View metadata, citation and similar papers at core.ac.uk brought to you by CORE

provided by National Documentation Centre - EKT journals

Mediterranean Marine Science

Vol. 11, 2010

Shift in spallanzanii (Polychaeta, ) spawning period in the Central Mediterranean Sea: a consequence of climate change?

GIANGRANDE A. Department of Biological and Environmental Sciences and Technologies, University of Lecce, Complesso Ecotekne, Via Prov. le Lecce- Monteroni, 73100 Lecce LICCIANO M. Dipartimento di Scienze e Tecnologie Biologiche ed Ambientali, Universitΰ del Salento 73100 (Lecce) MUSCO L. Dipartimento di Scienze e Tecnologie Biologiche ed Ambientali, Universitΰ del Salento 73100 (Lecce) STABILI L. Dipartimento di Scienze e Tecnologie Biologiche ed Ambientali, Università del Salento 73100 (Lecce) https://doi.org/10.12681/mms.86

Copyright © 2010

To cite this article:

GIANGRANDE, A., LICCIANO, M., MUSCO, L., & STABILI, L. (2010). Shift in Sabella spallanzanii (Polychaeta, Sabellidae) spawning period in the Central Mediterranean Sea: a consequence of climate change?. Mediterranean Marine Science, 11(2), 373-380. doi:https://doi.org/10.12681/mms.86

http://epublishing.ekt.gr | e-Publisher: EKT | Downloaded at 23/03/2020 05:21:22 | Mediterranean Marine Science Short Communication Indexed in WoS (Web of Science, ISI Thomson) The journal is available on line at http://www.medit-mar-sc.net

Shift in Sabella spallanzanii (Polychaeta, Sabellidae) spawning period in the Central Mediterranean Sea: a consequence of climate change?

A. GIANGRANDE1, M. LICCIANO1, L. MUSCO1 and L. STABILI1-2

1 Dipartimento di Scienze e Tecnologie Biologiche ed Ambientali, Università del Salento 73100 (Lecce) Italy 2 Istituto per l’Ambiente Marino Costiero, Sezione di Taranto, CNR, Italy

Corresponding author: [email protected]

Received: 28 July 2010; Accepted: 14 September 2010; Published on line: 5 November 2010

Abstract

Sabella spallanzanii is a large tubicolous common in the Mediterranean fouling assemblages, where it plays an important role in structuring the community. Its reproductive biology is well known and had has been investigated since 1993. During the past few years, a shift in its reproductive period has been observed. In 2008 the presence of ripe eggs in the females was observed at least two months in advance compared to the past. This was confirmed during the 2009 when spawning and fertilization were observed three months in advance compared to the past. Pos- sible causes of this shift may be related to the increasing surface temperature in the Central Mediter- ranean Sea.

Keywords: ; Reproduction; Sea temperature; Structuring ; Fouling communities.

Introduction found in the southernmost parts of the basin now being found in more northerly In recent years, numerous studies have locations (GRUBELIC et al., 2004; focused on the potential effects of global MIKAC & MUSCO, 2010). Comparing warming upon organisms and the interac- present data on hydroid distribution with tions between global warming and changes that of about 20 years ago, PUCE et al. in life cycles, physiology and behaviour for (2009) found that species have reacted to a wide range of organisms (PARMESAN increases in water temperature by modify- & YOHE, 2003). ing their seasonal patterns. Species that The change in the fauna of the were active only in the summer are now Mediterranean Sea in response to global present throughout the year, and norther- warming is becoming increasingly evident ly species are now occupying deeper and (BIANCHI, 2007), with species that were colder layers in the water column. Com-

Medit. Mar. Sci., 11/2, 2010, 373-379 373

http://epublishing.ekt.gr | e-Publisher: EKT | Downloaded at 23/03/2020 05:21:22 | munities are therefore changing with According to the most recent study regard to their composition, depth of (GIANGRANDE et al., 2000), S. spallan- occurrence and timing of reproduction in zanii reproduces once a year in winter, and response to increasing water temperature. in the Mediterranean the spawning occurs In the Mediterranean most studies on from January to February. Eggs reach up the consequences of climate change have to 250 Ìm and give rise to a lecithotrophic focused on the distribution patterns of the development with larvae spending up to 15 recently introduced thermophilic alien days in the water column. Gametogenesis species (OCCHIPINTI-AMBROGI & occurs from July to January and appears SAVINI, 2003; ZENETOS et al., 2005; synchronized within populations so that 2008). Few studies have dealt with the population dynamics were easily pre- impact of the increasing water tempera- dictable, with massive recruitment events ture on the biology and ecology of occurring regularly each year. The species autochthonous species (eg. PUCE et al., grows rapidly, reaching about 10 cm in 2009; CONVERSI et al., 2009; MAZARIS body length during the first year, and can et al., 2008), and on the ecological conse- live for more than 5 years, reaching up to quences that changes in the time of repro- 40 cm in length (GIANGRANDE & duction of some species can have on the PETRAROLI, 1994). The species is high- entire community. Response by individual ly efficient in removing POM, DOM and species to climate change may disrupt their from the water column interactions with others. Due to the differ- (LICCIANO et al., 2005; STABILI et al., ent response or susceptibility to change, 2006; CAVALLO et al., 2007). This, cou- the outcome of their interactions may be pled with the high density reached, led to altered, as long term data on both terres- hypothesise that this species plays an trial and marine organisms indicate important role in controlling bacterial (WALTHER et al., 2002). diversity (LICCIANO et al., 2007). We report observations on the shift in The species has an Atlantic-Mediter- reproduction period of a species playing ranean distribution, although about 15 an important functional role within years ago, it was introduced into West Mediterranean fouling communities, as Australia and subsequently into eastern well as a role as a structuring taxon. Australia where it became a pest species, heavily impacting on marine ecosystems Sabella spallanzanii (Gmelin, 1791): biol- with serious coastal economic conse- ogy and ecological role quences (CLAPIN & EVANS, 1995). Indeed, it has been estimated that the fil- Sabella spallanzanii is a large tubicolous tering activity of S. spallanzanii is of the filter feeder polychaete common within same order of magnitude as that of the Mediterranean fouling communities, both native seagrass community it replaced in pioneering and in the late stages of these (LEMMENS et al., 1996). Manipulative assemblages. The species colonizes every experiments conducted in the area where artificial substrate in eutrophic environ- the species was introduced, indicate that at ments where it can reach a density of about a high density, adults of S. spallanzanii are 800 specimens per square meter able to alter the structure of benthic com- (GIANGRANDE et al., 2005). munities (HOLLOWAY & KEOUGH

374 Medit. Mar. Sci., 11/2, 2010, 373-379

http://epublishing.ekt.gr | e-Publisher: EKT | Downloaded at 23/03/2020 05:21:22 | 2002a, b), with a selective action on the year. During 2006 and 2007 the complete settlement of other invertebrates. This absence of settled juveniles on collectors effect is related to its particular tree-like led us to reinvestigate on the reproductive morphology with the fan on the top of a cycle of this species by egg measurements. long slender tube creating a canopy of During 2008 we observed females carrying feeding fans, interfering with the settle- ripe eggs ready to be spawned, in ment of other invertebrates. advance early when compared to the pre- At present we are investigating the vious investigated period: eggs from role that S. spallanzanii can exert in the females collected in early November 2008 Mediterranean area, in the biotope where measured 225 ± 24 Ìm vs an average of it normally is a dominant taxon. Prelimi- 151 ± 45 Ìm observed during November nary observations suggest that this poly- 2000. A similar advance in egg maturation chaete can exert a role in structuring the was found during late October 2009, when community also during the early stage of individuals spawned in the laboratory and colonization when specimens are still too 100% of the fertilization occurred. This small to show a canopy effect (unpublished confirmed an advance in the spawning data). period of at least 3 months if compared to the past. Sabella spallanzanii: present observed changes Discussion

We have been studying this species in In the past, spawning of S. spallanzanii the Mediterranean since 1993. Initially we occurred when seawater temperatures investigated its life cycle (GIANGRANDE ranged from 11 to 14Æ C both in the & PETRAROLI, 1993; GIANGRANDE Mediterranean area (February) (GIAN- et al., 2000) also in the light of its employ- GRANDE et al., 2000) and in Port Phillip ment as a bioremediator of aquaculture Bay in Australia (August) (CURRIE et al., waste (GIANGRANDE et al., 2005). In a 2000), leading to the hypothesise that the pilot study the species was reared in poly- reproductive cycle was consistent with culture with Mytilus galloprovincialis, col- either temperature or photoperiod con- lecting juveniles using the same strategy trolling gametogenesis. However, accord- utilized for (CECERE et al., 2006; ing to CURRIE et al. (2000) the relative PIERRI et al., 2006). Recruitment of S. importance of these two physical parame- spallanzanii was easily observed over sev- ters in controlling the gametogenic cycle of eral years from 2001 to 2005. Although S. spallanzanii was difficult to determine. very variable in abundance from year to The present observed temporal shift in year, young settlers (few cm in length, cor- egg maturation (about three months in responding to about 1 month of life) were advance) suggests that temperature is the usually present in early March on collec- main factor in controlling reproduction of tors previously placed in October or this species. The change observed in the S. November. At the same time, the exami- spallanzanii life cycle could be interpreted nation of germinal products always con- as a very short physiological response to firmed the previous observed trend with increasing water temperature, i.e. the high spawning occurring at the beginning of the surface temperature recorded during the

Medit. Mar. Sci., 11/2, 2010, 373-379 375

http://epublishing.ekt.gr | e-Publisher: EKT | Downloaded at 23/03/2020 05:21:22 | past few years from July to October could the subsequent stages of the species’ life have produced the reduction of the game- cycle. togenesis period, leading to an earlier Each species may have its own pecu- spawning. In other polychaete species, the liar response to the environmental changes timing of gametogenesis is proved to be and ecological consequences can be higher controlled by a gonadotrophic hormone greater when species playing an important promoting egg protein synthesis in devel- role in their community are involved. Con- oping oocytes, which in turn is controlled sidering that S. spallanzanii is a structuring by environmental cues, particularly tem- taxon, the changes in its reproduction peri- perature, and which may be affected by cli- od might influence the entire community, mate change (LAWRENCE, 1996). with the possible disruption of the peculiar In the central Mediterranean Sea, tem- equilibrium that fouling communities have perature changes occurring over the last reached over an evolutionary time. The decades have led to progressively warmer next step will be to investigate the ecologi- summers, while winters have remained cal and economical consequences of the cold. In fact, while Mediterranean sea sur- shifted spawning period of this structuring face temperature (SST) has increased by taxon. 0.5Æ C between 1970 and 2005, this increase was not uniform over the year, Acknowledgments winter temperatures appear to shows no long-term change, while the spring, sum- This research was financed by the Pro- mer, and fall temperatures have increased ject ACTIBIOMAR granted by the Apulia by 0.6, 1.0, and 1.1Æ C, respectively Region and carried out within the (CONVERSI et al., 2009). Moreover, MARBEF Network of Excellence which is according to LUTERBACHER et al. funded in the Community’s Sixth Frame- (2007) autumn 2006 and winter 2007 have work Programme (Contract no. GOCE- been the warmest of the last 500 years. CT-2003-505446), the E.U. Integrated Interestingly, a similar shift in repro- Project SESAME and the CMCC (Centro duction is likely to also affect the co-occur- Euro- Mediterraneo per i Cambiamenti ring M. galloprovincialis, (PRATO, Climatici). personal communication), an important commercial species having similar ecologi- References cal and biological features of to S. spallan- zanii, including the spawning period. The BIANCHI, N.C., 2007. Biodiversity issues observed shifts in reproduction period for the forthcoming tropical Mediter- must be more deeper investigated, at a ranean Sea. Hydrobiologia, 580 (1): 7-21. range of sites within the Mediterranean CAVALLO A., PUSCEDDU A., DANO- Sea, to establish if this phenomenon is VARO R. & GIANGRANDE, A., widespread. 2007. Particulate organic matter uptake However, if the settlement of S. spal- rates of two benthic filter-feeders lanzanii is now occurring in October when (Sabella spallanzanii and Branchiomma the SST is higher than in February, which luctuosum) candidates for the clarifica- is the normal settlement period of the tion of aquaculture wastewaters. Marine worm, we suggest that this may impact on Pollution Bulletin, 54 (5): 622-625.

376 Medit. Mar. Sci., 11/2, 2010, 373-379

http://epublishing.ekt.gr | e-Publisher: EKT | Downloaded at 23/03/2020 05:21:22 | CECERE, E., PETROCELLI, A., chaeta, Sabellidae) from Mediter- SARACINO, O.D., ALABISO, G., ranean Sea. Marine Biology, 136 (5): CAVALLO, R.A., STABILI, L., 847-861. GIANGRANDE, A., PORTACCI, G. GIANGRANDE, A., CAVALLO, A., & FANELLI, G., 2006. Relazione LICCIANO, M., MOLA, E., PIERRI finale Progetto "PO.IN.T. Attività di C. & TRIANNI, L., 2005. Utilization Policoltura Integrata alla Mitilicoltura: of the filter feeder Sabella spallanzanii Progetto Pilota nei Mari di Taranto" Gmelin (Sabellidae) as bioremediator (POR Puglia 2000-2006 della Regione in aquaculture. Aquaculture Interna- Puglia) (2006) Asse IV – Sistemi locali tional, 13 (1-2): 129-136. di Sviluppo, Misura 4.13 – Interventi di GRUBELIC, I., ANTOLIC, B., DESPA- Supporto alla competitività del Sis- LATOVIC, M., GRBEC, B. & tema Pesca – Sottomisura 4.13.E. PAKLAR, G.B., 2004. Effect of climat- CLAPIN, G. & EVANS, D., 1995. The sta- ic fluctuations on the distribution of tus of the introduced marine fanworm warm-water coral Astroides calycularis Sabella spallanzanii in Western Aus- in the Adriatic Sea: new records and tralia: a preliminary investigation. review. Journal of Marine Biological CSIRO Technical Report, No. 2. Divi- Association UK, 84 (3): 599-602. sion of Fisheries, CSIRO, Hobart. HOLLOWAY, M.G. & KEOUGH, M.J., CONVERSI, A., PELUSO, T., FONDA- 2002a. An introduced Polychaete UMANI, S., 2009. Gulf of Trieste: A affects recruitment and larval abun- changing ecosystem. Journal of Geo- dance of sessile invertebrates. Ecologi- physical Research, 114 (C03S90): 1-10. cal Applications, 12 (6): 1803-1823. CURRIE, D.R, MCARTHUR, M.A & HOLLOWAY, M.G. & KEOUGH, M.J., COHEN, B.F., 2000. Reproduction 2002b. Effects of an introduced poly- and distribution of the invasive Euro- chaete, Sabella spallanzanii, on the pean fanworm Sabella spallanzanii development of epifaunal assemblages. (Polychaeta: Sabellidae) in Port Phillip Marine Ecology Progress Series, 236: Bay, Victoria, Australia. Marine Biolo- 137-154. gy, 136 (4): 645-656. LAWRENCE, A.J., 1996. Environmental GIANGRANDE, A. & PETRAROLI, P., and endocrine control of reproduction 1994. Observations on reproduction in two species of polychaete: potential and growth of Sabella spallanzanii bio-indicators for global climate (Polychaeta Sabellidae) in the change. Journal of Marine Biological Mediterranean Sea. p.51-56. In: Dau- Association UK, 76 (1): 247-250. vin, J.C., Laubier, I., & Reish, D.J. LEMMENS, J.W.T., CLAPIN, G., (Eds). Actes de la 4ème Conférence LAVERY, P. & CARY, J., 1996. Fil- Internationale des Polychètes. Mémoires tering capacity of seagrass medows and du Muséum National d'Histoire other habitats of Cockburn Sound, Naturelle, vol. 162. Western Australia. Marine Ecology GIANGRANDE, A., LICCIANO, M., Progress Series, 143: 187-200. PAGLIARA, P. & GAMBI, M., 2000. LICCIANO, M., STABILI, L. & Gametogenesis and larval develop- GIANGRANDE, A., 2005. Clearance ment in Sabella spallanzanii (Poly- rates of Sabella spallanzanii and Bran-

Medit. Mar. Sci., 11/2, 2010, 373-379 377

http://epublishing.ekt.gr | e-Publisher: EKT | Downloaded at 23/03/2020 05:21:22 | chiomma luctuosum (Annelida: Poly- globally coherent fingerprint of climate chaeta) on a pure culture of algi- change impacts across nature systems. nolyticus. Water Research, 39 (18): Nature, 421: 37-42. 4375-4384. PIERRI, C., FANELLI, G. & GIAN- LICCIANO, M., TERLIZZI, A., GRANDE, A., 2006. Experimental co- GIANGRANDE, A., CAVALLO, culture of low food-chain organisms, R.A. & STABILI, L., 2007. Filter-feed- Sabella spallanzanii (Polychaeta, Sabel- er macroinvertebrates as key players in lidae) and Cladophora prolifera culturable bacteria biodiversity con- (Chlorophyta, Cladophorales), in trol: a case of study with Sabella spal- Porto Cesareo area (Mediterranean lanzanii (Polychaeta: Sabellidae). Sea). Aquaculture Research, 37 (10): Marine Environmental Research, 64 (4): 966-974. 504-513. PUCE, S., BAVESTRELLO, G., DI LUTERBACHER J., LINIGER, M.A., CAMILLO, C.G. & BOERO, F., 2009. MENZEL, A., ESTRELLA, N., Long-term changes in hydroid DELLA-MARTA, P.M., PFISTER, (Cnidaria, Hydrozoa) assemblages: C., RUTISHAUSER, T. & XOPLA- effect of Mediterranean warming? KI, E., 2007. Exceptional European Marine Ecology, 30 (3): 313-326. warmth of autumn 2006 and winter STABILI, L., LICCIANO, M., 2007: Historical context, the underly- GIANGRANDE, A., FANELLI, G. & ing dynamics, and its phenological CAVALLO, R.A., 2006. Sabella spal- impacts. Geophysical Research Letters, lanzanii filter-feeding on bacterial 34 (L12704): 1-6. community: Ecological implications MAZARIS, A.D., KALLIMANIS, A.S., and applications. Marine Environmen- SGARDELIS, S.P. & PANTIS, J.D., tal Research, 61 (1): 74-92. 2008. Do long-term changes in sea sur- WALTHER, G.R., POST, E., CONVEY, face temperature at the breeding areas P., MENZEL, A., PARMESAN, C., affect the breeding dates and repro- BEEBEE, T.J.C., FROMENTIN, duction performance of Mediter- J.M., HOEGH-GULDBERG, O. & ranean loggerhead turtles? Implica- BAIRLEIN, F., 2002. Ecological tions for climate change. Journal of responses to recent climate change. Experimental Marine Biology & Ecology, Nature, 416: 389-395. 367 (2): 219-226. ZENETOS, A., INAR, M.E., PAN- MIKAC, B. & MUSCO, L., 2010. Faunal CUCCI-PAPADOPOULOU, M.A., and biogeographic analysis of Syllidae HARMELIN, J.G., FURNARI, G., (Polychaeta) from Rovinj (Croatia, ANDALORO, F., BELLO, N., northern Adriatic Sea). Scientia Mari- STREFTARIS, N. & ZIBROWIUS, na, 74 (2): 353-370. H., 2005. Annotated list of marine OCCHIPINTI-AMBROGI, A. & alien species in the Mediterranean SAVINI, D., 2003. Biological invasions with records of the worst invasive as a component of global change in species. Mediterranean Marine Science, stressed marine ecosystems. Marine 6 (2): 63-118. Pollution Bulletin, 46 (5): 542-551. ZENETOS, A., MER C, E., VERLAQUE, PARMESAN, C. & YOHE, G., 2003. A M., GALLI, P., BOUDOURESQUE,

378 Medit. Mar. Sci., 11/2, 2010, 373-379

http://epublishing.ekt.gr | e-Publisher: EKT | Downloaded at 23/03/2020 05:21:22 | C.F., GIANGRANDE, A., CINAR, ranean with special emphasis on M.E. & BILECENOGLU, M., 2008. Foraminifera and Parasites. Mediter- Additions to the annotated list of ranean Marine Science, 9 (1): 119-165. marine alien biota in the Mediter-

Medit. Mar. Sci., 11/2, 2010, 373-379 379

http://epublishing.ekt.gr | e-Publisher: EKT | Downloaded at 23/03/2020 05:21:22 |

Powered by TCPDF (www.tcpdf.org)