Download predation on young paracentrotus lividus settlers

Biol. Mar. Mediterr. (2010), 17 (1): 98-101
C. Bonaviri, C. Pipitone1, P. Gianguzza, B. Hereu2
Dipartimento di Ecologia Università di Palermo, Via Archirafi, 18 - 90123 Palermo, Italia.
[email protected]
1
CNR-IAMC, Sede di Castellammare del Golfo, Trapani, Italia.
2
Department d’Ecologia, Universitat de Barcelona, Spain.
PREDATION ON YOUNG PARACENTROTUS LIVIDUS SETTLERS:
IMPLICATIONS FOR MEDITERRANEAN ROCKY
INFRALITTORAL STABILITY
PREDAZIONE SU GIOVANILI DI PARACENTROTUS LIVIDUS:
IMPLICAZIONI PER LA STABILITÀ DEI SISTEMI INFRALITORALI
ROCCIOSI MEDITERRANEI
Abstract – Predation of young sea urchins settlers are often invoked as a key process in the control
of sea urchins populations and therefore in the structure and stability of rocky infralittoral communities.
In this study a number of decapod species were detected as predators of young settlers of the sea urchin
Paracentrotus lividus and their predation rates estimated by laboratory experiments. Abundance of
these predators also resulted significantly lower in barren than in macro algae forests, suggesting that
lack of predation of juvenile sea urchins facilitates the stability of Mediterranean barren systems.
Key-words: ecosystem stability, predator-prey interactions, sea urchin, crustaceans, hard bottoms.
Introduction - In the last decades temperate infralittoral ecosystems have
undergone a loss of habitat-forming algae. Erect macroalgae canopy can be massively
reduced by perturbation (e.g., loss of top-down control of grazers, destructive
harvesting) leading to a shift towards an alternative phase dominated by sea urchins
and encrusting organisms named barren (Sala et al., 1998). Whether encrusting- and
erect macroalgae dominated communities represent alternate stable states of rocky
systems has not been proven (Knowlton, 2004). Sea urchins biomass and abundance
maintain high in barren areas where few-months old individuals can be more
numerous than in macro algae forests (Rowley, 1989). Echinoids are invertebrates with
a planktonic larval phase and their population structure strictly depends on larval
supply, settlement process and post-settlement mortality. Some authors suggest that
mortality of young settlers could represent the bottleneck for sea urchin populations
in erect macroalgae forests (Jennings & Hunt, 2010 and reference therein). Given that
erect macroalgae are habitat-formers, they add physical complexity to the substratum
by increasing species richness and functional diversity of mobile epifaunal organisms
(Taylor, 1998). Density of small invertebrates is positively correlated with structural
complexity of the habitat, being low in barrens and high in erect algae assemblages
(Taylor, 1998). The fact that young settled sea urchins are vulnerable to predation
by various small invertebrates (Scheibling & Robinson, 2008), may make erect algae
systems less suitable for the survival of recruits. Mediterranean rocky littorals are
characterized by either barren or macro algae forests (Sala et al., 1998). The sea
urchin Paracentrotus lividus resides in both systems but displays always higher
biomass and abundance in the former. Since the settlement of P. lividus is probably
independent from the benthic assemblage (Hereu, 2004), the difference of the sea
urchin population structure may depend on the post-settlement mortality between the
two systems. Mortality of P. lividus recruits has been estimated to reach 75% during
the first six months in a macro algae system (Sala & Zabala, 1996). In this light,
considering the potential role of predation on P. lividus recruits in regulating their
abundance, this study planned: (1) to individuate the predators of P. lividus recruits
Predation on young P. lividus settlers
99
and evaluate their predation rates, (2) to compare the abundance of predators of
early settled P. lividus in barren and erect macroalgae systems.
Materials and methods – The study area included the Medes Island Marine Reserve
and the nearby Montgri unprotected area (NW Mediterranean Sea) in summer 2009.
The study was carried out on rocky bottoms at 5-8 m depth, characterized by two
distinct types of algal assemblage state including: (1) Barren State (BS), dominated
by encrusting corallines (Lithophyllum incrustans, Mesophyllum alternans, Spongites
notarisii) and (2) Erect macroalgae state (EAS) dominated by a canopy of perennial
(e.g. Cystoseira compressa, Codium vermillara) and seasonal (e.g.: Dictyota dichotoma,
Asparagopsis armata) macroalgae and understorey species (e.g.: Corallina elongata,
Rhodymenia ardissonei, Halopteris filicina).
In order to individuate the potential predators of P. lividus juveniles and their
predation rates, we exposed young sea urchin settlers to a variety of decapod
crustaceans in the laboratory, based on our previous experiments and on the literature
(Scheibling & Robinson, 2008). Decapods and sea urchin juveniles were collected by
scraping off rocky substrates. In the laboratory, small decapods (<20 mm) and newly
settlers of P. lividus (<2 mm) were sorted and taxonomically identified. Sea urchins
were maintained on coralline crusts and decapods in chilled Millipore-filtered (0.45
μm) seawater (FSW) until use in experiments (Scheibling & Robinson, 2008). In each
experimental trial, 10 P. lividus juveniles and an individual of a potential predator
were placed in a 250 ml beaker with 150 ml of FSW maintained at 19 °C. After
48 h, the surviving sea urchins were counted to calculate the predation rate, and
the length of predators measured. In each replicate trial (n=4-16, Tab. 1), different
individuals of prey and predators were used.
In order to evaluate the abundance of the predators in BS and EAS, macrofaunal
samples were collected by scraping off the rocky substrate defined by quadrats of
20×20 cm. In the laboratory, samples were sieved through a 0.5 mm mesh and
identified under a binocular microscope. The predators were counted. Two sites for
Tab. 1 - Species used in the predation experiments.
Specie usate negli esperimenti di predazione.
C. Bonaviri, C. Pipitone, P. Gianguzza, B. Hereu
100
each community state type (BS and EAS) and three replicates for each experimental
block were considered. Analysis of variance was performed using the GMAV5
software package (coded by A.J. Underwood and M.G. Chapman, University
of Sydney, Australia) to test for differences in the density of pistol shrimps and
crabs that consumed juveniles in the laboratory experiments (Tab. 1), in relation
to community state (State; fixed factor, two levels) and between sites within each
level of state (Site; nested factor, two levels). Variables were not transformed as they
held homogeneity of variances in Cochran’s C test. Subsequent pairwise comparisons
were performed by Student-Newman-Keuls (SNK) tests. No ANOVA was computed
on hermit crabs density as it did not hold homogeneity of variance, even after that
transformations were applied.
Results – Only some species of decapod crustaceans utilized in the trials predated
P. lividus juveniles. Among hermit crabs, Pagurus anachoretus and Calcinus tubularis
had a high predation rate (Tab.1). On the contrary, Cestopagurus timidus and
Clibanarius erythropus did not prey on the urchins (Tab. 1). Among 8 species of crabs
presented to young settlers of P. lividus, the two Pilumnus species and Liocarcinus
arcuatus resulted efficient predators, consuming almost all the sea urchins offered.
The two Xantho species had a low predation rate (Tab. 1). The pistol shrimp Alpheus
dentipes showed an intermediate predation rate (Tab. 1).
Predators of P. lividus were abundant in EAS and almost absent in the BS, where
only one individual of A. dentipes was found (Tab. 2).
Tab. 2 - ANOVA on the abundance of P. lividus predators.
ANOVA sulle abbondanze dei predatori di P. lividus.
Conclusions – In the Mediterranean Sea, high densities of P. lividus may maintain
coralline barrens state determining drastic changes on ecosystem functioning.
Theoretical and empirical studies suggest that resilience of alternative community
states can be enhanced by self-perpetuating process (Knowlton, 2004). Many
authors suggest that post-settlement events, like predation, may strongly influence
the abundance of sea urchins (Jennings & Hunt, 2010 and references therein). This
study for the first time investigates predation on young settlers of P. lividus by
small invertebrates. Our predation experiments provide laboratory evidence that
different crustacean decapods voraciously consume few days-weeks old P. lividus.
Unexpectedly, we found profound differences in predation rates among different
hermit crabs and among different crabs. The difference in the predation patterns
among species might depend on species-specific morphological and/or behavioural
traits and may have profound repercussions on the mortality of early-post settlement
sea urchins in natural conditions. As expected, predators were significantly more
abundant in the erect macroalgae assemblage and almost absent in barren areas.
Our findings strongly support the hypothesis that the absence of erect algae in a
Predation on young P. lividus settlers
101
barren system may cause the reduction of predators of P. lividus young-settlers, thus
enhancing sea urchin recruit survival and representing a self-perpetuating process
for the stability of Mediterranean barren systems. This study suggests different and
complementary roles of small invertebrate species in controlling the abundance of
sea urchin recruits and underlines the importance of the functional diversity of small
invertebrates in this process. We encourage future research aimed to understanding
the factors involved in the interaction strength between sea urchin recruits and their
small invertebrate predators.
References
HEREU B., ZABALA M., LINARES C., SALA E. (2004) - Temporal and spatial variability in
settlement of the sea urchin Paracentrotus lividus (Lmk). Mar. Biol ., 144: 1011-1018.
JENNINGS L.B., HUNT H.L. (2010) - Settlement, recruitment and potential predators and
competitors of juvenile echinoderms in the rocky subtidal zone. Mar. Biol ., 157: 307-316.
KNOWLTON N. (2004) - Multiple “stable” states and the conservation of marine ecosystems.
Prog. Oceanogr, 60: 387-3962.
ROWELEY R.J. (1989) - Settlement and recruitment of sea urchins (Strongylocentrotus spp.) in
a sea urchin barren ground and a kelp bed: are populations regulated by settlement or postsettlement processes? Mar. Biol., 100: 485-494.
SALA E., BOUDOURESQUE C.F., HARMELIN-VIVIEN M. (1998) - Fishing, trophic cascades,
and the structure of algal assemblages: evaluation of an old but untested paradigm. Oikos, 82:
425-439.
SALA E., ZABALA M. (1996) - Fish predation and the structure of the sea urchin Paracentrotus
lividus populations in the NW Mediterranean. Mar. Ecol. Prog. Se.r., 140: 71-81.
SCHEIBLING R.E., ROBINSON M.C. (2008) – Settlement behaviour and early post-settlement
predation of the sea urchin Strongylocentrotus droebachiensis. J. Exp. Mar. Biol. Ecol., 365:
59-66.
TAYLOR R.B. (1998) - Density, biomass and productivity of animals in four subtidal rocky reef
habitats: the importance of small mobile invertebrates. Mar. Ecol. Prog. Ser., 172: 37–51.