The operational sex ratio of the sea urchin paracentrotus lividus populations: the case of the mediterranean marine protected area of ustica island (tyrrhenian sea, italy)

The operational sex ratio of the sea urchin Paracentrotuslividus populations: the case of the Mediterranean marineprotected area of Ustica Island (Tyrrhenian Sea, Italy)Paola Gianguzza1, Fabio Badalamenti2, Fabrizio Gianguzza3, Chiara Bonaviri1 & Silvano Riggio1 1 Dipartimento di Ecologia, Universita` degli Studi di Palermo, Palermo, Italy2 CNR-IAMC Laboratorio di Biologia Marina, Castellammare del Golfo (Tp), Italy3 Dipartimento di Biologia Cellulare e dello Sviluppo Universita` degli Studi di Palermo, Palermo, Italy Adult sex ratio; echinoid; Marine ProtectedArea; natural predation; starfish; Tyrrhenian We investigated, with a series of field and laboratory observations, the possible effect of the starfish Marthasteria glacialis predation on the operational sexratio (OSR), i.e. the number of sexually mature males divided by the total number of sexually mature adults of both sexes at any one time, of the edible Paola Gianguzza, Dipartimento di Ecologia, sea urchin Paracentrotus lividus. The OSR was estimated three times during the Universita` degli Studi di Palermo, Via Archirafi sea urchin summer spawning period (July 2004, June 2005 and July 2006) on 18, 90123 Palermo, Italy.
E-mail: [email protected] barren substrates of Ustica Island Marine Protected Area (Southern TyrrhenianSea, Italy). Four sites were selected: two characterized by high M. glacialis den- sity (take zone C) and two controls with low starfish density (no-take zone A).
Mature sea urchins were independently collected by SCUBA diving and sexed.
The adult sex ratio was skewed towards males at high M. glacialis density sites,whereas it was balanced (1:1) at predator low-density sites. Results of sex-selec-tive feeding experiments in the laboratory showed that females of P. lividuswere more vulnerable to M. glacialis predation. These outcomes underline thepossible importance of M. glacialis in regulating the OSR of P. lividus popula-tions.
tance in determining the structure of rocky reefs (Verlaque 1987; Sala et al. 1998) and to its economic The operational sex ratio, hereafter OSR, is defined by value (Boudouresque & Verlaque 2001). It has been sug- Emlen & Oring (1977) as the number of sexually mature gested that its grazing may play a paramount role in the males divided by the total number of sexually mature and transition from macroalgal beds to ‘coralline barrens’, active adults of both sexes at a given moment. It is a characterized by lower complexity and diversity (Verlaque major factor influencing the intensity of sexual selection 1987; Sala et al. 1998). At the same time, P. lividus is (Clutton-Brock & Parker 1992). A skewed OSR usually intensively exploited in many Mediterranean areas, as leads to increased competition for mates among members both male and female gonads are considered a delicacy of the more abundant sex, while members of the other (Lawrence 1987; Boudouresque & Verlaque 2001).
sex may have a greater opportunity to exercise mate In July 2002, during the preliminary survey phase of a project aimed at defining the role of sea urchin P. lividus and Arbacia lixula (L.) (Echinodermata: Echinoidea) pop- (Echinodermata: Echinoidea) has been the object of a ulations in the process of formation and maintenance of number of studies in the Mediterranean Sea. The increas- barrens in the Ustica Island Marine Protected Area ing interest in this species is primarily due to its impor- (MPA), we found a male-skewed P. lividus OSR at the Marine Ecology (2008) 1–8 ª 2008 The Authors. Journal compilation ª 2008 Blackwell Publishing Ltd Gianguzza, Badalamenti, Gianguzza, Bonaviri & Riggio take zone C (high starfish M. glacialis density and a particular in the take area of the MPA (authors’ personal balanced OSR at the no-take zone A (low starfish den- observation). Unfortunately, due to the extremely cryptic sity). Given the ecological and economic importance of behaviour and nocturnal activity of this species (Savy P. lividus, this operational sex-ratio disparity was consid- 1987b), abundance estimates are problematic and may be ered worthy of further investigation. The apparent imbal- biased. However, a high number of M. glacialis have been ance in the OSR may reflect a sampling procedure bias, observed predating sea urchins in recent years, and the but if this pattern is confirmed, this may have important remains of sea urchins eaten by starfish are frequently consequences for fluctuations in population size and recorded, especially at the barren grounds of zone C structure, especially in a small population (Emlen & M. glacialis is a slow-moving predator, able to detect P. lividus is a species with a chromosomal (genetic) sex its prey using olfaction (Valentincic 1973). It could be determination mechanism expected to allocate equal hypothesized that during the P. lividus spawning period effort to producing male and female offspring because the starfish is more attracted by (and hence preferentially random meiosis would lead to a mean sex ratio of 0.5 consumes) females. The aim of this study was to explore (Lipani et al. 1996). In this case, environmental condi- possible variability in OSR of P. lividus populations tions, such as pronounced temperature fluctuations, inhabiting barren rocky substrates of Ustica Island MPA.
which may influence sex determination in other echi- By comparing areas with different densities of M. glacialis, noids (see Pearse & Cameron 1991), were not involved in low (the no-take zone A) versus high (take zone C), we assessed the potential importance of this predator in reg- According to Clutton-Brock & Vincent (1991), the ulating the OSR of the P. lividus population of the Ustica OSR of species with chromosomal sex determination can Island MPA. Furthermore, with a series of laboratory be influenced by the following factors: the adult sex ratio choice experiments we tested the prediction that M. gla- in the population, the spatial and temporal distribution cialis prefers to consume P. lividus females rather than of the two sexes, their differences in growth and mortal- ity, their potential reproductive output (i.e. number ofsperm delivered and eggs deposited) and reproductivebehaviour. Possible deviation from a 1:1 sex ratio may also be due to different habitat (i.e. higher food availabil- ity conditions typical of fringe habitats) that could attracthigher female numbers, as reported before in other The study was carried out on Ustica Island (MPA) in the echinoid species (McPherson 1965, 1968; Bernard 1977; Lessios 1979). Natural selective predation and fishing or 10°43¢43¢¢ E–38°42¢20¢¢ N), 60 km north of the Sicilian harvesting (in terms of sex and size) also affect the adult coast (Fig. 1). The MPA, created in 1986, encompasses a sex ratio and consequently the OSR of marine popula- total area of 16,000 ha and contains three zones with dif- ferent degrees of protection. The no-take zone (zone A) In the Mediterranean Sea, several predators such as covers 65 ha along the western part of the island, while fishes, lobsters, starfishes and gastropods are listed amongthe most important sea urchin predators (Savy 1987a),and human harvesting may affect the abundance and sizeof targeted species and have positive indirect conse-quences on algal assemblages (Guidetti & Sala 2007).
Gianguzza et al. (2006) showed that in the MPA of Ustica Island a regulated human harvesting (50 P. lividusindividuals per person per day, during the summer sea-son) may affect the size and have positive indirect conse-quences on non-target species such as A. lixula. AsP. lividus is a species that lacks sexually dimorphic struc-tures, it is not expected to exhibit differential vulnerabilityto human predation. However, other predators such asthe spiny starfish Marthasteria glacialis (L.) could beinvolved in explaining the observed OSR differences.
There is evidence that in the last 10 years, the Fig. 1. Zonation of the Ustica Island MPA and study sites. (A1: Punta M. glacialis population at Ustica Island has grown, in Megna; A2: Acquario; C1: Punta dell’Arpa; C2: Punta S. Paolo).
Marine Ecology (2008) 1–8 ª 2008 The Authors. Journal compilation ª 2008 Blackwell Publishing Ltd Gianguzza, Badalamenti, Gianguzza, Bonaviri & Riggio the general reserve (zone B) and the take zone (zone C) seven randomly located quadrats of 1 m2 on shallow (about 4–5 m depth) rocky barren substrates mostly According to the institutive decree of the MPA (D.I.
composed of gently sloping platforms. Sampling was con- 12 ⁄ 11 ⁄ 1986), only research activities are authorized in the ducted on days with good sea-weather conditions, around no-take zone A, whereas recreational activities, such as SCUBA diving, boat anchoring, swimming and angling, We collected sea urchins larger than 40–45 mm (test are strictly prohibited. There are no restrictions on recrea- diameter) and thus every year we analysed different tional activities in either the B or the C zones. Further- mature animals belonging to this size class. Collected ani- more, the law authorizes local professional fishing in mals were separated in numbered landing nets and these zones and, from 1994 to 2006, recreational sea brought to the laboratory in containers with ice, without urchin harvesting was regulated (50 P. lividus individuals water, as suggested by Buznikov & Podmarev (1975). Sex per person per day, during the summer season) in the determinations were made visually, by puncturing the tes- tes of freshly dissected specimens and recording, under aLeitz M3C dissection microscope, the presence or absenceof eggs or sperm (Byrne 1990).
Variability in the OSR of P. lividus was estimated over 3 years in July 2004, June 2005 and July 2006, during thesummer sea urchin spawning period (Sa´nchez-Espan˜a Differences in OSR were analysed using a three-way Anal- et al. 2004; G. Visconti, unpublished data) at two areas ysis of Variance (ANOVA) mixed model, with ‘time’ (Ti), with different density of starfish: the no-take zone A, three levels (July 2004, June 2005 and July 2006), and characterized by extremely low presence of Marthasterias ‘Marthasterias density’ (MD), two levels low versus high glacialis (0.1 ± 0.1 individuals per 250 m2, mean den- (L versus H), as fixed and orthogonal factors and site (Si), sity ± SE), and take zone C, characterized by a high pres- two levels, as a random factor nested in MD. Seven inde- ence of M. glacialis (3.8 ± 0.5 individuals per 250 m2, pendent replicates of OSR were used for each combina- mean density ± SE). Only adult urchins (test diameter tion of factors for a total of 84 observations. Each 40–45 mm to assure they were matures) were collected by replicate represents the OSR value estimated within a SCUBA diving at two sites in the no-take zone A (A1 and 1 m2 quadrat. Data were tested for normality with the A2, Punta Megna and Acquario, respectively; Fig. 1) and Bartlett test (Bartlett 1937). Homogeneity of variances at two sites in the take zone C (C1 and C2, Punta del- was also checked with Cochran’s C-test (Winer 1971).
l’Arpa and Punta S. Paolo, respectively; Fig. 1). All sites After ANOVA, means were compared (at a = 0.05) with were randomly selected, approximately 500 m apart. This Student–Newman–Keuls (SNK) tests (Underwood 1997).
distance ensured the independence of data: Hereu (2005) The GMAV 5.0 software (University of Sydney, Australia) demonstrated that P. lividus has low random mobility on was used to perform the statistical tests. Furthermore, sig- rocky bottoms (the total distance observed in a 3-month nificant deviations of the sex ratio from 0.5 were tested in study of this species ranged from 71.8 to 673.6 cm). The each site using a Chi-square test on pooled data across all study sites were similar in the physical structural com- replicate quadrats (Sokal & Rohlf 1995).
plexity of their habitat: shallow sublittoral flat basalticgrounds. From the surface to about 3 m depth, the rocky substrate is generally covered by macroalgae (chiefly artic-ulated Corallinaceae, Dictyotales and Cystoseira spp.) and sessile invertebrates (e.g. sponges, hydroids, bryozoans).
Thirty M. glacialis, measuring 20–30 cm in diameter (the From 4 m to about 8 m depth, flat basaltic barren diameter across the circle defined by the arm tips), were grounds grazed by sea urchins are present, similar to randomly collected by SCUBA diving in the study sites those described in other areas (Frantzis et al. 1988; Sala from September to October 2007 at a depth of 8 m. After et al. 1998; Bulleri et al. 1999; Shears & Babcock 2003).
collection, starfishes were placed in large sealed plastic Overall, apart from different degrees of exposure, there bags containing oxygenated seawater, for transportation are no macroscopic differences between locations in terms to the wet laboratory at the Department of Ecology of the of rocky substrate, physical heterogeneity, macroalgal University of Palermo. Starfishes were maintained in 35-l cover and sea urchin densities: only a small-scale spatial aquaria with circulating natural seawater, at ambient light variation (i.e. sites) in term of P. lividus density was (12 h light and 12 h darkness) and at a temperature of detected in the present study (F2.108 = 4.42, P = 0.014, 22 °C. Prior to the experiments, all animals were starved n = 10). At each site, sea urchins were collected along for a week and kept in separate glass vessels to ensure Marine Ecology (2008) 1–8 ª 2008 The Authors. Journal compilation ª 2008 Blackwell Publishing Ltd Gianguzza, Badalamenti, Gianguzza, Bonaviri & Riggio that all individuals had experienced similar conditions individualsÆm)2, mean ± SE). Average female density was and to prevent changes in natural feeding responses due maximum in July 2006 at site A2 (3.3 ± 0.6 individu- to the stress of collection and transfer (Rochette et al.
alsÆm)2, mean ± SE) and minimum in June 2005 at site C1 (0.1 ± 0.1 individualsÆm)2, mean ± SE, Fig. 2).
The laboratory experiment consisted in simultaneously A male-biased OSR was detected at the sites with high offering a male and a female P. lividus (test diameter Martasterias glacialis density but not at those with low 40–45 mm) to a M. glacialis. Sea urchins were sexed starfish density. Chi-squared results showed a male- before starting observations by injecting with a syringe skewed OSR at site C2 in July 2004, at site C1 in June about 0.1–0.2 ml of KCl 0.5 m into the sea urchin body 2005 and in both C sites in July 2006. In contrast, a cavity and recording the presence or absence of eggs or balanced equilibrium between sexes was detected at all sperm: females produce conspicuous orange eggs, males times at sites with low M. glacialis density (Table 1).
produce a milky white colour sperm. The injected female The proportion of male sea urchins ranged from 44.5% and male P. lividus, with egg and sperm appearing on the (A2 – June 2005) to 94% (C1 – June 2005) with a top of the aboral side, were simultaneously placed at the mean ± SE of 65.5 ± 5.7%, whereas that of females ran- opposite corners of the experimental aquaria and the ged from 55.5% (A2 – June 2005) to 6.0% (C1 – June M. glacialis attack was recorded. We considered an attack 2005) with a mean ± SE of 35.9 ± 6.0%. Mean OSR successful when we subsequently observed the following reached its maximum at site C1 in July 2006 (0.85 ± 0.05, starfish activity: ‘moving toward prey’, ‘capturing prey’ mean ± SE) and minimum in the same year and month (wrapping its arms around the prey) and ‘digesting prey’(extra-oral digestion with the stomach evaginated between Table 1. Males and females of Paracentrotus lividus (test diameter the spines of the sea urchin). Because this last activity 40–45 mm) recorded at the four studied sites in July 2004, June 2005 lasted up to 20–24 h, feeding observations stopped when and July 2006 and Yates corrected Chi-squared and P-values.
this started. To ensure the independence of data, no M.
glacialis specimens were used more than once (Under- wood 1997). Data from the experiment were analysed usin the Chi-square goodness-of-fit test, considering as null hypothesis the sea stars’ lack preference for either sex We collected a total of 523 sea urchins: 178 males and 185 females at the protected sites (A) and 134 males and 26 females at the harvested ones (C). Average Paracentro- tus lividus density was maximum in July 2006 at site A (1 ± 0.1 individualsÆm)2, mean ± SE) in June 2005 at site 1 (Fig. 2). Average male density was maximum in July 2006 at site A1 (4 ± 0.5 individualsÆm)2, mean ± SE)and minimum in July 2004 at site C *, p < 0.05, ***, p < 0.001; n.s., not significant.
Pooled and separate males and females of Paracentrotus lividus Fig. 2. Pooled and separate male and female Paracentrotus lividus density (mean ± SE) atthe four studied sites in July 2004, June 2005 Marine Ecology (2008) 1–8 ª 2008 The Authors. Journal compilation ª 2008 Blackwell Publishing Ltd Gianguzza, Badalamenti, Gianguzza, Bonaviri & Riggio Fig. 3. OSR (mean ± SE) of Paracentrotus lividus (test diameter 40–50 mm) at the four studied sites in July 2004, June 2005 and July Table 2. Outcome of the ANOVA on the effects of ‘time’ (July 2004 indicated that the female sex was more vulnerable and versus June 2005 versus July 2006), ‘Marthasterias density’ (high ver- that probably eggs were more attractive than sperm to sus low) and ‘site’ (two level) factors on OSR of Paracentrotus lividus M. glacialis, suggesting a different mortality between sexes Many species encounter spatial variation in OSR (Rohr et al. 2005). A male-biased OSR can be primarily caused 1 Different mating behaviour between sexes. For exam- ple, the OSR of the blue swimmer crab Portunus pelagicus (L.) is male-biased during the breeding season because females seem to require a sandy substrate to extrude their Data in bold are discussed in the text.
eggs successfully and attach them to the pleopods (Xiao & Kumar 2004). Similarly, a male-biased OSR wasobserved during the reproductive period in the echinoid Lytechinus variegatus (Lamarck) at shores of Virginia Key (0.36 ± 0.06, mean ± SE) (Fig. 3). ANOVA results revealed significant differences in ‘Marthasterias in Biscayne Bay; sex-specific aggregation and migration density’ only (P = 0.004, Table 1) with greater OSR have been invoked as possible explanations (McCarthy & values at the sites with high M. glacialis density. No statis- tical differences were detected for the factor ‘Time’ investment between the two sexes may also bias the OSR (Bateman 1948). For example in the crab Uca crenulata(Lockington), females typically invest more in each off-spring than males and thus may take longer to recover from producing offspring and will be available for mating In the laboratory experiments, 93.3% of available starfish- less often than mature males (de Rivera 2003).
es made successful attacks. In particular, 20 of 28 Different levels of natural predation on females than M. glacialis attacked P. lividus females significantly more on males (de Rivera 2003). For example, a male-biased often (v2 = 5.1; df = 1; P < 0.02; Fig. 4). Results clearly OSR is very common in the crab U. crenulata as avianpredators typically prefer the easier-to-handle females(Bildstein et al. 1989).
Potential predators of Paracentrotus lividus in Mediter- ranean sublittoral rocky habitats include large crustaceans, asteroids, gastropods and fishes (Sala et al. 1998).
However, only the seabreams Diplodus sargus (L.) and Diplodus vulgaris (E. Geoffroy St.-Hilaire 1817) have been reported to effectively control sea urchin populations (Sala & Zabala 1996; Guidetti 2004).
However, the importance of starfish in regulating Med- iterranean sea urchin populations has been and is still a Fig. 4. Feeding preferences of Marthasterias glacialis (n = 28).
matter of debate. According to Fanelli et al. (1999), Marine Ecology (2008) 1–8 ª 2008 The Authors. Journal compilation ª 2008 Blackwell Publishing Ltd Gianguzza, Badalamenti, Gianguzza, Bonaviri & Riggio Marthasteria glacialis may play a keystone role in regulat- protected sites due to their higher energy content. This ing abnormal populations of P. lividus, whereas field could encourage M. glacialis to prefer females to males: observations made by Guidetti (2004) revealed that this the effort required to handle and digest this particularly starfish preyed only occasionally upon P. lividus and well-defended prey (Guidetti & Mori 2005) would be Arbacia lixula, suggesting that it is probably unable to optimized by choosing the individual with higher energy content. In doing so, M. glacialis may maximize its energy The present study has been conducted at a place where gain and minimize the total energetic cost of foraging.
densities of the above-mentioned seabreams are histori- However, we recognize that detailed field experiments, cally low (La Mesa & Vacchi 1999) and consequently fish using a manipulative approach, are needed to confirm the predation should not exert an effective control on the role of M. glacialis in controlling the OSR of P. lividus.
abundance of sea urchins (Guidetti & Sala 2007; Guidetti Other factors, such as differences in growth or mortality et al. 2008). On the other hand, a high number of between sexes (McPherson 1965), and different reproduc- M. glacialis has been observed predating upon P. lividus, tive behaviour between sexes (i.e. spawning behaviour in particular in the take area C of the MPA (Bonaviri with different timing of gamete release, different seasonal 2007). The natural conditions of the MPA of Ustica Island sex migration and seasonal aggregation), which varies offered an opportunity to improve our knowledge of the above all at different density and habitat conditions (Ber- role of starfish predation in regulating population and nard 1977; Levitan 2004), may also explain the observed OSR of sea urchins, especially when fish predation is low.
The results of the present study provided evidence that This study confirms that regulation of sea urchin den- the male-skewed OSR observed in July 2002 was real and sity is a complex and unpredictable process. In fact, in consistent over time, and it is reasonable to assume that temperate coastal areas (for reviews, see Sala et al. 1998 this could be caused by a sex-selective predation process.
and Pinnegar et al. 2000) several factors are known to Laboratory experiment outcomes clearly showed that control sea urchin population density; among these it is P. lividus females were more vulnerable than males to possible to distinguish both extrinsic factors such as epi- predation by M. glacialis, suggesting a different mortality demic diseases, food availability, complexity of the sub- between sexes during the spawning event. This result strate and availability of refuges, and intrinsic factors could explain the observed P. lividus OSR pattern at the such as predation, recruitment, early mortality, migration MPA of Ustica Island. A male-skewed OSR was found at rates, etc. (Tegner & Dayton 1977; Jangoux 1987; McCl- the sites with a high M. glacialis density, whereas a bal- anahan & Shafir 1990; Sala & Zabala 1996; Lo`pez et al.
anced OSR was observed at sites with a low M. glacialis 1998; Shears & Babcock 2003; Tuya et al. 2005; Pais et al. 2007). As regards the predation factor, based on Several studies have tried to identify which elements our field and laboratory observations, we carefully make prey more vulnerable to starfish predators and hypothesize that starfish predation on P. lividus is a waterborne odours from prey have been proposed as the process that may be important in regulating population most important factor in determining predation (Jangoux & Lawrence 1982; Rochette et al. 1994; Himmelman et al.
To summarise, this preliminary study confirmed the 2005). We showed that the response of M. glacialis to importance of the sex-selective predation process in influ- female P. lividus specimens was strong and this is proba- encing the OSR of a species and in particular provided bly due to different chemical stimuli related to gamete important avenues for future work on the role of M. glacialis in regulating Mediterranean sea urchin popu- Furthermore, laboratory observations provided evi- dence that at Ustica MPA the overall gonadosomaticindex (GSI) of P. lividus (test diameter 40–45 mm) dur- ing the summer spawning period (June 2007) differedwith sex and sea urchin density. GSI was significantly The authors are indebted to Dr T. Vega Fernandez, higher in females at the non-protected sites (C area), Prof. D. Levitan, Dr G. Fanelli, Dr P. Galeotti and two under low density conditions and low intra-specific com- anonymous reviewers for their constructive and challeng- petition for habitat and resources, whereas no differences ing comments, which substantially improved this manu- were found at the protected sites (A area, high sea urchin script; Helen Main for revising the English; the Harbour density). GSI was also higher in the non-protected sites Office of Palermo and the MPA management body of Us- for females, whereas no differences were detected for tica Island for assistance. This study was funded by the males (P. Gianguzza, unpublished data). Thus, higher M.A.T.T.M. (Ministero dell’Ambiente Difesa del Territo- predation on P. lividus females could be expected at non- rio e del Mare) research project ‘Monitoraggio delle Marine Ecology (2008) 1–8 ª 2008 The Authors. Journal compilation ª 2008 Blackwell Publishing Ltd Gianguzza, Badalamenti, Gianguzza, Bonaviri & Riggio popolazioni di Paracentrotus lividus e Arbacia lixula ai fini Frantzis A., Berthon J.F., Maggiore F. (1988) Relation trophi- della tutela della diversita` biologica dell’ Area Marina que entre les oursins Arbacia lixula et Paracentrotus lividus Protetta Isola di Ustica. This paper is dedicated to Mario, (Echinoidea Regularia) et le phytobenthos infralittoral the little baby of P.G. who recently came into the world.
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