Stability and resilience in coastal copepod assemblages: The case of the Mediterranean long-term ecological research at Station MC (LTER-MC)

Abstract We analyzed the copepod assemblages over two decades (1984–2006) in a coastal ongoing time-series at Station MC in the inner Gulf of Naples (Tyrrhenian Sea, Western Mediterranean), which is part of the International network of Long-Term Ecological Research (LTER). The seasonal and interannual time courses of species abundance and composition were related to depth integrated temperature, salinity, and chlorophyll a , which provide essential information on the local environmental dynamics. Our aims were to characterize the main modes of copepod variability and to highlight possible changes occurred in the period in relation to the local environmental dynamics. Despite the great variability at seasonal and interannual scales, our site did not show evidence of discontinuities or trends in water column properties as compared to other Mediterranean sites for the same period, which we interpret as resulting from the position of Station MC that is exposed to the influence of a complex climate forcing. Abrupt changes did not appear for most of the key representative species (e.g., Acartia clausi , Centropages typicus , Paracalanus parvus , Temora stylifera , and juveniles of Clausocalanus spp./ P. parvus ) beyond the high interannual variability in the abundance patterns. A few indications suggest that our station might have acquired less coastal characters (e.g., decreasing chlorophyll a concentrations), but the signals from the copepod assemblages appeared only in rare species. A significant increase was observed in the occurrence of some typical offshore calanoids (e.g., Neocalanus gracilis , Scolecithricella spp.), while a few species typical of confined areas disappeared (e.g., Acartia margalefi , Paracartia latisetosa ). STATICO analysis showed a significant resilience in the seasonal cycle of the copepod assemblages at Station MC, even when there was high variability in the environmental parameters. While the changes recorded in the least abundant species may be indicative of long-term variations, we interpret the overall persistence of the basic community as resulting from the flexibility of coastal species to adapt to variation in environmental conditions.

[1]  A. Ianora,et al.  Egg viability in the copepod Temora stylifera , 1993 .

[2]  R. Ian Perry,et al.  Identifying global synchronies in marine zooplankton populations: issues and opportunities , 2004 .

[3]  K. Mann,et al.  Dynamics of marine ecosystems:biological-physical interactions in the oceans , 1992 .

[4]  John W. Tukey,et al.  Exploratory Data Analysis. , 1979 .

[5]  Dean Roemmich,et al.  Climatic Warming and the Decline of Zooplankton in the California Current , 1995, Science.

[6]  Grégory Beaugrand,et al.  Long‐term changes in phytoplankton, zooplankton and salmon related to climate , 2003 .

[7]  A. Ianora Copepod life history traits in subtemperate regions , 1998 .

[8]  J. H. Ward Hierarchical Grouping to Optimize an Objective Function , 1963 .

[9]  G. Gasparini,et al.  A possible influence of the North Atlantic Oscillation on the circulation of the western Mediterranean Sea , 1999 .

[10]  S. Souissi,et al.  North Atlantic climate and northwestern Mediterranean plankton variability , 2005 .

[11]  Jean Thioulouse,et al.  CO‐INERTIA ANALYSIS AND THE LINKING OF ECOLOGICAL DATA TABLES , 2003 .

[12]  A. Marco Niche separation of Clausocalanus species in the Mediterranean Sea and in the Atlantic Ocean , 2008 .

[13]  B. Planque,et al.  Long-term and regional variability of phytoplankton biomass in the Northeast Atlantic (1960-1995) , 2001 .

[14]  A. Conversi,et al.  Gulf of Trieste: A changing ecosystem , 2009 .

[15]  C. S. Holling Resilience and Stability of Ecological Systems , 1973 .

[16]  Douglas W. Nychka,et al.  Statistical significance of trends and trend differences in layer-average atmospheric temperature time series , 2000 .

[17]  S. Levitus,et al.  The Western Mediterranean Deep Water: A proxy for climate change , 2005 .

[18]  Micheli,et al.  Eutrophication, Fisheries, and Consumer-Resource Dynamics in Marine Pelagic Ecosystems. , 1999, Science.

[19]  Jean Thioulouse,et al.  Simultaneous analysis of a sequence of paired ecological tables , 2004 .

[20]  Daniele Iudicone,et al.  Coastal Phytoplankton Do Not Rest in Winter , 2010 .

[21]  E. Christou Interannual variability of copepods in a Mediterranean coastal area (Saronikos Gulf, Aegean Sea) , 1998 .

[22]  A. Ianora,et al.  Vertical zonation patterns for Mediterranean copepods from the surface to 3000 m at a fixed station in the Tyrrhenian Sea , 1984 .

[23]  F. Ibaňez,et al.  Long‐term fluctuations (1974‐99) of the salps Thalia democratica and Salpa fusiformis in the northwestern Mediterranean Sea: Relationships with hydroclimatic variability , 2006 .

[24]  A. Mariotti,et al.  River Discharge into the Mediterranean Sea: Climatology and Aspects of the Observed Variability , 2004 .

[25]  W. Peterson,et al.  Comparisons of interannual biomass anomalies of zooplankton communities along the continental margins of British Columbia and Oregon , 2004 .

[26]  Olga Mangoni,et al.  Seasonal patterns in plankton communities in a pluriannual time series at a coastal Mediterranean site (Gulf of Naples): an attempt to discern recurrences and trends , 2004 .

[27]  B. Manly,et al.  Resilience of North Sea phytoplankton spring bloom dynamics: An analysis of long‐term data at Helgoland Roads , 2008 .

[28]  I. Valiela,et al.  Estuarine calanoid copepod abundance in relation to season, salinity, and land-derived nitrogen loading, Waquoit Bay, MA , 2004 .

[29]  E. Napolitano,et al.  Barotropic aspects of the dynamics of the Gulf of Naples (Tyrrhenian Sea) , 2001 .

[30]  Corinne Le Quéré,et al.  Climate Change 2013: The Physical Science Basis , 2013 .

[31]  F. S. Russell,et al.  On the Value of Certain Plankton Animals as Indicators of Water Movements in the English Channel and North Sea , 1935, Journal of the Marine Biological Association of the United Kingdom.

[32]  Other,et al.  Mediterranean climate variability , 2006 .

[33]  A. Calbet,et al.  Mediterranean marine copepods: basin-scale trends of the calanoid Centropages typicus , 2008, Hydrobiologia.

[34]  M. Mazzocchi,et al.  Vertical and seasonal distribution of eight Clausocalanus species (Copepoda: Calanoida) in oligotrophic waters , 2004 .

[35]  S. F. Umani,et al.  Eleven years of time-series analysis on the net-zooplankton community in the Gulf of Trieste , 1995 .

[36]  Martin Edwards,et al.  Changing zooplankton seasonality in a changing ocean: Comparing time series of zooplankton phenology , 2012 .

[37]  M. Simier,et al.  The Gambia River estuary: A reference point for estuarine fish assemblages studies in West Africa , 2006 .

[38]  A. Eisenhauer,et al.  Calcium isotopic composition of high-latitude proxy carrier Neogloboquadrina pachyderma (sin.) , 2007 .

[39]  Neville Nicholls,et al.  commentary and analysis: The Insignificance of Significance Testing , 2001 .

[40]  F. Ibanez,et al.  Comparaison des évolutions à long terme (1977–1990) de deux peuplements macrobenthiques de la baie de Morlaix (Manche occidentale): relations avec les facteurs hydroclimatiques , 1993 .

[41]  G. Belmonte Diapause egg production in Acartia (Paracartia) latisetosa (Crustacea, Copepoda, Calanoida) , 1992 .

[42]  Robert Sabatier,et al.  The ACT (STATIS method) , 1994 .

[43]  I. Ferrari,et al.  Zooplankton variability related to environmental changes in a eutrophic coastal lagoon in the Po Delta , 1996, Hydrobiologia.

[44]  J. Colebrook Continuous plankton records - phytoplankton, zooplankton and environment, northeast atlantic and north-sea, 1958-1980 , 1982 .

[45]  G. Gorsky,et al.  Intercomparison of six Mediterranean zooplankton time series , 2012 .

[46]  F. Boero Fluctuations and Variations in Coastal Marine Environments , 1994 .

[47]  N. Stenseth,et al.  The Response of Terrestrial Ecosystems to Climate Variability Associated with the North Atlantic Oscillation , 2013 .

[48]  Jean Thioulouse,et al.  Les analyses multitableaux en écologie factorielle. I: De la typologie d'état à la typologie de fonctionnement par l'analyse triadique , 1987 .

[49]  P. C. Reid,et al.  Reorganization of North Atlantic Marine Copepod Biodiversity and Climate , 2002, Science.

[50]  C. Lorenzen,et al.  Fluorometric Determination of Chlorophyll , 1965 .

[51]  S. T. Buckland,et al.  An Introduction to the Bootstrap. , 1994 .

[52]  M. Alcaraz Coexistence and segregation of congeneric pelagic copepods: spatial distribution of the Acartia complex in the ría of Vigo (NW of Spain) , 1983 .

[53]  J. Molinero,et al.  Seasonal variability of copepod abundance in the Balearic region (Western Mediterranean) as an indicator of basin scale hydrological changes , 2008, Hydrobiologia.

[54]  K. Lau,et al.  The Hydrological Cycle in the Mediterranean Region and Implications for the Water Budget of the Mediterranean Sea , 2002 .

[55]  M. Llope,et al.  A decade of sampling in the Bay of Biscay: What are the zooplankton time series telling us? , 2007 .

[56]  Y. Escoufier LE TRAITEMENT DES VARIABLES VECTORIELLES , 1973 .

[57]  M. Mazzocchi,et al.  Temporal variability of Centropages typicus in the Mediterranean Sea over seasonal-to-decadal scales , 2007 .

[58]  Robert Tibshirani,et al.  Estimating the number of clusters in a data set via the gap statistic , 2000 .

[59]  M. d’Alcalà,et al.  Recurrent patterns in zooplankton structure and succession in a variable coastal environment , 1995 .

[60]  G. Hays,et al.  Climate change and marine plankton. , 2005, Trends in ecology & evolution.

[61]  F. Ibaňez,et al.  Changes of zooplankton communities in the Gulf of Tigullio (Ligurian Sea, Western Mediterranean) from 1985 to 1995. Influence of hydroclimatic factors , 2000 .

[62]  S. Pierini,et al.  A wind-driven circulation model of the Tyrrhenian Sea area , 1998 .

[63]  Grégory Beaugrand,et al.  The North Sea regime shift: Evidence, causes, mechanisms and consequences , 2004 .

[64]  H. Hirche,et al.  Hydrographic structure and zooplankton abundance and diversity off Paita, northern Peru (1994 to 2004) — ENSO effects, trends and changes , 2009 .

[65]  M. Mazzocchi,et al.  Mesozooplankton distribution from Sicily to Cyprus (Eastern Mediterranean) : II. Copepod assemblages , 1997 .

[66]  M. Hoffmeyer Decadal change in zooplankton seasonal succession in the Bahía Blanca estuary, Argentina, following introduction of two zooplankton species , 2004 .

[67]  J. Mcgowan,et al.  Climate and change in oceanic ecosystems: The value of time-series data. , 1990, Trends in ecology & evolution.

[68]  D. Markle,et al.  An evaluation of accuracy, precision, and speed of several zooplankton subsampling techniques , 1982 .

[69]  Christou,et al.  PATTERNS OF VERTICAL DISTRIBUTION OF PSEUDOCALANIDAE AND PARACALANIDAE (COPEPODA) IN PELAGIC WATERS (0 TO 300 M) OF THE EASTERN MEDITERRANEAN SEA , 2001 .