between the two sizes was

Table 1  M. glacialis overall Fi % Ei

diet: frequency of occurrence
(Fi %) and electivity index (Ei) Small (N = 79) Large (N = 39) Small (N = 79) Large (N = 39)
of prey items for small (up to
27 cm TL) and large (>27 cm Arbacia lixula 2.53 28.21 −0.46 0.61
TL) starfish Arca noae–Barbatia barbata 49.37 15.38 0.99 0.95
Cerithium vulgatum 5.06 0 −0.89 0
Columbella rustica 11.39 0 0.99 0
Euthria cornea 3.80 0 0.99 0
Hexaplex trunculus 7.59 2.56 0.94 0.84
Luria lurida 0 2.56 0 0.99
Paracentrotus lividus 5.06 51.28 0.25 0.89
Patella caerulea 1.27 0 0.37 0
Trochoidea 8.86 0 0.98 0
Other invertebrates 5.06 0 – –

Other invertebrates include: Diogenidae (Calcinus tubularis), Mitridae (Mitra cornicula) Muricidae
(Ocinebrina edwardsii). Trochoidea: Trochidae (Clanculus cruciatus, Gibbula umbilicaris, Jujubinus spp.),
Calliostomatidae (Calliostoma laugeri)

13
 65   Page 6 of 11 Mar Biol (2016) 163:65

Table 2  SIMPER results of Prey Small, average similarity = 70.65

M. glacialis diet on arcsine-
transformed data and Bray– Av. Abund. Av. Sim. Sim./SD Contrib. % Cum. %
Curtis similarity resemblance
matrix (prey species with Arca noae–Barbatia barbata 0.77 28.04 6.46 39.69 39.69
Fi < 3 % not shown) Columbella rustica 0.36 12.13 3.00 17.16 56.85
Trochoidea 0.31 10.34 4.62 14.64 71.49
Hexaplex trunculus 0.24 6.15 1.12 8.70 80.20
Cerithium vulgatum 0.20 5.36 1.13 7.58 87.78
Other invertebrates 0.17 2.69 0.60 3.80 91.58
Large, average similarity = 64.51
Av. Abund. Av. Sim. Sim./SD Contrib. % Cum. %

Paracentrotus lividus 0.76 32.58 3.97 50.50 50.50

Arbacia lixula 0.62 24.40 4.79 37.82 88.33
Arca noae–Barbatia barbata 0.32 7.53 0.88 11.67 100.00
Small and large average dissimilarity = 71.17
Small Large
Av. Abund. Av. Abund. Av. Diss. Diss./SD Contrib. % Cum. %

Paracentrotus lividus 0.17 0.76 13.78 2.03 19.36 19.36

Arbacia lixula 0.10 0.62 12.19 1.62 17.13 36.49
Arca noae–Barbatia barbata 0.77 0.32 10.73 1.64 15.08 51.57
Columbella rustica 0.36 0 8.48 3.33 11.92 63.48
Trochoidea 0.31 0 7.23 3.67 10.16 73.64
Cerithium vulgatum 0.20 0 4.75 1.73 6.68 80.32
Hexaplex trunculus 0.24 0.08 4.70 1.42 6.60 86.92
Other invertebrates 0.17 0 3.75 1.14 5.26 92.18

Small M. glacialis individuals up to 27 cm TL; large M. glacialis individuals >27 cm TL

Av. Abund. average abundance, Av. Sim. average similarity, Sim./SD similarity standard deviation, Con-
trib. % percentage contribution, Cum. % cumulative percentage contribution, Av. Diss. average dissimilar-
ity, Diss./SD dissimilarity standard deviation

low (Cik = 0.34), suggesting that small and large M. glacia-
lis exploited different food resources.
The SIMPER routine confirmed this result (Table 2)
with a 71.17 % of dissimilarity between the two sizes and
the following contribution of preys to the discrimination: P.
lividus (19.36 %), A. lixula (17.13 %), bivalves (15.08 %)
and C. rustica (11.92 %).
Starfish prey’s total length resulted functionally cor-
related with starfish total length (TLprey  = 0.11 ×  TLstar-
fish − 2.91; r = 0.61, P < 0.001). The mean size of A. lixula
preyed by large starfish (test diameter = 39.8 ± 5.4 mm,
mean  ± 1 SD) was significantly larger (F1,29  = 8.8;
P  = 0.005.) than that of P. lividus (test diameter
32.4 ± 7.2 mm, mean ± 1 SD).
Stable isotope analysis
Isotopic signatures significantly differed between the
two sizes (P = 0.023, Table 3), with mean values of δ13C
and δ15N higher in large (δ13C  =  −11.97  ± 1.00 ‰
and δ15N  = 7.19 ± 0.87 ‰, mean ± 1 SD) than in
small M. glacialis (δ13C  =  −14.50  ± 0.90 ‰ and
δ15N = 5.32 ± 0.35 ‰, mean ± 1 SD, Table 4). No signifi-
cant differences were recorded for factor site (P = 0.059).
Isotopic values of M. glacialis prey exhibited wide
ranges for both carbon and nitrogen: δ15N ranged from
2.4 ± 0.5 ‰ (mean ± 1 SD) of B. barbata to 6.5 ± 0.7 ‰
(mean  ± 1 SD) of H. trunculus; δ13C values varied
from −19.6  ± 0.3 ‰ (mean ± 1 SD) of B. barbata to
−12.4 ± 0.9 ‰ (mean ± 1 SD) of A. lixula (Fig. 3).
According to the mixing model output, small M. gla-
cialis had a diet composed of MG (macro-grazers 22.0 %),
BH (benthic herbivorous gastropods 18.6 %) and E. cor-
nea (14.6 %). The sea urchins P. lividus (14.8 %) and A.
lixula (10.2 %) also fitted with the model, although with
lower contributions (Table 4). Bivalves (FF) accounted
for 13.0 %. Large M. glacialis diet was instead character-
ized by a higher percentage contribution of sea urchins and

13
Mar Biol (2016) 163:65 Page 7 of 11  65

Table 3  PERMANOVA results Source DF SS MS Pseudo-F P (perm) Unique perms P (MC)

based on Bray–Curtis similarity
of untransformed δ13C and δ15N Size (S) 1 611.23 611.23 51.495 0.251 3 0.023*
data between small (up to 27 cm
Site (Si) 1 42.858 42.858 3.3677 0.059n.s. 9951 0.067
TL) and large (>27 cm TL)
individuals of M. glacialis SxSi 1 11.87 11.87 0.9327 0.384n.s. 9956 0.384
RES 16 203.62 12.726
TOT 19

n.s. not significant
* P < 0.05

Table 4  δ13C and δ15N mean values (‰) and percentage contribution of sources to the diet (mixing model output) of small and large M. glacia-
lis
Species/group (N) SIAR group δ13C δ15N Percentage contribution (%)
Mean SD Mean SD Small Large
Low High Mean Low High Mean

Marthasterias glacialis (10) Small −14.5 0.9 5.3 0.3

Marthasterias glacialis (10) Large −12.0 1.0 7.2 0.9
Columbella rustica (2) BH −12.4 0.4 3.2 0.2
Patella caerulea (6) BH −13.2 0.6 4.5 0.3 BH 0.7 34.2 18.6 0.0 31.4 12.1
Trochoidea (2) BH −13.4 0.0 3.4 0.3
Arca noae (7) FF −19.4 0.4 2.7 0.4 FF 0.8 24.5 13.0 0.0 7.4 2.5
Barbatia barbata (7) FF −19.6 0.3 2.4 0.5
Calcinus tubularis (10) MG −14.6 0.9 2.4 0.3 MG 5.9 38.1 22.0 0.0 15.0 5.3
Cerithium vulgatum (4) MG −14.4 0.8 3.0 0.2
Arbacia lixula (10) −12.4 0.9 6.2 0.7 0.0 21.9 10.2 18.6 79.1 51.2
Euthria cornea (7) −16.6 1.3 3.8 0.6 0.0 29.9 14.6 0.0 13.1 4.5
Hexaplex trunculus (10) −15.4 1.0 6.5 0.7 0.0 16.2 6.7 0.0 30.4 11.5
Paracentrotus lividus (10) −13.7 0.9 4.8 0.7 0.0 30.5 14.8 0.0 30.9 12.9

BH Benthic herbivores, FF filter feeders, MG macro-grazers, SD standard deviation, low lower 95th percentile proportion, high higher 95th per-
centile proportion

9
8
(12.1 %) and H. trunculus (11.5 %). MG (5.3 %), E. cornea
7 Hexaplex trunculus
Arbacia lixula (4.5 %) and FF (2.5 %) shared the residual partitioning.
6
δ15N ± s.d.

5 Paracentrotus lividus
Euthria cornea
4 Patella caerulea
Trochoidea
3
Arca noae Cerithium vulgatum
Columbella rustica
Discussion
2 Calcinus tubularis
Barbatia barbata
1
Based on in situ observations and stable isotope analy-
0 sis, the present study showed a clear size-dependent shift
-20.50 -18.50 -16.50 -14.50 -12.50 -10.50 in the diet of M. glacialis. A. noae, B. barbata, E. cornea,
δ13C ± s.d. C. rustica and Trochoidea were highly selected by small
starfish, whereas sea urchins were selected by large ones.
Fig. 3  Trophodynamic plot of small (white inner triangles) and large The observed shift was accompanied by a significant 15N
(black triangles) M. glacialis individuals and food sources (circles, enrichment (Table 4), suggesting that large individuals
prey pooled per sites) occupy a higher trophic position than smaller ones. The fact
that the diet of M. glacialis is basically made up by mol-
luscs, above all bivalves, has been proved worldwide and
gastropods (Table 4). The sea urchins A. lixula (51.2 %) it is not a novelty (Branch 1978; Griffiths 1981; Magennis
and P. lividus (12.9 %) were the most important sources 1981; Verling et al. 2003; Tuya and Duarte 2012). Gener-
of food (overall 64.1 %). Other sources of food were BH ally, the preferred prey are also locally very abundant: this

13
 65   Page 8 of 11
is the case of M. glacialis feeding on the clam A. ephip-
pium in Ireland (Kitching and Thain 1983), black mussel,
C. meridionalis, in South Africa (Penney and Griffiths
1984) and Mytilus galloprovincialis (Lamarck, 1819) along
subtidal Portuguese rocky reefs (Tuya and Duarte 2012).
Differently, the finding that sea urchins were important
preys of large M. glacialis is worthy of consideration and
supports the hypothesis that this starfish might represent
a potentially efficient controller of P. lividus and A. lixula
populations in locations characterized by low predation
rate of sea breams (i.e., D. sargus and D. vulgaris), usually
considered the major sea urchin predators (Bonaviri et al.
2009; Gianguzza et al. 2009a).
Branch (1978) suggested that if the preferred M. glacia-
lis prey is rare or absent, a wider range of species will be
selected in relation to their abundance in the field. Com-
mon Mediterranean prey of M. glacialis are the rock-boring
bivalve Lithophaga lithophaga (Linnaeus, 1758) (Fanelli
et al. 1999; Guidetti 2004) and the mussel M. galloprovin-
cialis (Tuya and Duarte 2012).
L. lithophaga is very rare in Ustica due to the lack of
calcareous rocks in the island that is of volcanic origin, and
large-sized Mytilidae are absent due to the oligotrophy of the
Southern Tyrrhenian waters (Riggio and Milazzo 2004; Sarà
et al. 2011). In contrast, A. noae and B. barbata were nearly
common and sea urchins are abundant in the shallow sub-
littoral flat basaltic grounds at the time of sampling (Gian-
guzza et al. 2006; Bonaviri et al. 2009; Agnetta et al. 2013).
The observed difference in the diet between small and large
M. glacialis can be explained by the opportunistic feeding
behavior of the starfish that, as suggested by Branch (1978),
selects its prey in relation to their abundance in the field.
Thus, the rationale is that in the barren of the Ustica Island,
both small and large M. glacialis selected the most available
and profitable prey items: bivalves and large sea urchins,
respectively. Densities of large P. lividus and the co-occur-
ring A. lixula increased enormously after enforcement of
protection in 1991. It is likely that the natural scarcity of fish
predators (La Mesa and Vacchi 1999) and the ban of human
harvesting favored this process (Gianguzza et al. 2006). As
a result, the mesopredator M. glacialis raised as the main
sea urchin predator as it has experimentally been shown in
a tethering test (Bonaviri et al. 2009). While for small star-
fish predation on medium–large sea urchins may result in
an excessive consumption of energy, due to handling and
chasing, for the large ones the superabundance of this prey
instead represents a profitable resource to be exploited.
Indeed, sea urchins are preferred prey of other starfish in all
of the world’s oceans (Duggins 1983; Schroeter et al. 1983;
Rodriguez and Ojeda 1998; Gaymer and Himmelman 2008).
Moreover, a recent observation made in Ustica sheds light on
the Thalassoma pavo (Linnaeus, 1758)—M. glacialis inter-
action that facilitates the sea urchin capture by the starfish.
13
Mar Biol (2016) 163:65
The proximity of the starfish triggers an escape response
in sea urchins which extend their tube feet; at this point, T.
pavo feeds on the exposed tube feet impairing urchin move-
ment and making them vulnerable to predation by the star-
fish (Galasso et al. 2015).
Field data showed that M. glacialis acts as a moder-
ate predator at Ustica (index of vacuity V  = 44 %). Field
observations also suggest that predation of large M. glacia-
lis resulted higher upon P. lividus than A. lixula and this
was probably due to different morpho-functional features
potentially involved in defensive responses to predators.
It is possible that A. lixula is less profitable than P. livi-
dus for M. glacialis due to its structural defenses, like test
robustness, length and robustness of spines, high attach-
ment tenacity in the barren grounds which could increase
handling costs (Guidetti and Mori 2005; Gianguzza et al.
2010; Agnetta et al. 2013). No niche overlap was detected
between small and large M. glacialis (Cik < 0.6). The SIM-
PER analysis confirmed these data, showing a high per-
centage of dissimilarity between the two sizes. This result
was supported by stable isotope analysis as large M. gla-
cialis recorded significantly more enriched values for both
δ13C and δ15N than small ones.
The mixing model results were in agreement with field
data, implying a size shift in feeding preferences: mol-
luscs were strongly consumed by small starfish, whereas
sea urchins are consumed by the larger ones. However, at
lower taxonomical resolution, discrepancies were observed
between SIA and field results. In more detail, according
to the model output, small starfish did not result to mainly
consume, as field data suggest, the bivalves A. noae and B.
barbata (only 13.0 %), but rather the gastropod C. vulga-
tum (22.0 %). Additionally, if direct dietary observations
indicated that larger starfish greatly preferred P. lividus
over A. lixula (Fi  = 51.3 and 28.2 %, respectively), the
mixing model highlighted that A. lixula (51.2 %) was the
principal source of carbon and nitrogen assimilated by
large M. glacialis, followed by P. lividus (12.9 %).
It is important to note that field data elucidated prey fre-
quency and dietary preferences for prey items and do not
offer information about the nutritional input of each prey,
as SIA do (Colombo et al. 2013). This point was clearly
illustrated in our study by the case of C. vulgatum, a species
that resulted negatively selected in the field (Ei  =  −0.89)
by small M. glacialis, but according to SIA, it is an impor-
tant prey of small M. glacialis.
Moreover, in this study, the importance of different prey
items from field data was calculated on the basis of the fre-
quencies of occurrence, but the contribution in weight of
each prey was not considered. This means that small and
large prey were supposed to give an equal contribution to
the diet of M. glacialis ultimately overestimating the role
of small preys. Although more frequent, preyed P. lividus
Mar Biol (2016) 163:65 Page 9 of 11  65
were significantly smaller and weighed on average roughly
40 % less than preyed A. lixula (according to the length–
weight relationship reported in Agnetta et al. 2013). Hence,
the amount of the potentially assimilated food from a single
P. lividus was on average smaller compared to that assimi-
lated from a single A. lixula. These considerations can par-
tially explain the differences observed between field and
stable isotope data. Moreover, the choice of larger A. lix-
ula is supported by the finding of Galasso et al. 2015 that
report an average escape speed response of A. lixula to M.
glacialis attacks significantly lower than that of P. lividus.
Whenever possible, to detect trophic relationships in rocky
reef ecosystems it is of fundamental importance to integrate
isotope data with more traditional dietary information.
To summarize, this is the first study reporting on size-
related shift in the diet of M. glacialis in the Mediterra-
nean Sea. M. glacialis, from small to large sizes, showed
a shift in feeding preferences due to different use of food
items: bivalves, E. cornea, C. rustica and Trochoidea, were
strongly selected by small starfish, whereas the larger ones
strongly consumed P. lividus and A. lixula. Large M. gla-
cialis revealed the potential to be important modulator of
Mediterranean sea urchin populations. Our results well
support the hypothesis of Bonaviri et al. 2009 on the role
of the mesopredator M. glacialis. The authors speculated
that in the barren system of Ustica MPA, where densities of
seabreams are low (La Mesa and Vacchi 1999) and conse-
quently fish predation should not exert an effective control
on the abundance of sea urchins (Guidetti and Sala 2007),
M. glacialis was a predator able to control sea urchins (P.
lividus and A. lixula) populations. Gaining realistic infor-
mation on the diet of mesopredators in the Mediterranean
sea is important as they may contribute to replace the
trophic role of larger predators when lacking due to over-
fishing. This paper showed an unprecedented strong selec-
tion for sea urchin by large-sized individuals of M. glacia-
lis that may have surrogated for the lack of predation of
larger sea urchin predators.
Due the critical roles played by P. lividus and A. lixula
in the creation and maintenance of barren areas (Kempf
1962; Verlaque 1987; Bonaviri et al. 2012; Agnetta et al.
2013, 2015), more research, at larger spatial and time
scales, will be instrumental in assessing the real impact of
the M. glacialis size-dependent predation and could help
to better understand and refine current trophic models for
Mediterranean rocky reefs.
Acknowledgments  N. Galasso and G. Aglieri significantly contrib-
uted to field sampling. Sample pre-treatment for stable isotope analy-
sis was carried out by A. Mirasole and S. Noè, while isotopic analysis
was performed by A. E. Aleo. Special thanks to Renato Chemello,
Giovanni Fanelli and the anonymous reviewer for their construc-
tive and challenging comments, which substantially improved
this manuscript. Michelle Bowri revisited the English text. Chiara
Bonaviri was supported by the Italian project FIRB (Contract No.
RBFR12RXW). This study was funded by the research project “Mon-
itoraggio delle popolazioni di Paracentrotus lividus e Arbacia lixula
ai fini della tutela della diversità biologica dell’AMP Isola di Ustica”,
under the Italian Ministry of the Environment (M.A.T.T.M - Ministero
dell’Ambiente e della Tutela del Territorio e del Mare), University
of Palermo (FFR 2012-13) and by the Flagship Project RITMARE –
Italian Research for the Sea - funded by the Italian Ministry of Educa-
tion, University and Research.
Compliance with ethical standards 
Conflict of interest  Sampling was conducted under a research per-
mit from MPA management body of the Ustica Island (Port Authority
of Palermo). All authors approved the final version of the manuscript,
and consent to submit has been received from all co-authors. The
authors declare no competing financial interests or conflict of interest.
References
Abitia-Cardenas LA, Galvan-Magaña F, Gutierrez-Sanchez FJ, Rodri-
guez-Romero J, Aguilar-Palomino B, Moehl-Hitz A (1999) Diet
of blue marlin Makaira mazara off the coast of Cabo San Lucas,
Baja California Sur, Mexico. Fish Res 44(1):95–100
Agnetta D, Bonaviri C, Badalamenti F, Scianna C, Vizzini S, Gian-
guzza P (2013) Functional traits of two co-occurring sea urchins
across a barren/forest patch system. J Sea Res 76:170–177
Agnetta D, Badalamenti F, Ceccherelli G, Di Trapani F, Bonaviri C,
Gianguzza P (2015) Role of two co-occurring Mediterranean
sea urchins in the formation of barren from Cystoseira canopy.
Estuar Coast Mar Sci 152:73–77
Bacha M, Amara R (2012) Inter-cohort differences in growth, condi-
tion and feeding of juvenile anchovy (Engraulis encrasicolus) in
the Gulf of Bejaia (Algerian coast, SW Mediterranean): implica-
tions for recruitment success. Fish Res 129:73–81
Berg J (1979) Discussion of methods of investigating the food of
fishes, with reference to a preliminary study of the prey of Gobi-
usculus flavescens (Gobiidae). Mar Biol 50:263–273
Bonaviri C, Fernandez TV, Badalamenti F, Gianguzza P, Di Lorenzo
M, Riggio S (2009) Fish versus starfish predation in controlling
sea urchin populations in Mediterranean rocky shores. Mar Ecol
Prog Ser 382:129–138
Bonaviri C, Fernandez TV, Fanelli G, Badalamenti F, Gianguzza P
(2011) Leading role of the sea urchin Arbacia lixula in maintain-
ing the barren state in southwestern Mediterranean. Mar Biol
158(11):2505–2513
Bonaviri C, Gianguzza P, Pipitone C, Hereu B (2012) Micropredation
on sea urchins as a potential stabilizing process for rocky reefs. J
Sea Res 73:18–23
Branch GM (1978) The responses of south african patellid limpets to
invertebrate predators. Zool Afr 13(2):221–232
Bulleri F, Benedetti-Cecchi L, Cinelli F (1999) Grazing by the sea
urchins Arbacia lixula (L.) and Paracentrotus lividus (Lam.) in
the Northwest Mediterranean. J Exp Mar Biol Ecol 241(1):81–95
Bulleri F, Bertocci I, Micheli F (2002) Interplay of encrusting cor-
alline algae and sea urchins in maintaining alternative habitats.
Mar Ecol Prog Ser 243:101–109
Chintiroglou C, Koukouras A (1991) Observations on the feed-
ings habits of Calliactis parasitica (Couch, 1842), Anthozoa,
Cnidaria. Oceanol Acta 14:389–396
Clarke KR, Gorley RN (2006) Primer v6: user manual/tutorial.
Primer-E, Plymouth
13
 65   Page 10 of 11
Clarke KR, Somerfield PJ, Gorley RN (2008) Testing of null hypoth-
eses in exploratory community analyses: similarity profiles and
biota-environment linkage. J Exp Mar Biol Ecol 366:56–69
Colombo F, Costa V, Dubois SF, Gianguzza P, Mazzola A, Vizzini
S (2013) Trophic structure of vermetid reef community: high
trophic diversity at small spatial scales. J Sea Res 77:93–99
Dance C, Savy S (1987) Predation on Paracentrotus lividus by Mar-
thasterias glacialis: an in situ experiment at Port-Cros (France,
Mediterranean). Posidonia Newsl 1(2):35–41
Di Trapani F, Aglieri G, Badalamenti F, Bonaviri C, Gianguzza P,
Riggio S (2009) Distribution and diet of Marthasterias glacialis
at Ustica Island MPA. Biol Mar Medit 16(1):262–263
Duggins DO (1983) Starfish predation and the creation of mosaic pat-
terns in a kelp-dominated community. Ecology 64(6):1610–1619
Ebling FJ, Hawkins AD, Kitching FA, Muntz I, Pratt VM (1966) The
ecology of Lough Hyne. XVI. Predation and diurnal migration in
the Paracentrotus population. J Anim Ecol 35:559–566
Estes JA, Terborgh J, Brashares JS, Power ME, Berger J, Bond
WJ, Carpenter SR, Essington TE, Holt RD, Jackson JBC
et al (2011) Trophic downgrading of planet earth. Science
333(6040):301–306
Fanelli G, Piraino S, Esposito L, Boero F (1999) Opposite roles of sea
urchins and starfishes in marine benthic communities. In: Car-
nevali C, Bonasoro F (eds) Echinoderm research. Balkema, Rot-
terdam, pp 453–457
Forster GR (1962) Observations on the ormer population of Guern-
sey. Haliotis tuberculata (Gastropoda). J Mar Biol Assoc U K
42(3):493–498
Freeman A (2006) Size-dependent trait-mediated indirect interactions
among sea urchin herbivores. Behav Ecol 17(2):182–187
Frid CLJ (1992) Foraging behavior of the spiny starfish Marthas-
terias glacialis in Lough Ine, Co Cork. Mar Behav Physiol
19(4):227–239
Galasso NM, Bonaviri C, Di Trapani F, Picciotto M, Gianguzza P,
Agnetta D, Badalamenti F (2015) Fish-seastar facilitation leads
to algal forest restoration on protected rocky reefs. Sci Rep
5:12409. doi:10.1038/srep12409
Gaymer CF, Himmelman JH (2008) A keystone predatory sea star in
the intertidal zone is controlled by a higher-order predatory sea
star in the subtidal zone. Mar Ecol Prog Ser 370:143–153
Gaymer CF, Dutil C, Himmelman JH (2004) Prey selection and pred-
atory impact of four major sea stars on a soft bottom subtidal
community. J Exp Mar Biol Ecol 313(2):353–374
Gianguzza P, Chiantore M, Bonaviri C, Cattaneo-Vietti R, Vielmini I,
Riggio S (2006) The effects of recreational Paracentrotus lividus
fishing on distribution patterns of sea urchins at Ustica Island
MPA (Western Mediterranean, Italy). Fish Res 81(1):37–44
Gianguzza P, Bonaviri C, Guidetti P (2009a) Crushing predation of
the spiny star Marthasterias glacialis upon the sea urchin Para-
centrotus lividus. Mar Biol 156(5):1083–1086
Gianguzza P, Badalamenti F, Gianguzza F, Bonaviri C, Riggio S
(2009b) The operational sex ratio of the sea urchin Paracentrotus
lividus populations: the case of the Mediterranean marine pro-
tected area of Ustica Island (Tyrrhenian Sea, Italy). Mar Ecol-
Evol Persp 30(1):125–132
Gianguzza P, Bonaviri C, Milisenda G, Barcellona A, Agnetta D, Fer-
nandez TV, Badalamenti F (2010) Macroalgal assemblage type
affects predation pressure on sea urchins by altering adhesion
strength. Mar Environ Res 70(1):82–86
Gianguzza P, Di Trapani F, Bonaviri C, Visconti G, Deidun A, Badala-
menti F (2015) New body metrics to determine asteroid size and
weight directly in the field. Thalassas 31(1):73–82
Griffiths RJ (1981) Predation on the bivalve Choromytilus meridi-
onalis by the gastropod Natica tecta. J Molluscan Stud
47(1):112–120
13
Mar Biol (2016) 163:65
Guidetti P (2004) Consumers of sea urchins, Paracentrotus lividus
and Arbacia lixula, in shallow Mediterranean rocky reefs. Helgol
Mar Res 58(2):110–116
Guidetti P (2006) Estimating body size of sea urchins, Paracentro-
tus lividus and Arbacia lixula, from stomach contents of Dip-
lodus sargus, a Mediterranean predatory fish. J Appl Ichthyol
22(1):91–93
Guidetti P, Mori M (2005) Morpho-functional defences of Mediter-
ranean sea urchins, Paracentrotus lividus and Arbacia lixula,
against fish predators. Mar Biol 147(3):797–802
Guidetti P, Sala E (2007) Community-wide effects of marine reserves
in the Mediterranean Sea. Mar Ecol Prog Ser 335:43–56
Guillou M (1996) Biotic and abiotic interactions controlling starfish
outbreaks in the Bay of Douarnenez, Brittany, France. Oceanol
Acta 19(3–4):415–420
Guler M, Lok A (2015) Foraging behaviors of sea stars, Marthaste-
rias glacialis and Astropecten aranciacus (Asteroidea) and pred-
ator-prey interactions with warty venus clam, Venus verrucosa
(Bivalvia). J Exp Mar Biol Ecol 465:99–106
Hyslop E (1980) Stomach contents analysis—a review of methods
and their application. J Fish Biol 17(4):19
Ivlev VS (1961) Experimental ecology of the feeding of fishes. Yale
University Press, New Haven
Kempf M (1962) Recherches d’écologie compareé sur Paracentrotus
lividus et Arbacia lixula. Rec Trav St Mar Endoume 25:47–116
Kitching JA, Thain VM (1983) The ecological impact of the sea
urchin Paracentrotus lividus (Lamarck) in Lough Ine, Ireland.
Philos Trans R Soc Lond 300(B):513–552
Krebs CJ (1989) Ecological methodology. Harper and Row, New York
La Mesa G, Vacchi M (1999) An analysis of the coastal fish assem-
blage of the Ustica Island marine reserve (Mediterranean Sea).
Mar Ecol PSZNI 20(2):147–165
Labropoulou M, Eleftheriou A (1997) The foraging ecology of
two pairs of congeneric demersal fish species: importance of
morphological characteristics in prey selection. J Fish Biol
50(2):324–340
Lawrence JM (1992) Arm loss and regeneration in Asteroidea (Echi-
nodermata). Echinoderm Res 1991:39–52
Lawrence JM, Larrain A (1994) The cost of arm autotomy in the star-
fish Stichaster striatus. Mar Ecol Prog Ser 109(2–3):311–313
Magennis B (1981) Feeding habits of Marthasterias glacialis (L). J
Sherkin Isl 1(2):27–34
Magnesen T, Redmond KJ (2012) Potential predation rates by the
sea stars Asterias rubens and Marthasterias glacialis, on juve-
nile scallops, Pecten maximus, ready for sea ranching. Aquac Int
20(1):189–199
McCutchan JH, Lewis WM, Kendall C, McGrath CC (2003) Variation
in trophic shift for stable isotope ratios of carbon, nitrogen, and
sulfur. Oikos 102(2):378–390
Milazzo M, Chemello R, Badalamenti F, Riggio S (2000) Molluscan
assemblages associated with photophilic algae in the Marine
Reserve of Ustica Island (Lower Tyrrhenian Sea, Italy). Ital J
Zool 67(3):287–295
O’Sullivan D, Emmerson M (2011) Marine reserve designation,
trophic cascades and altered community dynamics. Mar Ecol
Prog Ser 440:115–128
Paine RT (1974) Intertidal community structure. Oecologia 15:93–120
Parnell AC, Inger R, Bearhop S, Jackson AL (2010) Source partition-
ing using stable isotopes: coping with too much variation. PLoS
ONE 5(3):e9672. doi:10.1371/journal.pone.0009672
Penney AJ, Griffiths CL (1984) Prey selection and the impact of the
starfish Marthasterias glacialis (L.) and other predators on the
mussel Choromytilus meridionalis (Krauss). J Exp Mar Biol
Ecol 75(1):19–36
Mar Biol (2016) 163:65 Page 11 of 11  65
Pérez-Portela R, Villamor A, Almada V (2010) Phylogeography of the
sea star Marthasterias glacialis (Asteroidea, Echinodermata):
deep genetic divergence between mitochondrial lineages in the
north-western mediterranean. Mar Biol 157:2015–2028
Peterson BJ, Fry B (1987) Stable isotopes in ecosystem studies. Annu
Rev Ecol Syst 18:293–320
Pratchett MS (2005) Dynamics of an outbreak population of Acan-
thaster planci at Lizard Island, northern Great Barrier Reef
(1995–1999). Coral Reefs 24(3):453–462
Pratchett MS (2007) Feeding preferences of Acanthaster planci
(Echinodermata: Asteroidea) under controlled conditions of food
availability. Pac Sci 61(1):113–120
Prugh LR, Stoner CJ, Epps CW, Bean WT, Ripple WJ, Laliberte AS,
Brashares JS (2009) The rise of the mesopredator. Bioscience
59(9):779–791
R Development Core Team (2010) R: a language and environment for
statistical computing. R Foundation for Statistical Computing,
Vienna
Riggio S, Milazzo M (2004) Ricchezza specifica e biodiversità marina
nell’isola di Ustica. Naturalistasiciliano 28:559–586
Rodriguez RS, Ojeda FP (1998) Behavioral responses of the sea
urchin Tetrapygus niger to predators and food. Mar Freshw
Behav Physiol 31(1):21–37
Sala E, Zabala M (1996) Fish predation and the structure of the sea
urchin Paracentrotus lividus populations in the NW Mediterra-
nean. Mar Ecol Prog Ser 140(1–3):71–81
Sarà G, Lo Martire M, Sanfilippo M, Pulicano G, Cortese G, Maz-
zola A, Manganaro A, Pusceddu A (2011) Impacts of marine
aquaculture at large spatial scales: evidences from N and P
catchment loading and phytoplankton biomass. Mar Environ Res
71(5):317–324
Savy S (1987) Activity pattern of the sea-star, Marthasterias glacia-
lis, in Port-Cros Bay (France, mediterranean coast). Mar Ecol
PSZNI 8(2):97–106
Schroeter SC, Dixon J, Kastendiek J (1983) Effects of the starfish
Patiria miniata on the distribution of the sea urchin Lytechi-
nus anamesus in a southern Californian kelp forest. Oecologia
2:141–147
Tomas F, Alvarez-Cascos D, Turon X, Romero J (2006) Differential
element assimilation by sea urchins Paracentrotus lividus in sea-
grass beds: implications for trophic interactions. Mar Ecol Prog
Ser 306:125–131
Tuya F, Duarte P (2012) Role of food availability in the bathymetric
distribution of the starfish Marthasterias glacialis (Lamk.) on
reefs of northern Portugal. Scientia Marina 76(1):9–15
Valinassab T, Jalali S, Hafezieh M, Zarshenas G (2011) Evaluation
of some feeding indices of Pomadasys kaakan in the Northern
Persian Gulf. Iran J Fish Sci 10(3):497–504
Verlaque MV (1987) Relations entre Paracentrotus lividus (Lamarck)
et le phytobenthos de Mediterranee occidentale. In: Boudoresque
CF (ed) Colloque international sur Paracentrotus lividus et les
oursins comestibles. GIS Posidonie, Marseille, pp 5–36
Verling E, Crook AC, Barnes DKA, Harrison SSC (2003) Structural
dynamics of a sea-star (Marthasterias glacialis) population. J
Mar Biol Assoc UK 83(3):583–592
13