Long-term changes in hydroid (Cnidaria, Hydrozoa) assemblages: effect of Mediterranean warming

ORIGINAL ARTICLE

Long-term changes in hydroid (Cnidaria, Hydrozoa)assemblages: effect of Mediterranean warming?Stefania Puce1, Giorgio Bavestrello1, Cristina Gioia Di Camillo1 & Ferdinando Boero2

1 DiSMar, Universita Politecnica delle Marche, Ancona, Italy

2 DiSTeBA, Universita del Salento, Lecce, Italy

Problem

The Mediterranean Sea lies within the warm-temperatemarine region ranging from the northwestern coast ofAfrica to the entrance of the English Channel (Briggs1974; Vermeij 1980). The most typical Mediterraneanbiota lives in the Tyrrhenian Sea, the central sector of theWestern Mediterranean, with the most endemic species,Atlanto-Mediterranean elements, and a fairly high per-centage of species with subtropical affinities (Bianchi &Morri 1993). North of the Tyrrhenian Sea, in the LigurianSea, waters are colder and the subtropical element ismarkedly lower in importance, whereas species fromcold-temperate waters are present, giving the Ligurian Seaa boreal affinity (Rossi 1969; Albertelli et al. 1981; Catta-neo-Vietti et al. 1988). Southern, warm-water species havebeen sparsely reported from the Ligurian Sea, but theirsurvival in cold years is unlikely, explaining the rarity of

records. In a few cases warm-water species have succeededin establishing adult pseudopopulations unable to repro-duce (Bianchi & Morri 1994; Bianchi 1997). Nevertheless,Bianchi (1997) hypothesized that present sea-water warm-ing is allowing former sterile pseudopopulations to repro-duce in the Ligurian Sea, thus providing independencefrom the larval supply by the Tyrrhenian Current andallowing the establishment of stable populations of warm-water species. For example, Sara et al. (2005) documentedthe mating behaviour of the warm-water labrid fishThalassoma pavo in this area.

Substantial evidence demonstrates that the climate ischanging and that the average surface temperature of thesea is increasing (Bianchi 1997; Marullo & Guarracino2003). Grainger (1992) predicted that this global warmingwould probably make southern species extend theirrange northward. This prediction proved correct in theMediterranean Sea, where there has recently been an

Keywords

Benthic assemblages; Cnidaria; global

warming; Hydrozoa; marine hydroids;

Mediterranean Sea.

Correspondence

Dr Stefania Puce, DiSMar, Universita

Politecnica delle Marche, Via Brecce Bianche,

60131 Ancona, Italy.

E-mail: [email protected]

Accepted: 29 December 2008

doi:10.1111/j.1439-0485.2009.00283.x

Abstract

Marine hydroids are markedly seasonal in temperate seas, being extremely sen-sitive to climatic changes disrupting seasonal patterns. Modifications in thecomposition, seasonality, bathymetric distribution and reproductive period ofhydroid assemblages are useful to evaluate the influence of global warming onthe marine ecosystem. The hydroids on the rocky cliff of the Portofino Prom-ontory (Ligurian Sea, Italy) were carefully studied between 1976 and 1983; inparticular, in 1980 the study was carried out along a vertical transect. The hy-droids were sampled again throughout 2004, with the same techniques andalong the same transect. Species diversity decreased slightly in the 2004 survey.Some species present in 1980 had disappeared in 2004, but other species withsouthern affinity, never recorded from the area, became abundant in 2004.Species that were present in summer in the first period were also present inwinter in the second one. Furthermore, shallow summer species widened theirbathymetric distribution, reaching deeper levels. These data strongly suggestthat the Portofino hydroid assemblage reacted to the water temperatureincrease found in the Mediterranean Sea.

Marine Ecology. ISSN 0173-9565

Marine Ecology (2009) 1–14 ª 2009 Blackwell Verlag GmbH 1

increase in warm-water pelagic fish and benthic organ-isms in the northern sectors, such as the Ligurian Sea(Bianchi & Morri 1993, 1994, 2003, 2004; Francour et al.1994; Astraldi et al. 1995; Bianchi 1997, 2007). Bianchi &Morri (1993, 1994) provided a list of 20 southern epiben-thic species in the Ligurian Sea, including algae, sponges,cnidarians, molluscs, crustaceans, echinoderms and fishes,suggesting that the occurrence of warm-water species islinked to year-to-year climatic variability, rather than tothe establishment of a permanent ‘thermophilic oasis’.Summer temperatures are particularly high in shallowwaters, a surface thermocline separating them from colderdeeper waters. Most sessile species of cold water affinitycannot stand high summer temperatures: seasonal onessimply become inactive in the summer, often remainingactive below the thermocline, whereas perennial speciescan live only under the thermocline. The deepening ofthe surface thermocline therefore clearly affects the pres-ence and distribution of cold-water species (Boero et al.2003). Mass mortalities of sponges and gorgonians in theLigurian Sea are most probably due to this type of impact(Cerrano et al. 2000; Garrabou et al. 2001).Southward (1995) identified the lack of ‘historical’

long-term data as the major problem in relating fluctua-tions of marine communities to climate changes. Fisherystatistics often provide the longest available time series ofbiological data (Glantz 1992; Laevastu 1993). Long-termseries are also available both for plankton (e.g. Robinson& Hunt 1986; Maddock et al. 1989; McGovan 1990; Cata-letto et al. 1995; Degobbis et al. 1995; Molinero et al.2008) and the benthos (e.g. Ambrogi et al. 1994; Shillaber1995; Fromentin et al. 1997) but datasets are scarce (Cab-ioch et al. 1983; Warwick & Bayne 1993). In the case ofthe benthos, most time series have been studied only forthe last few decades (Heip et al. 1987; Keegan 1991),although Blacker (1957) was already considering benthicorganisms as indicators of climatic change.The hard-bottom macrobenthos is made up of both

slow- and fast-growing organisms and its compositionvaries mainly in relation to substrate competition. Hy-droids are an important macrobenthic group that under-goes sharp seasonal cycles (Boero 1984; Boero & Fresi1986; Calder 1990; Gili & Hughes 1995; Bavestrello et al.2006; Di Camillo et al. 2008) especially in the Mediterra-nean, a markedly seasonal sea whose summer and winterfaunas have different zoogeographical affinities and eco-logical requirements. The great differences in the hydroidspecies found at a given place according to the seasonbecome clear when considering that polyps can becomeencysted as resting hydrorhizae under adverse conditions(Boero et al. 1986, 2003). The available data suggest thata mosaic of physical factors, biotic interactions, and inter-nal clues triggers the hydroid cyclic behaviour (Brock

1974; Boero & Fresi 1986; Arillo et al. 1989; Bavestrello &Arillo 1992; Bavestrello et al. 2006), water temperatureprobably being strongly involved.

In the period 1976–1983 the most detailed study on aMediterranean hydroid assemblage was carried out on therocky cliff of the Portofino Promontory (Ligurian Sea,Italy) (Boero & Fresi 1986). In particular, during 1980,the hydroids were collected monthly along a vertical tran-sect from 0 to 20 m subdivided into five depth ranges: 83species were identified and their zonation pattern and theseasonal variations in their abundance and reproductiveactivity were reported (Table 1). The population dynam-ics of one of the most important hydroids in the area,Eudendrium glomeratum, were studied throughout 1983,helping to unravel the mechanisms of hydroid appearanceand disappearance according to the season (Boero et al.1986).

The above-mentioned bulk of records represent an his-torical database on the hydroid biodiversity of the Liguri-an Sea; the current new work aims at studying the samehydroid assemblage after more than two decades (2004),following identical sampling methods, to reveal possiblechanges in species composition, zonation and seasonality.

Seven years of observation (1976–1983) revealed a quiteconstant pattern in the seasonal dynamics of hydroidpopulations as most species are probably long-lived, asdemonstrated for Eudendrium glomeratum, even if theirpatterns of presence do not suggest so. A colony, in fact,remains viable for many years due to the permanence ofhydrorhizae during adverse seasons.

Therefore this study was aimed at evaluating whetherthe presence, seasonality and vertical distribution ofwarm- and cold-affinity hydroids changed according tothe parallel documented warming of the Ligurian Sea.

Material and Methods

The sampling techniques were identical to those used byBoero & Fresi (1986). Samplings were conductedmonthly, throughout 2004, by SCUBA diving on a rockycliff on the northern side of the Portofino Promontory,situated in the centre of the Ligurian Sea (NW Mediterra-nean Sea, Italy) (Fig. 1). The rocky cliff, in the localitynamed Aurora, is almost vertical to a depth of 10 m andthen begins to slope with a number of large steps. Thetransect, marked by an iron chain, was subdivided intofive depth zones (0–0.5, 0.6–5, 5.1–10, 10.1–15 and 15.1–20 m). Along the transect, hydroids were collectedmonthly by visually oriented sampling. Boero & Fresi(1986) first studied a series of standard samplings from20 · 20 quadrats carried out in November 1976, but itbecame immediately apparent that this technique did notlead to an efficient representation of species diversity and

Long-term changes in hydroid assemblages Puce, Bavestrello, Di Camillo & Boero

2 Marine Ecology (2009) 1–14 ª 2009 Blackwell Verlag GmbH

that, furthermore, species composition changed almostmonthly, especially for reproductive periods of the vari-ous species. Boero & Fresi (1986) compared the yield oftraditional sampling with that of visually oriented sam-pling, showing that the two techniques were almostequivalent in terms of species yields but that visual sam-ples were advantageous in terms of processing. Thenomenclature used here is based on Bouillon et al. (2004,2006).

Temperature regime in the studied area

Unfortunately, long-term temperature measurements arenot available for the Ligurian Sea. The only records referto air temperatures in the area of Genoa, close to the Por-tofino Promontory. To obtain a general scenario of thetemperature variation in the studied area in the last50 years we correlated the average annual surface watertemperatures available for Genoa harbour from 1999 to2006 with the air temperature obtained in the same placefor the same period (n = 9; r = 0.92). Using this correla-tion we inferred the annual sea surface temperature from1960 to 2006 and we plotted the thermal anomalies of eachyear on the average value obtained for the entire series(Fig. 2). Of the 17 years from 1960 to 1980, 12 show

negative thermal anomalies until 0.7 !C. The situationremains similar until 1988 when a period of 3 yearsshowed temperatures about 0.5 !C higher than the meanand from 1997 to 2004 with a long series of very warmyears.

These data agree with the trend in the average watertemperatures of the Tyrrhenian Sea showing, from 1985to 2003, an increase of about 0.5 !C (Marullo & Guarra-cino 2003). During this period some particularly intensethermal anomalies were recorded in the late summers,particularly in 1999 and 2003 (Bavestrello et al. 2000;Marullo & Guarracino 2003; Schiaparelli et al. 2007),affecting the water column almost to 30 m depth, withtemperatures 2–3 !C higher than normal.

Results

The total number of hydroid species recorded in thearea of the Portofino Promontory is 119: 98 specieswere recorded during both the studies carried out alongthe Aurora transect during 1980 and 2004 and thisbulk of data represents the basis of the followinganalysis (Table 1). Moreover, examination of the litera-ture on Ligurian Sea hydroids and other unpublishedrecords has revealed the existence of a further 21 spe-cies on the Portofino Promontory and surroundingcoasts (Table 2).

The comparison between the data obtained during1980 and 2004 showed that the number of species wasslightly lower (71) in 2004 than in 1980 (82) (Table 1).The number of anthomedusan species is identical (30),whereas Leptomedusae are less numerous (41 species in2004 versus 52 in 1980) (Table 1).

Species composition, furthermore, is noticeably differ-ent in the two periods studied: 26 species collected inthe reference period had disappeared (10 Anthomedusae

44°18’.32 N

09°10’.25 E

0 1 2 kmAurora

50-m

20 m

Fig. 1. Map of Portofino Promontory in the centre of the Ligurian

Sea.

Fig. 2. Thermal anomalies in the estimated average annual tempera-

tures of the surface sea water on the average temperature of the last

50 years.

Puce, Bavestrello, Di Camillo & Boero Long-term changes in hydroid assemblages

Marine Ecology (2009) 1–14 ª 2009 Blackwell Verlag GmbH 3

Table 1. List of the species collected along the Aurora transect of Portofino during 1980 and 2004.

Depth ranges: 1 = 0–0.5 m; 2 = 0.5–5; 3 = 5–10 m; 4 = 10–15 m; 5 = 15–20 m; r, reproduction. The grey zones represent the period during

which the species is present and the two different shades of grey refer to the two different years of sampling. Names in parentheses were used

by Boero & Fresi (1986) and are not applicable to the studied material due to misidentification or to nomenclatural update.

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4 Marine Ecology (2009) 1–14 ª 2009 Blackwell Verlag GmbH

Table 1. (Continued ).

Puce, Bavestrello, Di Camillo & Boero Long-term changes in hydroid assemblages

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Table 1. (Continued ).

Long-term changes in hydroid assemblages Puce, Bavestrello, Di Camillo & Boero

6 Marine Ecology (2009) 1–14 ª 2009 Blackwell Verlag GmbH

Table 1. (Continued ).

Puce, Bavestrello, Di Camillo & Boero Long-term changes in hydroid assemblages

Marine Ecology (2009) 1–14 ª 2009 Blackwell Verlag GmbH 7

and 16 Leptomedusae), and 16 species are new forthe considered zone (10 Anthomedusae and 6Leptomedusae). In particular, some Corynidae andAglaopheniidae, very abundant in shallow water during1980, had disappeared in 2004 (Dipurena halterata,Dipurena ophiogaster) or were drastically reduced(Coryne muscoides, Aglaophenia kirchenpaueri, Aglaophe-nia tubiformis). Conversely, in 2004 several neverrecorded species were collected (for instance Eudendri-um moulouyensis, Pennaria disticha and Clytia gracilis)or were reported as more abundant (Sertularella polyzo-nias and Halecium lankesteri).

The number of species present on the cliff during 2004varied seasonally. Values were high during winter (Janu-ary–April), with a maximum in February (46 species),then gradually decreased in May (37 species), reachingthe minimum in August (26 species), to increase again inautumn (Fig. 3A). The seasonal trend in 1980 overlapsthat of 2004 from January to May, whereas from June toDecember species numbers are higher than in 2004. InNovember 2004, the species number is half that recordedin the reference period (Fig. 3A).

The numbers of anthomedusan and leptomedusan spe-cies identified in 2004 and in 1980 along the annual cycle

Table 2. Species collected along the Portofino Promontory but not on the studied rocky wall.

species seasonality depth (m) substrates references

Anthomedusae

Bougainvilliidae

Dicoryne conybeari 10–25 gastropod shells Bavestrello (1985)

Corynidae

Coryne eximia October–March 0–25 iron chains Puce et al. (2003)

Cladonema sp. (as Sarsia sp.) summer 5 sponges Boero & Fresi (1986)

Cytaeididae

Cytaeis propagulata March–May 2–10 gastropod shells Bavestrello (1987)

Eudendriidae

Eudendrium simplex

(as Eudendrium motzkossowskae)

always present 0–1 Posidonia leaves Boero & Fresi (1986)

Hydractiniidae

Hydractinia areolata Sara et al. (1978)

Hydractinia exigua Sara et al. (1978)

Oceanidae

Corydendrium parasiticum summer 10–20 rocks, artificial substrate unpublished

Pandeidae

Neoturris pileata January–March 15–25 gastropod shells Bavestrello (1985)

Paracorynidae

Paracoryne huvei winter 0–1 rocks, mussels Boero & Fresi (1986)

Ptilocodiidae

Hydrichthella sp. summer gorgonian unpublished

Leptomedusae

Aglaopheniidae

Aglaophenia harpago always present 2–30 Posidonia leaves Boero & Fresi (1986)

Lytocarpia myriophillum July 40 and more mud Boero & Fresi (1986)

Campanulinidae

Cuspidella sp. April 25 concretions unpublished

Halopterididae

Antennella siliquosa Rossi (1961)

Halopteris liechtensternii Rossi (1961)

Hebellidae

Hebella scandens Sara et al. (1978)

Lafoeidae

Acryptolaria conferta Rossi (1949–50)

Plumulariidae

Nemertesia antennina July 40 and more mud, stones Boero & Fresi (1986)

Phialellidae

Phialella quadrata winter 100–120 Pteria hirundo Bavestrello (1983–84)

Tiarannidae

Modeeria rotunda winter 100–120 m Pteria hirundo Bavestrello (1983–84)

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8 Marine Ecology (2009) 1–14 ª 2009 Blackwell Verlag GmbH

follow a similar trend to that of the total hydroid assem-blage: from December to May the trends in both groupsoverlap those of 1980, with a strong reduction in speciesnumber in summer and autumn 2004. Unlike Anthome-dusae, the decrease in the leptomedusan species begins inJuly (Fig. 3B, C).

The trends in fertile species percentages are similar inboth periods. In 2004, the reproductive activity is lower,particularly during the summer (Fig. 4).

Considering the period of presence of the species, thesituation in 1980 was characterised by two main catego-ries: species present only in 1 month (17%) and speciespresent throughout the year (26%). During 2004, the per-centage of species present during 12 months is stronglyreduced (10%), whereas that of species recorded only in1 month increased (21%) (Fig. 5).

Past and recent seasonal distributions were markedlydifferent: 40% of the species recorded only duringspring–summer in 1980 had disappeared in 2004, 40% ofthem were active during autumn–winter, few showed awidened activity period and none remained active onlyduring the spring–summer period (Fig. 6). Conversely,more than 70% of the autumn–winter species found in1980 had disappeared, whereas about 12% had anunmodified or widened activity period and none wereactive during the spring–summer period (Fig. 6). Of thespecies recorded all year round during 1980, 54% werealso present throughout 2004, whereas about 25% ofthem had disappeared, 18% were active during the coldperiod and 4% during the summer (Fig. 7).

The bathymetric distribution analysis reveals anincrease in the number of species recorded at each depth

A

B

C

Fig. 3. Number of species along the annual cycle during 1980 (dot-

ted line) and 2004 (continuous line). (A) Total species, (B) Anthomedu-

sae, (C) Leptomedusae.

Fig. 4. Percentage of fertile species along the annual cycle during

1980 (dotted line) and 2004 (continuous line).

Puce, Bavestrello, Di Camillo & Boero Long-term changes in hydroid assemblages

Marine Ecology (2009) 1–14 ª 2009 Blackwell Verlag GmbH 9

in 2004 (Fig. 8): in fact, whereas in 1980 the species weremainly distributed at a single depth level, in 2004 almost40% of the species colonized all the studied depths(Fig. 9). Of the species recorded only in shallow water(0–5 m) during 1980, 27% had disappeared, 20% showedan unmodified distribution, and more than 50% had wid-ened their distribution (Fig. 10). On the other hand, 60%of the deep species in 1980 had disappeared in 2004,

Fig. 5. Percentage of species present in one or more months during

the sampling in 1980 (white bars) and 2004 (black bars).

Fig. 6. Percentage of species showing a spring–summer or autumn–

winter distribution during 1980 that had disappeared, maintained or

changed their temporal distribution during 2004.

Fig. 7. Percentage of species recorded all year round during 1980

that had disappeared, maintained or changed their temporal distribu-

tion during 2004.

Fig. 8. Number of species present at each depth level during the

sampling in 1980 (white bars) and in 2004 (black bars).

Fig. 9. Number of species present at one or more depth levels during

the sampling in 1980 (white bars) and 2004 (black bars).

Fig. 10. Percentage of species recorded during 1980 exclusively in

the shallow (0–5 m) and deep (10–20 m) stations that had disap-

peared, maintained or enlarged their bathymetric distribution in 2004.

Long-term changes in hydroid assemblages Puce, Bavestrello, Di Camillo & Boero

10 Marine Ecology (2009) 1–14 ª 2009 Blackwell Verlag GmbH

about 30% showed an unmodified distribution and lessthan 10% showed a widened distribution (Fig. 10).

Eudendrium capillare, a typically shallow-water species,was found at 20 m in 2004. Moreover, Aglaopheniaelongata, generally collected at 15–20 m in 1980, hadcompletely disappeared from this depth in 2004 and wasobserved only at deeper levels.

Several species modified both their bathymetric andseasonal distribution. Hydractinia fucicola, typicallypresent in 1980 all year round at the depth level 0–0.5 m,was collected in 2004 exclusively during the winter andnever at this depth, only from 5 to 20 m. Similarly,Plumularia setacea and Turritopsis dohrni, collected in1980 during summer–autumn at 0–5 m, in 2004 becamea winter species, reaching 20 m depth. Although Bougain-villia muscus and Kirchenpaueria pinnata show anunmodified bathymetric distribution, they changed theirseasonality, disappearing during summer. Moreover, Eu-dendrium racemosum, a typical summer–autumn species,was also collected between January and March in 2004.

Discussion

The response of the hydroid species assemblage showsmarked differences in the two studied periods, with aconsistent trend favouring warm-water species and disfa-vouring cold-water species.

The species number for the two periods is very similarduring winter–spring months (January–June), but clearlydecreased during summer and autumn (July–December).In 2004, bathymetric distributions became wider, beingunidirectional from shallow to deep water: almost 30% ofthe shallow water species had disappeared and more than50% had gone deeper. More than 60% of deep-water spe-cies had disappeared. Only a few deep-water species(< 10%) rose towards the surface, maybe colonizing thesubstrate freed by some of the species which had disap-peared.

Considering the whole transect, the number ofobserved species in 2004 was lower than that recorded in1980; conversely, for each depth zone the number ofobserved species was higher in 2004 than in 1980. This isdue to an increased number of species able to live at eachof the depth zones, producing a homogenization in thecomposition of the assemblage along the depth gradientand the loss of exclusive species. Problems of biotichomogenization driven by climate change have alreadybeen discussed in recent papers, even for the marine envi-ronment (Olden & Rooney 2006; Bolam et al. 2008).

In 1980 a large percentage of species (about 25%) wereactive all year round, whereas in 2004 they were drasti-cally reduced, having partially disappeared. The remainingspecies mainly restricted their active period to winter. A

unidirectional shift in the activity period from the warmto the cold season was observed: most of the species thatin 1980 were active during autumn or winter had disap-peared, and half of the spring–summer species were alsoactive in the cold season.

Moreover, in 2004 numerous species that were abun-dant in 1980 were not found, whereas species rare in 1980were common and widely distributed in 2004. Hydroidstypical of the Southern Mediterranean were recorded forthe first time in the area studied: Eudendrium moulouyen-sis, a species originally described from Morocco (Marqueset al. 2000) and recently observed in Southern Italy (DeVito et al. 2008) was frequent and reproductive. Pennariadisticha, very common in the southern part of the Tyrrhe-nian Sea, and sporadically recorded in the Ligurian Sea(Bianchi & Morri 1994), became actually extremely abun-dant at 0–5 m during summer.

Conclusions

Many observed patterns of temporal and spatial distribu-tion consistently suggest that the Portofino hydroid assem-blage has changed as a response to an increase in watertemperature, although is not possible to completely excludethe influence of other causative agents (e.g. an increase inwater pollution). Shallow-water species colonized deeperzones; deep-water species shifted to deeper levels; manywinter species disappeared; many species shifted their activ-ity period from summer to winter; southern speciesextended their range toward the Ligurian Sea.

Due to their ubiquitous presence and the tendency toform habitats for other species, marine algae are oftenused to describe the general conditions of coastal marinesystems, also using particular indexes. Algae, however, aremostly abundant in the spring–summer, so that indexes,such as the Carlit index, are only informative if per-formed in this period (Ballesteros et al. 2007; Mangialajoet al. 2007). Hydroids are the counterpart of algae in thecold season, being sharply seasonal in appearance, andhaving the possibility to form habitats for other species.Following the work by Boero & Fresi (1986) this studyshows that hydroids, due to their marked seasonality intemperate seas, are extremely sensitive to climatic changesand strongly suggests that the modifications observed inthe composition, seasonality, bathymetric distribution andreproductive period of hydroid assemblages must be con-sidered in the evaluation of the influence of global warm-ing on marine ecosystems.

Acknowledgements

Financial support was provided by MIUR (PRIN project),by the Euro-Mediterranean Centre for Climate Change

Puce, Bavestrello, Di Camillo & Boero Long-term changes in hydroid assemblages

Marine Ecology (2009) 1–14 ª 2009 Blackwell Verlag GmbH 11

(CMCC), by the European Union (SESAME project,MARBEF Network of Excellence).

References

Albertelli G., Cattaneo M., Drago N. (1981) Macrobenthos du

plateau continental Ligure et de l’Archipel Toscan: apercus

zoogeographiques. Rapport de la Commission Internationale

pour la Mer Mediterranee, 27, 127–128.

Ambrogi R., Fontana I., Sala P. (1994) Evoluzione a lungotermine del macrobenthos marino di fondo mobile davanti

al Delta del Po. Biologia Marina Mediterranea, 1(1),

179–188.

Arillo A., Bavestrello G., Boero F. (1989) Circannual cycle andoxygen consumption in Eudendrium glomeratum (Cnidaria,

Anthomedusae): studies on a shallow water population.PSZN: Marine Ecology, 10, 289–301.

Astraldi M., Bianchi C.N., Gasparini G.P., Morri C. (1995) Cli-

matic fluctuations, current variability and marine speciesdistribution: a case study in the Ligurian Sea (North-west

Mediterranean). Oceanologica Acta, 18(2), 139–149.Ballesteros E., Torras X., Pinedo S., Garcıa M., Mangialajo L.,

de Torres M. (2007) A new methodology based on littoralcommunity cartography dominated by macroalgae for the

implementation of the European Water Framework Direc-

tive. Marine Pollution Bulletin, 55, 172–180.Bavestrello G. (1983–84) Popolamento ad idroidi di agglomer-

ati di Pteria hirundo (L.) su fondali fangosi della riviera lig-

ure di levante. Nova Thalassia, 6, 685.Bavestrello G. (1985) Idroidi simbionti di paguri e gasteropodi

nella riviera ligure di levante. Oebalia, XI, N. S., 349–362.Bavestrello G. (1987) Description of the hydroid Perarella

propagulata sp. nov. (Cnidaria, Hydrozoa) and discussion of

relation within the superfamily Bougainvillioidea Petersen.

In: Bouillon J., Boero F., Cicogna F., Cornelius P.F.S. (Eds),

Modern Trends in the Systematics Ecology and Evolution

of Hydroids and Hydromedusae. Clarendon Press, Oxford:

19–27.

Bavestrello G., Arillo A. (1992) Irradiance, temperature andcircannual cycle of Eudendrium glomeratum Picard (Hydro-

zoa, Cnidaria). Bollettino di Zoologia, 59, 45–48.

Bavestrello G., Puce S., Cerrano C., Balduzzi A. (2000) Life

history of Perarella schneideri (Hydrozoa, Cytaeididae) in

the Ligurian Sea. Scientia Marina, 64 (Supl. 1), 141–146.

Bavestrello G., Puce S., Cerrano C., Zocchi E., Boero N. (2006)

The problem of seasonality of benthic hydroids in temperate

waters. Chemistry and Ecology, 22, 197–205.

Bianchi C.N. (1997) Climate change and biological response in

the marine benthos. Proceedings of the Italian Association forOceanology and Limnology, 12(1), 3–20.

Bianchi C.N. (2007) Biodiversity issues for the forthcomingtropical Mediterranean Sea. Hydrobiologia, 580, 7–21.

Bianchi C.N., Morri C. (1993) Range extension of warm-water

species in the northern Mediterranean: evidence for climatic

fluctuations? Porcupine Newsletter, 5(7), 156–159.

Bianchi C.N., Morri C. (1994) Southern species in the LigurianSea (Northern Mediterranean): new records and a review.

Bollettino dei Musei e degli Istituti Biologici dell’Universita diGenova (1992–1993), 58–59, 181–197.

Bianchi C.N., Morri C. (2003) Global sea warming and ‘‘tropi-

calization’’of the Mediterranean Sea: biogeographic and eco-

logical aspects. Biogeographia, XXIV, 319–327.Bianchi C.N., Morri C. (2004) Climate change and biological

response in Mediterranean Sea ecosystems – a need forbroad-scale and long-term research. Ocean Challenge, 13,

32–36.Blacker R.W. (1957) Benthic animals as indicators of hydro-

graphic conditions and climatic change in Svalbard waters.

Fishery Investigations Series II, 20(10), 1–49.

Boero F. (1984) The ecology of marine hydroids and effectsof environmental factors: a review. PSZN: Marine Ecology, 5,

93–118.

Boero F., Fresi E. (1986) Zonation and evolution of a rocky

bottom hydroid community. PSZN: Marine Ecology, 7, 123–150.

Boero F., Balduzzi A., Bavestrello G., Caffa B., Cattaneo Vietti

R. (1986) Population dynamics of Eudendrium glomeratum(Cnidaria: Anthomedusae) on the Portofino promontory

(Ligurian Sea). Marine Biology, 92, 81–85.Boero F., Bouillon J., Gravili C., Piraino S. (2003) Who cares

about the Hydrozoa of the Mediterranean Sea? An essay onthe zoogeography of inconspicuous groups. Biogeographia,

XXIV, 101–113.

Bolam S.G., Eggleton J., Smith R., Mason C., Vanstaen K.,

Rees H. (2008) Spatial distribution of macrofaunal

assemblages along the English Channel. Journal of the

Marine Biological Association of the United Kingdom, 88,675–687.

Bouillon J., Medel M.D., Pages F., Gili J.M., Boero F., Gravili

C. (2004) Fauna of the Mediterranean Hydrozoa. Scientia

Marina, 68 (Supl. 2), 5–438.

Bouillon J., Gravili C., Pages F., Gili J.M., Boero F. (2006) An

introduction to Hydrozoa. Memoires du Museum National

d’Histoire Naturelle. Publications Scientifiques du Museum.

Paris, 194, 1–593.Briggs J.C. (1974) Marine Zoogeography. McGraw-Hill, New

York: 1–475.

Brock M.A. (1974) Circannual rhythmicity in Invertebrates. In:Pengelley E.T. (Ed.), Circannual Clocks. Annual BiologicalRhythms. Academic Press, New York: 11–53.

Cabioch L., Glemarec M., Saiman J.F. (1983) Fluctuation et

succession dans les ecosystems marins. Oceanologica Acta

spec. vol., 1–225.

Calder D.R. (1990) Seasonal cycles of activity and inactivity in

some hydroids from Virginia and South Carolina, U.S.A.

Canadian Journal of Zoology, 68, 442–450.

Cataletto B., Feoli E., Fonda-Umani S., Cheng-Yong S. (1995)

Eleven years of time-series analysis on the net-zooplankton

community in the Gulf of Trieste. ICES Journal of Marine

Science, 52, 669–678.

Long-term changes in hydroid assemblages Puce, Bavestrello, Di Camillo & Boero

12 Marine Ecology (2009) 1–14 ª 2009 Blackwell Verlag GmbH

Cattaneo-Vietti R., Sirigu A.P., Tommei A. (1988) Mare di Lig-uria. Centro Studi Unione Camere Commercio Liguri, Ge-

nova: 162 pp.Cerrano C., Bavestrello G., Bianchi C.N., Cattaneo-Vietti R.,

Bava S., Morganti C., Morri C., Picco P., Sara G., Schiapar-

elli S., Siccardi A., Sponga F. (2000) A catastrophic mass-

mortality episode of gorgonians and other organisms in theLigurian Sea (North-western Mediterranean), summer 1999.

Ecology Letters, 3, 284–293.De Vito D., Boero F., Di Camillo C.G., Megina C., Piraino S.

(2008) Redescription of the zooxanthellate Eudendrium

moulouyensis Marques, Pena Cantero, Vervoort 2000 (Eu-

dendriidae, Hydrozoa) from the Mediterranean Sea. Journal

of the Marine Biological Association of the United Kingdom,88, 1655–1662.

Degobbis D., Fonda Umani S., Franco P., Malej A., Precali R.,

Smodlaka N. (1995) Changes in the Northern Adriatic Eco-

system and appearance of hypertrophic gelatinous aggre-gates. Science of the Total Environment, 165, 43–58.

Di Camillo C.G., Valisano L., Bavestrello G., Puce S. (2008)

Spatial and temporal variations in a tropical hydroid assem-blage. Journal of the Marine Biological Association of the Uni-

ted Kingdom, 88, 1589–1599.Francour P., Boudouresque C.F., Harmelin J.G., Harmelin-Viv-

ien M.L., Quignard J.P. (1994) Are the Mediterranean

waters becoming warmer? Information from biological indi-

cators. Marine Pollution Bulletin, 28(9), 523–526.

Fromentin J.M., Ibanez F., Dauvin J.C., Dawarumez J.M., Elk-

aim B. (1997) Long-term changes of four macrobenthic

assemblages from 1978 to 1992. Journal of the Marine Bio-

logical Association of the United Kingdom, 77, 287–310.Garrabou J., Perez T., Sartoretto S., Harmelin J.G. (2001) Mass

mortality event in red coral (Corallium rubrum, Cnidaria,Anthozoa, Octocorallia) populations in the Provence region

(France, North-western Mediterranean). Marine Ecology Pro-

gress Series, 217, 263–272.Gili J.M., Hughes R.G. (1995) The ecology of marine benthic

hydroids. Oceanography and Marine Biology: An Annual

Review, 33, 351–426.

Glantz M.H. (1992) Climate Variability, Climate Change and

Fisheries. Cambridge University Press, Cambridge: 450 pp.

Grainger J.N.R. (1992) The probable effects of climate changeon invertebrate growth and reproduction with particular ref-

erence to Ireland. Invertebrate Reproduction and Develop-ment, 22(1–3), 239–244.

Heip C., Keegan B.F., Lewis J.R. (1987) Long-term changes in

coastal benthic communities. Development in Hydrobiology,

Vol. 38. W. Junk Publishers, Dordrecht: 340 pp.

Keegan B.F. (1991) Space and Time Series Data Analysis inCoastal Benthic Ecology. Commission of the European Com-

munities, Directorate-General for Science, Research and

Development, Environment Research Programme, Brussels.

Laevastu T. (1993) Marine Climate, Weather and Fisheries.

Blackwell (Fishing News Books), Oxford: 204 pp.

Maddock L., Harbour D.S., Boalch G.T. (1989) Seasonal andyear-to-year changes in the phytoplankton from the

Plymouth area, 1963–1986. Journal of the Marine BiologicalAssociation of the United Kingdom, 69, 229–244.

Mangialajo L., Ruggieri N., Asnaghi V., Chiantore M., Povero

P., Cattaneo-Vietti R. (2007) Ecological status in the Liguri-an Sea: the effect of the coastline urbanisation and the

importance of proper reference sites. Marine Pollution Bulle-tin, 55, 30–41.

Marques A.C., Pena Cantero A.L., Vervoort W. (2000) Medi-terranean species of Eudendrium Ehrenberg, 1834 (Hydro-

zoa, Anthomedusae, Eudendriidae) with the description of anew species. Journal of Zoology, London, 252, 197–213.

Marullo S., Guarracino M. (2003) L’anomalia termica del 2003nel mar Mediterraneo osservata da satellite. Energia, Ambi-

ente e Innovazione, 6 ⁄ 03, 48–53.McGovan J.A. (1990) Climate and change in oceanic ecosys-

tems: the value of time-series data. Trends in Ecology and

Evolution, 5, 293–299.Molinero J.C., Ibanez F., Souissi S., Buecher E., Dallot S., Nival

P. (2008) Climate control on the long-term anomalouschanges of zooplankton communities in the Northwestern

Mediterranean. Global Change Biology, 14, 11–26.Olden J.D., Rooney T.P. (2006) On defining and quantifying

biotic homogenization. Global Ecology and Biogeography, 15,

113–120.Puce S., Bavestrello G., Azzini F., Cerrano C. (2003) On the

occurrence of Coryne eximia (Cnidaria, Corynidae) in the

Mediterranean Sea. Italian Journal of Zoology, 70, 249–252.Robinson G.A., Hunt H.G. (1986) Continuous plankton

records: annual fluctuations of the plankton in the Western

English Channel, 1958–83. Journal of the Marine Biological

Association of the United Kingdom, 66, 791–802.

Rossi L. (1949–50) Celenterati del Golfo di Rapallo. Bollettino

del Museo di Zoologia dell’Universita di Torino, 20, 194–235.

Rossi L. (1961) Idroidi viventi sulle scogliere del Promontoriodi Portofino (Golfo di Genova). Annali del Museo Civico di

Storia Naturale di Genova, 72, 69–85.Rossi L. (1969) Considerazioni zoogeografiche sul Bacino NW

del Mediterraneo, con particolare riguardo al Mar Ligure.

Archivio Botanico e Biogeografico Italiano, Serie XLV-40,

14(4), 139–152.

Sara G., Bianchi C.N., Morri C. (2005) Mating behaviour ofthe newly established ornate wrasse Thalassoma pavo

(Osteichthyes: Labridae) in the Ligurian Sea (North-western

Mediteranean). Journal of the Marine Biological Association

of the United Kingdom, 85, 191–196.

Sara M., Balduzzi A., Boero F., Pansini M., Pessani D.,

Pronzato R. (1978) Analisi di un popolamento bentonico di

falesia del Promontorio di Portofino: dati preliminari. Bol-

lettino dei Musei e degli Istituti Biologici dell’Universita di Ge-

nova, 46, 119–137.Schiaparelli S., Castellano M., Povero P., Sartoni G., Cattaneo-

Vietti R. (2007) A benthic mucilage event in North-Western

Puce, Bavestrello, Di Camillo & Boero Long-term changes in hydroid assemblages

Marine Ecology (2009) 1–14 ª 2009 Blackwell Verlag GmbH 13

Mediterranean and its possible relationships with the sum-mer 2003 European heatwave: short term effects on littoral

rocky assemblages. Marine Ecology: an evolutionary perspec-tive, 28(3), 341–353.

Shillaber N. (1995) Assessing the effectiveness of quality stan-

dards for marine benthos using data from Tees Bay moni-

toring programme. In: Eleftheriou A., Ansell A.D., SmithC.J. (Eds), Biology and Ecology of Shallow Coastal Waters.

Olsen & Olsen, Fredensborg: 199–204.

Southward A.J. (1995) The importance of long time-series in

understanding the variability of natural systems. HelgolanderMeeresunters, 49, 329–333.

Vermeij G.J. (1980) Biogeography and Adaptation. Patterns ofMarine Life. Harvard University Press, Cambridge, MA:

1–332.

Warwick R.M., Bayne B.L. (1993) Changes in marine commu-

nities. Journal of Experimental Marine Biology and Ecology,

172, 1–230.

Long-term changes in hydroid assemblages Puce, Bavestrello, Di Camillo & Boero

14 Marine Ecology (2009) 1–14 ª 2009 Blackwell Verlag GmbH