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hereu et al 2005 (mar bio)
Marine Biology (2005) 146: 293–299
DOI 10.1007/s00227-004-1439-y
R ES E AR C H A RT I C L E
Bernat Hereu Æ Mikel Zabala Æ Cristina Linares
Enric Sala
The effects of predator abundance and habitat structural
complexity on survival of juvenile sea urchins
Received: 7 March 2004 / Accepted: 9 July 2004 / Published online: 6 August 2004
Ó Springer-Verlag 2004
Abstract We studied the effect of the abundance of because sea urchin grazing beyond a particular density
predatory fishes and structural complexity of algal threshold can transform complex communities, dra-
assemblages on the survival of juveniles of the sea urchin matically decreasing biodiversity in many systems, such
Paracentrotus lividus on Mediterranean infralittoral as algal communities (e.g. Lawrence 1975; Andrew and
rocky bottoms. Post-settlement juveniles (2–10 mm) Choat 1982; Himmelman et al. 1983), seagrass beds (e.g.
´
were placed on four distinct natural substrates with Camp et al. 1973; Macia and Lirman 1999; Alcoverro
increasing structural complexity (coralline barren, algal and Mariani 2002) and coral reefs (e.g. Hughes et al.
turf, erect fleshy algal assemblages and small crevices) 1987; Carpenter 1990; McClanahan and Shafir 1990).
inside and outside the Medes Islands Marine Reserve. Despite its ecological importance, the relative contribu-
Predation on these sea urchins increased at greater tions of the processes that regulate sea urchin abun-
abundance of predatory fishes, and decreased with dance, such as predation and recruitment, are as yet
greater structural complexity. The refuge provided by unclear.
structural complexity, however, decreased with increas- Predation is a key process in determining sea urchin
ing size of sea urchin recruits. Predation on the smallest population structure and dynamics (e.g. Tegner and
post-settlers was carried out almost exclusively by small Dayton 1981; McClanahan and Shafir 1990; Shears and
fishes (<20 cm), mainly the labrid Coris julis, while the Babcock 2002). It has been suggested that predation on
dominant predator of larger juveniles was the sparid juveniles is the major bottleneck in sea urchin popula-
Diplodus sargus. Our results demonstrate the cascading tions (Tegner and Dayton 1981; McClanahan and
effects caused by the prohibition of fishing in marine Muthiga 1989; Sala 1997; Lopez et al. 1998), and that it
reserves, and highlight the potential role of small pred- might dampen large fluctuations in density which result
atory fishes in the control of sea urchin populations. from variability in recruitment (Sala and Zabala 1996;
Lopez et al. 1998). Therefore, sea urchin populations
should be smaller in the presence of abundant predators
(McClanahan and Sala 1997). In marine reserves, where
Introduction predatory fishes are more abundant and larger than in
unprotected areas (e.g. Halpern and Warner 2002), sea
Sea urchin abundance is highly variable in time and urchin densities are generally lower than outside the
space (Pearse and Hines 1987; Turon et al. 1995; Sala reserves (McClanahan and Muthiga 1989; Sala and
et al. 1998a). Small variations in sea urchin abundance Zabala 1996; Shears and Babcock 2002, 2003). However,
can have considerable effects on benthic communities, predation is not the sole factor regulating sea urchin
densities. Diseases (e.g. Lessios 1988) or recruitment
variability (e.g. Turon et al. 1995) can also modify sea
Communicated by O. Kinne, Oldendorf/Luhe
urchin populations. There is evidence of large spatial
and temporal fluctuations of local sea urchin densities in
B. Hereu (&) Æ M. Zabala Æ C. Linares
Departament d’Ecologia, Facultat de Biologia, marine reserves (e.g. Sala et al. 1998a) because of factors
Universitat de Barcelona, Diagonal 645,
such as refuges from predation, which may reduce
08028 Barcelona, Spain
predation rates (Sala et al. 1998b).
E-mail: hereu@bio.ub.es
The availability of shelter is a key factor in deter-
E. Sala
mining predation rates (Roberts and Ormond 1987;
Center for Marine Biodiversity and Conservation,
Hixon and Beets 1993; Beck 1995) and hence the dis-
Scripps Institution of Oceanography, La Jolla,
tribution and abundance of sea urchins (Tegner and
CA 92093-0202, USA
294
Dayton 1981; Carpenter 1984; McClanahan and Kurtis vermilara) and seasonal (e.g. Dictyota dichotoma,
1991; Andrew 1993). When shelter is available, sea D. fasciola, Asparagopsis armata) macroalgae and
urchins hide and graze around it, thus contributing to understorey species (e.g. Corallina elongata, Rhody-
the formation of local barren areas (Andrew 1993; Sala menia ardissonei, Halopteris filicina) (Sala and Bou-
1996). The importance of shelters decreases with douresque 1997).
increasing sea urchin size because small sea urchins are
more susceptible to predation by fishes than large adults
(Sala and Zabala 1996; Shears and Babcock 2002).
Predatory fish abundance
Furthermore, the availability of shelters may be limited
for adult sea urchins.
To quantify the abundance of urchin-feeding fishes in
The sea urchin Paracentrotus lividus (Lamarck) is the
the reserve and the unprotected area, we counted and
most common grazer in the Mediterranean infralittoral
visually estimated the size of all fishes along randomly
(e.g. Kempf 1962; Verlaque 1987). At high densities, this
located 50·5 m transects using SCUBA diving (Har-
species overgrazes complex algal assemblages composed
melin-Vivien et al. 1985). We conducted five transects in
of several hundred species, and turns them into barren
each of two randomly selected sites in both the reserve
areas dominated by a few species of encrusting algae
and the unprotected area (n=10 transects per level of
(Kempf 1962; Neill and Larkum 1965; Verlaque 1987;
protection). The different substrate types form small
Sala 1996). Barren areas, together with large sea urchin
patches (<10 m2), and fishes move between patches,
populations, occur mainly in areas with few urchin
hence we assumed that there were no differences in fish
predators (reviewed by Sala et al. 1998b; Pinnegar et al.
density between substratum types within sampling sites.
2000). However, there is also evidence of barren areas in
Fish biomass was calculated using length-biomass rela-
marine reserves with large fish densities (Sala et al.
tionships from E. Sala (unpublished data) and Bayle
1998a). The objective of this study was to determine the
et al. (2001).
effects of predator abundance and structural complexity
of the habitat (algal assemblages) on the survival of
juvenile P. lividus. We hypothesize that the survival of
juveniles decreases with increasing predator abundance, Predation experiments
and that increasing structural complexity (availability of
shelter) decreases the predation rate. To test this Juvenile P. lividus 2–10 mm in diameter (test without
hypothesis, we carried out experiments in the NW spines) were collected from crevices and beneath boul-
Mediterranean, in a marine reserve and in an unpro- ders in the study areas using SCUBA diving.
tected area with significant differences in the abundance All experiments were conducted in summer because
of predatory fishes. fish activity is higher (Garcia-Rubies 1996) and P. lividus
recruitment is strongest (Lopez et al. 1998). Nocturnally
active urchin-feeding fishes are uncommon (Savy 1987;
Sala 1997); therefore experiments and field observations
Materials and methods
were conducted during daylight.
Juvenile P. lividus were placed on the bottom using
Study site
tweezers and covered with 40·40·30 cm plastic cages
with 1-cm mesh size. After 5 min, a diver located on the
The study was carried out in the NW Mediterranean
bottom 10 m away lifted the cage using a string, thus
Sea, both in the Medes Islands Marine Reserve (where
exposing the urchins to predators. We believe we avoi-
fishing is prohibited) and the nearby Montgrı´ unpro-
ded artefacts caused by the attraction of fishes to divers,
tected area (where fishing takes place) (see Hereu et al.
and obtained independent estimates of predation. Fishes
2004 for a detailed map). The reserve (which was created
did not appear to be attracted to the cage, and therefore
in 1983), is located 1 km offshore from the town of
we believe that predation was not biased by the experi-
l’Estartit (42°16¢N, 03°13¢E) and encompasses a group
mental procedure. A digital video camera (Sony VCR
of small islands. The study was conducted on rocky
900) in an underwater housing (Gates Diego Housing)
bottoms 5–10 m deep, harbouring a mosaic of patches
was placed close to the cage, and experiments were
(103–105 cm2) dominated by distinct types of algal
filmed by remote control for 20 min (divers left the site
assemblages, including:
after pulling away the cage and exposing urchins to
predators). In the laboratory, we watched the videotape
1. Coralline barrens dominated by encrusting corallines
and noted the times at which each sea urchin was con-
(Lithophyllum incrustans, Mesophyllum alternans,
sumed by fishes, identified the predator species for each
Spongites notarisii);
individual sea urchin, and estimated their size using a
2. Turf algal assemblages dominated by small filamen-
plastic ruler placed at the study site as a reference. Pre-
tous algae (e.g. Rhodomelaceae, Ceramiaceae,
liminary trials showed that in most treatments sea urchin
Ulvaceae); and
survival showed asymptotes before 20 min after the
3. Erect algal assemblages dominated by a canopy
beginning of the experiments, suggesting that the
of perennial (e.g. Cystoseira compressa, Codium
295
experiments were run long enough to allow us to detect measured and estimation of fish size was possible. We
differences between treatments. also conducted additional experiments using sea urchins
To test how predation may be modified by the from 10 to 13 mm in diameter.
structural complexity of the habitat, four types of sub-
strate (see above for details) were selected on each area,
by increasing degree of protection from predation: (1) Results
coralline barrens without shelter (no crevices); (2) algal
turfs; (3) erect macroalgal assemblages; and (4) crevices Abundance of predatory fish
(0.5–3 cm width). In the treatment with crevices, sea
urchins were placed inside the crevices; in all other The major P. lividus predator, Diplodus sargus, showed
treatments sea urchins were placed on the substrate. In similar densities in the reserve and the unprotected area
both areas (inside and outside the marine reserve), we (ANOVA: F1,18=1.36, P=0.26). However, mean size
conducted five experiments randomly placed in each was significantly larger in the reserve, and hence biomass
habitat type. In each experimental replicate, 10 juvenile was higher in the reserve (F1,18=13.02, P=0.002;
sea urchins (2–4 mm diameter) were placed in each Fig. 1). The biomasses of Coris julis (F1,18=10.8,
treatment (habitat type). To test for differences in sur- P=0.005), Labrus merula (F1,18=7.57, P=0.013) and
vival of juvenile P. lividus between treatments and degree Thalassoma pavo (F1,18=7.56, P=0.013), the other main
of predator abundance, two-way ANOVAs were per- P. lividus predators (Sala 1997), were also significantly
formed, with predator abundance (reserve, unprotected greater in the marine reserve than in the nearby unpro-
area) and habitat type as independent variables, and tected area (Fig. 1). The biomass of other known pre-
survival at the end of the experiment as the dependent dators was not statistically different between the reserve
variable. Cochran’s test was conducted prior to ANO- and unprotected area. Nevertheless, the total biomass of
VA to test the assumption of homogeneity of variance. predator fishes was higher in the reserve, mainly due to
Data were log-transformed to satisfy this assumption. the contribution of D. sargus (Fig. 1).
To determine the relationship between the sizes of sea
urchins consumed by fish of particular size classes, we
conducted experiments as described above, using two Effects of predation and habitat structural complexity
size classes of sea urchins (2–6 and 6–10 mm), in the on sea urchin survival
marine reserve (n=3 replicates per size class and habitat
type). To test for differences in sea urchin survival The predatory fishes observed eating juvenile sea urchins
among sizes and substrata, two-way ANOVAs were during the experiments were the labrids C. julis,
performed. Cochran’s test was conducted prior to L. merula, Symphodus roissali and T. pavo, and the
ANOVA to test the assumption of homogeneity of sparids D. sargus and D. vulgaris. Predation rates on
variance. When necessary, data were log-transformed to juvenile P. lividus were significantly greater in the marine
satisfy this assumption. reserve than in the unprotected area for all substrate
To determine the relationship between predatory fish types except crevices (Fig. 2; Table 1). In the reserve, the
size and sea urchin size, we conducted a non-linear survival of sea urchins was higher with increasing
regression between fish length and sea urchin diameter, structural complexity of the algal assemblage, being
using data from experiments where sea urchin size was minimal on coralline barrens where shelter was absent,
Fig. 1 Biomass of predatory
fishes (mean±SD) inside and
outside the Medes Islands
Marine Reserve. Asterisks
indicate statistical significance
in an ANOVA analysis
(* P<0.05; ** P<0.01)
296
barrens was very low, in contrast with erect algae hab-
itats and crevices (Table 2).
Predation was highest during the first 5 min of the
experiments (Figs. 2, 3).
In the reserve, predation on sea urchins 6–10 mm in
diameter was greater than on smaller ones (2–6 mm)
except on crevices (Fig. 3; Table 3). Sea urchin survival
was similarly low in barrens and algal turfs regardless of
size, whereas survival of smaller sea urchins was greater
in erect algal assemblages. Crevices provided effective
refuge for both size classes.
Predator-prey size relationship
The identity of the major predators changed with
increasing sea urchin size (Fig. 4). Although D. sargus
was the most important predator of adult P. lividus (Sala
and Zabala 1996; Sala 1997), it did not feed effectively
on small juveniles (<4 mm). The labrid C. julis was the
most effective predator of small juvenile P. lividus. The
importance of C. julis as a predator decreased, while that
of D. sargus increased, with increasing sea urchin size.
As reported previously by Sala (1997), P. lividus of
>10 mm diameter are consumed mostly by D. sargus.
Other fish species made a limited contribution to total
Fig. 2 Mean survival (±SE, n=5) of juvenile Paracentrotus lividus
in distinct habitat types in a the Medes Islands Marine Reserve and predation (0–20%) (Fig. 4). Although L. merula was not
b the unprotected area nearby
observed eating sea urchins of >11.5 mm diameter in
this study, they are known to prey on large sea urchins,
including this size (Sala 1997).
and maximal inside crevices which provided the highest
The relationship between the size of the predatory
degree of physical protection. In the unprotected area,
fish (all species) and the size of sea urchins consumed
where predatory fishes were less abundant, all juvenile
by them was statistically significant although the
P. lividus on vegetated substrates survived the experi-
variance explained by the model was low (Fish =
ment, whereas in the reserve they experienced predation
13.361+1.679·Urchin; r2=0.31, P<0.001; Fig. 5).
in all vegetated treatments (Fig. 2; Table 2). In the re-
serve, the percentage survival for turf assemblages and There was a significant correlation between predator
Table 1 Results of ANOVA
Factor MS P level Tukey post-hoc test
df F
comparing the effect of
substrate type in protected and
Barren (B): R „ NR
Protection (P) 1 40.83 45.10
unprotected areas on the
Turf (T): R „ NR
survival of juvenile
Algae (A): R=NR
Paracentrotus lividus
Crevices (C): R=NR
Reserve (R): B=T „ A=C
Substrate (S) 3 18.27 20.19
Non-reserve (NR): B=T=A=C
P·S 3 9.19 10.16 <0.01
Error 32 0.905
Table 2 Survival of juvenile
2–6 mm 6–10 mm
P. lividusin each substrate type
and size class inside (MR) and
Mean % SD Mean % SD
outside (NR) the Medes Islands
Marine Reserve. Barren
MR Barren 0.00 0.00 0.00 0.00
Coralline barren; Turf algal
Turf 6.66 16.32 0.00 0.00
turf;Erect erect palatable algae
Erect 58.00 33.11 11.66 16.02
Crevices 100 0.00 100 0.00
NR Barren 56.66 30.76
Turf 100 0.00
Erect 100 0.00
Crevices 100 0.00
297
P=0.003 for D. sargus). In C. julis, females predomi-
nantly ate the smallest sea urchins, while males, which
are larger, monopolized predation of 9- to 10-mm
diameter urchins.
Discussion
The abundance of predatory fishes and the structure of
algal assemblages influenced survival of juvenile P. livi-
dus. Survival was higher with increasing habitat com-
plexity and at lower fish biomass. Adult P. lividus also
had greater mortality rates in the presence of abundant
predatory fishes (Sala and Zabala 1996). Our results
support the hypothesis that smaller fishes such as labrids
can play a major role in the regulation of recruitment by
eating the smaller size classes, although medium to large
fishes are the most effective predators of adult sea
urchins (Sala 1997).
As demonstrated for other species and systems, the
presence of shelter can reduce predation mortality
(McClanahan and Shafir 1990; Hixon and Beets 1993;
Andrew 1993; Beck 1995). In the present study,
increasing structural complexity of the habitat also
increased survival of juvenile sea urchins, at least in the
short term. Because P. lividus larvae do not appear to
exhibit habitat preferences for settlement (Hereu et al.
2004), we would expect the density of sea urchin recruits
to be larger at sites with shelter. However, the sub-
stantial mortalities of P. lividus settlers during the first
weeks after settlement in erect algal assemblages (Sala
and Zabala 1996; Hereu et al. 2004) may be due to other
factors, such as predation by micropredators such as
polychaetes and crustaceans, which inhabit erect algal
assemblages.
Our results involve only the first 20 min after the
beginning of experiments. The fact that predation by
fishes had virtually ended after less than 20 min suggests
that the sea urchins secured shelter and were no longer
detected by fishes. However, the presence of micropre-
dators probably causes additional mortality over time.
Absolute predation rates were not obtained from our
Fig. 3 Mean survival (±SE, n=5) of juvenile P. lividus belonging experiments because algal assemblages are not the only
to two size classes (2–6 mm and 6–10 mm) in distinct habitat types shelter available to juvenile sea urchins: crevices and
in the Medes Islands Marine Reserve
spaces beneath small boulders also provide abundant
shelter. In fact, predation in marine reserves with a high
and sea urchin size within taxa (Fish = 11.517+
0.791·Urchin; r2=0.32, P<0.001 for C. julis and abundance of predatory fishes may not reduce absolute
T. pavo; and Fish = 21.829+0.666·Urchin; r2=0.06, sea urchin densities, because most are sheltered in
Table 3 Results of ANOVA
Factor MS P level Tukey post-hoc test
df F
comparing the effect of
substrate type on the survival of
Small (S): B=T „ A „ C
Substrate 3 25,328.44 125.13
small (2–6 mm) and larger
Large (L): B=T=A „ C
(6–10 mm) juvenile P. lividus
Size 1 2,091.80 10.33 Barren (B): S=L
Turf (T): S=L
Algae (A): S „ L
Crevices (C): S=L
Substrate·size 3 1,484.06 7.33 <0.01
Error 40 1,484.06
298
Fig. 4 Proportion of mortality
caused by major predatory fish
species on juvenile P. lividus of
different sizes
Our results support the potential role of marine
reserves in the regulation of sea urchin populations, and
hence in preventing the development of sea urchin
barrens, as predicted by models (McClanahan and Sala
1997; Sala et al. 1998b). In Mediterranean marine
reserves, predatory fishes are more abundant and greater
in size than in unprotected areas (e.g. Garcia-Rubies and
Zabala 1990; Francour 1991; Harmelin et al. 1995),
therefore predation rates on sea urchins are greater in
these reserves (Sala and Zabala 1996; this study). The
significantly lower survival observed in the Medes
Islands Marine Reserve relative to that in unprotected
sites is a clear example of the predation effects that
follow effective protection of coastal habitats (Pinnegar
et al. 2000). We believe that the strength of predation on
Fig. 5 Size relationship between P. lividus and predatory fishes juvenile sea urchins by fishes is a good estimator of fish
during predation experiments in the Medes Islands Marine Reserve
build-up and trophic changes in marine reserves.
crevices and beneath boulders (Sala and Zabala 1996; Acknowledgements We are grateful to D. Diaz, M. Marı´ and J.M.
Sala et al. 1998a). However, simple predation experi- Llenas for field and laboratory assistance and to E. Ballesteros for
comments and discussions. This study was funded by grant
ments, like those carried out here, can provide a stan-
MAR1999-0526 of the Ministry for Science and Technology of
dardised protocol to assess the strength of predation in Spain, and by the Department of the Environment of the Catalan
coastal ecosystems. Government.
The partitioning of predation on P. lividus by fish
species and sizes can have implications for the regulation
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DOI 10.1007/s00227-004-1439-y
R ES E AR C H A RT I C L E
Bernat Hereu Æ Mikel Zabala Æ Cristina Linares
Enric Sala
The effects of predator abundance and habitat structural
complexity on survival of juvenile sea urchins
Received: 7 March 2004 / Accepted: 9 July 2004 / Published online: 6 August 2004
Ó Springer-Verlag 2004
Abstract We studied the effect of the abundance of because sea urchin grazing beyond a particular density
predatory fishes and structural complexity of algal threshold can transform complex communities, dra-
assemblages on the survival of juveniles of the sea urchin matically decreasing biodiversity in many systems, such
Paracentrotus lividus on Mediterranean infralittoral as algal communities (e.g. Lawrence 1975; Andrew and
rocky bottoms. Post-settlement juveniles (2–10 mm) Choat 1982; Himmelman et al. 1983), seagrass beds (e.g.
´
were placed on four distinct natural substrates with Camp et al. 1973; Macia and Lirman 1999; Alcoverro
increasing structural complexity (coralline barren, algal and Mariani 2002) and coral reefs (e.g. Hughes et al.
turf, erect fleshy algal assemblages and small crevices) 1987; Carpenter 1990; McClanahan and Shafir 1990).
inside and outside the Medes Islands Marine Reserve. Despite its ecological importance, the relative contribu-
Predation on these sea urchins increased at greater tions of the processes that regulate sea urchin abun-
abundance of predatory fishes, and decreased with dance, such as predation and recruitment, are as yet
greater structural complexity. The refuge provided by unclear.
structural complexity, however, decreased with increas- Predation is a key process in determining sea urchin
ing size of sea urchin recruits. Predation on the smallest population structure and dynamics (e.g. Tegner and
post-settlers was carried out almost exclusively by small Dayton 1981; McClanahan and Shafir 1990; Shears and
fishes (<20 cm), mainly the labrid Coris julis, while the Babcock 2002). It has been suggested that predation on
dominant predator of larger juveniles was the sparid juveniles is the major bottleneck in sea urchin popula-
Diplodus sargus. Our results demonstrate the cascading tions (Tegner and Dayton 1981; McClanahan and
effects caused by the prohibition of fishing in marine Muthiga 1989; Sala 1997; Lopez et al. 1998), and that it
reserves, and highlight the potential role of small pred- might dampen large fluctuations in density which result
atory fishes in the control of sea urchin populations. from variability in recruitment (Sala and Zabala 1996;
Lopez et al. 1998). Therefore, sea urchin populations
should be smaller in the presence of abundant predators
(McClanahan and Sala 1997). In marine reserves, where
Introduction predatory fishes are more abundant and larger than in
unprotected areas (e.g. Halpern and Warner 2002), sea
Sea urchin abundance is highly variable in time and urchin densities are generally lower than outside the
space (Pearse and Hines 1987; Turon et al. 1995; Sala reserves (McClanahan and Muthiga 1989; Sala and
et al. 1998a). Small variations in sea urchin abundance Zabala 1996; Shears and Babcock 2002, 2003). However,
can have considerable effects on benthic communities, predation is not the sole factor regulating sea urchin
densities. Diseases (e.g. Lessios 1988) or recruitment
variability (e.g. Turon et al. 1995) can also modify sea
Communicated by O. Kinne, Oldendorf/Luhe
urchin populations. There is evidence of large spatial
and temporal fluctuations of local sea urchin densities in
B. Hereu (&) Æ M. Zabala Æ C. Linares
Departament d’Ecologia, Facultat de Biologia, marine reserves (e.g. Sala et al. 1998a) because of factors
Universitat de Barcelona, Diagonal 645,
such as refuges from predation, which may reduce
08028 Barcelona, Spain
predation rates (Sala et al. 1998b).
E-mail: hereu@bio.ub.es
The availability of shelter is a key factor in deter-
E. Sala
mining predation rates (Roberts and Ormond 1987;
Center for Marine Biodiversity and Conservation,
Hixon and Beets 1993; Beck 1995) and hence the dis-
Scripps Institution of Oceanography, La Jolla,
tribution and abundance of sea urchins (Tegner and
CA 92093-0202, USA
294
Dayton 1981; Carpenter 1984; McClanahan and Kurtis vermilara) and seasonal (e.g. Dictyota dichotoma,
1991; Andrew 1993). When shelter is available, sea D. fasciola, Asparagopsis armata) macroalgae and
urchins hide and graze around it, thus contributing to understorey species (e.g. Corallina elongata, Rhody-
the formation of local barren areas (Andrew 1993; Sala menia ardissonei, Halopteris filicina) (Sala and Bou-
1996). The importance of shelters decreases with douresque 1997).
increasing sea urchin size because small sea urchins are
more susceptible to predation by fishes than large adults
(Sala and Zabala 1996; Shears and Babcock 2002).
Predatory fish abundance
Furthermore, the availability of shelters may be limited
for adult sea urchins.
To quantify the abundance of urchin-feeding fishes in
The sea urchin Paracentrotus lividus (Lamarck) is the
the reserve and the unprotected area, we counted and
most common grazer in the Mediterranean infralittoral
visually estimated the size of all fishes along randomly
(e.g. Kempf 1962; Verlaque 1987). At high densities, this
located 50·5 m transects using SCUBA diving (Har-
species overgrazes complex algal assemblages composed
melin-Vivien et al. 1985). We conducted five transects in
of several hundred species, and turns them into barren
each of two randomly selected sites in both the reserve
areas dominated by a few species of encrusting algae
and the unprotected area (n=10 transects per level of
(Kempf 1962; Neill and Larkum 1965; Verlaque 1987;
protection). The different substrate types form small
Sala 1996). Barren areas, together with large sea urchin
patches (<10 m2), and fishes move between patches,
populations, occur mainly in areas with few urchin
hence we assumed that there were no differences in fish
predators (reviewed by Sala et al. 1998b; Pinnegar et al.
density between substratum types within sampling sites.
2000). However, there is also evidence of barren areas in
Fish biomass was calculated using length-biomass rela-
marine reserves with large fish densities (Sala et al.
tionships from E. Sala (unpublished data) and Bayle
1998a). The objective of this study was to determine the
et al. (2001).
effects of predator abundance and structural complexity
of the habitat (algal assemblages) on the survival of
juvenile P. lividus. We hypothesize that the survival of
juveniles decreases with increasing predator abundance, Predation experiments
and that increasing structural complexity (availability of
shelter) decreases the predation rate. To test this Juvenile P. lividus 2–10 mm in diameter (test without
hypothesis, we carried out experiments in the NW spines) were collected from crevices and beneath boul-
Mediterranean, in a marine reserve and in an unpro- ders in the study areas using SCUBA diving.
tected area with significant differences in the abundance All experiments were conducted in summer because
of predatory fishes. fish activity is higher (Garcia-Rubies 1996) and P. lividus
recruitment is strongest (Lopez et al. 1998). Nocturnally
active urchin-feeding fishes are uncommon (Savy 1987;
Sala 1997); therefore experiments and field observations
Materials and methods
were conducted during daylight.
Juvenile P. lividus were placed on the bottom using
Study site
tweezers and covered with 40·40·30 cm plastic cages
with 1-cm mesh size. After 5 min, a diver located on the
The study was carried out in the NW Mediterranean
bottom 10 m away lifted the cage using a string, thus
Sea, both in the Medes Islands Marine Reserve (where
exposing the urchins to predators. We believe we avoi-
fishing is prohibited) and the nearby Montgrı´ unpro-
ded artefacts caused by the attraction of fishes to divers,
tected area (where fishing takes place) (see Hereu et al.
and obtained independent estimates of predation. Fishes
2004 for a detailed map). The reserve (which was created
did not appear to be attracted to the cage, and therefore
in 1983), is located 1 km offshore from the town of
we believe that predation was not biased by the experi-
l’Estartit (42°16¢N, 03°13¢E) and encompasses a group
mental procedure. A digital video camera (Sony VCR
of small islands. The study was conducted on rocky
900) in an underwater housing (Gates Diego Housing)
bottoms 5–10 m deep, harbouring a mosaic of patches
was placed close to the cage, and experiments were
(103–105 cm2) dominated by distinct types of algal
filmed by remote control for 20 min (divers left the site
assemblages, including:
after pulling away the cage and exposing urchins to
predators). In the laboratory, we watched the videotape
1. Coralline barrens dominated by encrusting corallines
and noted the times at which each sea urchin was con-
(Lithophyllum incrustans, Mesophyllum alternans,
sumed by fishes, identified the predator species for each
Spongites notarisii);
individual sea urchin, and estimated their size using a
2. Turf algal assemblages dominated by small filamen-
plastic ruler placed at the study site as a reference. Pre-
tous algae (e.g. Rhodomelaceae, Ceramiaceae,
liminary trials showed that in most treatments sea urchin
Ulvaceae); and
survival showed asymptotes before 20 min after the
3. Erect algal assemblages dominated by a canopy
beginning of the experiments, suggesting that the
of perennial (e.g. Cystoseira compressa, Codium
295
experiments were run long enough to allow us to detect measured and estimation of fish size was possible. We
differences between treatments. also conducted additional experiments using sea urchins
To test how predation may be modified by the from 10 to 13 mm in diameter.
structural complexity of the habitat, four types of sub-
strate (see above for details) were selected on each area,
by increasing degree of protection from predation: (1) Results
coralline barrens without shelter (no crevices); (2) algal
turfs; (3) erect macroalgal assemblages; and (4) crevices Abundance of predatory fish
(0.5–3 cm width). In the treatment with crevices, sea
urchins were placed inside the crevices; in all other The major P. lividus predator, Diplodus sargus, showed
treatments sea urchins were placed on the substrate. In similar densities in the reserve and the unprotected area
both areas (inside and outside the marine reserve), we (ANOVA: F1,18=1.36, P=0.26). However, mean size
conducted five experiments randomly placed in each was significantly larger in the reserve, and hence biomass
habitat type. In each experimental replicate, 10 juvenile was higher in the reserve (F1,18=13.02, P=0.002;
sea urchins (2–4 mm diameter) were placed in each Fig. 1). The biomasses of Coris julis (F1,18=10.8,
treatment (habitat type). To test for differences in sur- P=0.005), Labrus merula (F1,18=7.57, P=0.013) and
vival of juvenile P. lividus between treatments and degree Thalassoma pavo (F1,18=7.56, P=0.013), the other main
of predator abundance, two-way ANOVAs were per- P. lividus predators (Sala 1997), were also significantly
formed, with predator abundance (reserve, unprotected greater in the marine reserve than in the nearby unpro-
area) and habitat type as independent variables, and tected area (Fig. 1). The biomass of other known pre-
survival at the end of the experiment as the dependent dators was not statistically different between the reserve
variable. Cochran’s test was conducted prior to ANO- and unprotected area. Nevertheless, the total biomass of
VA to test the assumption of homogeneity of variance. predator fishes was higher in the reserve, mainly due to
Data were log-transformed to satisfy this assumption. the contribution of D. sargus (Fig. 1).
To determine the relationship between the sizes of sea
urchins consumed by fish of particular size classes, we
conducted experiments as described above, using two Effects of predation and habitat structural complexity
size classes of sea urchins (2–6 and 6–10 mm), in the on sea urchin survival
marine reserve (n=3 replicates per size class and habitat
type). To test for differences in sea urchin survival The predatory fishes observed eating juvenile sea urchins
among sizes and substrata, two-way ANOVAs were during the experiments were the labrids C. julis,
performed. Cochran’s test was conducted prior to L. merula, Symphodus roissali and T. pavo, and the
ANOVA to test the assumption of homogeneity of sparids D. sargus and D. vulgaris. Predation rates on
variance. When necessary, data were log-transformed to juvenile P. lividus were significantly greater in the marine
satisfy this assumption. reserve than in the unprotected area for all substrate
To determine the relationship between predatory fish types except crevices (Fig. 2; Table 1). In the reserve, the
size and sea urchin size, we conducted a non-linear survival of sea urchins was higher with increasing
regression between fish length and sea urchin diameter, structural complexity of the algal assemblage, being
using data from experiments where sea urchin size was minimal on coralline barrens where shelter was absent,
Fig. 1 Biomass of predatory
fishes (mean±SD) inside and
outside the Medes Islands
Marine Reserve. Asterisks
indicate statistical significance
in an ANOVA analysis
(* P<0.05; ** P<0.01)
296
barrens was very low, in contrast with erect algae hab-
itats and crevices (Table 2).
Predation was highest during the first 5 min of the
experiments (Figs. 2, 3).
In the reserve, predation on sea urchins 6–10 mm in
diameter was greater than on smaller ones (2–6 mm)
except on crevices (Fig. 3; Table 3). Sea urchin survival
was similarly low in barrens and algal turfs regardless of
size, whereas survival of smaller sea urchins was greater
in erect algal assemblages. Crevices provided effective
refuge for both size classes.
Predator-prey size relationship
The identity of the major predators changed with
increasing sea urchin size (Fig. 4). Although D. sargus
was the most important predator of adult P. lividus (Sala
and Zabala 1996; Sala 1997), it did not feed effectively
on small juveniles (<4 mm). The labrid C. julis was the
most effective predator of small juvenile P. lividus. The
importance of C. julis as a predator decreased, while that
of D. sargus increased, with increasing sea urchin size.
As reported previously by Sala (1997), P. lividus of
>10 mm diameter are consumed mostly by D. sargus.
Other fish species made a limited contribution to total
Fig. 2 Mean survival (±SE, n=5) of juvenile Paracentrotus lividus
in distinct habitat types in a the Medes Islands Marine Reserve and predation (0–20%) (Fig. 4). Although L. merula was not
b the unprotected area nearby
observed eating sea urchins of >11.5 mm diameter in
this study, they are known to prey on large sea urchins,
including this size (Sala 1997).
and maximal inside crevices which provided the highest
The relationship between the size of the predatory
degree of physical protection. In the unprotected area,
fish (all species) and the size of sea urchins consumed
where predatory fishes were less abundant, all juvenile
by them was statistically significant although the
P. lividus on vegetated substrates survived the experi-
variance explained by the model was low (Fish =
ment, whereas in the reserve they experienced predation
13.361+1.679·Urchin; r2=0.31, P<0.001; Fig. 5).
in all vegetated treatments (Fig. 2; Table 2). In the re-
serve, the percentage survival for turf assemblages and There was a significant correlation between predator
Table 1 Results of ANOVA
Factor MS P level Tukey post-hoc test
df F
comparing the effect of
substrate type in protected and
Barren (B): R „ NR
Protection (P) 1 40.83 45.10
unprotected areas on the
Turf (T): R „ NR
survival of juvenile
Algae (A): R=NR
Paracentrotus lividus
Crevices (C): R=NR
Reserve (R): B=T „ A=C
Substrate (S) 3 18.27 20.19
Non-reserve (NR): B=T=A=C
P·S 3 9.19 10.16 <0.01
Error 32 0.905
Table 2 Survival of juvenile
2–6 mm 6–10 mm
P. lividusin each substrate type
and size class inside (MR) and
Mean % SD Mean % SD
outside (NR) the Medes Islands
Marine Reserve. Barren
MR Barren 0.00 0.00 0.00 0.00
Coralline barren; Turf algal
Turf 6.66 16.32 0.00 0.00
turf;Erect erect palatable algae
Erect 58.00 33.11 11.66 16.02
Crevices 100 0.00 100 0.00
NR Barren 56.66 30.76
Turf 100 0.00
Erect 100 0.00
Crevices 100 0.00
297
P=0.003 for D. sargus). In C. julis, females predomi-
nantly ate the smallest sea urchins, while males, which
are larger, monopolized predation of 9- to 10-mm
diameter urchins.
Discussion
The abundance of predatory fishes and the structure of
algal assemblages influenced survival of juvenile P. livi-
dus. Survival was higher with increasing habitat com-
plexity and at lower fish biomass. Adult P. lividus also
had greater mortality rates in the presence of abundant
predatory fishes (Sala and Zabala 1996). Our results
support the hypothesis that smaller fishes such as labrids
can play a major role in the regulation of recruitment by
eating the smaller size classes, although medium to large
fishes are the most effective predators of adult sea
urchins (Sala 1997).
As demonstrated for other species and systems, the
presence of shelter can reduce predation mortality
(McClanahan and Shafir 1990; Hixon and Beets 1993;
Andrew 1993; Beck 1995). In the present study,
increasing structural complexity of the habitat also
increased survival of juvenile sea urchins, at least in the
short term. Because P. lividus larvae do not appear to
exhibit habitat preferences for settlement (Hereu et al.
2004), we would expect the density of sea urchin recruits
to be larger at sites with shelter. However, the sub-
stantial mortalities of P. lividus settlers during the first
weeks after settlement in erect algal assemblages (Sala
and Zabala 1996; Hereu et al. 2004) may be due to other
factors, such as predation by micropredators such as
polychaetes and crustaceans, which inhabit erect algal
assemblages.
Our results involve only the first 20 min after the
beginning of experiments. The fact that predation by
fishes had virtually ended after less than 20 min suggests
that the sea urchins secured shelter and were no longer
detected by fishes. However, the presence of micropre-
dators probably causes additional mortality over time.
Absolute predation rates were not obtained from our
Fig. 3 Mean survival (±SE, n=5) of juvenile P. lividus belonging experiments because algal assemblages are not the only
to two size classes (2–6 mm and 6–10 mm) in distinct habitat types shelter available to juvenile sea urchins: crevices and
in the Medes Islands Marine Reserve
spaces beneath small boulders also provide abundant
shelter. In fact, predation in marine reserves with a high
and sea urchin size within taxa (Fish = 11.517+
0.791·Urchin; r2=0.32, P<0.001 for C. julis and abundance of predatory fishes may not reduce absolute
T. pavo; and Fish = 21.829+0.666·Urchin; r2=0.06, sea urchin densities, because most are sheltered in
Table 3 Results of ANOVA
Factor MS P level Tukey post-hoc test
df F
comparing the effect of
substrate type on the survival of
Small (S): B=T „ A „ C
Substrate 3 25,328.44 125.13
small (2–6 mm) and larger
Large (L): B=T=A „ C
(6–10 mm) juvenile P. lividus
Size 1 2,091.80 10.33 Barren (B): S=L
Turf (T): S=L
Algae (A): S „ L
Crevices (C): S=L
Substrate·size 3 1,484.06 7.33 <0.01
Error 40 1,484.06
298
Fig. 4 Proportion of mortality
caused by major predatory fish
species on juvenile P. lividus of
different sizes
Our results support the potential role of marine
reserves in the regulation of sea urchin populations, and
hence in preventing the development of sea urchin
barrens, as predicted by models (McClanahan and Sala
1997; Sala et al. 1998b). In Mediterranean marine
reserves, predatory fishes are more abundant and greater
in size than in unprotected areas (e.g. Garcia-Rubies and
Zabala 1990; Francour 1991; Harmelin et al. 1995),
therefore predation rates on sea urchins are greater in
these reserves (Sala and Zabala 1996; this study). The
significantly lower survival observed in the Medes
Islands Marine Reserve relative to that in unprotected
sites is a clear example of the predation effects that
follow effective protection of coastal habitats (Pinnegar
et al. 2000). We believe that the strength of predation on
Fig. 5 Size relationship between P. lividus and predatory fishes juvenile sea urchins by fishes is a good estimator of fish
during predation experiments in the Medes Islands Marine Reserve
build-up and trophic changes in marine reserves.
crevices and beneath boulders (Sala and Zabala 1996; Acknowledgements We are grateful to D. Diaz, M. Marı´ and J.M.
Sala et al. 1998a). However, simple predation experi- Llenas for field and laboratory assistance and to E. Ballesteros for
comments and discussions. This study was funded by grant
ments, like those carried out here, can provide a stan-
MAR1999-0526 of the Ministry for Science and Technology of
dardised protocol to assess the strength of predation in Spain, and by the Department of the Environment of the Catalan
coastal ecosystems. Government.
The partitioning of predation on P. lividus by fish
species and sizes can have implications for the regulation
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