Elsevier

Journal of Sea Research

Volume 108, February 2016, Pages 30-49
Journal of Sea Research

Calcareous assemblages of the southeastern Mediterranean low-tide estuaries — Seasonal dynamics and paleo-environmental implications

https://doi.org/10.1016/j.seares.2015.12.002Get rights and content

Highlights

  • Foraminifera, ostracods and molluscs are distributed in SE Levantine estuaries.

  • Multivariate analyses determined ecological preferences of living species.

  • Death assemblage provides a basis for paleoenvironmental reconstruction.

  • Living species distribution is seasonally and environmental controlled.

  • Paleostorm events in estuaries are identified by influx of allochthonous organisms.

Abstract

The study of estuarine ecosystems is essential for protecting and reestablishing their threatened biota. In this research the spatio-temporal variations in the distribution patterns of foraminifera, ostracods and molluscs are analyzed in surficial sediments sampled in 2012/13 at six low-tide estuaries of the southeastern Mediterranean coast. Live assemblages are studied using multivariate statistical analyses to determine their ecological preferences and seasonal dynamics whereas the dead assemblages are used to establish a reference baseline for future paleoenvironmental reconstruction.

The statistical analysis indicates that salinity, TOC and % carbonate are the main environmental factors explaining 60% of the cumulative variance and controlling the distribution pattern of the different brackish taxa encountered in these estuaries. The foraminifera Ammonia tepida and some miliolids (Quinqueloculina and Varidentella) inhabit most estuaries during summer when salinities of 13–18 psu and temperatures of 26–34 °C occur. At the Naaman stream the agglutinated species Birsteiniolla macrostoma and Trichohyalus aguayoi dominate the assemblage during autumn and winter, respectively when salinities of 3–7 psu and temperature of 18–24 °C prevail. High abundance of the monospecific assemblage of the ostracod Cyprideis torosa was encountered at the Tanninim year round in oligohaline water. The gastropod Heleobia phaeniciaca prefers living at the Naaman and Tanninim streams while Pyrgophorus sp., an invasive and low salinity species, continue colonizing more stream reaches along the Israeli coast.

The dead assemblages are composed of high numbers of local and transported species. It includes post storm-surge sediments containing high numbers of inland fresh and brackish water species transported by the floods. Those are mixed with inner to mid-shelf benthic and planktonic foraminifera, ostracods and molluscs. Transportation of the marine organisms a few hundred of meters inland via the estuaries indicates that the coastal areas are prone to storm surge events that are preserved clearly on the coast.

The present study demonstrates that the combined use of different multi-proxy faunal records enhances significantly the understanding of the dynamics of low-tide estuaries. This can be applied also to other low-tide estuaries worldwide and facilitate better management of these threatened environments. Additionally, it enables understanding of the post-mortem processes that control the transition from the living to the death assemblages and by that improve paleoenvironmental reconstruction of the lower reaches of low-tide estuaries.

Introduction

Estuaries are often heavily populated and represent regions of utmost economic value (e.g. Ducrotoy and Elliott, 2006). Anthropogenic activity and intensive exploitation of these water resources cause disturbance to the biota living in this ecosystem. This includes overfishing, physical habitat modifications, habitat loss, organic enrichment and pollution (e.g. Bar Or, 2000, Bianchi and Morri, 2000, Crossland et al., 2005). Estuaries are also at risk of invasions of alien aquatic species diminishing biodiversity (Occhipinti-Ambrogi and Savini, 2003). Hence, studying these vulnerable ecosystems (e.g. Costanza et al., 1997) and carefully monitoring their fauna are imperative for efficient management and their continuous utilization in the future and for protecting or reestablishing their distinctive biodiversity (e.g. Poff et al., 2007). This is especially significant in small estuaries vulnerable to anthropogenic activity that have a small tidal range known worldwide e.g., South Africa (e.g. Bell et al., 2001, Cooper, 2001), Australia (e.g. Ranasinghe and Pattiaratchi, 2003), southwestern USA (Elwany et al., 1998), and the southeastern Levant (e.g. Reinhardt et al., 2003) and which were studied mainly for their geomorphological aspects but rarely for their biota.

Estuaries represent a dynamic ecosystem characterized by high environmental variability in salinity, temperature, primary productivity, bottom water dissolved oxygen content and sediment type (e.g., Lu et al., 2008, Bárcena et al., 2012). These variables affect the abundance, distribution patterns and the community structure of the calcareous benthic organisms that live there generally in low diversity and with frequent shifts in species dominance (Marques et al., 1993, Cognetti and Maltagliati, 2000).

Among the calcareous organisms living in estuaries molluscs are increasingly employed as bio-indicators of environmental quality. They are used to evaluate water/sediment relation and to determine the state of health of the estuary ecosystem (e.g. Koutsoubas et al., 2000, McLusky and Elliott, 2004, Afli et al., 2008). This group plays a role in cycling nutrients and in exchanging materials between sediments and water column in addition to being a source of food for secondary consumers of higher trophic levels (McLusky and Elliott, 2004).

Ostracods and benthic foraminifera also comprise a significant part of this ecosystem, being increasingly used as environmental bioindicators evaluating water/sediment quality conditions (e.g., Debenay et al., 2003, Debenay et al., 2006) and especially in polluted environments (e.g. Ruiz et al., 2004, Ruiz et al., 2005, Bergin et al., 2006). The sensitivity of these organisms to environmental change might be expressed either by disappearance, replacement, appearance of specific species or by the occurrence of morphological anomalies (e.g. Ruiz et al., 2004, Ruiz et al., 2005 and references therein).

The occurrence of molluscs, ostracods and foraminifera in several microtidal estuaries along the Israeli coast was reported so far only in few papers and mainly in internal reports. Herbst and Mienis (1985) and Mienis and Ortal (2001) studied the distribution of molluscs in Tanninim and Naaman streams, respectively. Reinhardt et al. (2003) studied the dead foraminiferal assemblages of the Tanninim estuary and the Sr isotope composition of shell material (foraminifera, ostracods, molluscs, algae) as salinity proxy. Almogi-Labin et al. (2001) and Siman Tov and Almogi-Labin (2002) characterized different stream mouths and coastal plain inland brackish habitats based on a semi-quantitative survey of live and dead groups of diatoms, thecamoebians, foraminifera, ostracods and molluscs. Almogi-Labin et al., 2002, Almogi-Labin et al., 2004 and Flako-Zaritsky et al. (2011) studied the brackish water foraminifers and ostracods of the inland brackish Enot Timsah pond (32°33.9′N/34°55.41′E; 193537E/717650N new Israeli grid), the current main water source of the Tanninim stream. The distribution of foraminifera, ostracods and molluscs was studied also in the inland Nur pond located adjacent to the Naaman estuary (Almogi-Labin et al., 2007). They focused on salinity alternation between brackish and freshwater during the last few decades based on the faunal distribution. The main variables controlling ostracod species distributions in the Israeli inland aquatic environments (lakes, ponds and streams) were studied by Mischke et al., 2010, Mischke et al., 2014. In these studies an ostracod-based electrical conductivity transfer function was developed and applied onto fossil ostracod assemblages from Pleistocene–Holocene in order to trace the hydrologic history of water bodies in the region.

For the coastal plain of the southeastern Mediterranean shelf, with its dense population and the ongoing disappearance of natural coastal habitats, the need to restore streams is pressing (Bar Or, 2000, Gafny, 2013), particularly estuaries, which received so far only little attention. Due to the limited information on this vulnerable ecosystem and due to plans to rehabilitate this environment we aimed in this study to: (1) identify and describe the distribution of the living foraminifera, ostracods and molluscs over an annual cycle, in six estuaries along the Israeli coast (Fig. 1); (2) determine the relationships between environmental factors and the fauna using multivariate statistical analyses in order to improve their use as environmental bio-indicators; (3) add information on aliens/invasive species and their association with the local ecosystem as part of the efforts to improve environmental conservation; and (4) study the time-averaged death assemblage of the three calcareous groups in order to create a reference baseline for future paleogeographic, paleoenvironmental and paleoecological studies.

Section snippets

Study area

The studied coast of the southern Levant extends 180 km along the southeastern Mediterranean, in a nearly straight NE–NNE direction (Fig. 1). This coastal area includes two main sedimentary provinces: a southern one, part of the Nile siliciclastic (quartz)-rich littoral cell (e.g. Zviely et al., 2007, Hyams-Kaphzan et al., 2008) and a northern one that ranges from Akko promontory northward to Lebanon and is composed of carbonate-rich sediments of local sources forming mainly rocky and coarse

Field sampling

Surface sediments and water samples were collected once in every season over a period of one year (2012–2013) from six estuaries located on the southern, central and northern Israeli coast (Fig. 1; Table 1, Table 2). Samples were taken between 5 and 35 cm water depth, near the riverbanks, a depth interval that was relatively well oxygenated. The samples were taken along an E–W gradient with Station 1 in our notation being the closest to the river mouth and 3 the most inland one (Table 1a).

During

Environmental properties

Water temperature (WT) varies between 12 °C and 22 °C in winter and 26 °C and 32 °C during summer (Fig. 2a; Table 1a). Differences in WT for example in the Naaman are related to differences in sampling time, during the day, in each season. The coldest WT of 12 °C was measured in Poleg 2. The lowest pH was measured in Tanninim 3A (7.48) and the highest in Alexander 1A and Lachish 1W (8.6 and 8.7, respectively). The electrical conductivity varies between 1.35 in Poleg 1W and 42.80 mS/cm in Alexander

Faunal distribution pattern and species richness in low-tidal estuaries

The current study focuses on the lower reaches of the low-tidal estuaries of the southeastern Mediterranean continental shelf, an environment common in semi-arid subtropical regions worldwide (e.g. Bell et al., 2001, Cooper, 2001, Ranasinghe and Pattiaratchi, 2003, Elwany et al., 1998)). The numbers of living species of ostracods, molluscs and foraminifera are low and seem to be associated with the low salinity values of the Tanninim and Naaman estuaries (≤ 7 psu) and the oscillating salinity

Conclusions

A regional reference baseline of foraminifera, ostracods and molluscs was established for the first time, for the low-tide estuaries of the southeastern Mediterranean coast that can be used for any future paleoenvironmental reconstruction. The calcareous fauna that lives there is affected by mainly the natural seasonality combined with anthropogenic interference.

The living benthic foraminiferal assemblage composition is rather similar in most stream reaches, except that of the Naaman. It is

Acknowledgments

This study was carried out with the support of the Ministry of Science and Technology and of the Ministry of Energy and Water Resources (Grant nos. 3-7818 and 212-17-022 respectively). We gratefully acknowledge the technical assistance received from M. Kitin and C. Netzer-Cohen of the Geological Survey of Israel and A. Yurman and M. Bachar from the RIMS diving workshop, of the Department of Maritime Civilizations and the Leon Recanati Institute for Maritime Studies, Haifa University. H. K.

References (106)

  • J.-P. Debenay et al.

    Multi-bioindicator study of a small estuary in Vende'e (France)

    Estuar. Coast. Shelf Sci.

    (2003)
  • J.-P. Debenay et al.

    Spatio-temporal distribution of benthic foraminifera in relation to estuarine dynamics (Vie estuary, Vende'e, W France)

    Estuar. Coast. Shelf Sci.

    (2006)
  • J.P. Ducrotoy et al.

    Recent developments in estuarine ecology and management

    Mar. Pollut. Bull.

    (2006)
  • R.J. Edwards et al.

    Surface distributions of salt-marsh foraminifera from Connecticut, USA: modern analogues for high-resolution sea level studies

    Mar. Micropaleontol.

    (2004)
  • S. Flako-Zaritsky et al.

    The environmental setting and microfauna of the oligohaline Timsah pond, Israel: the last remnant of the Kabara swamps

    Mar. Micropaleontol.

    (2011)
  • P. Frenzel et al.

    The use of ostracods from marginal marine, brackish waters as bioindicators of modern and Quaternary environmental change

    Palaeogeogr. Palaeoclimatol. Palaeoecol.

    (2005)
  • B.W. Hayward et al.

    Recent New Zealand Shallow-water Benthic Foraminifera: Taxonomy, Ecologic Distribution, Biogeography and Use in Paleoenvironmental Assessment

    (1999)
  • B.P. Horton

    The contemporary distribution of intertidal foraminifera of Cowpen Marsh, Tees Estuary, UK: implications for studies of Holocene sea level changes

    Palaeogeogr. Palaeoclimatol. Palaeoecol.

    (1999)
  • B.P. Horton et al.

    The sedimentary record of the 2005 hurricane season from the Mississippi and Alabama coastlines

    Quaternary International

    (2009)
  • O. Hyams-Kaphzan et al.

    Natural oligotrophy vs. pollution-induced eutrophy on the SE Mediterranean shallow shelf (Israel): environmental parameters and benthic foraminifera

    Mar. Pollut. Bull.

    (2009)
  • S. Kortekaas et al.

    Distinguishing tsunami and storm deposits: an example from Martinhal, SW Portugal

    Sediment. Geol.

    (2007)
  • M. Lichter et al.

    Morphological patterns of southeastern Mediterranean river mouths: the topographic setting of the beach as a forcing factor

    Geomorphology

    (2010)
  • B. Mamo et al.

    Tsunami sediments and their foraminiferal assemblages

    Earth Sci. Rev.

    (2009)
  • A. Occhipinti-Ambrogi et al.

    Biological invasions as a component of global change in stressed marine ecosystems

    Mar. Pollut. Bull.

    (2003)
  • J. Rodriguez-Lazaro et al.

    Recent benthic foraminifers as indicators of the sedimentary dynamics of the Tina Mayor and Tina Menor estuaries (S Bay of Biscay, N Spain)

    J. Mar. Syst.

    (2013)
  • F. Ruiz et al.

    Comparative ecological analysis of the ostracod faunas from low and high-polluted southwestern Spanish estuaries: a multivariate approach

    Mar. Micropaleontol.

    (2000)
  • F. Ruiz et al.

    Ostracoda and foraminifera as short-term tracers of environmental changes in very polluted areas: the Odiel Estuary (SW Spain)

    Environ. Pollut.

    (2004)
  • F. Ruiz et al.

    Marine and brackish-water ostracods as sentinels of anthropogenic impacts

    Earth Sci. Rev.

    (2005)
  • J. Schönfeld et al.

    The FOBIMO (FOraminiferal BIo-MOnitoring) initiative—towards a standardized protocol for soft-bottom benthic foraminiferal monitoring studies

    Mar. Micropaleontol.

    (2012)
  • G. Almagor et al.

    Marine sand resources offshore Israel

    Mar. Georesour. Geotechnol.

    (2000)
  • A. Almogi-Labin et al.

    Living Ammonia from a hypersaline inland pool, Dead Sea area, Israel

    J. Foraminifer. Res.

    (1992)
  • A. Almogi-Labin et al.

    Survey of the Brackish Water Habitats of the Israeli Mediterranean Coastal Plain (Summer, 2001), Israel Geological Survey Report TR-GSI/18/01

    (2001)
  • A. Almogi-Labin et al.

    The brackish water foraminifera of the inland Enot Timsah ponds, Mount Carmel coastal plain, Israel

    Isr. Geol. Surv. Curr. Res.

    (2002)
  • A. Almogi-Labin et al.

    Micro-faunal ecosystem of the Timsah springs: environmental and stable isotopes characterization

  • A. Almogi-Labin et al.

    The living and the dead assemblage of the calcareous fauna of Berekhat Nur as a proxy for determining the fluctuations in the quality and stability of the pond system

  • P. Anado'n et al.

    Paleoenvironmental reconstruction of marginal marine environments from combined paleoecological and geochemical analyses on ostracods

  • Z.M. Arnold

    Discorinopsis aguayoi (Bermudez) and Discorinopsis vadescens (Cushman and Brönniman): a study of variation in cultures of living foraminifera

  • Y. Bar Or

    Restoration of the rivers in Israel's coastal plain

    Water Air Soil Pollut.

    (2000)
  • A. Barash et al.

    Fauna Palaestina: Mollusca 1 — Annotated List of Mediterranean Molluscs of Israel and Sinai

    (1992)
  • J.F. Bárcena et al.

    Spatial and temporal flushing time approach in estuaries influenced by river and tide. An application in Suances Estuary (Northern Spain)

    Estuar. Coast. Shelf Sci.

    (2012)
  • P. Bouchet et al.

    Classification and nomenclator of gastropod families

    Malacologia

    (2005)
  • J.S. Bradshaw

    Laboratory studies on the rate of growth of the foraminifer “Streblus beccarii (Linne) var. tepida (Cushman)”

    J. Paleontol.

    (1957)
  • J.H. Cann et al.

    Fossil Quaternary and living foraminifera from athalassic (non-marine) saline lakes, Southern Australia

    J. Paleontol.

    (1981)
  • A. Cearreta et al.

    Late glacial and Holocene environmental changes in Portuguese coastal lagoons 2: microfossil multiproxys reconstruction of the Santo André coastal area

    The Holocene

    (2003)
  • F. Cimerman et al.

    Mediterranean Foraminifera

  • R. Costanza et al.

    The value of the world's ecosystem services and natural capital

    Nature

    (1997)
  • C.J. Crossland et al.

    The coastal zone — a domain of global interactions

  • S.J. Culver

    Benthic foraminifera of Puerto Rican mangrove–lagoon system: potential for paleoenvironmental interpretations

    Palaios

    (1990)
  • S. de Rijk

    Salinity control on the distribution of salt marsh foraminifera (Great Marshes, Massachusetts)

    J. Foraminifer. Res.

    (1995)
  • J.-P. Debenay et al.

    Distribution trends of foraminiferal assemblages in paralic environments: a base for using foraminifera as early warning indicators of anthropic stress

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