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Recent advances in the Mediterranean researches on zooplankton: from
spatial-temporal patterns of distribution to processes oriented studies
Serena Fonda Umania; Marina Montib; Roberta Minutolic; Letterio Guglielmoc
a
Department of Life Sciences, University of Trieste, I-34127 Trieste, Italy b Department of Biological
Oceanography, Istituto Nazionale di Oceanografia e Geofisica Sperimentale - OGS, I-34151, Trieste,
Italy c Department of Animal Biology and Marine Ecology, University of Messina, 98166 Messina, Italy
Online publication date: 08 December 2010
To cite this Article Umani, Serena Fonda , Monti, Marina , Minutoli, Roberta and Guglielmo, Letterio(2010) 'Recent
advances in the Mediterranean researches on zooplankton: from spatial-temporal patterns of distribution to processes
oriented studies', Advances in Oceanography and Limnology, 1: 2, 295 — 356
To link to this Article: DOI: 10.1080/19475721.2010.494413
URL: http://dx.doi.org/10.1080/19475721.2010.494413
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Advances in Oceanography and Limnology
Vol. 1, No. 2, December 2010, 295–356
Recent advances in the Mediterranean researches on zooplankton:
from spatial–temporal patterns of distribution to
processes oriented studies
Serena Fonda Umania*, Marina Montib, Roberta Minutolic and Letterio Guglielmoc
a
Department of Life Sciences, University of Trieste, v. Valerio 28/1, I-34127 Trieste, Italy;
Istituto Nazionale di Oceanografia e Geofisica Sperimentale – OGS, Department of Biological
Oceanography, Via A. Piccard 54, I-34151, Trieste, Italy; cDepartment of Animal Biology
and Marine Ecology, University of Messina, Viale Ferdinando Stagno D’Alcontres 31,
98166 Messina, Italy
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b
(Received 25 February 2010; final version received 14 May 2010)
In this review we focus on research performed by Italian scientists on pelagic
communities, from microzooplankton to micronekton, mainly in the Italian Seas.
We considered published data, mostly as grey literature, and unpublished ones.
Firstly we describe data collected over a time span of more than 30 years, during
several cruises all around the Italian peninsula on zooplankton composition and
distribution. We identified rare vs. common species, which enhanced biodiversity
of the pelagic ecosystem. Time series, some also very long, allowed us to describe
seasonal recurrent patterns, interannual fluctuations and recent shifts driven by
climatic changes. More recently Italian researches were processes oriented and we
analyzed results obtained on the impact of predation of both micro- and
mesozooplankton on both autotrophic and heterotrophic preys. Carbon fluxes
through zooplankton components were variable in space and time, but accounted
for important phytoplankton losses, and when this resource became scarce they
relied on heterotrophic production. Through respiration measurements of
mesozooplankton another aspect of the C flux was estimated showing an
increase in C demand in the most oligotrophic area. Egg production by copepods
appeared to be mostly controlled by temperature and quantity/quality of
available food.
Keywords: microzooplankton; mesozooplankton; micronekton; Italian Seas;
biodiversity; biological processes
1. Introduction
The term plankton was coined in 1887 [1] and embraces all those organisms drifting in the
water whose abilities of locomotion are insufficient to withstand currents. Zooplankton
may be distinguished from phytoplankton on the basis of mode of nutrition, autotrophic
or heterotrophic. Zooplankton may be defined as the community of all phagotrophic
organisms. According to their food preferences they can be classified as herbivorus,
detritivorus, omnivorous or carnivorous. Heterotrophic plankton also includes the
osmotrophic bacteria. Mixotrophy, the combination of auto and heterotrophy, is quite
*Corresponding author. Email: s.fonda@units.it
ISSN 1947–5721 print/ISSN 1947–573X online
ß 2010 Taylor & Francis
DOI: 10.1080/19475721.2010.494413
http://www.informaworld.com
296
S. Fonda Umani et al.
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commonly found in flagellates and other protozoans (e.g. dinoflagellates, foraminiferans,
radiolarians, ciliates), and can occur in some metazoans phyla (e.g. cnidarians, mollusks).
Species spending all their life in the pelagic realm are termed holoplanktonic, while
meroplankton lives as a drifter only part of its life. Marine zooplankton comprises a large
variety of different organisms with some 10,000 species if meroplankton is included. Their
sizes range from bacteria up to giant jellyfish of 2 m in diameter and thus span 7 orders of
magnitude [2]. Nowadays Sieburth classification [3] is widely accepted. In this review we
will consider only three size ranges: microzooplankton (10 or 20 mm to 200 mm),
mesozooplankton (0.2–2 mm), and micronekton (2.0–10.0 cm). The first are usually
sampled by bottles while the latter by nets, and 200 mm is the mesh size most often used,
particularly in coastal Mediterranean waters.
2. Microzooplankton
Since the ‘changing paradigm’ of planktonic food webs [4,5] microzooplankton has gained
a pivotal role in the transfer of energy from lower trophic levels (microbial food web) to
the ‘classical grazing food web’. On the other hand Calbet and Landry [6] stated that
grazing of microzooplankton represents the major loss term for phytoplankton cell growth
across a broad range of ocean regions and habitats. They suggested that this might be true
also in the more productive coastal waters, where mesozooplankton has traditionally been
considered the major grazer. Because of microzooplankton’s ability to grow at the same
speed as phytoplankton cells, it may have a considerable advantage over larger metazoans
in exploiting ephemeral changes in food availability. Therefore microzooplankton, which
in turn is a substantial part of the diet of larger grazers like copepods [7–14], can in the
same contest be a prey and a competitor for the upper level consumers within the so called
mistivorus food web [15]. When available, microzooplankton and especially ciliates are
selectively eaten by mesozooplankton [10–12,14,16–18] but the reported contribution of
microzooplankton to mesozooplankton carbon ration is very variable [12,19].
Microzooplankton is composed by a wide assemblage of organisms in the size range
10 or 20 (depending on the classification used) to 200 mm: mainly protists like ciliates,
heterotrophic (and mixotrophic) dinoflagellates, foraminiferans, radiolarians, acantarians,
heliozoans; and the first larval stages of many marine metazoans, usually called
micrometazoans.
Despite the recognized importance of this fraction there is neither a commonly
accepted method to sample (net vs. bottle), nor a common consensus on the volume to
observe or the best fixative (and relative concentration) to use [20–27]. Consequently, any
comparison among quantitative data must be considered with caution and keeping in
mind the adopted methods. For these reasons in this paper we will focus more on species
composition rather than on abundances and biomasses and, more particularly, on
tintinnids. Although heterotrophic dinoflagellates and naked ciliates dominate the
microzooplankton fraction both in terms of abundance and biomass, tintinnids are a
species rich group, found in nearly all marine and estuarine systems [28], which sometimes
represent up to 50% of microzooplankton abundance and biomass. They are characterized
by the possession of a species-specific shell (lorica), shaped like a bowl or vase or tube [29]
on which their taxonomy is based. Tintinnids form an order of the ciliate subclass
Choreotricha and represent a monophyletic group, in agreement with traditional
ciliate taxonomy and, more recent molecular data, even among competing ciliate
Advances in Oceanography and Limnology
297
classification [30,31]. They are easily identified on the basis of the lorica shape into which
the ciliate cell can withdraw, and for this reason there is a rich literature on their
biogeography [29,32–34], as well as their ecology [35].
In the Mediterranean Sea (as all over the world) the first researches on
microzooplankton were strictly taxonomic [36–41], in the 1980s researches were only
devoted to distribution patterns and ecology, and it was not until the early 1990s that
heterotrophic dinoflagellates were considered.
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2.1. Microzooplankton and particularly tintinnid’s distribution in the Italian Seas
In this section we report all data that we were able to find (published and unpublished) on
patterns of microzooplankton, and particularly of tintinnids, distribution in the Italian
Seas, following an anticlockwise order from the North Tyrrhenian Sea to the North
Adriatic Sea.
2.1.1. North Tyrrhenian Sea
First data on microzooplankton distribution in the Tyrrhenian Sea date back to the late
1980s. Cruises were carried out within the frame of MARE project in an area around the
Elba Island (9 450 –11 100 E and 42 120 –43 N) in November 1986 and March 1987,
whereas in a more northern area (9 230 –10 280 E and 42 560 –44 N) samples were
collected in April, July and November 1988, February and July 1989 on a total of more
than 300 stations [42]. Samples of 5 L were collected at the surface, intermediate layers and
near the bottom. They were concentrated to 250 mL by inverse filtration on 10-mm mesh
size and fixed in buffered formaldehyde. Abundance of total microzooplankton (dinoflagellates not included) varied from total absence (in some deep sample) to 1387 ind. L1.
Among ciliates, aloricate genera (e.g. Strombidium, Lacrimaria) accounted on average for
less than 13% of total specimens, but we must keep in mind that the filtration step
eliminated all small ciliates (nanociliates) and that formaldehyde is not the best
preservative for naked ciliates. On the other hand micrometazoans, that in some cruises
were more than 50% of total microzooplankton and tintinnids, which clearly dominated
the community in all cruises, were well preserved. In Table 1 we reported all tintinnid’s
species registered for the North area (where sampling was performed in the four seasons)
and South area (where it was sampled only in spring and autumn). A total of 167 species
were identified and 30 of these were reported for the first time in the Mediterranean Sea.
Thirty-six species were collected in the North area in all seasons, but of these only 21 were
present in the two southern cruises. Over all tintinnids with agglutinated lorica were more
abundant in the coastal area, while hyaline tintinnids clearly prevailed off shore. In spring
and summer there was a sharp coastal–off shore gradient, whereas in the other seasons,
and particularly in the deep layers, a South–North gradient was more evident [42–44].
2.1.2. South Tyrrhenian Sea
In the area around Aeolian islands (38 47.70 N–14 39.00 E and 38 34.00 N–15 37.50 E)
two cruises were carried out in July 1994 and 1995. Samples of 5 L were collected at the
surface, intermediate layers and near the bottom. They were concentrated to 250 mL by
inverse filtration on 10-mm mesh size and fixed in buffered formaldehyde. A total of 49
species were reported for the two cruises (Table 1). In July 1994 tintinnid’s community was
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Species
North
Tyrrhenian
42°12' - 44° N
9°23' - 11°10'
E
Gulf of
Naples
40°48'N,
14°15'E
South
Tyrrhenian
Gulf of
Milazzo
Ionian
Sea
38°34' -38°47'N
14°39'-15°37'E -
38°18'N,
15°33'E
37°50'N,
15°20'E
x
x
xx
x
Acanthostomella conicoides
x
xx
Acanthostomella lata
x
x
Acanthostomella minutissima
x
Acanthostomella norvegica
x
South Adriatic
45°30' - 45°40' N
18°30' -19°30' E
PRISMA
x
x
x
Amphorella amphora
Mid Adriatic
North Adriatic
North Adriatic
43°45' - 44°25' N
13°10' - 14°10' E
PRISMA
North
Adriatic
41°50' - 43°50' N
13 55' - 17°20' E
SERPA
41°50 - 43°55' N
16°50' - 17°50' E
PRISMA
42°55' - 43°55'N
13°55' - 15° E
PRISMA
42°55' - 43°55'N
13°55' - 15° E
MAT
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
44° 55' - 45° N
43°30 - 45° 40 N
12°30' - 13°30' E 12° 30' - 13° 40' E
MAT
Sesame/Vector
x
Gulf of
Trieste
45°42'N,
13°42'E
x
x
x
x
x
x
x
x
x
xx
x
x
x
xx
x
x
x
x
xx
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
Amphorellopsis acuta
Amphorellopsis acantharus
x
Amphorellopsis tettragona
x
Amplectella tricollaria
x
Canthariella brevis
x
Canthariella pyramidata
x
Climacocylis digitula
x
Climacocylis elongata
x
Climacocylis scalaria
x
Climacocylis scalaroides
x
Codonaria australis
x
Codonaria cistellula
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
Codonella acerca
Codonella acuta
North Adriatic
x
x
x
x
x
x
x
x
x
S. Fonda Umani et al.
Amphorella quadrilineata v minor
Mid Adriatic
45° - 45°40' N
12°30' - 13°40' E
ASCOP/ Alpe
Adria/ Fertimont
x
x
Amphorella intumescens
Amphorella quadrilineata
Mid Adriatic
x
Acanthostomella obtusa
Amphorella laackmanni
Mid Adriatic
298
Table 1. Tintinnid species distribution in the Italian seas: x indicates the presence of species; xx indicates the dominance of the species. For full colour
reproduction of this table, please refer to the online version.
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x
Codonella amphorella
x
Codonella apicata
x
Codonella aspera
x
x
Codonella brevicollis
x
x
Codonella cistellula
x
x
x
x
xx
x
x
x
x
x
x
x
x
x
x
Codonella nationalis
x
Codonella pacifica
x
Codonella perforata
x
Codonellopsis contracta
x
Codonellopsis ecaudata
x
Codonellopsis monacensis
x
Codonellopsis orthoceras
x
Codonellopsis pusilla
x
Codonellopsis schabi
x
Codonellopsis tubercolata
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
Coxliella ampla
x
x
Coxliella helix
x
x
Craterella armilla
xx
xx
Craterella oxyura
xx
x
x
Craterella torulata
x
xx
x
x
x
x
x
x
x
Coxliella fasciata
Craterella protuberans
x
x
x
Coxliella annulata
x
xx
x
x
xx
x
x
x
x
x
x
x
x
x
x
xx
x
xx
Advances in Oceanography and Limnology
Codonella galea
Craterella urceolata
x
x
Codonella laticollis
Coxliella laciniosa
x
x
x
x
x
x
(continued )
299
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300
Cyttaroc yl is brandti
x
Cyttarocylis cassis
x
Cyttarocylis eucecryphalus
x
Cyttarocylis magna
x
Cyttarocylis mucronata
x
Dadayiella cuspis
xx
Dadayiella pachytoecus
x
Dictyocysta ampla
x
Dictyocysta elegans
x
Dictyocysta elegans lepida
x
Dictyocysta elegans speciosa
x
Dictyocysta entzi
x
Dictyocysta lepida
x
Dictyocysta mitra
x
Dictyocysta mülleri
x
Dictyocysta obtusa
x
Dictyocysta pacifica
x
Dictyocysta reticulata
x
Dictyocysta tiara
x
Epiplocylis acuminata
x
xx
xx
x
x
x
x
x
xx
x
xx
xx
x
x
xx
x
x
x
x
x
x
x
xx
x
x
xx
x
xx
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
Epiplocylis blanda
Epiplocylis constricta
x
x
xx
x
S. Fonda Umani et al.
Dadayiella ganymedes
x
x
x
x
x
x
x
x
Epiplocylis undella
Eutintinnus apertus
x
Eutintinnus birictus
x
Eutintinnus elegans
x
x
xx
x
xx
x
x
x
x
x
x
xx
x
x
x
x
x
x
x
x
x
x
xx
x
x
x
x
x
x
x
x
x
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Eutintinnus elongatus
x
Eutintinnus fraknoii
x
x
x
x
x
x
x
x
x
x
x
Eutintinnus macilentus
x
x
x
x
x
x
x
x
x
xx
xx
x
x
x
x
x
x
x
x
x
x
x
x
x
xx
x
x
x
Eutintinnus stramentus
x
x
x
x
x
x
x
x
x
Eutintinnus tenuis
x
xx
xx
x
x
x
x
x
xx
x
x
x
x
x
xx
x
x
x
x
x
Eutintinnus turris
Favella azorica
x
x
x
x
x
x
x
x
x
x
x
Favella composita
Favella ehrenbergii
x
Favella serrata
x
x
x
Helicostomella edentata
x
Helicostomella longa
x
Helicostomella subulata
x
xx
Metacylis jorgenseni
x
xx
Metacylis mediterranea
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
xx
x
Leprotintinnus nordqvisti
x
Metacylis annulifera
x
x
x
x
xx
x
x
x
Advances in Oceanography and Limnology
x
Eutintinnus pinguis
Metacylis cfr mereschkowskyi
x
x
Eutintinnus perminutus
Favella campanula
x
x
Eutintinnus pacificus
Eutintinnus tubulosus
x
x
Eutintinnus maculatus
Eutintinnus medius
x
x
x
Eutintinnus latus
Eutintinnus lusus-undae
x
x
(continued )
301
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302
Ormosella apsteini
x
Ormosella bresslaui
x
Ormosella haeckeli
x
Ormosella trachelium
x
x
Parundella aculeata
x
x
Parundella lohmanni
x
Parundella longa
x
Parundella messinensis
x
x
Petalotricha ampulla
x
x
Petalotricha major
x
x
x
x
x
x
x
x
x
x
x
x
Proplectella claparedei
Proplectella columbiana
Proplectella ostenfeldi
x
x
x
x
x
x
x
x
Proplectella urna
x
x
x
Ptychoccylis obtusa
x
xx
x
x
x
x
x
x
x
x
x
x
Rhabdonella amor
Rhabdonella chiliensis
x
x
Protorhabdonella simplex
x
x
x
Rhabdonella cornucopia
Rhabdonella conica
x
Rhabdonella cuspidata
x
x
x
Rhabdonella elegans
Rhabdonella exilis
x
Rhabdonella hebe
x
Rhabdonella henseni
x
x
S. Fonda Umani et al.
x
Proplectella pentagona
Protorhabdonella curta
x
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Rhabdonella inflata
x
Rhabdonella lohmanni
x
Rhabdonella spiralis
x
Rhabdonella striata
x
Salpigacantha unguiulata
x
Salpingacantha crenulata
x
Salpingacantha ampla
x
Salpingella acuminata
xx
Salpingella attenuata
x
xx
Salpingella decurtata
xx
Salpingella faurei
xx
Salpingella glockentögeri
xx
Salpingella gracilis
x
Salpingella lackmanni
x
Salpingella minutissima
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
xx
Salpingella subconica
x
Steenstrupiella gracilis
x
xx
x
x
x
x
x
x
x
x
x
x
xx
xx
xx
xx
xx
x
x
x
x
x
x
x
x
x
x
xx
x
x
xx
xx
x
x
x
x
x
x
x
x
x
xx
xx
x
x
x
x
x
x
x
x
x
x
x
x
xx
xx
x
x
x
x
xx
x
x
x
x
x
x
x
x
x
x
x
Salpingella rotundata
xx
x
xx
x
x
x
x
x
x
x
x
x
x
xx
Steenstrupiella intumescens
x
x
Steenstrupiella robusta
Steenstrupiella steenstrupii
x
xx
xx
xx
xx
x
x
x
x
xx
x
Stenosemella oliva
Stenosemella nivalis
xx
Stenosemella pacifica
Stenosemella ventricosa
Tintinnidium incertum
xx
x
x
x
x
xx
xx
xx
x
xx
x
x
x
xx
x
x
x
x
xx
xx
x
xx
x
x
x
x
x
x
Advances in Oceanography and Limnology
Salpingella curta
x
x
(continued )
303
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x
Tintinnopsis acuminata
x
Tintinnopsis amphora
x
Tintinnopsis angulata
x
Tintinnopsis aperta
x
304
Tintinnidium mucicola
x
x
Tintinnopsis butschlii
x
Tintinnopsis campanula
x
Tintinnopsis cincta
x
Tintinnopsis compressa
x
x
x
x
x
x
xx
x
x
x
x
x
x
x
x
Tintinnopsis baltica
Tintinnopsis beroidea
x
xx
x
xx
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
xx
x
x
x
x
x
Tintnnopsis coxliella
x
Tintinnopsis cylindrica
x
Tintinnopsis fennica
x
Tintinnopsis gracilis
x
Tintinnopsis karajacensis
x
Tintinnopsis laevigata
x
Tintinnopsis lindeni
x
Tintinnopsis lobiancoi
x
Tintinnopsis loricata
x
Tintinnopsis minuta
x
Tintinnopsis nana
x
Tintinnopsis nucula
x
Tintinnopsis parvula
x
Tintinnopsis plagiostoma
x
Tintinnopsis radix
x
x
x
x
x
x
x
x
x
x
x
x
xx
x
x
x
x
x
x
xx
xx
x
x
x
x
x
x
x
x
x
x
x
x
x
xx
xx
x
x
x
x
x
x
x
x
x
x
x
xx
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
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Tintinnopsis cyanthus
xx
x
x
x
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Tintinnopsis rotundata
x
Tintinnopsis sinuata
Tintinnopsis tregoubofii
x
Tintinnopsis tubulosa
x
Undella angustior
x
Undella claparèdei
x
Undella clevei
x
Undella declivis
x
x
xx
x
x
x
x
x
x
x
x
x
xx
x
x
x
x
x
xx
x
Undella hyalina
x
x
Undella ostenfeldi
x
x
x
x
x
x
x
xx
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
Undella subcaudata acuta
Undella subcaudata subcaudata
x
Undella turgida
x
Undellopsis marsupialis
x
x
x
x
x
x
x
x
x
x
x
x
x
x
Undellopsis subangulata
x
Xystonella clavata
Xystonella lohmanni
x
Xystonella longicauda
x
x
x
x
x
x
x
x
x
x
x
xx
x
Xystonella minuscula
Xystonella treforti
x
Xystonellopsis brandti
x
x
x
x
x
x
x
x
x
x
Xystonellopsis cymatica
x
x
x
Xystonellopsis heroica
Xystonellopsis paradoxa
Xystonellopsis scyphium
x
Xystonellopsis spicata
x
x
166
x
x
Xystonellopsis treforti
Total species 216
x
x
Undella mamillata
Undella perpusilla
x
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Undella hemispherica
x
x
55
79
54
65
65
84
69
x
46
42
68
39
38
42
51
305
In pink species present in all lists. In orange species esclusive of the North Tyrrhenian Sea. In light green species present only in the Gulf of Naples. In
grey species present in the Gulf of Milazzo. In light cream species present only in the South Adriatic. In light blue species recorded in the Mid Adriatic
during the SERPA cruises. In yellow species found in Mid Adriatic during the PRISMA cruises (41 50–43 550 N and 16 500 –17 500 E). In brown
species found in Mid Adriatic (42 550 –43 550 N and 13 550 –15 E). In dark green species found in North Adriatic (43 30–45 40 N and 12 300 –13 400 E)
during the VECTOR and SESAME cruises. In blue species reported only in the Gulf of Trieste. For each list in the table are reported latitude and
longitude of the area covered by samplings and the name of project(s) that funded the researches.
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relatively rich and along the water column more abundant at the Deep Chlorophyll
Maximum (DCM). The most abundant species were Acanthostomella conicoides,
Amphorella quadrilineata var. minor, Craterella armilla, Dadayiella ganymedes,
Eutintinnus tubulosus, Salpingella decurtata and the genus Undella. In the same cruise a
comparison between filtered and unfiltered samples was performed at one sampling
station, where it was sampled each 6 h, giving results very different for aloricate ciliates,
particularly for the smallest fraction (nanociliates), but not so diverse for tintinnids [45].
In the same area in July 1995 10 stations were sampled and 25 tintinnids species were
identified [46]. Only 11 of them (A. quadrilineata var. minor, Craterella armilla, C. torulata,
D. ganymedes, Epiplocylis acuminata, Eutintinnus apertus, E. fraknoi, E. tubulosus,
Tintinnopsis compressa, T. tregouboffi, Xystonella longicauda) were reported also in the
1994 cruise, nonetheless sampling was performed in the same month. Abundance was very
low and the dominant species was E. apertus. In two stations dilution experiments on
microzooplankton grazing on microphytoplankton were performed (see later) [47]. In the
same area in November 2002 and May 2003 sampling was performed at six sites
(unpublished data). In respect to previous studies 16 new species for this area were
identified, therefore total species in the Aeolian area account for 79 (Table 1). Tintinnids
represented more than 50% of total microzooplankton abundance (heterotrophic
dinoflagellates included) and were dominated by A. quadrilineata var. minor,
D. ganymedes, Steenstrupiella steenstrupii, A. conicoides and the genus Salpingella.
2.1.3. Adriatic Sea
The review by Coats and Revelante [48] in 1999 reported only sporadic researches in the
Adriatic Sea since the beginning of the 1980s [49–55].
Thereafter there were many cruises under the umbrella of national and international
projects like ASCOP (three cruises in 1983–1984 in the Northern Adriatic), Fertimont (two
cruises in the northern basin in 1986), CNR Strategic Projects (SERPA two cruises in
September 1988 and April 1990 in the Mid Adriatic), ALPE ADRIA (six to eight cruises
per year from 1990 to 1995 in the coastal northern basin) PRISMA Fluxes (1995–1996,
four seasonal cruises along four transects from the northern to the southern Adriatic),
MAT (19 cruises on three transects in the northern basin, 1999–2002) to the more recent
VECTOR and SESAME (two cruises in February and October 2008) (Figure 1).
Data obtained by these efforts were only partially published [56–58] and most of the
papers were devoted more to distribution of total microzooplankton abundance rather
than to community composition. In Table 1 we report all species identified in the different
cruises. All samples, if not specified, were of 5 L volume, filtered on 10-mm mesh net and
fixed in buffered formalin.
2.1.3.1. South Adriatic. Along the southernmost transect (M, 45 300 –45 400 N; 18
300 –19 300 E) crossing the Strait of Otranto during the PRISMA Fluxes project, sampling
was performed on a seasonal basis (May, August, October 1995, February 1996). During
this project samples (2–5 L) collected at 4–10 depths at three stations were unfiltered and
fixed in buffered formalin. A total of 65 species were identified: Stenosemella nivalis
dominated in February and was still abundant in May; in August Tintinnopsis genus and
in October Salpingella genus were prevalent.
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Figure 1. In the map we report the sites where time series were (and are) performed with a red star:
1, Ligurian Sea; 2, Gulf of Naples; 3, Gulf of Milazzo; 4, Ionian Sea; 5, Gulf of Trieste. Marine areas
and islands cited in the text are as well reported. For the Adriatic, besides areas and sites of interest
cited in the text, we reported also the main transects (at Otranto Strait, at the Pelagruza sill, in the
Mid Adriatic, and in the North Adriatic the transect from Senigallia to Susak and from the Po River
mouth to Rovinji as well cited in the text and in Table 1.
2.1.3.2. Mid Adriatic. It is evident the general decreasing trend of species richness from
the southern to the northern Adriatic basin as usually observed for all plankton
components (see [59] and reference therein). However, the richest area in term of
tintinnid’s diversity is the Mid Adriatic (41 500 –43 500 N; 13 550 –17 200 E), where 19 and
36 stations were occupied in September 1988 and April 1990, respectively (SERPA
project). In the two seasons a total of 89 species were registered (Table 1): in September
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tintinnid’s abundance was very low and clearly dominated by Eutintinnus stramentus. Low
values can be attributable to the specific period (the demise of the spring–summer
phytoplankton bloom), but also to the presence of large mucus aggregates in the period
immediately precedent the cruise [60], which strongly impacted this planktonic fraction
[61]. In April 1990, when the cruise covered a larger area of the Mid Adriatic,
microzooplankton, particularly tintinnids, were by far more abundant. The prevalent
species were D. ganymedes, S. steenstrupii and Stenosemella ventricosa, and the genus
Eutintinnus [62]. Overall, hyaline species prevailed in the offshore area, more influenced by
Levatine Intermediate Water (LIW), while along the coast species with agglutinated lorica
were more abundant, thanks to the coastal terrigenous supply, necessary to build up this
kind of lorica [57].
During the PRISMA Project, along the transect H (41 500 –43 550 N; 16 500 –17
0
50 E), crossing the Mid Adriatic from the Gargano Promontory toward Dubrovnik
(Pelagruza Sill), samples were collected (with the same protocol used in the South Adriatic)
at five stations at 5–10 depths. Total identified species were 69 (Table 1): in May at each
station different tintinnids were prevalent (S. nivalis and D. ganymedes in the western
region and Salpingella decurtata and Eutintinnus tubulosus in the eastern part); in August
Eutintinnus apertus prevailed in the western and D. ganymedes and Dictyocysta mitra in the
eastern part; in October E. tubulosus prevailed in two out of the five stations; in February
S. nivalis prevailed in the western and D. ganymedes in the eastern part.
Along the transect E (42 550 –43 550 N; 13 550 –15 E) of the PRISMA project in the
Central Adriatic sampling was carried out at five stations (5–8 depths). Tintinnid’s
richness sharply decreased in respect to transect H (46 species) (Table 1) and at the most
coastal station in February there was an almost monospecific bloom of S. nivalis, which
clearly prevailed also in May. In August S. decurtata dominated all along the transect,
while in October the genus Salpingella was more abundant in the western and the genus
Eutintinnus in the eastern part of the transect.
The transect C (42 550 –43 550 N; 13 550 –15 E) of the project MAT corresponded to
transect E of the PRISMA Project. Sampling was performed at three stations and three
depths at each transect on 19 occasions from June 1999 to July 2002. Samples (5 L) were
unfiltered and preserved in formalin [58]. Numbers of identified species was the same as in
the PRISMA cruises (40 vs. 39) (Table 1), but only partially corresponded to those found
some years before. In summer 2000, species D. ganymedes, Eutintinnus lusus-undae,
Rhabdonella spiralis and Xystonella longicauda, which characterize warm and salty waters,
significantly contributed to the total abundance. Helicostomella subulata and Tintinnopsis
compressa, which were typical of the northern basin in the past and almost completely
absent in previous years, appeared again in summer 2002 [58].
2.1.3.3. North Adriatic. The northernmost transect of the PRISMA fluxes project crossed
the northern Adriatic from Senigallia toward Susak (43 450 –44 250 N, 13 100 –14 100 E).
Here number of species identified at the five stations (three to seven depths) decreased to
39 (Table 1), but abundances were higher than in the rest of the Adriatic, particularly in
summer. In February and May the community was dominated by S. nivalis, in August,
except at the most coastal station were S. nivalis still prevailed, the most abundant genus
was Salpingella, as well as in October, when at the most coastal station Metacylis
annulifera was prevalent.
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In the North Adriatic within the framework of the Project MAT sampling was
performed along two transects (A, B) (44 550 –45 N; 12 300 –13 300 E) at three stations
and three depths at each transect on 19 occasions from June 1999 to July 2002. Transect B
corresponded to the transect B of PRISMA, transect A corresponded to the historical
transect from the Po River mouth to off shore Rovinji, where Croatian researchers are
operating since the 1970s [63]. Samples (5 L) were unfiltered and preserved in formalin [58].
Numbers of identified species was 38 (Table 1), similar to those found during the PRISMA
Project, but only partially corresponded to those found some years before.
Microzooplankton communities sampled at the two transects were dominated by aloricate
ciliates, with the exception of summer 2001 when, all over the basin, heterotrophic
dinoflagellates reached the same densities. Over the entire basin, the most frequent and
abundant heterotrophic dinoflagellates belonged to Gymnodinium/Gyrodinium group and
to genus Protoperidinium (P. diabolum, P. depressum, P. oblongum, P. oceanicum,
P. divergens, P. conicum, P. pyriforme, P. steinii) and Diplopsalis group. In late summer–
fall, Hermesinum adriaticum, a small ebriida, probably a mixotrophic species because of
numerous endosymbiontic cyanobacteria, reached high abundances. Tintinnids were
scarce until autumn 2001 when a significant increase occurred which lasted until January
2002. The species Stenosemella nivalis was present throughout the whole period, more
abundantly in winter. Genus Salpingella characterized summer and autumn. S. steenstrupii
was present in summer [58].
If we sum the species identified in the northern Adriatic during PRISMA and MAT
projects we reach 64 species which is very close to the total findings of the old projects (68)
carried out mostly in the coastal northern Adriatic from ASCOP (1983) to Alpe Adria
project (1994) (45 –45 400 N; 12 300 –13 400 E), but also in this case the lists (Table 1)
only partially overlapped each other. Particularly, in the more recent period, among the
genus Codonella, only C. aspera is reported, while in the past other five species were
recorded. The same is true for the genus Tintinnopsis represented in the past by 11 species,
reduced to three in the 1990s. With regard to the ASCOP cruises, Fonda et al. [56] reported
that in May 1983 the community was mostly constituted by tintinnids (but at that time
heterotrophic dinoflagellates were not yet considered), and the most representative species
was Eutintinnus acuminatus, particularly abundant in the coastal area influenced by the
Po River outflow. In August microzooplankton was more abundant in the easternmore
stations, tintinnids were scarce and the prevalent species was E. lusus-undae. Also in July
1984 higher abundances characterized the eastern part of the basin; tintinnids were as well
scarce and the most representative species was T. beroidea.
The most recent two cruises (SESAME and VECTOR) (43 300 –43 400 N; 12 300 –13
0
40 E) were carried out in February and October 2008, and were characterized by very
poor tintinnid’s communities both as abundances and species richness (Table 1).
Particularly, in February, among the 42 species globally reported, we encountered only
15 species represented by very low numbers. Unpublished results revealed that the late
winter phytoplankton bloom, which characterized the northern Adriatic, was not yet
developed and consequently also predator’s communities were very scarce.
2.2. Time series
In this section we report results obtained during annual or pluriannual monitoring
programmes. Short (1 year) studies provided evidences on temporal tintinnid’s seasonal
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dynamics while longer time series highlighted interannual fluctuations and changes over
time in tintinnid’s community composition. Long time series, as we will see also for the
mesozooplankton, are particularly useful to detect the effects of climate changes, and
particularly of global warming, on zooplankton communities, which proved to be very
sensitive in several different oceanic regions (see [64] and reference therein). As this Author
observed, long time series are rather scarce and never exceeding 50 years, thus strongly
limiting our ability to forecast any possible future evolution of pelagic ecosystems under
different stressor factors (not only global warming, but also pollution, eutrophication,
invasions, etc.). This limitation is more dramatically evident for microzooplankton time
series that are very few and short all over the world.
2.2.1. Gulf of Naples (1997 on)
In the Gulf of Naples first data on microzooplankton date back to 1984–1985 [65], when a
year round survey on microzooplankton collected at the surface was carried out. Three
peaks of abundance were reported (two in spring and one in autumn) corresponding to
phytoplankton blooms, dominated by one or few species. A high variability in tintinnid’s
abundance and fast changes in specific composition of the community were observed as
well. Researches on protists resumed in 1997 with weekly sampling at the surface at the
same fixed station of the previous study and are still going on [66,67]. The first part of the
data set (1997–1999) was analyzed in order to define the abundance and role of
photosynthetic ciliates, which proved to be 49% of total ciliates, heterotrophic naked
choreotrichs and tintinnids contributed 25 and 16%, respectively. Mixotrophic
choreotrichs dominated the ciliate assemblage in spring and summer while the maximum
contribution of autotrophic ciliates occurred in winter [66]. Afterward [67] published in
2002 their results on ciliate’s abundance and composition of a 4-year study at the same
fixed station in the Gulf of Naples. Samples were unfiltered and fixed in formaldehyde in
the first three years and in both Lugol’s solution and formaldehyde in the last year. For
tintinnids no significant differences were observed between the two preservatives, and they
ranged from 0 up to 30.5 103 ind. L1; while naked ciliates constituted 74% of the total
abundance in the Lugol’s samples and only 68% in the formalin samples due to the poorer
preservation of naked ciliates in formalin. Over the 4 years 55 species of tintinnids were
reported (Table 1), among them only 15 were signaled as ‘common’, eight out of the latter
corresponded to the species found all year round in the Northern Tyrrhenian Sea, and only
seven species accounted for 81% of total tintinnid numbers. Species of the genus
Tintinnopsis showed maximum occurrence in early spring, Helicostomella subulata in late
spring, Metacylis annulifera and Eutintinnus tubulosus in summer, Salpingella decurtata in
late summer and S. curta from late summer to autumn.
2.2.2. South Tyrrhenian Sea (2003–2004)
In a southern Tyrrhenian coastal site (Gulf of Milazzo) a 15-month study on tintinnids
was conducted from March 2003 to May 2004 [68]. Samples of 10 L were collected
fortnightly at three depths (surface, DCM and 100 m) and concentrated through inverse
filtration to 200 mL then fixed with Lugol’s solution (2% final concentration). Tintinnid’s
abundance average through the water column was generally 510 ind. L1, with a
maximum of 126 ind. L1 in December at the DCM, and an almost monospecific
Tintinnopsis beroidea bloom at the surface at the end of July 2003. For 54 out of the 67
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311
taxonomic entities identified, Authors were able to reach species level (Table 1). Among
the latter three species (e.g. D. ganymedes, Undella clevei and S. steenstrupii) accounted for
more than 40% of total tintinnids. Diversity (H0 ), calculated on the pooled samples
throughout the water column, varied between 1.3 and 2.3 and was lower in summer.
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2.2.3. Ionian Sea (2003–2004)
Along the eastern coast of Sicily another 15 months study on tintinnid’s temporal
succession was conducted from March 2003 to May 2004 [69]. Methods were the same as
in the Gulf of Milazzo. Here 50% of specimens belonged to four species (D. ganymedes,
S. steenstrupii, Craterella torulata and Stenosemella nivalis) out of the 65 species identified
(Table 1). Diversity (H0 ) was in the same order of the previous study. Two main changes in
species composition were observed, one in spring and the second in the late autumn.
2.2.4. Gulf of Trieste (1986–1992; 1998 on)
In the Gulf of Trieste, the northernmost edge of the northern Adriatic, researches on
microzooplankton date back, as sporadic observations, to 1984 [52]. In 1986 a long lasting
time series began [53] on at least one fixed station (C 1, 45 420 N, 13 420 E) and are still
going on, although there is a 6-year gap (1992–1998). In some years sampling was carried
out in four stations along a coast–off shore transect and the microzooplankton
abundances showed a decreasing trend along the transect [70]. Unfiltered samples of 2 L
were fixed with 2% (final concentration) buffered formaldehyde. Through comparative
analyses it was possible to evidence the negative impact of the mucilage events (1988, 1989,
1991) on the whole microzooplankton [61,70]. The first part of the series (1986–1992) was
analysed by means of cluster analysis and time series analysis (Fast Fourier
Transformation) was applied on each cluster in order to find the (possible) seasonality
of each group. It was possible to identify only two groups with a clear seasonality: one in
winter, mainly composed by tintinnids with agglutinated lorica (Stenosemella–
Steenstrupiella) and the other in summer dominated by hyaline tintinnids
(Helicostomella–Favella–Eutintinnus) [71]. Among the 51 species of tintinnids (Table 1)
globally identified in this area over a time span of almost 25 years, very few can be
considered important: Eutintinnus (E. apertus, E. lusus-undae), Salpingella (S. subconica,
S. rotundata), Stenosemella nivalis, Tintinnopsis (T. beroidea, T. nana) and in the first
period Helicostomella subulata, which almost totally disappeared in the most recent years.
In the second period, beside some exceptional almost monospecific blooms, total
microzooplankton, particularly tintinnids, showed a drastic reduction, compared to the
late 1980s (unpublished data).
2.3. Conclusive remarks on microzooplankton distribution
To summarize this overview of published and unpublished data on microzooplankton, and
particularly on tintinnids, along the Italian coasts we can point out that:
– Total number of identified species accounts for 216, which, compared to 90
species reported by Dolan (2000) [35] for two transmediterranean cruises, results
particularly high. The high number is probably due to the classification mainly
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–
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–
–
–
–
–
based on [72,73], which is still under continuous revision because for many
researchers it is redundant.
Among the 216 identified species (Table 1) only very few were present in all lists,
namely Eutintinnus apertus, E. fraknoi, E. tubulosus, Dadayiella ganymedes,
Salpingella curta, S. decurtata, Steenstrupiella steenstrupii, Stenosemella nivalis,
and often these species dominated each community. Eutintinnus and
Steenstrupiella are considered by [32] cosmopolitan genera; Stenosemella a neritic
and Dadayiella a warm genus. D. ganymedes was considered part of the ‘core’
species in the north-west Mediterranean Sea by [28]: this species was present in the
western, central and eastern Mediterranean [74] and considered a common species
for the Mediterranean Sea [35]. The same is true for S. steenstrupii, S. nivalis,
E. fraknoi, and E. tubulosus [35].
Fifty species out of 167 encountered in the northern Tyrrhenian Sea were
exclusive for this area: among these only Codonellopsis tubercolata and Ormosella
bresslaui were found in all cruises.
Six species were exclusively reported in the Gulf of Naples, namely Proplectella
columbiana, P. ostenfeldi, P. urna; Stenosemella pacifica; Tintinnopsis sinuata,
Undella declivis. During the PRISMA Project one species were reported in the
South Adriatic (Rhabdonella amor); eight species were reported exclusively in the
Mid Adriatic in the late 1980s (Amphorella intumescens, Eutintinnus latus,
E. maculatus, E. turris; Favella composita; Undella mamillata, Xystonella
minuscola) and two during the PRISMA Project (Coxliella ampla, Xystonella
clavata). In the mid Adriatic only Xystonellopsis treforti was exclusively reported
during PRISMA survey. In the northern Adriatic during the recent VECTOR and
Sesame cruises three species were found for the first time (Proplectella urna,
Stenosemella oliva and Xystonella heroica). Only two species (Metacylis cfr
mereschkowskii and Leprotintinnus nordqvisti) were exclusively reported in the
long time series of the Gulf of Trieste.
Overall there is a continuous decreasing trend of tintinnid’s richness moving form
the northern Tyrrhenian all around the Italian peninsula to reach the minimum in
the northern Adriatic. Only in the Gulf of Trieste, where the ongoing survey on
microzooplankton started in 1986, are the species more than 40.
Rarefaction particularly affects Climacocylis, Codonella, Codonellopsis,
Cyttarocylis, Dictyocysta, Ormosella, Parundella, Rhabdonella, Tintinnopsis,
Xystonella and Xystonellopsis genera, that, besides Tintinnopsis, Codonella and
Codonellopsis, are all hyaline genera.
As a general rule hyaline species are more abundant and diversified in off shore
areas rather than in the more coastal sites. In the Adriatic Sea, where, as it was
observed for all planktonic organisms [59], the south–north decreasing trend is
particularly evident, hyaline species are often associated with southern intrusions
of salty waters, deriving from modified LIW.
3. Mesozooplankton and micronekton
3.1. Introduction
Zooplankton is composed by free-swimming animals that live in all acquatic ecosystems.
Marine zooplankton comprises a large variety of different organisms, with some
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thousands of species. Most are small, large only few microns (from flagellates to ciliates),
but some jellyfishes and pyrosomes are one meter large and several meters long.
Mesozooplankton (0.2–20 mm) is constituted by copepods, cladocerans, ostracods,
pteropods and heteropod mollusks, appendicularians, amphipods, chaetognaths, fish
eggs and small larvae together with the older stages of crustacean plankton and
meroplanktic larvae. In the last years, it has become popular to distinguish gelatinous
macrozooplankton (2–20 cm) from other zooplankton. These are the species that have very
large ratios of water to organic matter (often 98% of their wet mass, like jellyfishes, salps,
doliolids, ctenophores). In using the term plankton, we separate the weak swimmers from
more active organisms that swim with sufficient strength to travel despite ocean currents.
It was recommended the term micronekton, to define active pelagic crustaceans and other
forms intermediate between thrusting nekton and feebler-swimming plankton. Within the
size range 2.0–10.0 cm, large decapods (sergestids, panaedids), fish larvae, small adult
fishes, small cephalopods, large euphausiids and mesopelagic fishes, predominate.
Zooplankton occupies a key position in the pelagic food web as it transfers the organic
energy produced by unicellular algae by photosynthesis to higher trophic levels such as
pelagic fish stocks exploitable by man. Animal protozoans, like ciliates, constitute the
summit of the microbial loop, instead copepods and pelagic tunicates constitute the
primary herbivores in the classic food web. Many studies have analysed the distribution
patterns, feeding mechanisms and rates, food selectivity, growth rates, reproductive
biology and vertical migration.
3.2. Patterns of spatial distribution in the Italian Seas
As for microzooplankton fraction in this section we report all data that we were able to
find regarding patterns of mesozooplankton (and micronekton) distribution in the Italian
Seas following a counterclockwise order.
3.2.1. North Tyrrhenian Sea
In the northern Tyrrhenian Sea during the seven cruises carried out within the frame of
MARE project (see section 2) mesozooplankton was collected by vertical hauls form 50 m
depth or from bottom to the surface with a WP2 200-mm mesh size net. Stations sampled
were less than those occupied for microzooplankton, for a total of 140 samples. A total of
107 taxa were identified (68 copepods, 10 tunicates, six cladocerans, five protozoans, three
amphipods, two coelenterates and pteropods, and one each for euphasids, cumaceans,
chaetognathes).
Dominant species however were very few: cladocerans Evadne spinifera, E. nordmanni
and Penilia avirostris in summer, copepods Paracalanus parvus, P. nanus, Clausocalanus
arcuicornis, C. furcatus, C. pergens, C. paululus, and Acartia clausi in spring–summer,
Euterpina acutifrons, and genera Oithona, Oncaea and Corycaeus in autumn–winter. Total
number of specimens ranged from 328 217.6 ind. m3 in December 1989 to
5754 2357 ind. m3 in April 1988. On average biomass as dry weight ranged from
2.36 0.96 mg m3 in December 1989 to 24.16 15.9 mg m3 in November 1986.
Mesozooplankton communities were mostly constituted by fine filter feeders
(e.g. Penilia avirostris, Paracalanus parvus), in spring and autumn herbivores
(e.g. Clausocalanus pergens, C. paululus) increased, while mistivores (e.g. Oithona) were
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better represented in the most neritic areas, carnivores (e.g. Oncaea, Corycaeus) increased
in the northernmost part of the study area [75].
Mesozooplankton biomass and abundance were evaluated in epipelagic waters at 59
stations in the Ligurian Sea during December 1990 [76]. At the end of autumn,
mesozooplankton biomass ranged between 0.80 and 4.24 mg DW m3 and abundance
between 833.8 and 932 ind. m3. Copepods and appendicularians dominated the
mesozooplankton community, the main taxa being the copepods Clausocalanus spp.
(46% of total zooplankton) and Oithona spp. (15%) and the appendicularian Fritillaria
spp. (12%). The bulk of the community was concentrated in the upper 200 m, small
copepods being dominant particularly in the upper 50 m, the copepod community was
more diversified in sub-superficial waters, with a maximum observed in the 200–400-m
layer.
Others zooplankton samples were collected in autumn 1996 from two stations in the
Gulf of Rapallo [77]. At both stations the community was dominated by copepods, mainly
juveniles and adults of different species of Acartia and Oithona, and meroplankton, mainly
polychaete larvae. Total zooplankton abundance was in the harbour waters significantly
higher than in the nearby bay. Acartia grani was recorded for the first time in this area.
3.2.2. South Tyrrhenian Sea
Aeolian Islands waters (SE-Tyrrhenian Sea) were sampled in July 1994 and July 1995 by
BIONESS multinet system in order to study zooplankton abundance, distribution and diel
vertical migration of some key species from surface to 2000-m layer depth [78]. Copepods
were found to be the most common zooplankters, being Clausocalanus arcuicornis,
C. furcatus, Corycella rostrata, Corycaeus latus, Temora stylifera and Centropages typicus
the core coastal species. Relationship between larval fish biomass and plankton
production in the coastal waters of South Tyrrhenian Sea was studied by Bruno et al.
[79]. Ichthyoplankton standing stocks peaked in February (6.28 g m2), preceding the first
primary production peak and the spring maximum of mesozooplankton biomass in May.
A relevant contribute to the knowledge of mesozooplankton distribution and composition in the south Tyrrhenian Sea was given by Scotto di Carlo et al. [65], during an entire
year of observations at a fixed station in the Gulf of Naples. Zooplankton community
showed during the sampling period large and frequent quantitative variations, as biomass
(11.87 7.58 mg m3 wet weight) and abundance (2108 2270 ind. m3). For both parameters, three peaks were registered: from May to June, from July to September, and from
October to November. Zooplankton was always dominated by copepods with 90 identified
species that represent 77% of the community. Their percentage decreased only during the
enhancement of cladocerans in summer and of appendicularians in autumn. A clear
seasonal variation in zooplankton composition was evidenced. During winter, when there
were low abundances (1161 ind. m3), the relevant organisms were Oikopleura spp., the
copepods Clausocalanus paululus, C. furcatus and Centropages typicus, Cirripeda and
Decapoda larvae, that all togheter were the 42% of the entire community. In spring the total
density increased (up to 21140 ind. m3), and among the copepods, that reached 90% of
total mesozooplankton, the most abundant species were: Acartia clausi, Oithona similis,
C. typicus, Clausocalanus pergens and Paracalanus parvus. During summer, P. parvus
increased and in July it was the 55% of the entire community. Annual peaks of abundance
were showed by Clausocalanus jobei, Centropages kroyeri, C. ponticus and Oithona
longispina. At the end of August started to increase Temora stylifera, while the total
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copepods decreased and the cladocerans increased, particularly Penilia avirostris and
Evadne tergestina. In autumn the abundances were similar to those registered in spring
(up to 1866 ind. m3). Important were the copepods P. parvus, T. stylifera, C. furcatus and
the appendicularians Oikopleura spp. and Fritillaria pellucida.
An oceanographic cruise was carried out around the Egadi Islands, a central
Mediterranean key region, where zooplankton was sampled by BIONESS at 12 sites,
located along inshore–offshore sections in front of Sicily coastline and crossing throughout
Marettimo, Favignana and Levanzo islands.
Spatial diversity patterns of copepod’s assemblage were examined using species
richness and Shannon-Weaver diversity indices. A total of 109 copepod species were
identified. Four major copepod assemblages were identified by cluster analysis, differing in
species composition and abundances in relation to the depth. They seemed to be correlated
to the different water bodies. In fact there were identified four different water bodies from
chemical physical parameter analyses [80]. In the entire study area, the copepod
abundances were markedly lower than those reported for other regions of the
Mediterranean Sea, but the species richness was very high.
Zooplankton sampling was carried out between Capo Milazzo and Capo d’Orlando
during April and May 1968 along the Tyrrhenian coast of Sicily [81]. It was showed the
predominance of Cladocerans that were always about the 80% of the total community,
represented by Evadne spinifera ed E. tergestina. Copepod species recorded mainly
belonged to the genera Sapphirina and Pleuromamma, appendiculiarns to the genus
Oikopleura and siphonophores to the genus Dyphies.
Six chaetognatha species (Sagitta bipunctata, S. minima, S. enflata, S. lyra,
S. serratodentata and S. exaptera) have been found in 28 zooplankton samples collected
during the month of August in the South Tyrrhenian Sea [82]. The bathymetric
distribution of these species in the 0–100-m layer has been correlated to their biology.
S. exaptera findings in surface waters, have suggested the presence of deep water coming
from the Straits of Messina.
Within the research programmes concerning the qualitative and quantitative composition of DSL (Deep Scattering Layer) in the Western Mediterranean Sea, a total of
47 samples were collected in February–March 1972 in the Algero-Provencal Basin and in
the Central Tyrrhenian Sea [83]. A total of 11 species were detected, which showed a
diversified composition related to the different water masses structure. Three species
dominated in both areas: Euphausia krohni, Nematoscelis megalops and Thysanopoda
aequalis. In the deepest hauls N. atlantica took a dominant role. In the Algero-Provencal
Basin euphausiids reached a mean biomass of 1.15 g WW/1000 m3, while in the
Tyrrhenian Basin the biomass was lower (0.94 g WW/1000 m3).
Stomach content analysys was carried out on squid Todarodes sagittatus caught montly
in the coastal waters off Aeolian Islands: on a total of 20 prey items, 17 species were
identified [84]. Three main groups of organisms dominated the diet: cephalopods (41%),
fishes (38%) and crustaceans (21%).
3.2.3. Strait of Messina
The Mediterranean is a semi-closed basin, which communicates with the Atlantic Ocean
through the Strait of Gibraltar. The low depth of this channel (320 m) involves that only
epipelagic species, or those with wide vertical migrations, can enter into the Mediterranean
basin. Some time ago Colosi [85] showed faunistic relationships between Mediterranean
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and Atlantic seas. In the zoogeography of the Mediterranean Sea, the Strait of Messina
plays a role of primary importance as an area of passage and a point of contact between
water masses having different origins. From the time of Vercelli [86] and Vercelli and
Picotti [87] to today, physical oceanographic studies have concurred in affirming that the
Strait of Messina must be considered another path of communication between the eastern
and western basins of the Mediterranean and a site of intense and complex hydrodynamic
phenomena. Tidal and upwelling currents are the principal factors that determine the
structure of the zooplankton and micronekton communities. In fact, mixed with the typical
Tyrrhenian and Ionian waters (the former being warmer and less salty than the latter),
there are the Atlantic, Middle-East and deep waters that reach the more superficial layers
in certain parts of the Strait. Among the different masses of deep water, there are the
‘Levantine Intermediate Waters’ (LIW) which originate in the eastern basin and spread
throughout the rest of the Mediterranean in the water layer between 200 and 700 m. To
complicate this environment there is a series of collateral effects caused by the
superimposition of the stationary currents.
On numerous occasions, it has been pointed out that physico-chemical studies alone
are not sufficient to identify these bodies of water, while more precise indicators can be
provided by the study of the biological ‘indicator communities’. Starting with Russel [88]
and applied subsequently by Furnestin [89,90] in the Mediterranean, this concept has been
extended on a number of occasions to the area of the Strait of Messina with the study of
taxonomic groups suitable for this purpose (Copepoda, Chaetognata, Euphausiacea,
Mollusca Pteropoda). If one adds that the intense hydrodynamism and the turbulence of
the waters hinder the establishment of a clear thermocline even in summer, one can
appreciate the complex ecological factors that determine the vertical and seasonal
distribution of the communities. Many species indicated as ‘rare’ in the Mediterranean
reach significant concentrations of individuals in the Strait of Messina (e.g. Krohnitta
subtilis, Oikopleura rufescens, Folia gracilis), which identify this area as a zone of
‘accumulation’ that produces a subsequent ‘insemination’ of the neighbouring Tyrrhenian
and Ionian areas. In fact, it is common to find deep species at the surface and viceversa, or
open-sea species along the coast. It remains to be seen whether this phenomenon is
transitory or if, and in what way, some species that undergo a bathymetric inversion adapt
to the environment of the Strait of Messina, which with its ‘mixed’ waters assures an
annual thermic regime that is, on average, cold.
Stranding mechanisms of mesopelagic fishes in the Strait of Messina have been
reported first by Mazzarelli [91] and successively defined by Genovese et al. [92]. In the
1960s and 1970s, their taxonomic lists was updated and expanded including also other
species of fishes [93–96], zooplankton crustaceans [97–99], pelagic molluscs [100] and
cephalopods [101,102]. More than 41 species of meso- and bathypelagic fishes were
collected, including many species of migratory and non-migratory fishes, among which
Argyropelecus hemigymnus, Myctophum punctatum, Hygophum benoiti, Vinciguerria
attenuata and Cyclothone braueri. Long ago, Currieri [103,104] noted that, in some
zones of the Strait, there were accumulations of plankton on account of the coastal
counter-currents, while Lohman [105–107], studying the vertical distribution of the
appendicularians, concluded that the currents of the Strait had a great influence on the
spatial and vertical distribution of the organisms. They noted that some species were
subjected to a passive transport, first to the surface in the area of divergence and then to
deeper layers in the zone of convergence, essentially along the Ganzirri-Punta Pezzo sill.
Marini [108] also studied the distribution of plankton in relation to the currents.
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The passage of these waters into the Strait of Messina [109] leads one to infer that this
area is one of the paths of communication of deep-water copepod populations between
the eastern and western parts of Mediterranean. This is theoretically possible since the
Mediterranean lacks a deep planktonic fauna and its place is occupied by species of
mesopelagic waters which have a wide vertical distribution [110]. The upper limit of the
range of distribution of these species inhabiting the deep Mediterranean is within
the vertical extent of the Middle-East intermediate waters. The possibility of transit of the
deep-water species, both through the Strait of Messina and the Sicilian Channel, is
further shown by the uniformity of population structure found throughout the entire
basin of the Mediterranean [111]. The presence of deep-water copepod species in the
Strait of Messina, found in samples still being studied, could greatly confirm these
observations.
The zooplankton and micronekton communities, which can be found in the Strait of
Messina are very similar to the communities present in the eastern Mediterranean.
Together with the ubiquitous, meso- and bathypelagic species, such as Gennadas elegans,
Sergestes robustus, Sagitta lyra, S. hexaptera, Lensia conoidea, etc., the majority of species
that form the faunal populations of the Strait are of subtropical origin, which exhibit
maximum abundance in the eastern part of the Mediterranean (Stylocheiron suhmi, Sagitta
serratodentata, Krohnitta subtilis Cavolinia gibbosa gibbosa, Hyalocilix striata, Sergestes
vigilax, S. corniculum, etc.). This confirms the homogeneity of the Mediterranean fauna,
with a clear differentiation, in addition to that between East and West, between the
northern and southern parts of the Mediterranean [112]. In fact, the most common species
in the Strait of Messina have a southern distribution, while the northern ones are similar to
those present in the western sector of the Mediterranean. This is the case of Sagitta setosa,
a northern species of Atlantic origin, well represented in the northern Adriatic Sea, which
are not able to enter the Strait of Messina at the southern entrance [113]. The few reports
in the Strait of species of Atlantic origin, often identified in the nearby Tyrrhenian waters
influenced by the branch of the Atlantic current that laps the Sicilian coast before flowing
North, are due to the already low abundance of such species in the Mediterranean (Diacria
trispinosa, D. quadridentata, Thysanoessa gregaria, Centropages chierchiae, Limacina
bulimoides, L. lesueuri). The biological role of the ‘Lusitanian’ currents remains to be
clarified, in view of the fact that forms considered rare in the Mediterranean, such as
Cymbulia peroni and the jellyfish Solmissus albescens assume a certain ecological
importance in the Strait of Messina [114,115].
The knowledge about the ecology of the zooplankton and micronekton of the Strait of
Messina is until today scarce and fragmentary. The impossibility of adopting strategies
suitable for an environment with such a high hydrodynamism has limited the knowledge of
the spatial and vertical distribution of the species, of their daily migrations and of the
influence of the frontal zones on planktonic production. Really, much information about
the discovery and biology of the most common copepod species of the Strait of Messina
has been furnished by Crisafi and co-workers [116–128], mostly based on sampling
performed on the surface at a fixed station off Ganzirri. Later, some oceanographic
campaigns were carried out in order to collect samples down to 800 m in depth
[96,113,115,129–131], and a series of dives were made with the mesoscaphe vehicle ‘F.A.
Forel’ by J. Piccard [114,115]. In this way, it has been possible to study the zooplanktonic
and micronektonic fauna and in particular the behaviour of the mesopelagic fishes in their
natural habitat.
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3.2.3.1. Siphonophora. From 1940 to the present, no studies have been carried out
specifically on this group of zooplanktonic organisms, even though findings of
siphonophores in the Strait of Messina were rather frequently reported between 1850
and 1935 [132–143]. The last study of the biogeography of the Mediterranean, in which
there was specific reference to the Strait of Messina, was made by Bigelow and Sears [144]
who examined the material from the Thor campaigns (1908–1909 and 1910). It was
essentially from these studies that the list of species of siphonophores found in the Strait
was compiled. Other more recent studies on the distribution of the zooplankton have
confirmed some of the previous findings [115]. At the present, there are 19 species divided
among 14 genera. The first record of Amphicaryon acaule in the Mediterranean comes
from the Thor campaign, in which a single individual was found in the Strait of Messina
(Location 282). The only place in which Vogtia pentacantha reaches the surface is the Strait
of Messina [144], and this exceptional fact leads one to infer that also the larval stages, like
the life of the adult, take place in deep waters.
3.2.3.2. Pelagic Mollusca. Following the first reports of the genus Corolla in the Strait of
Messina [145–148] compiled a preliminary list of pelagic molluscs (Hyalea tridentata,
H. gibbosa, H. depressa, H. cuspidata, Creseis spiniformis, Atlante keraudreini, A. peroni).
Later Issel [149] after examining the material collected in the Strait by Luigi Sanzo,
provided a systematic revision of the Atlantidae (Oxygyrus keraudreni, Protatlanta sculpta
var. mediterranean, Atlanta peroni, A. lesueri, A. inflata, A. fusca); the same author
described Carinaria lamarki. Mazzarelli [150] reported the presence in the Strait of Messina
of Fiona marina and Janthina communis, which behaved as predators when there were
great quantities of the siphonophore Velella spirans. From the data on strandings of
pelagic gastropods [93,151–153], from the stomach contents of mesopelagic fishes [154],
from the list of molluscs found in the Strait [155], from collections with ORI-NET 1.6 [115]
from the Thor campaign, and from the monograph of [156] the number of species
recovered in the Strait of Messina today is 35.
3.2.3.3. Copepoda. The copepods in the Strait of Messina have been studied since the
second half of the eighteenth century. In 1863, while studying the copepods of the
Mediterranean, Claus [157] found many new species in the Strait of Messina, on account
of the peculiar hydrological characteristics of the area. He created the genus Hemicalanus
in which he described five species: H. plumosus, H. mucronatus, H. filigerus, H. longicornis
and H. longicaudatus. In 1898, he replaced this genus with Haloptilus. Among the other
new species found at Messina by Claus [157] were: Ichthyophorba violacea (which
suggested been replaced by Centropages violaceus), Pontella mediterranea (indicated at first
as Pontellina mediterranea), Euchirella messinensis, Pleuromamma gracilis, Candacia
longimana, Paracandacia bispinosa, Sapphirina auronitens, S. nigromaculata and Oithona
spinirostris. After the work of Claus there was a long interruption of the study of copepods
in the Strait of Messina, which lasted until 1958 when it was taken up again by Crisafi.
This author was interested, until 1976, mainly in the development and morphology of a
number of copepod species from the Strait of Messina. Crisafi and Mazza [158] completed
a revision of the genus Sapphirina, which in the Strait comprises 16 out of 17 species of the
genus. Crisafi [159] discovered three new species of copepods, among which was
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Acartia josephinae, found for the first time in the port of Milazzo. Subsequently, this
species was found in the Strait of Messina and in other areas of the Mediterranean.
Further studies on copepods in the Strait of Messina described the trophic relations
between copepods and the two mesopelagic fishes, Hygophum benoiti and Myctophum
punctatum, from analyses of the stomach contents of fishes stranded along the coast of
some areas of the Strait [154]. Recently, there have been some studies on the short-term
variations of the population structure of copepods in relation both to the tidal cycles in the
Strait of Messina and to the daily nyctimeral migrations [160]. From this data, it has been
possible to determine in which way the above-mentioned variations of the zooplankton
influence the daily feeding rhythm of juvenile specimens of Lithognathus mormyrus in an
area close to the Strait of Messina [161]. From all the studies carried out in the Strait of
Messina, 132 species of copepods have been recorded, out of the 480 present in the
Mediterranean. This difference in number is due mainly to the fact that the studies
conducted in this area have been on a spatio-temporal scale that is not entirely adequate
for the complete monitoring of all the species whose presence and absence might alternate
during the course of successive seasons.
3.2.3.4. Mysidacea. Sars [162] and Zimmer [163] started to study the mysids in the Strait
of Messina, while Colosi [164] provided the first systematic list of the group. To date, there
has been no research aimed exclusively at this group. The reports of its presence derive
from studies of the feeding habits of mesopelagic fishes [154], strandings [98] and
collections with ORI-NET 1.6 [115]. Although at the present there are records of 15 species
from 11 genera, it is thought that the list could be considerably lengthened. Lophogaster
typicus is the only species found stranded with a certain frequency, although even then
only a few individuals. Riggio [165] examined 10 specimens of L. typicus from sampling
carried out in the Strait of Messina and noted some slight differences between them and
the type species.
3.2.3.5. Amphipoda. Riggio [165] cited the finding of Phrosina semilunata and Platyscelus
ovoides, while Senna [166] reported that, in the plankton of Messina, there could be found
a large number of species of amphipods hyperiids, which Lo Bianco [167,168] listed for the
first time in the Mediterranean on the basis of abyssal collections carried out by the ‘Maia’
and the ‘Puritan’ in the Gulf of Naples. Subsequently, Crisafi [169] provided a list of
species, limited to the zooplankton samplings carried out at the fixed location of Ganzirri.
Later, the taxonomic list was up-dated with the addition of meso- and bathypelagic species
found stranded [98], and above all it was enriched by information about their behaviour
[114] and vertical distribution [115]. Really, the amphipods hyperiids constitute an
important component of the mesopelagic fauna of the Strait of Messina. At the present,
the list numbers 35 species divided into 24 genera, which preferentially occupy the layer
between 300 and 500 m. Some species perform vertical migrations up to 100 m, while
Vibilia armata and Platyscelus serratulus seem to exhibit marked aggregations in the subsuperficial waters. Great quantities of Phronima sedentaria have observed in the barrels of
tunicates. Their importance in the pelagic food web of the micronekton is shown by the
large number of species and individuals found in the stomach contents of the two most
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abundant mesopelagic fishes of the Strait of Messina, Myctophum punctatum and
Hygophum benoiti [154].
3.2.3.6. Euphausiacea. The importance of euphausiids as active vehicles of energy transfer
along the water column, from the surface to the bottom, as well as an important direct
food source for many fishes of high commercial value, have led many researchers to be
interested in this group of crustaceans for a very long time. The first list of species found in
the Strait of Messina was compiled by Claus [170] and was subsequently revised by Thiele
[171]. The former author was the first to describe Euphausia krohni as E. muelleri. A more
accurate study of the taxonomy and distribution was made later by Colosi [164,172]. From
the collected material, the same author described two new species, based on only a few males
for E. messanensis [172] and some females for Meganyctiphanes calmani [164,173].
E. messanensis was attributed to the ‘gibba’ group, with a clear resemblance to
E. hemigibba, from which it is distinguished by the peculiar conformation of the antennal
peduncles, by the presence of a simple pre-anal spine (instead of bidentate) and by the
greater length of the median lobe of the male copulatory organ (the petasma) with
respect to the internal lobe. However, since E. messanensis has not subsequently been
found in the Strait of Messina, it is now considered to be a dubious species. With regard
to M. calmani, it has been demonstrated, first by Ruud [174] and subsequently by
Costanzo and Guglielmo [175], it is a juvenile form of M. norvegica, as seen by the
morphology of the thelycum.
Today in the Strait of Messina, there are 12 of the 13 species present in the
Mediterranean. In fact, only Nyctiphanes couchi has never been collected from the Strait,
even though this species has been reported very close in the Ionian Sea [174,176]. The most
abundant species are M. norvegica, Thysanopoda aequalis, E. krohni, N. megalops.
M. norvegica was cited frequently [164,165,171], while T. aequalis was mentioned [164,174].
The former species prefers waters with a temperature between 3 and 15 C for its
reproduction, which might explain its abundance in the Strait of Messina (Harbour,
S. Raineri), where it can be observed also in enormous swarms, sometimes found stranded
from November to April [97,98]. M. norvegica and E. krohni are also the two most
abundant species in the diet of M. punctatum and H. benoiti [154]. Stylocheiron maximum
has been captured during dives with the deep-diving vehicle ‘F.A. Forel’ between 400 and
560 m [114]. In samplings carried out with ORI-NET 1.6 at night, down to a depth of
800 m, E. krohni was found to be the most abundant species between 100 and 300 m, while
Nematoscelis atlantica was most abundant from 500 to 800 m [115]. Among the indicator
species of Atlantic waters, Thysanoessa gregaria has been found in the Tyrrhenian Sea
close to the Strait of Messina, although in a limited number of individuals [177], while the
species of eastern origin, such as S. suhmi, are more abundant [177,178]. Diversity and
vertical diel migration of euphausiids in the South Tyrrhenian Sea and North Ionian Sea,
across the Strait of Messina, were studied by Brancato et al. [179]. The maximum
sampled depth by BIONESS was 2030 m. A total of 5801 specimens of juvenile and
adult euphausiids, belonging to 11 species, were found and species composition of the
two basins was related. Nematoscelis megalops and Euphausia krohni were the most
common specie in the Ionian Sea-Strait of Messina area, while in the South Tyrrhenian
Sea Thysanopoda aequalis, E. hemigibba and Stylocheiron abbreviatum were the dominant
species.
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3.2.3.7. Pelagic Decapoda. Thiele [171] referred to samplings at Messina in which
Pasiphaea sivado was present, while, in the list of decapods in the Strait, Riggio [165]
enumerated 20 females of P. sivado (including three ovigerous ones), in addition to
Gennadas elegans and Sergestes robustus. P. sivado was also found stranded [91]. Among
the species of Acanthephyra, Riggio [165] reported that A. purpurea and A. eximia were the
two species that could most easily be collected in the Strait of Messina. Magrı̀ [180] cited
A. eximia very infrequently in the waters of Augusta (Ionian Sea).The list of pelagic
decapods species was up-dated and lengthened with the studies on strandings [98] and
stomach contents [154] and with the ORI-NET 1.6 collections [115]. At the present, there
are 13 species from eight genera. Gennadas elegans is found stranded in abundance in the
month of March, while it is common between 500 and 800 m in nocturnal sampling in the
Strait of Messina. Both Cocco [181] and De Natale [182] referred to strandings of
Sergestes arcticus at Messina, adding that this species is not very common. Riggio [165]
described a specimen deriving from sampling carried out in the Strait. S. robustus can be
found stranded in abundance from November to April, often with S. corniculum. The
length of the individuals is between 50 and 60 mm. S. corniculum was reported in the Strait
of Messina for the first time [98]. It is common in nocturnal samplings carried out between
100 and 300 m in depth, and the mean length of the individuals is about 46 mm [115].
Numerous individuals of S. vigilax with a mean length of 25 mm for males and 28 mm for
females, can be found stranded. A certain resemblance to S. vigilax was found by Riggio
[165] in a specimen coming from Messina and called by him S. aracnopodus De Natale
(ex Cocco). It had earlier been referred by Thiele [171] to the arcticus group and was
assigned definitively [183] to S. arcticus, particularly on account of the form of the
petasma. However, among the same group of crustaceans, Riggio [165] found a
mastigopus stage of 18 mm belonging to S. vigilax. Among the species of Sergestidae
found in the Strait of Messina, S. vigilax and S. arcticus were recorded in the Thor
sampling, and the latter species also in the Atlantis II campaign (May–June 1969), while
Gennadas elegans has been collected in the adjacent Tyrrhenian and Ionian waters. With
regard to their geographical distribution, it can be seen that there is a ‘melange’ of
northern, ubiquitous and subtropical species, with an abundance of both cold-water
(G. elegans) and warm-water ones (S. robustus) [112].
3.2.3.8. Chaetognatha. Numerous reseaerchers [184–187] turned their attention to this
group for their taxonomic and histological studies. Among them Grassi [185] discovered
some new species in the material deriving from the Strait of Messina: Sagitta inflata,
S. minima, Krohnitta subtilis. Ghirardelli [188] reported biometric data from 30 specimens
from the Strait, with which he developed the concept of ‘hydrological indicators’.
Furnestin and co-workers [89,90,189] attributed to some chaetognathes (such as Sagitta
serratodentata and Krohnitta subtilis) a role of primary importance in the recognition of
the water masses that pass through the Strait of Messina. The most recent work was [113],
in which the spatial abundance distribution of various species in the Ionian and
Tyrrhenian basins and the influence of the currents on the vertical distribution of the
species were discussed. To date, nine species of chaetognathes from two genera have been
found. Sagitta bipunctata and S. inflata are the most common species, while those that
characterize the special nature of the Strait, on account of their close link with the water
masses that pass through the area, were S. minima, S. neodecipiens and K. subtilis. The first
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species is characteristic of waters of the continental shelf while the other two are indicative
of deep waters that reach more superficial levels near the entrance.
3.2.3.9. Appendicularia. The first study of the appendicularians in the Strait of Messina
was by Fol [190], who discovered three new species of Oikopleura (O. dioica, O. fusiformis,
O. rufescens), four new species of Fritillaria (F. formica, F. haplostoma, F. megaschile,
F. urticans) and new genus Kowalevskia represented by the species K. tenuis. The same
author stated that the difficulty with this group was mainly the great morphological
variety of the different species. Later Lohman [105–107] carried out valuable studies on the
contributions of appendicularians in relation to the currents passing through the Strait of
Messina from the Ionian and Tyrrhenian Seas. Lohman [105] reported at Messina 27 of
the 36 species of appendicularians found in the Mediterranean. This group was ignored for
many years. However, given the great variability of species and a reasonable biomass, the
appendicularians constitute an important fraction of the total zooplankton of the Strait of
Messina. In 1979 a study of this group in the hydrographic area of the Strait was carried
out, utilizing a WP2 net with a 200-mm mesh. In all samples from three sampling
campaigns (in April, July and November), including the two neighbouring areas of the
Ionian and Tyrrhenian basins, 22 species were identified, belonging to three families:
Oikopleuridae, Fritillaridae and Kowalevskiidae. The total number of individuals was
4188 (2520 Oikopleuridae, 1665 Fritillaridae and three Kowalevskiidae). However, if only
the data from sampling locations in the Strait are considered, the number of species drops
to 17, and these had a different abundance in the three sampling periods. If only the
variations in percentage among the families in the 3 months are considered, one can
observe the small percentage of Kowalevskiidae (1%), represented only in July, whereas
the highest percentage of Oikopleuridae (89%) occurred in April and that of the
Fritillaridae (70%) in July. With regard to the distribution of the species in the three
periods the major part of Oikopleuridae was constituted by O. intermedia in April and in
July and by O. longicauda in November, followed by O. intermedia. The dominant species
of Fritillaridae in April and even more in July was F. pellucida, while in November this
species was slightly outnumbered by F. borealis f. intermedia.
3.2.4. Ionian Sea
An oceanographic cruise, named ‘INTERREG Italia-Grecia’, was carried out in the
northern Ionian Sea, in March 2000. The samples were collected up to a 600 m depth, by
the electronic multinet BIONESS, off the Apulian Italian coast. The purpose of [191], was
to study the spatial distribution, the abundance and the composition of fish larvae in the
northern Ionian Sea. A total of 46 early stages of teleosts, belonging to 38 genera and 22
families, were collected. Over 52% of the larvae identified were mesopelagic species,
almost 27% were demersal and about 21% pelagic. A total of 307 myctophids, 69 clupeids
and 61 gadid post-larvae dominated the community. Benthosema glaciale (mean 6.1 mm
SL) was the most abundant species (21.6%), the most frequent in the samples (28.8%),
dominant in the whole study area (mean 1.4 ind. 100 m3). A more detailed study was
carried out on horizontal and vertical distribution and abundance of the three dominant
postlarval species: Benthosema glaciale, Sprattus sprattus sprattus and Notoscopelus
elongatus.
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The displacement volume, wet weight, dry weight and abundance of zooplankton
samples were analysed in the coastal waters of the Ionian Sea in August 1970 [129].
Cladocerans, copepods and appendicularians constituted the main part of the total
biomass. Cladocerans were represented by Evadne spinifera, E. tergestina and Penilia
avirostris. The distribution of this last species was considered in relation with a passive
transport in more diluted waters.
During POP-EOCUMM 1995 oceanographic cruises, zooplankton was collected in
the southern Ionian Sea by multinet BIONESS [192]. The earlier life stages of fishes
were sorted and studied to characterize their horizantal and vertical distribution.
Gonostomatids Cyclothone braueri and C. pygmaea, mictophid Myctophum punctatum
and sternopycthid Argyropelecus hemygimnus were the most abundant species.
In the frame of the Project Cluster 10 (SAM) a characterization of the hydrological and
chemico-physical features of the Marine Protected Area ‘Isole Ciclopi’ (Ionian coast of
Sicily) has been performed during 2003 [193]. Montly sampling included the study of
phyto- and zooplankton communities. Richness and dominance reflected links between
coastal and pelagic systems.
A study on the effect of the changes in circulation (named EMT, Eastern
Mediterranean Transient) observed in the eastern Mediterranean, starting from 1988 as
a transient effect of climate forcing on mesozooplankton of the Ionian Sea, was carried out
by Mazzocchi et al. [194]. A temporal comparison was performed on data obtained in the
springs of 1999 and 1992, periods characterized by opposite patterns in the upper
circulation that in 1998 reversed from an anticyclonic to a cyclonic gyre. Interannual
differences were observed in the distribution of mesozooplankton abundance in the upper
layer that might be related to the EMT dynamics and the effects of the reversed
circulation. In 1999, abundance and composition of epipelagic mesozooplankton differed
between the northwestern and eastern areas of the Ionian Sea. The distribution of species,
trophic groups and copepod gut pigments suggested that different pelagic food webs took
place at the opposite sides of the basin. A ‘classic’ food web prevailed in the northwestern,
more productive area, whereas the microbial loop prevailed in the eastern, more
oligotrophic area. The characteristics of the northwestern area may in large part be due to
the enrichment effects of the cyclonic circulation enhanced by the nutricline uprise due to
the EMT, and to the interaction between the cyclonic circulation and the continental slope.
3.2.5. Adriatic Sea
About 600 papers were listed in 1979 [195] on zooplankton taxonomy, distribution and
seasonal dynamics in the Adriatic Sea; now, we think, the number has been increased by at
least other two hundreds scientific works.
3.2.5.1. Biomass distribution. The standing stock of zooplankton in the Adriatic Sea has
generally been measured using vertical hauls (WP2) from above bottom in the shallow
northern Adriatic and near shore areas and from 50 m to surface in the other regions.
Little is known about the zooplankton biomass of the deep southern Adriatic basin.
Benovic et al. [196] indicated that zones of generally high biomass were located in the
northern Adriatic including the Gulf of Trieste, with average dry weight of over 14 mg m3
and an ash-free dry weight (AFDW) of about 12 mg m3. The estimates of zooplankton
biomass in near shore waters along the eastern coast, with the exception of some bays
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like Kastela [197], gave mean values below 10 mg m3 dry weight and below 8 mg m3
AFDW. Significantly higher values were recorded along the western coast [198], except
during lower river outflows, when maximal values were located in the eastern part of the
basin [199]. Generally higher values are linked with areas characterized by increased
phytoplankton biomass and production (areas influenced by the River Po plume and the
SW region approaching the Strait of Otranto). During winter [200] found a high
zooplankton standing stock in the region above the Jabuka trench. In April of 1990 high
values of biomass (12 mg m3 AFDW) were observed in the South Adriatic trench [59].
Generally the biomass of net-zooplankton decreases from the northern to southern
part and from coastal to open waters.
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3.2.5.2. Mesozooplankton communities. The characteristic distribution of mesozooplankton in the entire Adriatic Sea was described by Hure and co-workers [201–204] and can be
summarizes as follow:
(1) The number of species belonging to the mesozooplankton increases along the
north–south gradient (e.g. from 30 species of copepods encountered regularly in
the Gulf of Trieste [205,206] to more than 130 in the southern part [201]; three
species of chaetognatha in the northern part and 9–10 in the southern part
[207,208], four species of calicophora in the north and 22 in the south [207], nine
species of appendicularians in the north and 27 in the south [209] etc., with
cladocerans an exception, being better represented in the northern area [210].
(2) It is possible to distinguish three communities of copepod fauna [201], which
characterize the different areas of the Adriatic Sea i.e. estuarine, coastal and
oceanic.
(3) Concerning mesozooplankton as a whole [199] identified four characteristic
associations:
(a) a northern coastal association characterized by strictly neritic species, low
diversity, clear prevalence in summer of Penilia avirostris and during the rest of
the year of Acartia clausi which can spread to the southern areas inside the
20-m bathymetry line;
(b) a neritic central one which includes the whole central area south of the
Ravenna–Lussino transect; still characterized by neritic species and by an
increase in the percentage of Paracalanus parvus;
(c) an offshore central association, which can include in some seasons the whole
southern area as far as the South trench, which is characterized by a high
diversity, the presence of P. parvus and the increase of ‘oceanic’ species [201];
and
(d) a southern oceanic association, present only in autumn–winter, confined to the
South trench, characterized by a high faunistic paucity, probably due to the
depth of sampling (from 50 m to surface) which does not include any deeper
community [59].
3.2.5.3. South Adriatic. During the PRISMA Fluxes project (see section 2) vertical hauls
from a 50 m depth to the surface with a WP2 standard net were carried out at the same
stations investigated for microzooplankton.
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In the southern Adriatic (Otranto Strait) a clear westward decreasing gradient was
evident in all seasons except in August 1995 when at the easternmost station
mesozooplankton community resulted more abundant. In May 1995 copepods Oithona
and Oncaea dominated the community and only at the easternmost station, the thaliacean
Salpa fusiformis prevailed. In August Penilia avirostris and Temora prevailed at the
western side, while Centropages, Oithona and Corycaeus in the eastern one. In October
Oncaea was the most abundant genus, followed by Paracalanus parvus, Clausocalanus,
Oithona and the larvacean Oikopleura. In February 1996 P. parvus was the dominant
species, Oncaea was still abundant as well as Clausocalanus, Acartia clausi, Oithona and in
the eastern part the larvacean Fritillaria.
Observations on euphausiids vertical distribution in the Southern Adriatic deep sea
waters were carried out in July 1974 by IKMT trawl net [211]. A total of 11 species were
found, being Stylocheiron maximum the most abundant in the samples.
3.2.5.4. Mid Adriatic. Also, along the Palagruza transect the westward decreasing
gradient was observed with the only exception of February 1996 when the central station
was the richest. As along the most southern transect copepods Oithona and Oncaea
dominated the community. In August P. avirostris was the most abundant organism in the
western part of the transect, followed by the mollusk Creseis acicula, the larvacean
Oikopleura and the thaliacean Doliolum.
In the northernmost transect in the central Adriatic the westward decreasing trend was
even more evident, without any exception. The dominant species in all seasons was
P. parvus. P. avirostris and Evadne spinifera dominated in summer 1995 and along the
Italian coast P. avirostris still in October, in May A. clausi, Oithona, Oncaea and
particularly at the eastern end of the transect the thaliacean Salpa fusiformis became more
important. In August, beside cladocerans, other dominant species were Clausocalanus,
Temora stylifera, A. clausi and Oncaea. In October Clausocalanus, T. stylifera and Oncaea
prevailed. In February 1996, beside P. parvus, Oithona, Oncaea and Euterpina acutifrons
were abundant.
Within the framework of the PRISMA II Proiect, four oceanographic cruises were
carried out in the northern and central Adriatic Sea from June 1996 to March 1997 [212].
Samples were collected both by BIONESS electronic multinet (204 samples at 54 sites) and
by WP2 (101 samples at 19 sites) along inshore–offshore sections. In early June, copepods
and cladocerans represented on average 52 and 20% of the zooplankton community,
respectively, while in late summmer they represent 17 and 66%. During late spring–
summer, the cladoceran population was dominated by Penilia avirostris which in some
coastal sites costituted more than 90% of the total zooplankton. Copepod’s population
was characterized by low species diversity and the clear dominance of Acartia clausi,
Paracalanus parvus and Temora stylifera (73% of the population). Because of their spatial
distribution patterns, Pseudocalanus elongatus and Temora longicornis, typical of estuarine
environments, can be considered as hydrological indicators species of different water
masses of the Adriatic neritic system.
3.2.5.5. North Adriatic. Surprising the decreasing gradient was no more evident in the
northernmost transect of the PRISMA Fluxes Project, only in October 1995 the most
abundant mesozooplankton community corresponded to the westernmost station.
P. parvus was again one of the dominant species, but in this area cladocerans
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(namely P. avirostris and Evadne) were by far the most abundant species in August and
October. In May Clausocalanus, Acartia and Oithona were abundant, particularly in the
central and eastern stations. In October Oncaea was very abundant in the western station.
In February 1996 Oithona and Oikopleura dominated the community (Fonda Umani,
unpublished data).
Two oceanographic cruises were carried out in the northern Adriatic Sea, in June 1996
and February 1997 [213]. A total of 504 samples on 54 stations were collected along
inshore–offshore sections by BIONESS electronic multinet. Zooplankton abundance and
biomass both in the northern basin (mean 2787 1735 ind. m3; mean DW
29.3 26.7 mg m3) and in the southern basin (4698 5978 ind. m3 and
25.4 15.3 mg m3) were estimated in relation to the variability of temperature, salinity
and fluorescence. Zooplankton community was constituted essentially by copepods,
cladocerans, appendicularians and larvae of invertebrates.
On all three transects investigated between June 1999 and July 2002 during the MAT
project (see section 2), mesozooplankton temporal evolution showed a regular pattern with
maxima in the late spring–summer (with evident dropping off in June 2000 and May 2002)
and autumn–winter minima. Total mean integrated abundances were very similar on
transects A and B, whereas on C they significantly decreased, particularly during the
summer peaks. Summer maxima were particularly relevant in 2001 when they exceeded
14,000 ind. m3. In June 2002, high abundance registered on the transect B was due to a
heterotrophic dinoflagellate Noctiluca scintillans bloom. A less intense bloom of
N. scintillans was registered on transects A and B also in April–May 2001. In the entire
basin, copepods prevailed over the entire period, with the exception of summer. Most
abundant species throughout the year were Paracalanus parvus, Acartia clausi, Oithona
similis, Ctenocalanus vanus and Temora longicornis; while in spring and particularly in the
last year Calanus helgolandicus became relevant. Cladocerans, namely Penilia avirostris,
were dominant in summer. Their prevalence was significantly more important in summer
2001 and in the northern part of the basin, whereas in summer of 2000 and 2002 their
swarming started only in July instead of May–June and was less intense, due to the
presence of large mucus aggregates. Generally cladoceran’s contributions in total
abundance decreased southwards [58].
Mesozooplankton community composition at the species/taxa level was investigated
on a monthly base from January to December 2001, at eight stations in the northern
Adriatic Sea [214]. Annual dynamics, taxonomical composition and spatial diversity in
relation to different trophic conditions were discussed as related to previous studies and to
different conditions, such as the presence of mucilage events occurred in other years.
Zooplankton communities all over the northern sub-basin were dominated by the
cladoceran Penilia avirostris in summer, and by the calanoids Paracalanus parvus, Acartia
clausi and the poecilostomatoids Oncaea during the rest of the year. While coastal
communities were more variable with time and location, it was possible to identify a group
of offshore stations with a similar species/taxa composition and annual dynamics.
Significant changes in community composition in the time scale of 20 years were observed,
mostly due to a general decrease of A. clausi as dominant species, being replaced by
P. parvus. Also, P. avirostris swarms appeared to have extended their temporal occurrence
and were present for longer periods of time when compared to past records. These changes
might be related to the observed general increase of the average temperature in the
northern Adriatic Sea.
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3.3. Time series
All over the world long time series on zooplankton are the result of multidecadal
monitoring programmes. Continuation of these time-series in the past has been extremely
difficult at times. During the 1980s, 40% of the marine time-series that were initiated after
World War II were discontinued because monitoring was viewed as poor science by
administrators and many scientists. Monitoring programmes have experienced a renaissance since the 1990s, because it has been realized that long-term datasets are key to
documenting and understanding impacts of climate change. We are fortunate to have the
long-term zooplankton timeseries that we do, the result of the persistence and vision of
individual scientists decades ago. We must be aware when interpreting the impacts of
climate change that almost all zooplankton timeseries are no longer than 50 years in
duration. A truly integrated marine observing system needs to have a strong biological
component, otherwise it will run the risk of being able to detail future physical and
chemical changes but be unaware of biological consequences [64]. Only collecting all
information available at the different trophic levels is possible to recognize climate signals,
and only after a more or less long time lag. Obviously the first analyses always rely on local
environmental conditions or changes, both natural and anthropogenic. We need much
more time to realize the biological response to large scale events driven by climatic
changes. Recently, Conversi et al. [215] were able to identify a climate shift, which
occurred in the late 1980s all over the European Seas, on the base of a large data set
spanning from hydroclimate to ecological parameters. The shift affected the pelagic
community (as indicated by plankton, jellies, fish, mucilage, red tides, anchovies) in the
western and eastern Mediterranean basins, and was paralleled by analougus dramatic
changes in the North Sea, Baltic Sea and Black Sea.
3.3.1. Ligurian Sea
Year to year variations in abundance and composition of zooplankton were studied in the
Ligurian Sea, by twice monthly sampling at a fixed station between 1985 and 1995
[216,217]. These papers mainly focus on the numerical approach used to analyse
zooplankton variability and its relationship with physical and climatic factors. STATIS
method was chosen instead of time series analysis. A strong seasonal variation was evident
for most species and the years 1987, 1992 and 1994 were different from the others.
Trajectories indicated which species were stable and which were characterized by small or
large fluctuations during the 9 years.
3.3.2. Gulf of Naples
The research team at the Zoological Station ‘A. Dorhn’ in Naples has for many years been
involved in studying the inter-annual variations of the planktonic communities in the Gulf
of Naples [65,218–223]. Zooplankton sampling was carried out from 1984 to 1990 in
surface waters (0–50 m) at a coastal station in the Gulf of Naples [222]. Total zooplankton
abundances followed repetitive annual patterns throughout the study period. Minimum
abundances were always recorded in winter ranging from 223 ind. m3 in 1988 to
491 ind. m3 in 1987. The highest numbers occurred in spring and summer with a
maximum abundance of 11,148 ind. m3 in 1984. High numbers of cladocerans regularly
occurred in summer (up to 84% of the total), while planktonic tunicates were always more
abundant in winter, represented mainly by appendicularians Oikopleura dioica and
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Fritillaria spp., constituing more than 45% of the entire zooplankton community in
december 1984. A total of 125 copepod species was identified. The main species were
Paracalanus parvus, A. clausi, C. typicus and T. stylifera followed by O. similis, C. paululus,
C. furcatus, P. nanus, O. media, F. rostrata and C. pergens.
In the review of Ribera d’Alcalà et al. [224], temporal variations of plankton biomass
and abundance were analyzed together with the underlying abiotic dynamics at a fixed site
in a coastal area of the Gulf of Naples, which has been monitored for 14 years in the
period 1984–2000. The main aim was to depict general patterns in the seasonal evolution
of phyto- and zooplankton populations and inter-annual trends. Results confirmed that
the magnitude of phytoplankton and zooplankton peaks and their timing may vary from
year to year but the different phases of the annual cycle are recognizable with a high degree
of reliability. The winter and autumn blooms are very likely related to large-scale
meteorological events, whereas late spring–summer blooms are local phenomena being
driven by lateral advection of nutrients and biomass from coastward sites. Diatoms and
phytoflagellates dominated for the largest part of the year. Mesozooplankton increased in
March–April, reaching maximum concentrations in summer. Copepods were always the
most abundant group, followed by cladocerans in summer. A remarkable feature is the
regularity in the succession within all the compartments of plankton. The abundance and
timing of occurrence of each species may change from year to year and some species also
apparently disappear in some years. At inter-annual scale, a high variability and a
decreasing trend were recorded over the sampling period for autotrophic biomass.
Mesozooplankton biomass showed a less marked inter-annual variability. The regularity
in the occurrence of species against the quantitative inter-annual variability suggests that
biological rhythms regulate the temporal dynamics of the communities, whereas the
abiotic forcing modulates the amplitude of the growth phases. This stresses the need for
studying the biological variability at the organism level, taking into account the functional
morphology and the life strategies of the single species [225–228]. On the basis of the latter
concept, the climatology and inter-annual variability of winter phytoplankton was more
recently analyzed at the Long Term Ecological Research Station Marechiaro (LTER-MC,
Gulf of Naples) using data collected from 1985 to 2006 [229]. Blooms were most often
determined by colonial diatoms such as Chaetoceros spp., Thalassiosira spp. and
Leptocylindrus danicus. In recent years, the same authors observed more modest and
sporadic winter biomass increases, mainly determined by small flagellates and small noncolonial diatoms. Physical and meteorological conditions apparently exert a strict control
of winter blooms, hence significant changes in winter productivity can be foreseen under
different climatic scenarios.
3.3.3. Gulf of Trieste
Much of our knowledge on the Gulf of Trieste mesozooplankton is owed to the monthly
time series collected at station C1 since early 1970s. This is the longest lasting zooplankton
collection in Italy and one of the longest in the Mediterranean Sea, providing a picture,
spanning more than three decades, of the mesozooplankton species composition, its
diversity, and its temporal variability.
The mesozooplankton community in the Gulf of Trieste is characterized by a few
(approximately 30) coastal and estuarine species, which in turn can exhibit high
dominance. Copepods dominate in all months except from June to September, when
cladocerans (especially Penilia avirostris) take over [230]. In particular, the calanoid
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copepod Acartia clausi is dominant for most of the year, comprising at some points480%
of the total biomass, according to Fonda Umani [231], followed by P. avirostris, which can
account for 437% in summer. Other species of copepods like Oithona, Clausocalanus,
Temora, Paracalanus, and more recently Oncaea, can be considered relevant [58,232–235].
First studies on this time series have focused on group associations. Cataletto et al.
[230] found, during the first decade of study (1970–1980), a regular late spring–summer
appearance in a group characterized by Acartia clausi and Temora longicornis, and a
regular autumn–winter appearance in a group characterized by Temora stylifera and
Oncaea spp. Two main groups related to spring–summer and winter–autumn prevalence
are also identified [235], who find several differences in patterns of abundance between
1970–1980 and 1986–1999 and attribute them to climate changes (NAO, ENSO, EMT,
SST increase) in the northern hemisphere from 1987.
Recently, Conversi et al. [236] have indicated that the zooplankton community in the
Gulf of Trieste is undergoing a number of changes between the two periods 1970–1987 and
1988–2005, with a circa doubling in total zooplankton abundance accompanied by a shift
toward smaller species, the arrival/increase of southern species (Diaixis pygmoea,
Paracalanus parvus), the rise (Oncaea spp., Oithona spp., and Euterpina acutifrons) or
decline (Pseudocalanus elongatus, Clausocalanus spp.) of several taxa, and changes in the
phenology in several species, with predominantly forward shifts in the timing of the
maximum peak. Forcing factor appeared to be sea water temperature, which increased
after 1987 particularly in summer and autumn.
Copepod long time series is accompanied by an almost analogous long lasting series of
records of mesozooplankton biomass (as dry weight – DW). Kamburska and Fonda
Umani [237] analysed this time series and found a shift in the annual and winter mean
temperature in 1977–1978, which provoked a shift in the DW in the 1979 to a lower level.
The subsequent regime was marked by higher means of mesozooplankton descriptors
during the second half of the 1980s, with agreement with the temperature shift (after 1987).
The large-scale seasonal variability at interannual and multi-decadal scale of mesozooplankton standing stock in the Gulf of Trieste is linked to the shifts in mesozooplankton
taxonomic structure, phytoplankton composition and hydro-climatic component
(temperature and NAO). Altered seasonality of mesozooplankton biomass could be
seen as a response to modified environmental conditions in the Gulf caused by the regime
shifts in phytoplankton dynamics, and hydro-climatic signal, especially during the
1990–2000s. A high variability of carbon and nitrogen contents of mesozooplankton DW,
and the C:N ratio was constrained to seasonal fluctuations and forced by phytoplankton
taxonomic structure alterations and water temperature. Over all the plankton communities
of the Gulf of Trieste revealed to be very sensitive to climate changes, because of the
shallowness, the land confinement, and the high latitudinal position of this area, which
represents the northernmost bay of all Italian seas.
4. Processes
In the most recent years Italian researches devoted more efforts in measuring biological
processes under the increasing need to understand pelagic food web dynamics rather than
only to elucidate temporal or spatial distribution of one or another planktonic component.
The final aim of this kind of researches was most of the time to evalute Carbon fluxes
flowing through the pelagic food web, from bacteria up to mesozooplankton.
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4.1. Microzooplankton (and heterotrophic nanoplankton) predation
Due to the intrinsic difficulty of separating predator and prey when they belong to the
same size class, to estimate microzooplankton (and heterotrophic nanoplankton) grazing
in the last decades Italian researchers have used the dilution method [238] in different
areas. The method relies on the modulation of the contact rates between predators
(microzooplankton and heterotrophic nanoplankton) and preys (autotrophic and heterotrophic prokaryotes and nanoplankton, and microphytoplankton). To do so, natural
water samples are added with increasing proportions of pre-filtered seawater, thus creating
a dilution series. Grazing rate is then estimated as the increase in apparent prey growth
rate (i.e. prey abundance over time) with increasing dilution (i.e. decreasing predator’s
abundance). Predator’s grazing rates are calculated from the slope of the regressions of the
apparent prey growth rate at different dilutions vs. the dilution factor. Growth rate of the
prey is estimated as apparent growth rate extrapolated to 100% dilution (i.e. the growth in
absence of grazers [239]. Apart from the classic method, which monitors chlorophyll
concentration [240], microscopical counts of micro-nanoplankton and prokaryotes were
used in the experiments [19,47,241].
4.1.1. Gulf of Naples
Between 2004 and 2008 eight dilution experiments were carried out in the Gulf of Naples
[240]. In this case the ‘classical’ Landry and Hasset method was applied, using chlorophyll a
concentration to follow phytoplankton growth over time. Furthermore, chlorophyll size
fractions as well as diagnosis of phytoplanktonic pigments (via HPLC) were assessed.
Microzooplankton consumed most of phytoplankton daily production, between 40 and
92% in stratified water column conditions and more than 100% of PP in winter.
Grazing rates were independent of Chl a concentrations at 51 mg Chl a L1, whereas a
significant negative correlation was found at higher concentrations.
4.1.2. South Tyrrhenian Sea
Two experiments were carried out during the cruise around Aeolian islands in July 2005
using on the deck incubations of 24 h. Analyses were performed on microphytoplankton
and nanophytoplankton preys by using inverted microscopy [242]. In both experiments
microzooplankton and its possible preys were very scarce. Nonetheless it was possible to
detect microzooplankton grazing, mostly on the smaller size fraction (5–20 mm) (small
dinoflagellates, prymnesiophytes and nanophytoplankton). Grazing rates varied from 0.32
to 1.77 mg C L1 d1. Daily grazing rate (0.31 d1 g 1.85 d1) was higher than phytoplankton growth rate (0.14 d1 k 1.48 d1), indicating a strong top down control.
4.1.3. Gulf of Trieste
In the Gulf of Trieste 21 dilution and grazing experiments were simultaneously run on a
seasonal basis from November 1998 to August 2005. Incubations lasted 24 h at in situ
simulated conditions. For the experiments of grazing the cladocerans Penilia avirostris was
used as predator in summer and the copepod Acartia clausi for the rest of the year.
Individual grazing rates were extrapolated to the entire zooplankton community [19].
In these experiments all possible microzooplankton preys were considered: auto- and
heterotrophic bacteria, auto- and heterotrophic nanoplankton that were analysed at the
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epifluorescent microscopy; microphytoplankton at the inverted microscopy [241].
Microzooplankton ingestion rates on microphytoplankton (mostly small diatoms) were
negligible in eight experiments but exceptionally reached 173.6 mg C L1 d1 in summer
2000; generally in this season ingestion was ca 4 mg C L1 d1. On average, grazing rates on
microphytoplankton were higher in winter, decreased in spring and summer and raised
again in autumn. Microzooplankton ingestion rates and microphytoplankton biomass was
significantly linearly related.
On average, microzooplankton grazing on microphytoplankton exceeded that of
mesozooplankton in winter, whereas in spring in most of the experiments mesozooplankton was more efficient than microzooplankton, in summer and autumn the scarce
microphytoplankton was mostly consumed by micrograzers.
Microzooplankton grazing on autotrophic nanoplankton (AN) was not registered in
four experiments and ingestion rates ranged from 0.05 mg C L1 d1 in winter 2004 up to
39 mg C L1 d1 in spring 1999. A significant linear regression was found between
microzooplankton ingestion rates and AN biomass. Ingestion rates of mesozooplankton
were highly variable on AN, from negligible amounts in several occasions up to
74.3 mg C L1 d1 in spring 2002 and the regression against AN biomass was not
significant.
Microzooplankton ingestion rates on total autotrophic fraction (comprising autopicoplankton, see later) varied from 0.4 mg C L1 d1 in autumn 1999 to 183.5 mg C L1 d1
in the anomalous summer 2000, accounting for a removal of the total autotrophic standing
stock variable form 0% in winter 1999 to 4200% in spring 2000. The percentage removal
of primary production varied from 1.1% in autumn 1999 to 4200% in winter 2000 and
2003, in spring 2000 and in summer 2002. The linear regression between microzooplankton
ingestion rates and total autotrophic biomass was highly significant.
Ingestion rates of mesozooplankton on microphytoplankton were undetectable in four
experiments and ranged from 0.08 mg C L1 d1 in winter 2003 up to 358.37 mg C L1 d1 in
the anomalous summer 2000.
Mesozooplankton consumed autotrophic biomass and primary production in percentages varying from 0.01% in spring 2004 up to4200% in spring 1999 and summer 2000 and
from 0.06% in winter 2004 to 4200% in summer 2005, respectively.
In four out of the seventeen experiments simultaneously performed mesozooplankton
was more efficient than microzooplankton in consuming primary production (PP) and
autotrophic standing stock (winter 1999, spring 1999 and 2002, summer 2005) but, on
average, it removed 76% of the PP, while the mean removal by microzooplankton was
4100%. Mean removal of the autotrophic standing stock was 50% for mesozooplankton
and 66% for microzooplankton.
Predation on the heterotrophic nanoplankton (HNF) by the sole microzooplankton
was sporadic and ingestion rates ranged from 0.2 mg C L1 d1 in autumn 1998 to
4.8 mg C L1 d1 in spring 2000. Cyanobacteria were an almost constant component of
microzooplankton diet (directly or through HNF ingestion, see later), and ingestion rates
varied from 0.22 mg C L1 d1 in autumn 2000 up to 28.2 mg C L1 d1 in summer 2001.The
linear regression between ingestion rates and cyanobacterial biomass was highly
significant.
Heterotrophic bacteria always appeared to be grazed by microzooplankton and
ingestion rates ranged from 2.2 mg C L1 d1 in winter 2000 up to 66.9 mg C L1 d1 in the
anomalous summer 2000 and, as a general rule, ingestion was higher in summer. In this
case the relationship between ingestion rates and heterotrophic picoplankton biomass was
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not linear but followed the Frost equation, indicating possible food saturation at
about 30 mg C L1.
The impact of the sole HNF was assessed on both autotrophic and heterotrophic
picoplankton by removing through filtration all larger organisms. HNF ingestion rates on
cyanobacteria ranged from negligible amounts up to 38 mg C L1 d1 in August 2001 and
they were higher in summer and very low in winter. There was a significant linear
regression between HNF ingestion rate and cyanobacterial biomass, slightly higher than
the one found for microzooplankton ingestion rates. In almost all experiments
microzooplankton ingestion rates were higher than those of HNF, indicating a direct
impact of microzooplankton on cyanobacteria, with the relevant exception of August 2001
when the high (the highest of the entire data set) HNF ingestion was significantly reduced
by microzooplankton predation on HNF.
HNF grazing on heterotrophic bacteria was always detected and ranged from
1.15 mg C L1 d1 in winter 2000 to 53.8 mg C L1 d1 in autumn 2000. Maxima were
regularly registered in summer but only in winter were grazing rates relatively low. Also in
this case the relationship between HNF ingestion rates and bacterial biomass followed the
Frost equation, indicating the same possible food saturation, but it was less significant
than the one found for microzooplankton. In 13 out of the 21 experiments simultaneously
carried out, microzooplankton ingestion rates on heterotrophic bacteria were higher than
those registered for HNF alone, indicating a direct grazing of microzooplankton on this
prey and particularly in all summer experiments. On the contrary, on six occasions the
grazing impact of HNF on bacteria was reduced by microzooplankton predation on HNF.
Only in one case (April 2004) was more or less the same ingestion rate in both experiments
assessed.
Mesozooplankton always integrated its diet with microzooplankton: ingestion rates
varied between 0.02 mg C L1 d1 in spring 2004 up to 40 mg C L1 d1 in autumn 2003 and
generally they were lower in winter and higher in summer. In twelve experiments it was
possible to detect HNF secondary production: in particular, in all winter experiments,
when it spanned from 0.21 up to 30.61 mg C L1 d1, in two spring experiments, in three
during summer and only one in autumn, with values comprised in the range of winter
variability. Microzooplankton secondary production was observed only in nine experiments, in particular in all summer ones when it varied between 1.44 and 5.32 mg C L1 d1.
4.2. Mesozooplankton
4.2.1. Grazing
The marine zooplankton structure complexity, as biodiversity and large size range of
organisms, leads to a large variety of trophic behaviours inside this community. Within the
food web, zooplankton indeed occupies more than one level and organisms of the same
species can simultaneously belong to different trophic levels. The link between the first and
second level of the food web is represented by the grazing of herbivores on algae [243]. The
variability of trophic factors, linked to the food particle quantity and quality, plays a key
role on the structure and association patterns (on different temporal scales) of
zooplanktonic communities. On the other hand, grazing controls and regulates
phytoplankton abundance and diversity. Only in the presence of a zooplanktonic
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community with a large size range of dominant species can an equilibrate repartition of
different taxa and sizes of phytoplankton be established
Main attention must be given to grazing mechanisms and rate estimation in the main
‘filter feeding’ taxa, like copepods, euphausiids, salps and appendicularians.
In marine ecosystems copepods represent the highest percentage of total zooplanktonic
biomass, mainly in superficial layers, where the food particle spectrum is in accordance
with trophic behaviour of these filter feeders. Copepods are mainly herbivorous, even if
they feed also on microzooplankton and non-living particulate organic matter. On filtering
mechanisms of different species there is more than one hypothesis, that follow: (a)
copepods are passive filter feeders that feed on all the material that they can capture in a
determinate water volume [244]; (b) copepods operate selective grazing on particles with a
selection determined by the ‘porosity’ of filter apparatus [245]; and (c) copepods are
‘opportunistic’ species, not operating any selection but filtering the food particles,
particularly the algal cells inside a dimensional range [246]. Copepods can select their food,
discriminating among different types and sizes of the particles. Poulet and Marsot [247]
demonstrated the presence of chemical receptors in Acartia clausi. The same flexibility that
many copepods show in respect of variations of physical and chemical parameters, is
shown also in respect to variations of particulate food structure, composition and density.
Any species has its peculiar feeding behaviour that can show more than one method of
food use in relation to food availability and features.
Euphausiids are crustaceans very important in pelagic food webs. Their peculiarity to
effect wide vertical migrations, plays an important role in the energy flux from superficial
layers to the bottom. Much information has been gained from stomach content analysis.
But it is very difficult to obtain quantitative information because present in the stomach
are only the remains of ingested organisms that cannot be identified, being damaged by
oral appendixes and by the stomach walls into organic shapeless material. Detritus as well
can be found in the stomach content, due to the resuspension caused by pleiopods
movement. Other information on euphausiids trophic behaviour can be taken studying the
oral and thoracic appendixes morphology. Studies carried out by Mauchline and
co-workers [248–251] illustrated the feeding behaviour of many euphausiids.
Meganyctiphanes norvegica is an omnivorous-predator, the three Mediterranean species
of Euphausia (E. krohni, E. brevis and E. hemigibba) are omnivorous-filter feeders. Species
of the genera Nematoscelis and Stylocheiron are carnivorous, by a mechanism named
‘encounter-feeding’, for which the predator after touching the prey capture them within the
oral appendixes. Also euphausiids, like copepods, show more than one type of
alimentation, adapting themselves to food availability between an herbivorous and an
omnivorous or carnivorous diet [248].
Another group of organisms, that are also filter-feeders, are the tunicates, like salps
and appendicularians. They extract the food particles from the water current produced by
pharynx movement. First in situ observations on salps feeding behaviour was carried out
by [252] that measure filter rates as high as more than 100 mL1 animal1 min1. Tunicates
operate an important feedback on phytoplanktonic communities by high population
development rates, high filtering rates and by the capacity to reconstruct immediately the
filtering apparatus (10–300 s) if obstructed. Studies on filtering rate of appendicularians on
natural phytoplankton populations were carried out by [253]. Oikopleura dioica filtering
rate ranged from 100 to 204 mL1 animal1 d1. As for the salps, their peculiarity is the
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capability to reconstruct the filtering apparatus in a few hours. Furthermore, there is a
continuous ‘rain’ of mucus aggregating small planktonic organisms.
Regarding grazing rate estimation methods, it must be underlined that a global method
that provides information on the different filter-feeders categories in natural conditions
simultaneously does not exist.
Among the most used techniques to estimate grazing rates there is the incubation
method which is applied mainly for large copepods rather than for small organisms or
gelatinous herbivorous, like salps or appendicularians. The grazing rate during the
incubation period, generally less than 24 h, is calculated by estimating the decrease of algal
cell number or of the chlorophyll concentration [244]. But in using the incubation
technique there are some doubts about the real in situ situation. This step is solved by
methods applied to herbivorous organisms directly taken from their natural environment.
Mackas and Boher [254] proposed a grazing estimation method studying the chlorophyll
concentration variations in the stomach content of copepods and the ‘transit times’
throughout the stomach of the ingested material. The gut fluorescence technique is widely
used for the measurement of in situ grazing rates of zooplankton [255–257]. This technique
is quick and inexpensive and provides relatively accurate estimates of in situ ingestion
rates. The method requires three assessments: the gut pigment content of recently captured
animals, the gut clearance or evacuation rate and the measure of gut pigment destruction.
All these parameters, that can be determined fluorometrically, give ingestion rates of
zooplankton and daily ration estimates of autotrophic carbon. Chlorophyll a and
phaeopigment values per individual were calculated with the equations of Strickland and
Parsons [258] modified by Conover et al. [255] and expressed as total pigments
(ng pigm. ind.1). When using the gut fluorescence technique to estimate grazing, several
assumptions must be addressed. Firstly the results from the experiments are assumed to be
a reflection of in situ feeding rates. The specimens used for the analyses are collected often
at depth and, although they are healthy, the capture, barotrauma and confinement in
container may affect the feeding behaviour of the animals [259]. Secondly, the method for
the gut evacuation experiments relies on the assumption that each individual reflects the
feeding of the population as a whole.
4.2.1.1. Tyrrhenian Sea. A study on natural grazing by copepods in Italian waters was
carried out by Guglielmo et al. [260] that allowed them to correlate the filtration and
ingestion rates with the initial concentration of phytoplankton. Not all of the algal species
were ingested, but there was a selection operated by copepods linked to the initial density
of the autrophic species. The main group predated was diatoms, mainly the genus
Chaetoceros. A very low selection was shown in respect to the algal cell sizes. For example,
small species like Nitzschia closterium, N. seriata, Navicula sp. and Thalassionema
nitzschioides were not preferred by the selected copepods, instead species larger but more
abundant in the community were selected. This relation between predation and food
availability was confirmed by filtering and ingestion rate which, at the different stations,
showed different values linked to the different phytoplankton density. For the species
Centropages typicus it was estimated to have a filtration (F) rate of 1.45 mL1 ind.1 h1
and an ingestion (I) rate of 9.3 mm3 106 ind.1 d1 (0.65 mg C ind.1 d1); for
Clausocalanus parapergens 3.00 mL1 ind.1 h1 and 26.3 mm3 106 ind1 d1, respectively
(1.37 mg C ind.1 d1);
for
Clausocalanus
furcatus
4.23 mL1 ind.1 h1
and
3
6
1 1
1 1
30.2 mm 10 ind. d , respectively (1.47 mg C ind. d ). Andreoli et al. [261] report
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results on grazing rates of unselected zooplankton populations. Zooplanktonic community
fed with diversified grazing not only on diatoms or on the more abundant species but
mainly on dinoflagellates and coccolithophores. The grazing rate was logically lower than
those found by Guglielmo et al. [260] because of the choice of an unselected population
which included the presence of carnivorous specimens, with respect to a population
constituted only by copepods and copepodites.
4.2.1.2. Gulf of Trieste. In the Gulf of Trieste, Fonda Umani and Cocchietto [233]
performed a series of eight grazing experiments on a monthly basis, by using Acartia clausi
as predator. Copepod diet was mainly constituted by small phytoflagellates (euglenophytes, prasinophytes, dinoflagellates) and small diatoms (e.g. Skeletonema, Chaetoceros).
Filtration rates varied from 2.78 to 7.8 mL1 ind.1 h1, ingestion rates from 0.245 to
1.534 mg C ind.1 d1. The lowest rates were measured in December and the highest in July.
Both rates correlated with food availability following the [244] equation. Successively, on
the same fixed station in the Gulf of Trieste, a series of 21 dilution and grazing experiments
were simultaneously run on a seasonal basis from November 1998 to August 2005 on
natural assemblage [19] (see in the section 2).
4.2.2. Respiration
For many years the global CO2 cycle, its accumulation and segregation in the ocean and
the role of marine organisms has been a main topic of high scientific interest. All abiotic
and biotic compartments are involved in the transport and/or transformation of Carbon.
Zooplankton, particularly, plays a fundamental role in the transport of C between
different compartments along the water column in the ocean and to the remineralization of
Particulate Organic Carbon (POC) [262–269]. In the marine environment the primary
source of the Particulate Organic Matter (POM) is the autotrophic carbon-fixing
phytoplankton [270]. POM cycling in the ocean’s interior is controlled by the interaction of
physical, chemical and biological forces [271]. Many organisms use this material as food,
reducing its availability as depth increases. Only 10% of surface POM reaches the
sediments, while the main part is consumed and remineralized into new biomass along the
water column by microrganisms, zooplankton and nekton [266,272]. In the oceans, with
the death of plants and animals, residues are accumulated as POM that is added to the
waste products of all marine organisms, like faecal pellets or exuvie. Determination of
zooplankton community respiration provides a useful indication of secondary production
and of Oxygen and C utilization. Zooplankton passively participates in the C vertical flux,
contributing with their spoils, molting products and with waste and excrement to the
formation of non-living POC [273]. On the other hand, zooplankton is actively involved in
the C flux in oceans. Many species show vertical day–night migrations: in order to avoid
predators during the day when they would be visible and attacked, they move downward,
while at night toward the surface to feed on phytoplankton. This phenomenon plays a key
role in the C cycle, being in large part responsible of the C transfer from the surface to the
bottom, where this element is stored [266]. Zooplankton that have fed on phytoplankton at
the surface during the night will then in turn be preyed upon by carnivorous zooplankton
or fish, transferring C to deeper layers. Zooplankton has also a role in the remineralization
of C: for the formation of its esoskeleton, it assimilates C from POC, reducing the vertical
flow of organic C and converting non-living C in living structures.
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Direct determination of O2 consumption in animals from deep-sea net hauls is usually
impossible due to extensive physical damage sustained during capture and retrieval [274].
A specific and highly sensitive indirect method to evaluate the zooplankton respiration and
the C requirement from the sinking flux is the estimation of the mitochondrial and
microsomal respiratory Electron Transport System (ETS) activity as respiration rate [274–
277]. The ETS, as indicator of organic matter remineralization, consists of a complex chain
of cytochromes, flavoproteins and metabolic ions that transports electrons from
catabolized foodstuffs to O2. The rate-limiting step is the oxidation of the coenzyme
Q-cytochrome B complex and it can be measured by its reaction with the artificial electron
acceptor 2-(p-iodophenyl)-3-(p-nitrophenyl)-5-phenyl tetrazolium chloride [275]. This
enzymatic transport is influenced by various factors, such as temperature, salinity, and
sexual stage [278–280], even if the adaptations to environmental conditions are possible
[281]. High and low ETS values of the zooplankton samples may indicate growing or
declining populations, or the beginning or end of a bloom. The relationships between
respiratory activity and growth, reproduction, crowding and starvation have been largely
demonstrated [282] as well as the strong correlation between ETS activity and in vivo
respiration [84,274,283,285,286].
The activity as a measure of potential respiration and C demand is currently estimated
according to [266,271,274,275,285] and calculated by the following equation:
ETSassay ðmL O2 gwwt1 h1 Þ ¼ Acorr HS60=1:42 Wft,
where Acorr is the absorbance of sample at 490 nm corrected for blank and reagents, H is
the homogenate volume (mL), S is the reaction mixture volume (mL), 60 to convert
minutes to hour, 1.42 is the conversion factor of INT-formazan into O2 as mL, W is the wet
weight of the incubated sample (grams), f is the volume of the homogenate in the assay
(mL) and t is the incubation time (min). Zooplankton samples during the ETS analysis are
incubated at a determined temperature, but all final activities are recalculated for in situ
temperature with the Arrhenius equation, assuming activation energy (Ea) of
13.2 kcal mol1 for bathypelagic zooplankton [287]:
ETSin situ ðmL O2 gwwt1 h1 Þ ¼ ETSassay eððEa=R
ð1=Tassay 1=Tin situ ÞÞ
where R is the gas constant, Tassay is the temperature of the assay and Tin situ is the in situ
temperature of the sampled sea water layers.
The O2 consumption rate per hour is converted into C demand per day, expressed as
mg C gww1 d1, assuming a respiration factor of 0.85 [266,288]:
ETSassay ðmg C gwwt1 d1 Þ ¼ ETSassay ðmL O2 gwwt1 h1 Þ 0:85 12 24=22:4,
where 12 is the weight of 1 C mole (g), 24 converts hours in day and 22.4 is the gas
volume mol1.
The ETS:respiration ratio for natural zooplankton assemblages was stated as 0.5
[266,276,285] to translate the O2 consumed measured throughout the ETS methodology to
in situ respiration. Packard [275] and Packard and Richards [289] suggested that ETS
activity, as measured by INT reduction in homogenates, can be used as a reliable index of
in situ oxygen consumption. The values computed for R: ETS are reasonable assuming
that the ETS activity is measured at or near the Vmax of electron transfer.
Geographical, seasonal and vertical differences in respiratory activity of zooplankton
were shown many times [290–292], but until now, to the best of our knowledge, data are
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scarce for mesozooplankton and micronekton in the Mediterranean Sea. In the Levantine
Sea, near Crete, [269, 271, 293] reported ETS data but only on the deeper zooplankton
(ca. 1000 m depth) and the nictimeral cycle was not analysed. The oligotrophic character of
the Mediterranean Sea was reflected in the low POC flux rate at deep layers. The higher
temperature of the deep waters in the Levantine Sea compared to the open ocean leads to
the suggestion that remineralization of organic material is enhanced due to higher
metabolic activities at elevated temperatures. Koppelmann et al. [271] suggested that the
deep eastern Mediterranean is similar to high-latitude productive regions in terms of
relative deep water remineralization, even if at much lower absolute rates. Possibly, it was
caused by the high temperature and/or the dominance of some species in the environment,
like the copepod Lucicutia longiserrata.
In the whole Mediterranean Sea the first research on spatial mesozooplankton ETS
variability on a large geographical scale is very recent. Minutoli and Guglielmo [294]
focused on spatial distribution of zooplankton O2 and C demand and its day/night
variability from the Atlantic Ocean to the eastern Mediterranean, at 10 stations along a
west–east transect. At each station samples were carried out in accordance with a 24-h
cycle to study the changes in zooplankton composition due to day–night vertical
migrations and the potential relation with ETS values. Sampling was performed during the
oceanographic cruise ‘TRANSMED’ (May–June 2007), within the framework of the
national project VECTOR ‘VulnErability of Coasts and marine Italian ecosystems to
climaTic changes and their rOle in mediterranean caRbon cycle’. A total of 35 vertical
samples were collected in the upper 200 m, using the Indian Ocean Standard Net (IOSN),
(1-m2 mouth; 335-mm mesh size). A Hydro Bios Kiel fluximeter was connected at the net to
measure the filtered volume. The environmental parameters of sampling stations were
registered on board by a CTD SBE911, equipped with primary sensors for: conductivity
(mS), temperature ( C), depth (m), fluorescence (V) and dissolved O2 (mL L1). The
relationship between ETS activity (O2 and C demand) and composition and/or abundance
of zooplankton and temperatures of the sea water, were studied.
The O2 and C requirements per unit of zooplankton biomass indicated day/night and
spatial geographical differences in the studied area. The biochemical analyses showed
differences in mean C consumption rate between the western and eastern Mediterranean
stations: mean value of the samples 290 (28.52 SD) and 387 (46.21 SD) mg C g1 d1 in
the western and eastern sectors, respectively. An increasing gradient was evidenced from
the Atlantic Ocean, (mean value 241 mg C g1 d1), to the easternmost station near Rhodes
(419 mg C g1 d1). The relationship between latitude and ETS was highly significant
(r2 ¼ 0.86). ANOVA analysis of variance confirmed a statistically significant difference
between these mean values from west to east (F ¼ 2.32; P50.5%). ANOVA analysis of
variance, applied instead to the groups of data for the four time samplings, showed a
statistically significant trend for any time, from west to east (F ¼ 3.15; P50.1%). This
geographical enhancing west–east gradient, was also observed separately for all morning,
midday, afternoon and midnight samples that showed as well an enhanced trend.
Considering that there were not significant differences in total zooplankton density and
composition between the western and eastern sector and that there was an almost equal
ratio between gelatinous and crustacean taxa from west (mean ratio 1:7.2) to east (mean
ratio 1:7), the trend in increasing C demand, confirmed by ANOVA analysis, could be
explained with a relation between zooplankton ETS activity and sea-water temperature.
The increase of only a few degrees, leads to higher enzymatic activities [282]. The same
linear relation has already been demonstrated by Packard et al. [284], who reported that
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90% of differences in geographical ETS activity is linked to temperature. Zooplankton
samples from stations with higher temperature, as in the levantine basin, showed higher
ETS activity because of the metabolic activities, like the remineralization of organic
material, that are directly correlated to the temperature.
During the 24-h cycle at all stations, ETS activity peaked at midnight or in the morning
before sunrise, decreasing in the afternoon and midday. For this reason it was
hypothesized that the cause could be the changes of zooplankton composition in the
surface layer. ETS activity is standardized for biomass, therefore differences only in
density do not justify these results, although the O2 demand is a function of body mass
[295]. Daily differences were probably caused by actively migrating organisms that mediate
the vertical transport of material in the sea [296]. Taxonomical analyses revealed that
adults and furcilia stages of euphausiids actively migrated from deeper layers to 200–0 m
interval during the night, residing instead at deeper depths during the day. This taxon
shows day–night vertical migration feeding, returning to deeper and colder layers during
the day to avoid predators [179,248,297]. During the daily cycle, some species like
Thysanopoda aequalis, Euphausia species and Nematoscelis megalops showed a strong
migratory behaviour in both Mediterranean basins. The absence or the few specimens
caught in the morning and at midday demonstrated that the great part of these species
remained below the 200-m depth. At night the number of individuals increased,
concentrating in the upper layer. Euphausiid migrating species have a higher ETS activity
than the deeper-living and non-migrating species [287,298–301]. The eastern
Mediterranean Sea is a very oligotrophic region in respect to the western part and all
marine ecosystems, in term of species richness and abundance [302–305]. With the results
obtained during the VECTOR cruise, it was possible to show that the zooplankton from
the eastern part of the Mediterranean Sea contributes, with the high C demand, to C losses
from the known scarce POC sinking flux in the water column [293], amplifying the features
of an impoverished region.
4.2.3. Egg production
Seasonal fluctuations in copepod fecundity are one of the major factors affecting seasonal
oscillations in copepod abundances in the marine ecosystem. The dominant copepod
communities of Mediterranean coastal, neritic and surface pelagic waters is constituted by
few perennial species of the genera Acartia, Paracalanus, Temora and Centropages, whose
species follow one another during the year, characterizing with their dominance different
seasonal periods [65]. One of the most remarkable life history traits of copepods living in
subtemperate and tropical regions is that they are continuous breeders, with most species
having peaks of egg production rates in spring–summer except for Temora stylifera, which
spawns mainly in autumn [306]. Generally, there are periods of lower and higher breeding
intensity or the breeding season may be interrupted due to the production of dormant
eggs. Breeding cycles in these regions generally give rise to a large numbers of consecutive
generations (up to four or five generations are reported by Christou and Verriopoulos
[307] for Mediterranean populations of Acartia clausi). Conversely, copepods that live
at higher latitudes have a very limited breeding season with a spawning period lasting only
8–9 weeks, generally from March to May.
Over the last 50 years, many field and laboratory studies on copepod egg production
rates have demonstrated a positive correlation between fecundity and temperature up to a
maximum level beyond which egg production is arrested and females may die.
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This maximum level of production seems to be relatively constant in subtemperate species,
ranging from 15 C for Temora stylifera, Centropages typicus, and T. longicornis [308–310]
to 20 C for Acartia tonsa [311]. The Mediterranean population of Pseudocyclops
xiphophorus shows maximum egg production rates in summer when environmental
temperatures range from 26 to 28 C [312]. As demonstrated by Uye [313] for A. omorii, at
higher temperatures, although the average number of eggs produced per female per day by
P. xiphophorus is higher, the period of egg-laying is reduced. Consequently, overall mean
egg production rate is lower. Average number of eggs is higher because of the acceleration
in the metabolic activity and accumulation rate of material in the developing oocytes so
that egg production is higher and spawning intervals are shortened [313].
Temperature also markedly affects development rate of eggs. McLaren et al. [314] were
the first to show that the eggs of the same species will develop faster at higher temperatures
and their development times are faster in tropical vs. cold dwelling species. Egg
development times in subtemperate species tend to be quite rapid, ca. 24–72 h within a
temperature range of 15–30 C.
Egg production rates are also positively correlated to female body size [315] and food
concentrations/food quality [316–318]. In the laboratory, fecundity has been shown to be
food quantity dependent up to a saturation level beyond which the reproductive rate
remains unchanged [316]. Saturation levels for most copepod species range between 102
and 103 cells mL1 of cultured microalgae, depending on the species. Runge [319]
demonstrated that there are species better adapted to exploit phytoplankton blooms than
others. Also, the maximum reproductive potential differs among species, with some species
(Paracalanus parvus) more fecund than others (A. clausi). Kiørboe and Sabatini [320] have
reported that the less fecund species are those that bear egg sacs such as Pseudocalanus,
whereas the most fecund are those that belong to the genus Centropages. In more recent
studies Brugnano and co-workers [312,321] have demonstrated that the species belonging
to the benthoplanktonic genus Pseudocyclops have low fecundity rates similar to those that
bear egg sacs.
Food quality, therefore quantity, was demonstrated to strongly affect copepod egg
production, embryonic and post-embryonic development and hatching success with some
diets that are poorer than others in inducing maximum fecundity. According to Kleppel
et al. [322] production increase depends on the diet so that diatoms5dinoflagellates5
ciliate þ dinoflagellates. The inadequacy of diet to supply all nutritional components, such
as fatty acid, amino acids and carbohydrates affects various copepod rate processes (egg
production, hatching success, naupliar and copepodid development). In the last years,
scientific interest has been concerned with the paradox of diatom-copepod interactions
[323]. Traditionally, diatoms were considered to be at the base of the marine food web and
their blooms can initiate and support the increasing of copepod populations in marine
ecosystems. However, more recent evidence of Poulet and co-workers [324,325] has raised
serious doubts that diatoms are good and harmless food items for the reproduction and
development of their planktonic predators, in particular the herbivorus copepods. Studies
of Miralto and co-workers [325,326] reported that damaged cells of diatoms produce
insidious compounds ( , , , unsaturated aldehydes) with anti-cell growth activity in
that they block the development of copepod embryos. Pohnert [327] showed that when
diatoms are grazed by copepods they become damaged after copepod digestion and there
is a rapid onset of aldehyde production seconds after cell disruption, similar to the wound
reaction in higher plants [328]. Copepod species, such as Calanus helgolandicus, Temora
stylifera, Acartia clausi, fed on diatoms and flagellates [324,329,330], show different effects
340
S. Fonda Umani et al.
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on egg production reflecting species specific nutritional responses associated with size,
taste and food assimilation rates. Not only, but a study covering a wide range of different
ecosystems argued that extrapolation to natural environments of results obtained in
laboratory experiments must be considered with caution, also when natural environments
are characterized by high diatom abundances [331].
Furthermore, egg viability and female fertility may largely depend on female age and
remating success [332], as shown for Calanus finmarchicus [283], Temora stylifera [306],
and P. xiphophorus [312], whereas Ianora et al. [330] demonstrated that males do not
modify the reproductive success (i.e. fecundity and egg viability) of A. clausi females. Also
in Centropages typicus the remating was demonstrated less frequent or not necessary to
maintain high egg viability [329]. A reduction in fecundity in older females seems to be due
to shrinkage of the oviducts after a long interval of continuous spawning as shown in
Temora stylifera [333]. In the case of egg viability, as shown for fish, older females may
synthesize less lipids, which are essential for egg development [334].
5. Concluding remarks
We are perfectly aware that we did not report all Italian researches on zooplankton
communities performed in the last 30 years, because in the past data were only
sporadically published in peer reviewed journals. For most of the time they were published
in Italian journals or reported in internal project reports, preventing an easy access to the
future generation of researchers. And maybe more important all data are not gathered
together and stored in any free access data bank, only some of them are indeed stored in
some data bank created for each project and dispersed over the national territory. Some
projects do not allow any access to these data (and others, of course), consequently in our
review we mostly relied on our own data, or the few already published. In this review we
tried to find as many reports as possible, but of course we did not cover all Italian efforts
in this field. We hope anyway that our effort can be a useful starting point to more focused
analysis on changes in community composition and biomasses occurring in the last years
in respect to the past. In this sense, efforts devoted to carrying on long-term series on
zooplankton (but not only) revealed to be of fundamental importance in describing
climatic impacts on this sensitive pelagic component. Unfortunately, as it is evident in this
review, some geographical areas wer not covered at all in the past. Nowadays there is a
national monitoring program, which anyway covers only a very narrow coastal belt, but
all along the 8000 km of the Italian coasts. We hope that all information collected by this
monitoring program will be available to the scientific community for comparisons with old
data to reveal climatic forcing on pelagic ecosystems. In the more recent years Italian
researchers increased their international visibility together with an evident shift towards
more processes oriented studies. The main focus of these kinds of experiments was to
understand the role of zooplankton components in the global C fluxes, and how abiotic
factors constrain the final fate of autotrophic (and heterotrophic) production in the marine
ecosystem. Our final suggestion is therefore to maintain as long as possible the long time
series on going (and recently entered in the LTER international network) on all abiotic
and biotic components of the pelagic ecosystem, to improve analysis methodology to
reveal the role of climatic change impact on the modification occurring in the zooplankton
communities over the last 30 years all over the Italian seas, and to improve the efforts to
Advances in Oceanography and Limnology
341
quantify C fluxes throughout these components in the different trophic and latitudinal
ecosystems that characterise the Italian seas.
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