Ecostructuring of marine nematode communities by submarine groundwater discharge

Accepted Manuscript Ecostructuring of marine nematode communities by submarine groundwater discharge Katarzyna Grzelak, Joseph Tamborski, Lech Kotwicki, Henry Bokuniewicz PII:

S0141-1136(17)30701-8

DOI:

10.1016/j.marenvres.2018.01.013

Reference:

MERE 4442

To appear in:

Marine Environmental Research

Received Date: 15 November 2017 Revised Date:

19 January 2018

Accepted Date: 21 January 2018

Please cite this article as: Grzelak, K., Tamborski, J., Kotwicki, L., Bokuniewicz, H., Ecostructuring of marine nematode communities by submarine groundwater discharge, Marine Environmental Research (2018), doi: 10.1016/j.marenvres.2018.01.013. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

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Ecostructuring of marine nematode communities by

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submarine groundwater discharge

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Katarzyna Grzelak1,2,*, Joseph Tamborski3,4, Lech Kotwicki1, Henry Bokuniewicz5

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1 Marine Ecology Department, Institute of Oceanology, Polish Academy of Sciences, 81-712 Sopot, Poland

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2 Laboratory of Polar Biology and Oceanobiology, Faculty of Biology and Environmental Protection, University

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of Łódź, 90-237 Łódź, Poland

3 Department of Geosciences, Stony Brook University, Stony Brook, New York, USA

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4 LEGOS, Observatoire Midi Pyrénées, 14 Ave Edouard Belin, 31400 Toulouse, France

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5 School of Marine and Atmospheric Sciences, Stony Brook University, Stony Brook, New York, USA

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*corresponding author: e-mail address: [email protected]

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KEYWORDS

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groundwater seepage, meiofauna, nematode, diversity, coastal zone

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Abstract Inputs of submarine groundwater discharge (SGD) to the coastal ocean may alter local

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and regional-scale biology. Here, we report on nematode assemblages along the north shore of

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Long Island, NY. We test if nematode communities differed between sites impacted by mixed

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fresh-saline SGD and where SGD is exclusively saline. Diversity of nematodes was low at

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sites impacted by fresh SGD and communities were dominated by a few opportunistic genera.

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Moreover, a set of typical freshwater nematode genera restricted to impacted sites was

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observed. Their presence in the marine coastal zone is exceptional and underlines the

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structuring role that fresh SGD plays in the local ecosystem. Saline SGD structured nematode

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assemblages differently compared to sites impacted by fresh SGD. The number of nematode

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genera was markedly higher at saline SGD sites, with a different community structure. This

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study highlights the importance to which inputs of fresh SGD may have on local ecosystem

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diversity in marine coastal environments.

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1. Introduction Submarine groundwater discharge (SGD) is an important vector between marine and

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terrestrial water reservoirs, driven by a hydrological connection between land and the coastal

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ocean. SGD is generally a mixture between fresh, meteoric groundwater driven by a positive

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terrestrial hydraulic gradient and saline, recirculated seawater (i.e. marine groundwater)

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driven by physical forcing mechanisms which include tidal pumping, wave-setup and density-

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driven flow (Burnett et al., 2003; Santos et al., 2012). Such discharge supplies both fresh

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groundwater to lower pore-water salinities and dissolved chemicals, including nitrogen and

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phosphorus (Valiela et al., 1990; Knee and Paytan, 2011). Excess nutrients, as might be

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supplied by SGD (Slomp and Van Cappellen, 2004), influence benthic food webs through the

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stimulation of primary productivity (Sugimoto et al., 2017) and subsequent consumption by

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grazers and detrivores (Posey et al., 2006), which may alter community structure and

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population dynamics of benthic fauna (Widbom and Elmgren, 1988; Rossi and Lardicci,

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2002; Schlacher and Hartwig, 2013). Moreover, changes in surface and pore water salinity,

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due to fresh SGD, can be expected to markedly affect the distribution and zonation of near-

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shore benthic communities (Santoro, 2010; Lee et al., 2017), as well as primary productivity

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and biomass (Kohout and Kolipinski, 1967; Miller and Ullman, 2004; Sugimoto et al., 2017).

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SGD may influence the physical environment by altering the grain-size distribution of bottom

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sediments, enhancing sediment stability and altering the vertical position of the redox and pH

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gradient, all of which effect the distribution of benthic fauna within the sediment (Miller and

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Ullman, 2004; Zipperle and Reise, 2005). SGD might also moderate pore-water temperatures

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and provide a refuge in the sediments for macrofauna against extreme temperatures (Miller

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and Ullman, 2004), because terrestrial groundwater tends to remain at the average, annual, air

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temperature (Anderson, 2005).

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However, SGD’s influence on ecology is poorly known, both on a local and global scale,

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including its role in ecological productivity, composition, diversity and functioning of benthic

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ecosystems. Kohout and Kolipinski (1967) first studied the influence of SGD on marine biota

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in Biscayne Bay, Florida, where they showed that the distribution of benthic communities

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varied with changes in salinity driven by groundwater inputs. Ecological consequences of

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SGD have been presented by e.g. Johannes (1980), Valiela et al. (1990) and Bussmann et al.

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(1999), who found alterations of the structure and function of aquatic communities in coastal

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waters impacted by SGD, such as increased growth of macroalgae and phytoplankton,

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reduction of seagrass beds, or reductions of the associated fauna. Most SGD focused

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investigations use macrofauna as a model taxa (Miller and Ullman, 2004; Silva et al., 2012;

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Encarnacão et al., 2015). The research presented here adds to a spare body of work on the

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impacts of SGD on meiofaunal taxa. Meiofauna is a collective name for organisms less than 500µm in size that inhabit various

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aquatic sediments (Giere, 2009). Most animal phyla are represented as meiofauna (20 of the

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35 metazoan phyla), thus, meiofauna are the most phyletically diverse faunal group. Due to

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their widespread distribution, high abundance and diversity, meiofauna constitutes an

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important structural and functional component of the benthos. In some habitats, including

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beach sediments, meiofauna may rival macrofauna in terms of standing stocks and may

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significantly contribute to secondary production (McLachlan and Brown, 2006). Meiofauna

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are closely associated with the sediment matrix, due to their small body size and limited

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mobility; thus, the biogeochemistry of the surrounding sediments and pore waters may

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significantly affect meiofaunal abundance and diversity (Kennedy and Jacoby, 1999).

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Therefore, meiofauna organisms are implemented in many studies examining the impact of

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natural or anthropogenic disturbances (i.e. organic enrichment) and constitute a valuable tool

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in the assessment of ecological quality status in aquatic ecosystems (e.g. Schratzberger et al.,

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2000; Grzelak et al., 2009; Alves et al., 2015; Semprucci et al., 2017; Schratzberger & Ingels,

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2017). Nematodes and copepods make up the bulk of meiofauna biomass in most marine

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sediments, thus, these two meiofauna taxa are the most studied. Nematodes are used as

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potential indicators of environmental pollution and alteration in marine systems (Gallucci et

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al., 2012; Losi et al., 2013; Semprucci et al., 2015), as they may provide information about

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past and episodic pollution events. Nematode and copepod communities, of various

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interacting species, are uniquely sensitive to different environmental parameters, including

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temperature, pH, dissolved oxygen, oxidation-reduction potential and the heavy metal content

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of the sediment matrix (Moreno et al., 2011; Vanaverbeke et al., 2011; Meadows et al., 2015).

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While meiofauna analysis has been recognized as a tool in marine environmental studies,

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the influence of SGD on meiofaunal assemblages is poorly known. To our knowledge, only

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three studies have focused on meiofaunal assemblages in the regions of groundwater seepage.

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Studies in the coastal zones of France (Migne et al., 2011; Ouisse et al., 2011), Portugal

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(Encarnacão et al., 2013) and Poland (Kotwicki et al., 2014) have shown that SGD can alter

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meiofaunal community characteristics (abundance, diversity, biomass), but this process is

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spatially variable and dependent on the local site characteristics. In France, the abundance and

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distribution among major meiofauna groups did not exhibit differences between a control site

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(no seepage) and a site with fresh groundwater inputs (Ouisse et al., 2011); however, fresh

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SGD increased meiofauna biomass and enhanced total benthic metabolism (Minge et al.,

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ACCEPTED MANUSCRIPT 2011). Groundwater discharge stimulated an increase in meiofauna diversity but had no

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significant impact on meiofauna abundance along the southern coast of Portugal (Encarnacão

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et al., 2013). These findings contrast with the results presented by Kotwicki et al. (2014) from

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a coastal zone in Poland, where markedly lower meiofauna abundances were found at a site

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impacted by fresh SGD. In Poland, dominant taxa (nematodes and harpacticoids) were

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present at significantly lower densities at the fresh SGD impacted site, while significant

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differences in meiofauna assemblages were observed between sites impacted by fresh SGD

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and sites without SGD (Kotwicki et al., 2014). All the above mentioned meiofauna studies

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were performed at a high taxonomic level only. Detailed insight into one of the dominant

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taxa, such as nematodes or harpacticoids, may provide a better understanding of the effect of

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SGD on meiofauna communities, and, subsequently, on the ecological ‘fingerprint’ of SGD in

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the benthic system.

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The purpose of this study was to document meiobenthic community structures at three

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beach sites along the northern coast of Long Island, NY, where SGD inputs were previously

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characterized (Tamborski et al., 2015). Using meiofaunal organisms and free-living nematode

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communities as bioindicators, we hypothesize that SGD has a direct impact on coastal biota

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and can be reflected by changes in diversity patterns. We describe the meiobenthic

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communities in the shallow coastal zone of Long Island Sound, NY, affected by SGD in terms

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of nematode standing stock, structural diversity and functional indices. In this study, we will

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assess if 1) meiofaunal and nematodes assemblages differ between sites under the influence of

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fresh SGD and sites without fresh SGD (i.e. saline SGD driven by tidal seawater

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recirculation) and 2) whether there are nematode genera/species which could be reliably used

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as indicators of fresh SGD inputs.

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2. Material and methods

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2.1. Study site

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The studied area was on the north shore of Long Island, NY in Smithtown Bay in

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southern Long Island Sound (Figure 1). The water depth of Smithtown Bay is less than 20 m,

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salinity ranges from approximately 24.5 to 29.5, and annual water temperature range from -

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1.0 to 28.0 ˚C. The tides are semidiurnal with a tidal range of 2.1 m. Smithtown Bay

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represents a diverse ecosystem that contributes to the social, economic, and ecological

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community. Living marine resources include bluefish, striped bass, winter flounder, fluke,

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scup, tautog, oysters, crabs, lobsters and weakfish (Lopez et al., 2014). Locally, however,

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water quality is impaired by recurring hypoxia (Swanson et al., 2015). Smithtown Bay overlies the thick, unconsolidated Upper-Glacial aquifer of Long

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Island. The semi-circular shoreline geometry of Smithtown Bay concentrates SGD within

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Smithtown Bay, not allowing for full tidal flushing of SGD inputs (Bokuniewicz et al., 2015).

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Total SGD into Smithtown Bay, concentrated within 200 m of the shoreline, has been

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estimated to range between 0.4 x 108 m3 yr-1 to 2.2 x 108 m3 yr-1, and is composed of

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approximately 10 – 20% fresh groundwater (Tamborski et al., 2017a). SGD supplies a

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substantial N flux to Smithtown Bay, which may play an important role in the development of

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summer-time hypoxia (Tamborski et al., 2017a).

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Figure 1. Study area on the north shore of Long Island, NY, USA in Long Island Sound.

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Three beaches were chosen along Smithtown Bay’s shoreline (Table 1; Figs. 1 and 2)

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where SGD had been previously characterized using geochemical methods and airborne

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thermal infrared (TIR) over-flights (Tamborski et al., 2015). Geochemical tracers radium and

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radon are commonly measured to detect SGD (Burnett et al., 2006) and, because terrestrial

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groundwater tends to remain at the average, annual, air temperature (Anderson, 2005), the

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distribution of SGD along the shoreline can also be detected with TIR imagery (Johnson et al.,

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2008). These two methods were previously used in parallel to detect locations of fresh SGD

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and quantify their relative rates along the Smithtown Bay shoreline (Tamborski et al., 2015,

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2017a). The first location, Makamah Beach, showed both a lowered surface water temperature

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anomaly and salinities lower that the adjacent open water between two jetties, indicating fresh

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SGD inputs (Fig. 2a). A second location, Callahan’s Beach, lies before a coastal bluff and was

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ACCEPTED MANUSCRIPT identified as an area of fresh SGD (Fig. 2b). Direct measurements of SGD using vented

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benthic chambers yielded seepage rates between 5 and 47 cm d-1 over a tidal cycle with higher

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rates occurring at low tide (Tamborski et al., 2015). Fresh groundwater persists with depth

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above the high tide mark of the beach, and a well-defined salinity transition zone occurs

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within the intertidal portion of the beach (Tamborski et al., 2017b). Pore waters are well

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oxygenated at Callahan’s Beach and contain elevated levels of anthropogenic NO3-, derived

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from residential wastewater and fertilizer inputs, and does not vary seasonally (Tamborski et

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al., 2017a). A third location, Long Beach (Fig. 2c), was characterized by a lack of a TIR

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anomaly, however, saline (i.e. marine groundwater) SGD occurs at rates between 5 and 28 cm

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d-1 over a tidal cycle (Tamborski et al. 2015). Intertidal pore waters at Long Beach are saline,

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often low in dissolved oxygen and enriched in N due to organic matter remineralization,

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which varies seasonally (Tamborski et al., 2017a). Fresh SGD does not occur at Long Beach;

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this is a site that is not impacted by fresh SGD inputs (hereafter “unimpacted”, for simplicity)

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where saline SGD is driven primarily by tidal pumping. Two sampling sites were chosen at

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both Callahan’s and Makamah beaches based on previous TIR imagery and pore water

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salinity measurements. The first sampling site was an “impacted” site where a prominent

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surface water TIR anomaly was observed, and where surface water and pore water salinities

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were reduced, indicative of fresh SGD. The second site was a nearby, “unimpacted” site

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where a surface water TIR anomaly was not seen, and where pore waters were relatively

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higher in salinity (Table 1; Fig. 2). Because the unimpacted sites are situated on permeable

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sediment and subject to large tidal variations in sea level (~2.1 m), they are likely to be of

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recirculated, saline SGD, like Long Beach. A summary of previously collected environmental

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parameters for each site, over multiple sampling seasons (Tamborski et al., 2015; Tamborski

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et al., 2017a,b) is presented in Table 1.

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188 189 190 191 192 193 194 195 196

Table 1. Sampling stations and ancillary environmental parameters (averaged over multiple sampling months ± one standard deviation). Pore water samples were collected along the low tide shoreline at 50 cm depth below the surface. “Impacted” locations are sites where fresh SGD has been observed and measured, as indicated by the relatively lower pore water salinities; “Unimpacted” locations are sites where fresh SGD is absent and SGD is composed of recirculated seawater, as indicated by the relatively higher pore water salinities (Tamborski et al., 2015, 2017a,b). Sediment descriptors: CS = coarse sand, MS = medium sand, FS = fine sand, MWS = moderately well sorted, PS = poorly sorted. Beach Makamah

Impacted

Lat Lon (°N) (°W) 40.922 73.289

Unimpacted

40.922 73.288

Site

4.0 ± 0.7

DO (µM) 207 ± 20

NO3(µM) 279 ± 6

NH4+ (µM) 0±0

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Salinity

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# Grain Size Sorting months (µm) (µm) 3 296, MS 1.571, MWS 2

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1.471, MWS

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Impacted*

40.921 73.284

25.6 ± 3.1

196 ± 55

120 ± 285

0±1

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947, CS

2.483, PS

Unimpacted

40.919

73.28

27.6 ± 0.2

175 ± 9

11 ± 12

0±0

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537, CS

2.684, PS

Unimpacted* 40.920 73.174

28.2 ± 1.1

168 ± 45

37 ± 31

49 ± 161

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974, CS

2.388, PS

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Figure 2. Airborne TIR imagery of investigated beaches: A) Makamah, B) Callahan’s, C) Long Beach,

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with sampling sites indicated by black dots (TIR maps from Tamborski, 2015). The cooler temperature

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colours along the shoreline are indicators of fresh SGD.

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2.2.Field sampling and sample processing Each field location was sampled in August 2016 for meiofauna analyses (five replicate

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samples) and grain-size analysis (one replicate sample). Samples were taken using a meiocore

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sampler (plexiglass tube) with an inner diameter of 3.6 cm and a sampling surface area of 10

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cm2. Meiocore samplers were inserted to a depth of 10 cm by hand, avoiding sediment

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compaction. In the laboratory, sediments were dried at 60 °C for 24h and sieved through

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twelve 0.5-phi intervals. Grain-size statistics (mean, sorting) were calculated using Gradistat

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software (Blott and Pye, 2001) and sediment characteristics were classified according to Folk

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and Ward (1957). 8

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Bengal stain. To extract the meiofaunal organisms from the sandy sediment, a standard

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decantation method with shaking was used (Pfannkuche and Thiel, 1988). All metazoan

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meiobenthic organisms that retained on a 32 µm mesh size were counted and classified at

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higher taxonomical levels using a stereomicroscope. Nematodes were hand-picked and

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mounted on glass slides in anhydrous glycerin and identified to the genus level under a light

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microscope. All identified nematode specimens were allocated to four trophic groups based

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on buccal morphology, following the Wieser (1953) classification. Nematodes without buccal

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armature were grouped either as: 1A- selective deposit feeders or 1B- non-selective deposit

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feeders. Nematodes with buccal armature were grouped as either 2A- epistrate feeders or 2B-

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predators/omnivores. Representatives of Dorylaimidae, freshwater nematodes that are

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classified as suction-feeders (Traunspurger, 1997), are considered to be predators/omnivores

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here. Nematode identification was based on pictorial keys and relevant taxonomic literature

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(Platt & Warwick, 1983, 1988; Warwick et al., 1998; Fonseca & Decraemer, 2008; Schmidt-

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Rhaesa, 2014; Guilini et al., 2017). At least 200 nematode individuals (or all if sediment

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contained a lower number of individuals) were examined per sediment core.

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2.3.

Data analysis Both

univariate

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and

multivariate

non-parametrical

permutational

ANOVA

(PERMANOVA; Anderson, 2001; Anderson et al., 2008) were used to test for differences in

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meiofauna and nematode characteristics between beaches and sampling sites. Univariate

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descriptors of meiofauna included the total meiofauna density and the number of meiofaunal

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higher taxa. Characteristics of the nematode community were based on the genus richness, the

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expected number of genera for a theoretical sample of 50 specimens (EG(50)), Pielou’s

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evenness (J’) and the index of trophic diversity (θ) (Hurlbert, 1971; Pielou, 1975, Heip et al.,

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1985). The latter was calculated based on the Wieser’s (1953) feeding group classification in

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order to assess the contribution of each trophic group to the total nematode density (Heip et

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al., 1985). Here, trophic diversity is presented as the reciprocal value θ-1, which means that

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higher values correspond to a higher trophic diversity. A two-factor crossed model design was

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used, with ‘beach’ and ‘site’ as fixed factors, with three ‘beach’ (Makamah Beach, Callahan’s

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Beach and Long Beach) levels and two ‘site’ (fresh SGD impacted and non-impacted

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sampling sites) levels, respectively. All calculations of Pseudo-F and p values were based on

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999 permutations of the residuals under a reduced model. Pair-wise comparisons were

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performed when significant P values were obtained. For pair-wise tests, due to a restricted

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permutation p-value (Anderson and Robinson, 2003). The PERMDISP test was used to test

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for homogeneity of multivariate sample dispersion (Anderson et al., 2008), but results were

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never significant, revealing no differences in dispersion. Because Long Beach is only

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classified as ‘unimpacted’, the Long Beach environmental information cannot contribute to

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the comparison between impacted/unimpacted status, or the interaction between factors

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‘Beach’ and ‘Site’. Even though, the PERMANOVA test will still provide unbiased estimates

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of the different effects, and such an unbalanced design does not invalidate the interaction test

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itself.

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Euclidean distance similarity was used to calculate the resemblance matrix based on

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untransformed data for all univariate analyses, while Bray-Curtis similarity matrix, based on

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square-root transformed and presence/absence data, was used for the multivariate analysis of

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the meiofauna and nematode community. Principal coordinate analysis (PCO) was conducted

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to visualize multivariate variability among different sampling stations based on the genera

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community composition data matrix used for the PERMANOVA analysis. Spearman rank

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correlation vectors of nematode genera abundances with axes were overlaid on the PCO plots

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to visualize the relationships between ordination axes and the directions and degrees of

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variability in the biological variables. Additionally, ‘shade plot’ analysis was carried out

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(Clarke et al., 2014) to visualize the abundance matrix of variables against the samples, where

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the intensity of grey-scale shading is proportional to abundance. Nematode genera with

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similar patterns of abundance across sampling stations were clustered together on the resultant

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dendrogram (y-axis of the shade plot). The samples (x-axis) were ordered by sampling

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stations, based on their Bray-Curtis similarities. Only the 20 most abundant genera were

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included in this analysis. Prior to the analyses, meiofauna abundance, nematode abundance

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and other nematode characteristics were integrated from the surface down to 10 cm. All

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analyses were performed with PRIMER and PERMANOVA+ add-on software (Clarke and

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Gorley, 2006; Anderson et al., 2008) and STATISTICA software.

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3.

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3.1.

Results Sediment characteristics

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Sediment grain size distribution pattern, for 0-10 cm of sediment, varied between the

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different study sites investigated here (Table 1, Fig. 3). Overall, the finest substrate was found

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at Makamah beach, where the sediment was moderately well sorted. The remaining sites were

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sites had coarser substrates than the unimpacted sites (Fig. 3).

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Figure 3. Grain size distribution of the beaches and sites investigated here.

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3.2.

Meiofaunal community

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A total of 13 metazoan meiofauna higher taxa (two represented by larval stage

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Copepoda nauplii and Cirripedia nauplii) were identified at the study sites. Nematodes were

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the most abundant (51%), followed by gastrotrichs (18%), harpacticoids (11%) and

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oligochaetes (6%). The remaining taxa collectively represented 14% of all meiofauna

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collected. Between 7 and 11 taxa were recorded at each sampling station, with no significant

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differences in the number of meiofaunal taxa between impacted and unimpacted sites (Table

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2, Fig. 4). Seven taxa were always present, regardless of the site, including Acari, Copepoda

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nauplii, Gastrotricha, Harpacticoida, Nematoda, Ostracoda and Turbellaria. Nematodes

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dominated both impacted and unimpacted locations where they constituted between 50% and

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93% of the total meiofauna density, apart from the Callahan’s unimpacted station, where

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Gastrotrichs outnumbered all other taxa and constituted 76% of the community (Appendix

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Table A1).

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Table 2. PERMANOVA results for the univariate and multivariate descriptors of the meiofauna and nematodes community, with significant pair-wise comparisons results for interaction term ‘BeachxSite’. Abbreviations: C- Callahan’s; M- Makamah; Imp- impacted; unImp- unimpacted.

Meiofauna

299 300 301 302 303

Abundance

Meio taxa

Source df Beach 2 Site 1 BeachxSite 1 Res 20 Beach 2

MS Pseudo-F P(perm) pair-wise contrasts 139.34 1.2781 0.277 219.12 2.0097 0.173 1446.5 13.267 0.005 M: Imp≠unImp 109.03 5.03 5.9881 0.061

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Nematodes

EG(50)

Pielou

Trophic index

Community (multi)

2.9167 6.2024

0.093 0.045

15.787 24.329 16.047

0.001 0.001 0.001

10.28 8.0624 0.1299

0.004 0.015 0.697

38.526 29.095 0.3592

0.001 0.002 0.562

41.773 8.432 16.264

0.001 0.016 0.001

C: Imp≠unImp

25.726 1.0309 20.969

0.001 0.384 0.003

C: Imp≠unImp

4.800 1.153 11.752

0.031 0.341 0.008

C: Imp≠unImp

7.7053 6.8291 2.471

0.001 0.001 0.005

M: Imp≠unImp; C: Imp≠unImp

M: Imp≠unImp; C: Imp≠unImp

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Richness

2.45 6.05 0.84 3563.2 5491.1 3621.8 225.7 3.35E+06 2.63E+06 42320 3.26E+05 223.45 168.75 2.0833 5.8 96.061 19.39 37.4 2.2996 0.1129 4.52E-03 9.20E-02 0.1036 0.997 0.235 2.392 0.204 7059.2 6256.4 2263.8 916.14

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Abundance

1 1 20 2 1 1 20 2 1 1 20 2 1 1 20 2 1 1 20 2 1 1 20 2 1 1 20 2 1 1 20

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Site BeachxSite Res Beach Site BeachxSite Res Beach Site BeachxSite Res Beach Site BeachxSite Res Beach Site BeachxSite Res Beach Site BeachxSite Res Beach Site BeachxSite Res Beach Site BeachxSite Res

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Average meiofauna densities for the upper 10 cm of the sediment varied between 1649

306

± 1294 ind/10cm2 and 3442 ± 964 ind/10cm2 (Appendix Table 1; Fig. 4). Results from the

307

two-way PERMANOVA for meiofauna abundance showed a significant interaction effect

308

between beach and the occurrence of fresh SGD (interaction factor ‘BeachxSite’; Table 2).

309

Post-hoc comparison revealed significant differences between impacted and unimpacted

310

locations only at Makamah beach. Sediments at the impacted Makamah station had

311

significantly higher meiofauna density than those from the unimpacted site (p<0.05, Fig. 4).

312

This pattern was not seen at Callahan’s beach, where impacted and unimpacted locations did

313

not show statistically significant differences in meiofauna densities.

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Figure 4. Meiofauna total density (a) and number of meiofauna taxa (b).

317

Meiofauna multivariate community analyses showed significant differences between

319

investigated beaches and the occurrence of fresh SGD (factors ‘beach’ and ‘site’; Table 2).

320

Each unimpacted site (identified as “M_unImp”, “C_unImp” and “LB_unImp”; Fig.5a)

321

harbored distinct meiofaunal assemblages that were significantly different from the impacted

322

sites (identified as “M_Imp”, “C_Imp”; Figure 5A). Oligochaetes (particularly families

323

Enchytraeidae and Naidinae) and turbellarians occurred in high abundance at fresh SGD

324

impacted sites regardless of differences in grain-size of the substrate. Moreover, unimpacted

325

sites were markedly different from one another in terms of meiofauna community. Long

326

Beach (LB) had the highest abundance of nematodes and harpacticoids; Callahan's Beach was

327

characterized by the presence of gastrotrichs and the unimpacted Makamah site had an overall

328

low abundance of all taxa, with the exception of tardigrades.

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Figure 5. PCO analysis for meiofauna higher taxa based on abundance data (A), nematode assemblages based on abundance data (B) and presence/absence data (C), showing all taxa which were significantly correlated with the PCO coordinates (r>0.75). Genera that were among the 20 most dominant (see Fig. 10) are printed in bold and their vectors are shown as a solid line (B).

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3.3.Nematode community

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Average nematode densities ranged from 373 ± 199 ind. 10cm-2 to 1990 ±821 ind. 10cm-2; the

339

density pattern depends on the both investigated beach and site (the presence or absence of

340

fresh SGD; Table 2). Long Beach (LB) was characterized by the highest nematode density

341

values. Callahan’s and Makamah beaches had markedly lower values in nematode density for

342

the unimpacted locations compared to the impacted locations (Fig. 6a).

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Figure 6. Nematode total density (A), genus richness (B), expected number of genera for 50 individuals (C), Pielou’s evenness (d), and trophic diversity index (e).

348

Significant differences in the number of genera and in genera composition were found

349

between the three beaches and sampling sites. Average genus richness per station was the

350

highest at Long Beach and significantly higher numbers of genera were found at the

351

unimpacted sites when compared to the impacted sites (Table 2, Fig. 6b). The total genera

352

number per sampling stations varied from 24 (Makamah Impacted site) to 51 (Long Beach),

353

but many of the recorded genera occurred in low numbers per station; 29 genera (out of 88

354

recorded in total; Appendix Table A2) occurred with a mean relative abundance >2%. Among

355

the 88 nematode genera that were found, 24 genera were restricted to Long Beach, three

356

genera for Makamah impacted site, six genera per each Makamah unimpacted and Callahan’s

357

impacted stations, while five genera were restricted to Callahan’s unimpacted station (Fig. 7).

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Only six genera were common for all stations (Fig. 7); these were Chromadorina,

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Chromadorita, Daptonema, Metadesmolaimus, Theristus and Xyalidae spp. The latter four

360

genera (all belonging to Xyalidae family) displayed a significant contribution to the nematode

361

community at the investigated stations (Fig. 8). Metadesmolaimus, Daptonema and Theristus

362

dominated at Makamah beach (at both the impacted and unimpacted site) and at the impacted

363

site of Callahan’s beach, where they represented over 60% of the nematode community. This 15

ACCEPTED MANUSCRIPT resulted in significantly lower Pielou’s evenness at those sites (Table 2; Fig. 6d). The index of

365

trophic diversity (θ-1) differed between impacted and unimpacted sites at Callahan’s beach

366

(Table 2); mean trophic diversity was significantly higher at the unimpacted station

367

(2.69±0.55 vs. 1.52±0.14, respectively), while no differences were detected between the two

368

sampling sites at Makamah beach (Fig. 6e). In general, the highest mean trophic diversity was

369

observed for Long Beach (LB; 2.78±0.47). Each of the sampling stations were dominated by

370

non-selective deposit feeders (1B; average 42.5-92.1%), followed by predators and omnivores

371

(2B; average 6.0-33.2%). The contribution of epistrate feeders (2A) to the total number of

372

genera varied from 1.7% to 21.8%, but this feeding guild was always lower in abundance.

373

Selective deposit feeders (1A) were the least common group at all sites. This feeding group

374

was absent entirely at the impacted site at Makamah while, at other stations, their contribution

375

to the total number of genera ranged from 0.2% to 8.2%.

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Figure 7. Veen diagram showing the shared and restricted number of nematode genera between the investigated sites.

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Figure 8. Community structure of nematode assemblage at the investigated stations.

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The results for the nematode multivariate community analyses based on nematode

384

genera abundance showed significant differences between beaches and sites (Table 2). Pair-

385

wise comparison revealed that fresh SGD impacted stations harbor markedly different

386

nematode communities in comparison to unimpacted sites. Moreover, Long Beach was

387

distinct from all other sites (Figs. 5b,c, 8, 9). PCO plots based on nematode genera abundance

388

and presence/absence data clearly illustrates the extent to which sites differ (Fig. 5b,c).

389

Separation of the nematode assemblages is very similar and distinctive, regardless of the

390

transformation used (square-transformation of abundance data or presence/absence data),

391

indicating that the observed differences are connected not only with differences in abundance

392

of genera but also by the presence or absence of particular nematode genera. The genera

393

vectors indicate that Tripyla, Eutobrilus, Eudorylaimus, Anaplectus, Epidorylaimus and

394

Achromadora were the most important in shaping the nematode communities at the impacted

395

locations; Metadesmolaimus was the most significant genera for the unimpacted station at

396

Makamah, while the presence of Enoplolaimus, Ascolaimus and Microlaimus were distinctive

397

for the unimpacted station at Callahan’s beach. The nematode community structure at Long

398

Beach contained a markedly different set of nematode genera, including Sabatieria,

399

Pseudodesmodora, Stygodesmodora, Perepsilonema, Metepsilonema and Thrichotheristus.

400

These genera were not only abundant at this site (Fig. 5), but together with Setosabatieria,

401

Pseudochromadora, Kosswigonema and Pselionema, these nematode genera appeared

402

exclusively in the sediment of Long Beach (Fig. 5c).

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ACCEPTED MANUSCRIPT Patterns of genera abundance and the shift in their occurrence across the stations were

404

pronounced, with notable distinctions between impacted and non-impacted SGD sites (Fig. 9).

405

A common set of genera for Long Beach and the unimpacted locations can be distinguished

406

from the fresh SGD impacted sites; these genera are exclusive to the unimpacted locations

407

and include Sigmophoranema, Hypodontolaimus, Rhynchonema, Bolbolaimus, Microlaimus,

408

Camacolaimus, and Paracanthonchus (Figs. 5b,c and 9). Genera that appeared exclusively at

409

impacted locations with fresh SGD include Mononchus, Tobrilus, Eudorylaimus,

410

Epidorylaimus, Tripyla, Anaplectus, and Mesocanthion (Appendix Table A2). The list of

411

genera that are highly correlated with the POC axes and explain most of the variability in

412

nematode communities among the investigated stations (Fig. 5) corresponds well with the list

413

of dominant genera (Fig. 9).

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415 416 417 418 419 420 421

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Figure 9. Shade plot of the 20 most abundant genera at the sampling sites. Different colour shades indicate abundance intensity. On the left side: examples of characteristic nematode genera for impacted (filled symbol) and unimpacted (hollow symbol) stations at Callahan’s (square) and Makamah (circle) beaches, and the unimpacted Long Beach site (cross). Drawings made by the first author, based on the images captured nematode individuals.

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4.

Discussion Submarine groundwater discharge is a well-recognized process along the north shore

425

of Long Island, NY, supplying large nitrogen loadings to surface waters (Garcia-Orellana et

426

al., 2014; Bokuniewicz et al., 2015; Young et al., 2015; Tamborski et al; 2017a;). Along the

427

north shore of Long Island, permeable sandy sediments facilitate relatively high fresh

428

groundwater seepage rates, while physical processes, including tidal pumping, produce a

429

considerable flux of recirculated seawater SGD (Tamborski et al., 2015; Tamborski et al.,

430

2017a). The freshwater component of SGD might be up to 20% of the total SGD within the

431

first 200 m of the Long Island Sound shoreline, and is volumetrically equivalent to riverine

432

inputs (Tamborski et al., 2017a). Large inputs of fresh SGD along the north shore of Long

433

Island may directly influence coastal ecology, including benthic communities (e.g. Waska and

434

Kim, 2010; Welti et al., 2015; Sugimoto et al., 2017).

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In the investigated area of Long Island, the observed habitat alteration caused by SGD

436

had a pronounced effect on the meiobenthic communities. Density and diversity of

437

meiobenthic assemblages are driven by sediment grain size (Steyaert et al., 1999;

438

Vanaverbeke et al., 2002), which also controls groundwater seepage rates as a function of

439

permeability and hydraulic conductivity (Waska and Kim, 2010; Kotwicki et al., 2014).

440

Coarse-grained sediments support higher nematode densities and a more diverse nematode

441

community (Rodriguez et al., 2003; Gheskiere et al., 2005), because coarser-grained

442

sediments offer larger interstitial spaces between sediment grains and a wider variety of

443

potential food items that can be utilized by nematodes (Vanaverbeke et al., 2011). However,

444

for Long Island Sound, we did not observe a relationship between meiofauna and nematode

445

univariate parameters (i.e. total meiofauna abundance, number of meiofauna taxa, nematode

446

abundance, diversity) with respect to sediment grain size. This is despite the presence of

447

markedly coarser sediment at Callahan’s Beach and Long Beach (mean grain size > 500µm)

448

compared to Makamah beach, where much finer-grained sediment was observed (mean grain

449

size < 250 µm; Figure 3). The number of meiofauna taxa did not differ between investigated

450

sites and beaches (Table 2), while meiofauna density and nematode characteristics were rather

451

driven by SGD-related variables.

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In general, the number of nematode genera and the values of most diversity indices

453

were higher at the unimpacted sites (Fig. 6). In terms of total meiofauna abundance, the

454

opposite trend was found, where the density of nematodes was significantly higher at the

455

impacted sites of Makamah and Callahan’s beaches with respect to the unimpacted sites.

456

Greater nematode abundances at sites with fresh SGD are likely driven by the local 19

ACCEPTED MANUSCRIPT geochemical conditions. High dissolved oxygen (DO), together with low NH4+ and high NO3-

458

(Table 1), may influence the spatial distribution of the bacterial community. Fresh SGD-

459

driven NO3- inputs can stimulate autotrophic growth and primary production (Valiela et al.,

460

1990; Santos et al., 2013), and may contribute to greater phyto-detritus sedimentation and

461

microphytobenhtos biomass. Sinking phyto-detritus is mineralized by bacterial degradation,

462

which in turn may attract bacterivorous meiofauna and/or epistrate feeding nematodes that

463

can graze on microphytobenthos and support overall nematode densities at impacted sites

464

(Table 2, Fig.6). Moreover, other meiobenthic taxa, such as oligochaetas, acari and

465

turbellarians, may take advantage of the specific environmental conditions supplied by fresh

466

SGD. The high occurrence of Enchytraeidae and Naidinae oligochaete representatives at the

467

impacted sites of Callahan’s and Makamah beach (Fig.5a; Table A1) underlines favorable

468

conditions for these euryhaline opportunistic brackish-water organisms (Giere and

469

Pfannkuche, 1982, Silva et al., 2012; Leitão et al., 2015). Similarly, many halacarid mites can

470

withstand a range of salinities, while certain species are specialized inhabitants of

471

subterranean groundwater (Giere, 2009). Enhanced abundance of organisms at SGD impacted

472

sites is in agreement with previous macrobenthic studies (Zipperle&Reise, 2005; Encarnacão

473

et al., 2015; Leitão et al., 2015). However, our results are in contrast with previous

474

observations for SGD impact on meiofauna abundance along a coastal zone in Portugal and

475

Poland (Encarnacão et al., 2013; Kotwicki et al., 2014), where SGD had a negative or at least

476

neutral impact on meiofaunal abundance. Thus, the response of nematode abundance to the

477

presence of groundwater discharge is not always unequivocal and may positively influence

478

meiofaunal abundance, as observed herein.

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The nematode community of Long Island’s north shore is clearly influenced by the

480

presence of SGD. At the investigated beaches, communities associated with lower salinity and

481

higher nutrient concentrations (impacted sites; Table 1) were markedly different from those

482

associated with higher salinity and lower nutrient concentrations (unimpacted sites; Figs.5 and

483

9). Salinity and oxygen availability have a direct effect on the structure of intertidal

484

nematodes communities (Soetaert et al., 1995; Steyaert et al., 2007; Alves et al., 2013), and is

485

well documented for estuarine systems (e.g. Adão et al. 2009; Alves et al., 2015). Similarly to

486

the abovementioned studies, nematode communities at Makamah and Callahan’s sites

487

impacted by fresh SGD comprised a relatively low number of genera (<30), with few

488

dominant genera (Figs.6 and 8). Four genera (Metadesmolaimus, Daptonema, Theristus,

489

Tripyla) outcompeted other nematodes at the Callahan’s Beach and Makamah Beach

490

impacted sites, comprising a very high percentage of the overall nematode density (65-75%,

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ACCEPTED MANUSCRIPT respectively; Fig. 8). This observation is in accordance with other studies, which have shown

492

that Metadesmolaimus, Daptonema and/or Theristus exhibit ability to overcome salinity

493

fluctuations and tolerate low-oxygen conditions (Heip et al., 1985; Forster, 1998; Guilini et

494

al., 2012; Alves et al., 2015). Groundwater seeps are sites of not only significantly reduced

495

salinity, but also increased nutrient fluxes that alter local biogeochemical cycles (Waska and

496

Kim, 2011) and may thus contribute to oxygen depletion in sediments. Overall, such

497

conditions may hamper the development of a diverse nematode community. SGD-associated

498

genera along the north shore of Long Island (Metadesmolaimus, Daptonema, and Theristus)

499

can withstand variable salinity and dissolved oxygen conditions with respect to other genera

500

with a narrower ecological amplitude. Adaptation to stressful environmental conditions, as

501

related to body morphology, may be the cause of high local success of opportunistic genera as

502

Daptonema or Metadesmolaimus. Their elongated body, and thus, higher surface-area/volume

503

ratio, increase the capacity for oxygen uptake and may be advantageous for organisms to

504

actively move through the sediment (Jensen, 1987; Soetaert et al., 2002). Many opportunistic

505

genera are also characterized by trophic plasticity and can easily switch between different

506

food sources (Vanhove et al., 2000; Moens et al., 2005; Pasotti et al., 2012), an advantage in a

507

disturbed habitat where food resources may become limited or are temporarily variable.

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Aside from the abovementioned dominant genera, there appears to be a set of

509

nematode genera specific to sites impacted by fresh SGD (Figs. 5 and 9). Genera exclusively

510

found at sites with fresh SGD were Anaplectus, Epidorylaimus, Eudorylaimus, Mononchus cf,

511

Tobrilus/Eutobrilus and Tripyla, where they contributed approximately 15% to the total

512

nematode abundance at each impacted site. All of these genera belong to typical freshwater or

513

terrestrial habitats (Simmons et al., 2009; Schmidt-Rhaesa, 2014; Kerfahi et al., 2017), and

514

are only occasionally found in brackish waters. Occurrence of freshwater nematodes

515

including Anaplectus, Eudorylaimus, Tripyla, and Torbilidae representatives (e.g. Tobrilus)

516

have been previously noted in oligo-haline zones of estuaries (Ferrero et al., 2008; Adaõ et al.

517

2009; Alves et al., 2013) and at arctic beaches after ice melt (Urban-Malinga et al., 2009).

518

However, the presence of freshwater nematodes in a marine coastal zone, as found in the

519

present study, is exceptional and underlines the structuring role that fresh SGD plays in the

520

local ecosystem. The presence of freshwater nematodes in Long Island Sound reflects the

521

long-term influence of freshwater outflow to the coastal ocean at the impacted sites. In this

522

regard, freshwater nematode genera can be treated as indicators of fresh groundwater

523

discharge and could support conventional geochemical and geophysical SGD monitoring

524

activities, thus offering complementary information on the ecological impact of SGD. Habitat

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ACCEPTED MANUSCRIPT modification created by fresh SGD has a direct effect on the structural complexity of

526

nematode assemblages and local biodiversity. Freshwater taxa increase the species pool in the

527

subtidal zone and may impact trophic interactions. The abovementioned freshwater genera are

528

relatively large in size (~1.5-2.5cm in length), making them an important link in the food

529

chain. Such large nematodes may be better prey than smaller sized nematodes to higher-level

530

consumers, particularly to macrofauna and juvenile bottom-feeding fish (Spieth et al., 2011),

531

including the commercially important winter flounder (Pseudopleuronectes americanus) that

532

is found in the coastal waters of Long Island (e.g. Yencho et al., 2015). Therefore, fresh SGD

533

can locally alter all trophic levels, from bacteria, through primary producers and up to higher

534

consumers (Dale and Miller, 2008; Welti et al., 2015; Lee et al., 2017).

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Distinct faunal assemblages were also observed for non-impacted sites (sites without

536

fresh SGD; Table 1). The presence of recirculated, saline SGD structured nematode

537

assemblages differently than sites impacted by fresh SGD (Fig. 5). The number of nematode

538

genera were markedly higher at non-impacted sites (Fig. 6), with a highly different

539

community structure (Fig. 5 and 8). There were a number of nematode genera shared between

540

and restricted to non-impacted sites (Figs. 5 and 7), including Sigmophoranema,

541

Hypodontolaimus,

542

Pseudodesmodora and Paracanthonchus. Furthermore, 24 additional genera were restricted to

543

Long Beach, with Perepsilonema, Metepsilonema, Thrichotheristus, Stygodesmodora,

544

Sabatieria, and Setosabatieria as dominant nematode genera. The majority of the genera

545

restricted to non-impacted sites are commonly encountered in intertidal and subtidal areas

546

worldwide (e.g. Semprucci et al., 2010; Maria et al., 2013). Many of these genera are

547

characterized by coarse cuticle and numbers of long setae (cephalic, somatic and/or

548

ambulatory), which appears as a morphological adaptation to sediment instability and may be

549

used to facilitate an organisms’ mobility (Raes et al., 2006). Such body characteristics seem to

550

be particularly necessary at Long Beach, a barrier beach with dynamic hydrological

551

conditions. The exclusive presence of Epsilonematidae (Perepsilonema, Metepsilonema) at

552

Long Beach, which are morphologically and ecologically well-adapted to physical

553

disturbances (Reas and Vanreusel, 2006), and a high abundance of Rhynchonema at this site,

554

both seem reflect the prevailing physical conditions at Long Beach. A high number of genera

555

restricted to Long Beach suggests that the biogeochemical conditions in the sediments are the

556

most favorable for nematodes at this site, enabling the establishment of the most diverse

557

community in the study area. Co-existence of genera with different feeding modes and life-

Bolbolaimus,

Microlaimus,

Camacolaimus,

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history strategies indicates the availability of complex environmental niches that can be

559

occupied by nematodes at Long Beach. The site-specific nematode assemblages and high variability of nematodes at a small

561

spatial scale demonstrates how fresh SGD is an important structuring factor within seemingly

562

homogenous sediments. Temporally and spatially variable SGD, and thus variable

563

geochemical conditions, create different microhabitats that influence the diversity of

564

nearshore nematodes. Nematodes not only play an important role in ecosystem functioning

565

but may also be used as environmental indicators, a potentially desirable tool in the

566

assessment of habitat alteration as it may relate to environmental management (Schratzberger,

567

2012). Meiofaunal assemblages can reflect ecological quality of the vulnerable coastal

568

ecosystem and thus are important in the assessment of ecosystem state and change

569

(Schratzberger, 2012; Alves et al., 2013; Semprucci et al., 2013). Long Island Sound is a

570

naturally stressed area due to freshwater discharge and is subjected to increased

571

anthropogenic stresses connected with concentrated human activities along the shore (Latimer

572

et al., 2014). Therefore, information regarding the biodiversity and functionality of Long

573

Island Sound’s waters are essential for proper coastal zone management plans. The usefulness

574

of nematode assemblages and their attributes in the discrimination of environmental quality

575

may prove important from this perspective.

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5. Conclusions The present work represents the first study examining the influence of submarine

579

groundwater discharge (SGD) on intertidal nematode assemblages. Our results highlight the

580

sensitivity of nematodes to habitat alteration caused by fresh SGD. SGD to the nearshore

581

marine zone affects the local meiofauna and nematode assemblages, in terms of both

582

abundance and community composition, providing a unique set of environmental conditions

583

for freshwater nematode genera to be present in a marine environment. Fresh SGD drives

584

small-scale, local changes in the distribution of nematodes and hampers their overall

585

diversity. However, fresh SGD increases the regional biodiversity by providing the habitat for

586

freshwater and brackish water adopted fauna. Maintenance of biodiversity is considered to be

587

essential to ecosystem stability (Loreau et al., 2001), thus, the impact of fresh groundwater to

588

the nearshore environment requires further investigations.

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6. Acknowledgments We gratefully acknowledge Molly Graffam (SOMAS) for help during field work and David

593

Hirschberg for nutrients analyses. Oleksandr Holovachov (Swedish Museum of Natural

594

History), Daniel Leduc (NIWA) and Reyes Peña Santiago (Universidad de Jaén) are greatly

595

acknowledged for their comments on some nematode identification. We are also much

596

grateful to Prof. K.R. Clarke (PML) for his advice on statistical analysis performed with use

597

of PERMANOVA+. Special thanks go to Adam Kubicki (Geo Group Wilhelmshaven) who

598

prepared the map of Long Island. This study was completed thanks to funding provided by

599

The Kosciuszko Foundation through a fellowship to KG for conducting research at Stony

600

Brook University. The current position of the first author is funded by a FUGA Postdoctoral

601

Fellowship, Polish National Science Centre (grant no. 2016/20/S/NZ8/00432). HJB and JJT

602

acknowledge funding by NY Sea Grant (project R/CMC-12).

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Alves, A.S., Adão, H., Ferrero, T.J., Marques, J.C., Costa, M.J., Patricío, J. 2013. Benthic meiofauna as indicator of ecological changes in estuarine ecosystems: The use of nematodes in ecological quality assessment. Ecological Indicators 24, 462-475

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Alves, A.S., Caetano, A., Costa, J.L., Costa, M.J., Marques, J.C. 2015. Estuarine intertidal meiofauna and nematode communities as indicator of ecosystem’s recovery following mitigation measures. Ecological Indicators 54, 184-196

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Anderson, M. 2005. Heat as a ground water tracer. Ground Water 43, 951-968

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Anderson, M.J. 2001. A new method for non-parametric multivariate analysis of variance. Austral Ecology 26, 32-46

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Anderson, M.J., Robinson, J. 2003. Generalized discriminant analysis based on distances. Australian & New Zealand Journal of Statistics 45, 301–318

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Anderson, M.J., Gorley, R.N., Clarke, K.R. 2008. PERMANOVA for PRIMER: guide to software and statistical methods. PRIMER–E Ltd., Plymouth, United Kingdom, 214pp.

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Blott SJ, Pye K. 2001. Gradistat: a grain size distribution and statistics package for the analysis of unconsolidated sediments. Earth Surface Processes and Landforms 26, 1237-1248

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Bokuniewicz, H., Cochran, J.K., Garcia-Orellana, J., Rodellas, V., Daniel, J.W., Heilbrun, C. 2015. Intertidal percolation through beach sands as a source of 224,223Ra to Long Island Sound, New York, and Connecticut, United States. Journal of Marine Research 73, 123-140

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Burnett, W.C., Bokuniewicz, H., Huettel, M., Moore, W.S., Taniguchi, M., 2003. Groundwater and pore water inputs into the coastal zone. Biogeochemistry 66, 3–33

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Appendix

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Table 1. Mean abundance (individuals per 10cm2) of meiofauna taxa at the investigated sites. Values denote data for the upper 10 cm of the sediment ±SD

Rotifera

mean SD mean SD mean SD mean SD

Tardigrada Turbellaria

886 887

0.6 0.9 25.4 10.7 11.2 12.7 1648.8 1291.4

AC C

Total

23.8 29.4 20.8 45.4 50.8 19.1 3441.8 964.7

TE D

mean SD

EP

Polychaeta

33

Long Beach unimpacted 3 2.2 6.6 6.1 685 340.6 253.8 175.0 24 14.7 1989.8 822.0 70.6 72.7 17.6 16.8

RI PT

Callahan’s impacted unimpacted 193.2 59 203.3 72.4 0.4 1.4 0.5 2.6 6 2426.4 5.1 1903.3 124.6 36.6 62.7 9.0 32.8 17.2 31.1 20.4 1005.6 373 359.7 199.0 340.2 91.6 179.7 52.7 61.8 22 51.5 12.5

SC

Makamah impacted unimpacted 64 10.4 36.1 7.3 2.6 5.3 66.4 0.6 71.4 0.9 657.6 29.8 390.9 16.6 116 13 119.1 11.0 1950.8 1534.2 717.7 1257.5 419 184.5 70 23.6 37.7 16.3

M AN U

Site location Acari mean SD Collembola mean SD Gastrotricha mean SD Harpacticoida mean SD Nauplii copep. mean SD Nauplii cirrip. mean SD Nematoda mean SD Oligochaeta mean SD Ostracoda mean SD Taxon

57.6 53.5 205.2 133.6 2027.4 724.6

24.6 13.7 118.6 24.6 3170.4 1711.0

53 38.9 6 2.5 66.8 43.6 3176.2 1243.8

ACCEPTED MANUSCRIPT Table 2. Nematode genus list (in an alphabetic order) recorded during the study in the investigated area of the Long Island; a-absent, p-present Makamah Callahan’s impacted unimpacted impacted unimpacted

EP

a a a a a p p a p p p p a a a p a p p p a a p a p a p p a a p a a a a a p a p p a a

34

a p a a a a p p p a a p p p a p a p p a p a p p p p p a a a a a a p p p p p p a a p

RI PT

p a p a a a a a a a a a a a p p a p p a a a p a p a a a p p a a p a a a a a a p p a

Long Beach unimpacted

SC

p a a a p p p a p p p p a a p a p p p a a a p a a a p p a a a p a a a a p a a p a a

M AN U

p a p p a a p a a a a a a a a a a p p a a p p a p a p p a p a a a a a a a a a a p a

TE D

Site Genus / location Achromadora Ammotheristus Anaplectus Anoplostoma Araeolaimus Ascolaimus Axonolaimus Bathyeurystomina Bolbolaimus Bradylaimus Camacolaimidae sp Camacolaimus Ceramonema Chaetonema Chromadora Chromadorella Chromadoridae sp. Chromadorina Chromadorita Cobbia Comesomatidea sp. Cyatholaimus Daptonema Dasynemella Dichromadora Disconema Echinodesmodora Enoplolaimus Epacanthion Epidorylaimus Epsilonema Euchromadora Eudorylaimus Eurystomina Fenestrolaimus Halalaimus Hypodontolaimus Kosswigonema Latronema Leptolaimus Mesacanthion Metacomesoma

AC C

888 889

ACCEPTED MANUSCRIPT

EP

AC C

p a p a a a a p a p a p p p p a p a p a a p a a a a a p a a p a a a a a p a a a p a p p p a

890

35

p p p a a a p p a a a a p a a p p p p p a p a p p p p p p p p p p a p a p a p a a p p a a p

RI PT

p a a p p a p a a a a p a a a p a a a a p a a a a a a a a a a a a p a p p p a p a a p p p p

SC

p a p a a p p p p a p p p p a p p a p a a p a p a a p p a a p a p p a a p a a a a a p p a a

M AN U

p a a a p a p p a a a a a p a p a a a a a a p a a a a a a a a a a a a a p p a p a a a p a a

TE D

Metadesmolaimus Metepsilonema Microlaimus Monochidae Mononchus cf Monoposthia Neochromadora Neonyx Nudora Odontophora Oncholaimellus Oncholaimus Paracanthonchus Paracyatholaimus Paramicrolaimus Paramonhystera Parodontophora Perepsilonema Polygastrophora Pomponema Pontonema Procamacolaimus Prochromadora Prochromadorella Pselionema Pseudochromadora Pseudodesmodora Rhynchonema Sabatieria Setosabatieria Sigmophoranema Spirinia Stygodesmodora Stylotheristus Synonchiella Thalassomonhystera Theristus Tobrilus_Eutobrilus Trichotheristus Tripyla Trissonchulus Trochamus Viscosia Xyalidae spp. Xyalidae sp2 Xyalidae sp3

ACCEPTED MANUSCRIPT 1

Appendix

2 3 4

Table 1. Mean abundance (individuals per 10cm2) of meiofauna taxa at the investigated sites. Values denote data for the upper 10 cm of the sediment ±SD

Rotifera

mean SD mean SD mean SD mean SD

Tardigrada Turbellaria

5 6

0.6 0.9 25.4 10.7 11.2 12.7 1648.8 1291.4

AC C

Total

23.8 29.4 20.8 45.4 50.8 19.1 3441.8 964.7

TE D

mean SD

EP

Polychaeta

1

Long Beach unimpacted 3 2.2 6.6 6.1 685 340.6 253.8 175.0 24 14.7 1989.8 822.0 70.6 72.7 17.6 16.8

RI PT

Callahan’s impacted unimpacted 193.2 59 203.3 72.4 0.4 1.4 0.5 2.6 6 2426.4 5.1 1903.3 124.6 36.6 62.7 9.0 32.8 17.2 31.1 20.4 1005.6 373 359.7 199.0 340.2 91.6 179.7 52.7 61.8 22 51.5 12.5

SC

Makamah impacted unimpacted 64 10.4 36.1 7.3 2.6 5.3 66.4 0.6 71.4 0.9 657.6 29.8 390.9 16.6 116 13 119.1 11.0 1950.8 1534.2 717.7 1257.5 419 184.5 70 23.6 37.7 16.3

M AN U

Site location Acari mean SD Collembola mean SD Gastrotricha mean SD Harpacticoida mean SD Nauplii copep. mean SD Nauplii cirrip. mean SD Nematoda mean SD Oligochaeta mean SD Ostracoda mean SD Taxon

57.6 53.5 205.2 133.6 2027.4 724.6

24.6 13.7 118.6 24.6 3170.4 1711.0

53 38.9 6 2.5 66.8 43.6 3176.2 1243.8

ACCEPTED MANUSCRIPT Table 2. Nematode genus list (in an alphabetic order) recorded during the study in the investigated area of the Long Island; a-absent, p-present Makamah Callahan’s impacted unimpacted impacted unimpacted

EP

a a a a a p p a p p p p a a a p a p p p a a p a p a p p a a p a a a a a p a p p a a

2

a p a a a a p p p a a p p p a p a p p a p a p p p p p a a a a a a p p p p p p a a p

RI PT

p a p a a a a a a a a a a a p p a p p a a a p a p a a a p p a a p a a a a a a p p a

Long Beach unimpacted

SC

p a a a p p p a p p p p a a p a p p p a a a p a a a p p a a a p a a a a p a a p a a

M AN U

p a p p a a p a a a a a a a a a a p p a a p p a p a p p a p a a a a a a a a a a p a

TE D

Site Genus / location Achromadora Ammotheristus Anaplectus Anoplostoma Araeolaimus Ascolaimus Axonolaimus Bathyeurystomina Bolbolaimus Bradylaimus Camacolaimidae sp Camacolaimus Ceramonema Chaetonema Chromadora Chromadorella Chromadoridae sp. Chromadorina Chromadorita Cobbia Comesomatidea sp. Cyatholaimus Daptonema Dasynemella Dichromadora Disconema Echinodesmodora Enoplolaimus Epacanthion Epidorylaimus Epsilonema Euchromadora Eudorylaimus Eurystomina Fenestrolaimus Halalaimus Hypodontolaimus Kosswigonema Latronema Leptolaimus Mesacanthion Metacomesoma

AC C

7 8

ACCEPTED MANUSCRIPT

EP

AC C

p a p a a a a p a p a p p p p a p a p a a p a a a a a p a a p a a a a a p a a a p a p p p a

9

3

p p p a a a p p a a a a p a a p p p p p a p a p p p p p p p p p p a p a p a p a a p p a a p

RI PT

p a a p p a p a a a a p a a a p a a a a p a a a a a a a a a a a a p a p p p a p a a p p p p

SC

p a p a a p p p p a p p p p a p p a p a a p a p a a p p a a p a p p a a p a a a a a p p a a

M AN U

p a a a p a p p a a a a a p a p a a a a a a p a a a a a a a a a a a a a p p a p a a a p a a

TE D

Metadesmolaimus Metepsilonema Microlaimus Monochidae Mononchus cf Monoposthia Neochromadora Neonyx Nudora Odontophora Oncholaimellus Oncholaimus Paracanthonchus Paracyatholaimus Paramicrolaimus Paramonhystera Parodontophora Perepsilonema Polygastrophora Pomponema Pontonema Procamacolaimus Prochromadora Prochromadorella Pselionema Pseudochromadora Pseudodesmodora Rhynchonema Sabatieria Setosabatieria Sigmophoranema Spirinia Stygodesmodora Stylotheristus Synonchiella Thalassomonhystera Theristus Tobrilus_Eutobrilus Trichotheristus Tripyla Trissonchulus Trochamus Viscosia Xyalidae spp. Xyalidae sp2 Xyalidae sp3

ACCEPTED MANUSCRIPT Highlights - fresh submarine groundwater discharge has significant impact on local diversity - presence of recirculated, saline SGD structured nematode assemblages differently than sites impacted by fresh SGD. - presence of freshwater nematodes in a marine coastal zone, underlines the structuring role that fresh SGD plays in the local ecosystem

AC C

EP

TE D

M AN U

SC

RI PT

- fresh SGD can locally alter all trophic levels, from bacteria, through primary producers and up to higher consumers