An assessment of seabird influence on Arctic coastal benthic communities

    An assessment of seabird influence on Arctic coastal benthic communities Katarzyna Zmudczy´nska-Skarbek, Piotr Balazy, Piotr Kuklinski PII: DOI: Reference:

S0924-7963(14)00318-2 doi: 10.1016/j.jmarsys.2014.11.013 MARSYS 2661

To appear in:

Journal of Marine Systems

Received date: Revised date: Accepted date:

25 April 2014 21 November 2014 24 November 2014

Please cite this article as: Zmudczy´ nska-Skarbek, Katarzyna, Balazy, Piotr, Kuklinski, Piotr, An assessment of seabird influence on Arctic coastal benthic communities, Journal of Marine Systems (2014), doi: 10.1016/j.jmarsys.2014.11.013

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ACCEPTED MANUSCRIPT An assessment of seabird influence on Arctic coastal benthic communities Katarzyna Zmudczyńska-Skarbeka*, Piotr Balazyb, Piotr Kuklinskib, c a

University of Gdańsk, Department of Vertebrate Ecology and Zoology, Wita Stwosza 59, 80-308 Gdańsk,

Polish Academy of Sciences, Institute of Oceanology, Marine Ecology Department, Powstańców Warszawy

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Poland

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55, 81-712 Sopot, Poland

Natural History Museum, Department of Life Sciences, Cromwell Road, London SW7 5BD, United Kingdom

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Corresponding author: [email protected], tel. (fax) +48 585236141

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ACCEPTED MANUSCRIPT Abstract It is well recognized that seabirds, particularly those nesting in coastal colonies, can provide significant nutrient enrichment to Arctic terrestrial ecosystems. However, little is known about the fate of bird-derived nutrients that

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return to the marine environment and potentially concentrate below the colonies. To attempt to assess the

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influence of this potential nutrient enrichment of the coastal benthic community, samples of macroalgae, sea

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urchins (mainly algivores), and hermit crabs (scavengers) were collected at two Arctic localities (Spitsbergen), (1) below a mixed colony of guillemots and kittiwakes, and (2) in an adjacent geomorphologically similar location not influenced by the seabirds colony. A much higher nitrogen stable isotope ratio (δ15N) and total

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nitrogen content were found in terrestrial plants sampled below the colony than away from it. In benthic macroalgae, however, there were no δ15N differences. This might result from the timing of an intensive growth

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period in macroalgae in late winter/early spring, when there is little or no runoff from the land, and/or ornithogenic nutrients being directly incorporated by phytoplankton. Sea urchins showed higher δ15N and total N in the control site comparing to the colony-influenced area, suggesting differential food sources in their diet and

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a role of scavenging/carnivory on higher trophic levels there. Opportunistically feeding hermit crabs showed

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δ15N and total N enrichment below the seabird colony, suggesting dependence on detritus derived from food chains originating from pelagic producers. Our results indicate that seabirds in the Arctic may fertilize coastal

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benthic communities through pelagic-benthic coupling, while having no direct impact on bottom primary production.

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Keywords: benthos; guano; nutrients; seabirds; Spitsbergen; stable isotopes

1. Introduction

Arctic terrestrial ecosystems typically reach their greatest levels of development close to the coast, and are otherwise characterized by very low primary production. A range of factors, including short growing season, low temperatures and liquid water availability, presence of permafrost, and chronic nutrients deficiency underlie this low productivity (Callaghan, 2011). In parallel, low levels of nutrients such as nitrogen and phosphorus lead to low productivity in the upper layers of the Arctic deep open seas (Thomas et al., 2008). However, locally intense production occurs at the outflow of Atlantic and Pacific waters, and the Siberian and North American rivers as a result of relatively high nutrient inputs (Dunton et al., 2006; Fichot, et al. 2013; Thomas et al., 2008). Additionally intense nutrient influx takes place near the sea ice margin and over the continental shelf due to

ACCEPTED MANUSCRIPT vertical mixing of water masses (Bluhm and Gradinger, 2008; Hunt and Megrey, 2005; Saskaug, 2004;Wassmann et al., 2006). In the latter situation, nutrients from the bottom water and sediments are thereby brought to the surface and made available for use by phytoplankton. The bulk organic matter they produce forms

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the base of the local food chain. Such highly productive locations also concentrate representatives of higher

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trophic levels, such as zooplankton, fish and marine birds and mammals feeding there. Within relatively shallow

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areas, any primary production that is not utilized in the pelagic zone, sinks through the water column, ultimately supporting benthic communities (a phenomenon called pelagic-benthic coupling; Iken et al., 2005; Renaud et al., 2008, 2011; Søreide et al., 2013; Tamelander et al., 2006).

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Seabirds play an important role in Arctic ecosystems. These homoeothermic organisms feed on marine resources over vast areas of the pelagic zone, but necessarily breed and moult on land, often in colonies of several hundred

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thousand individuals. During their reproductive season seabirds effectively transport huge amounts of organic matter, produced in the marine environment, to the nutrient-poor land (e.g. Stempniewicz, 2005). Deposition on land is mainly in the form of guano, but also as feathers, egg shells and carcasses (Bokhorst et al., 2007; Bosman

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and Hockey, 1986; Polis et al., 1997). These deposits contain allochtonous biogenic nutrients which significantly

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fertilize the soil, stimulating characteristic lush vegetation growth around the colonies in Arctic locations such as Svalbard (Anderson and Polis, 1999, Mulder et al., 2011; Zmudczyńska et al., 2008; Zmudczyńska-Skarbek et

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al., 2013; Zwolicki et al., 2013). However, ornithogenic nutrients not incorporated into the terrestrial ecosystem can return through runoff and leaching to the sea. Therefore, seabirds can potentially exert not only a wellknown ‘top-down effect’ on marine ecosystem, as consumers of plankton and fish, but they can also have a

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‘bottom-up effect’ through the concentration of nutrients from vast marine feeding areas into the relatively small coastal area immediately adjacent to a colony, which may constitute a locally important resource for marine producers and subsequent consumers (Young et al., 2011). There are four different ways in which nutrients derived from guano may enter the sea (Stempniewicz et al., 2007; Young et al., 2011): (i) deposition of faeces directly into the water during foraging trips (Wainright et al., 1998); (ii) run-off from the land adjacent to nesting areas; this is encouraged when the nesting slope is steep, the colony is large and dense, there is little vegetation (thus plants do not assimilate the excess nutrients), and/or there is heavy rainfall (Kolb et al., 2010; Staunton Smith and Johnson, 1995); (iii) nutrients derived from guano are leached into ground water and then disperse into the sea during tidal oscillation (Staunton Smith and Johnson, 1995); and (iv) ammonia volatilized from guano (from uric acid) dissolves in rain and is deposited into the sea (Lindeboom, 1984). Regardless of the mechanism of transfer, there is a high probability of nutrient

ACCEPTED MANUSCRIPT accumulation close to the colony area, and therefore of enhancement of primary and secondary production in this littoral zone, as is seen in the adjacent terrestrial ecosystems (Ellis et al., 2005; Jakubas et al., 2008; Kolb et al., 2010). However, this enhancement may not be as apparent in the marine system as it is on land. In the terrestrial

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environment, nutrients may be stored in soil and available for use by microbial and plant communities over a

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longer period (Anderson and Polis, 1999). In the sea, waves and currents effectively mix the water, leading to

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nutrients dispersion and flushing out (Young et al., 2011), therefore being available to support marine producers on the local scale for a shorter period.

In contrast with terrestrial and freshwater environments, the influence of seabirds on marine systems through the

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local concentration of nutrients has not been thoroughly studied (Mulder et al., 2011 and references therein), particularly in the polar regions. Existing studies are difficult to compare as they have considered various marine

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systems, such as the Baltic (Kolb et al., 2010) and Mediterranean Seas (Gagnon et al., 2013), regions with low or no tidal fluctuation, and under weak wave or current influence, and more open and shelf seas that freely exchange with surrounding oceans (Wainright et al., 1998). Other studies describe tidal pools and coastal

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lagoons (Bosman and Hockey, 1986; Loder et al., 1996; Methratta, 2004; Palomo et al., 1999; Wooton, 1991),

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nutrient-rich (Bedard et al., 1980; Tatur, 2002) or oligotrophic (Lapointe et al., 1992) waters, and areas that differ in the intensity of seabird impact primarily through colony size (Kolb et al., 2010; Signa et al., 2012).

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Response variables examined have included nutrient content in water column and/or sediments, abundance, quality, condition and/or behavior of marine producers and consumers and, most recently, studies have started to address stable isotope levels in suspended and sedimented organic matter and in marine producers (Gagnon et

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al., 2013; Kolb et al., 2010; Signa et al., 2012). To date, there have been few studies of seabird impact on the marine littoral zone in the High Arctic. Earlier studies (Golovkin, 1967; Golovkin and Garkavaya, 1975; Zelickman and Golovkin, 1972) described high water nutrient content and high productivity of phyto- and zooplankton in the vicinity of seabird colonies on the coast of the Russian Arctic (Novaya Zemlya, Murmansk Coast). Wainright et al. (1998) documented a well-defined enrichment in both 15N and 13C in marine phytoplankton, kelp and some zooplankton near seabird colonies on the Pribilof Islands. They suggested, however, that the ornithogenic nutrient supplement was relatively small and insignificant in the context of these producers’ overall requirements. Similar conclusions were drawn by Kurle et al. (2008) in a study of rocky intertidal community structure at the Aleutian Islands. However, both the latter areas are situated in or in close proximity to the Bering Sea shelf, an area that is recognized as one of the most

ACCEPTED MANUSCRIPT nutrient-rich and most productive marine habitats in the world (Hunt and Megrey, 2005; Sakshaug, 2004), regardless of the seabird impact. The study area of the current investigation, Spitsbergen, is located in the High Arctic (76°–80° N), at the north-

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west edge of the relatively productive Barents Sea shelf (Hunt and Megrey, 2005; Sakshaug, 2004). Its benthic

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communities are well described (e.g. Balazy and Kuklinski, 2013; Kędra et al., 2012; McMahon et al., 2006;

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Renaud et al., 2011) but, as yet, the role of ornithogenic nutrients in their food web structure and functioning has not been considered. Nitrogen stable isotope ratio (15N/14N) is the most commonly used proxy for estimating the influence of seabirds on the ecosystem (e.g. Gillies et al., 2012; Kolb et al., 2010). Higher measured δ15N values

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in the vicinity of a seabird colony result from the isotopic fractionation of N occurring, first, with progress through the food web (seabirds are the top predators), and second, when ammonia volatilizes from guano

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(Hobson and Welch, 1992; Kelly, 2000; Michener and Lajtha, 2007; Wainright et al., 1998). The carbon stable isotope ratio (13C/12C) is also used as an indicator in trophic ecology as different food sources, such as macroalgae and pelagic, sediment and sea ice particulate organic matter (POM), as well as terrestrial supplies,

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have distinct δ13C values, and carbon shows much lower fractionation than nitrogen (Barrett et al., 2005; Budge

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et al., 2008; Kędra et al., 2012; Kolb et al., 2010; Tamelander et al., 2006). Therefore, the aim of this study was to assess the influence of local ornithogenic nutrient enrichment on the coastal benthic communities of

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Spitsbergen. Two hypotheses were addressed:

(1) that nitrogen stable isotope ratios (δ15N) in benthic producers and consumers are expected to be higher in the immediate vicinity of a large seabird colony.

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(2) the impact of ornithogenic nutrient enrichment close to a seabird colony is less pronounced in the marine than the terrestrial ecosystem. As a complementary tool to δ15N we measured carbon stable isotope ratios (δ13C) in all the samples. Since this parameter reflects the isotopic signal of producers if the consumers use them to a great extent, and may indicate other than expected trophic pathways.

2. Materials and methods 2.1. Study area The study was conducted in early August 2013 on the south-east coast of Isfjorden (west Spitsbergen, Svalbard, Fig. 1), the largest fjord on the west coast of Spitsbergen. Seabirds and their chicks were still present in their

ACCEPTED MANUSCRIPT colonies at this time. Isfjorden is 170 km long, up to 24 km wide and includes four side-fjords. About 55 % of the Isfjorden system is shallower than 100 m (Nilsen et al., 2008). The fjord has no distinct sill at its entrance, which enables inflow of relatively warm and nutrient-rich Atlantic water from the West Spitsbergen Current (a

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branch of the Gulf Stream), and to a lesser extent cold and nutrient-poor Arctic water from the East Spitsbergen

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Current from the Arctic Ocean (Loeng, 1991). In late spring and summer, the hydrology of Isfjorden is also

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influenced by surface waters derived from glacial melt and river runoff (Nilsen et al., 2008). Samples were collected nearshore both from the marine environment (benthic macroalgae and invertebrates) and from the land (plants), at two localities (Fig. 1):

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(1) SEABIRD area (78°12’N 15°14’E) – below a mixed colony of Brunnich’s guillemots (Uria lomvia) and kittiwakes (Rissa tridactyla) situated on Fuglefjella cliff at about 200 m a.s.l. The slope beneath the colony is

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exposed to the north-west and has an inclination of ca. 50°. The very luxuriant vegetation developing on this slope below the colony is composed mainly of Oxyria digyna, Cerastium arcticum, Alopecurus borealis and Poa alpina v. vivipara.

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The sea bottom in this location is primarily composed of hard bedrock. Beaches and the shallowest depths (0–2

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m) consist of pebbles, cobbles and boulders. Due to the tidal and wave disturbance, and ice scour this shallowest zone is almost devoid of life. Deeper parts (2–15 m) include steep (30°–45°) rocky shelves and mixed boulder

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fields, giving substrata for dense kelp forests (Laminaria spp., Saccharina latissima, Alaria esculenta) and a very rich epibenthic community. Coralline algae, sedentary polychaetes, barnacles, bryozoans, cnidarians (Urticina crassicornis, Hormathia nodosa, Cribrinopsis sp.), ascidians (Halocynthia sp.) and sponges are well represented.

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Common benthic predatory and scavenging fauna include hermit crabs (Pagurus pubescens), spider crabs (Hyas araneus), shrimps (Lebbeus polaris, Eualus gaimardii, Sclerocrangon boreas), starfish (Crossaster papposus, Henricia sp.) and bottom-dwelling fish (e.g. Myxocephalus scorpius). At 15–20 m depth the bottom flattens out (10°–15° slope), descending towards the fjord axis. The epibenthic grazing echinoid Strongylocentrotus droebachiensis, although also found at shallower depths, occurs here in large densities. (2) CONTROL area (78°11’N 14°74’E) – Nordhallet area, ca. 10 km from the seabird colony towards the fjord mouth. The landward geomorphology is much less steeply inclined (ca. 5°) than that of the SEABIRD location while the immediate coastal area is almost flat. Vegetation is dominated by mosses, Carex sp. and Salix polaris, with smaller contributions by herbs such as Polygonum viviparum and Oxyria digyna (the latter inland from the coast).

ACCEPTED MANUSCRIPT The seabed zonation is similar to that of the SEABIRD area. The beach, and the shallowest (0–2 m) and deeper (2–20 m) areas include a similar mix of rocky substrata, but those at the greater depth are partly overlain by mud. The inclination of the seabed is lower (15°–30°) and includes no sharp changes in gradient. As above, dense kelp

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forests are present down to 10–15 m depth. Epibenthos however is not as species rich at the CONTROL site as at

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the SEABIRD and no actiniarians were found there.

2.2. Sampling protocol

LAND – At each study location, 10 samples of the aboveground vegetation were harvested at each of the three

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sites at different distances from the seashore (Fig. 1). At each site, samples were obtained a few meters apart, and equidistant from the shore.

At the SEABIRD area we collected a total of 30 samples of Oxyria digyna from sites located (1) 50 m

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from the colony (to avoid guano potentially covering the plants) and 170 m from the seashore, (2) 60 m below site 1, and (3) a further 60 m from the colony and 50 m from the shore (to avoid direct sea spray

Since O. digyna was very rare in the CONTROL area and then only at distances greater than 300 m

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influence).

from the seashore, we doubled all the distances used previously. Hence, we collected samples (N = 10)

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of this plant at site 1 – 340 m away from the shore. At sites close to the shore another species of the family Polygonaceae was sampled, Polygonum viviparum, at (2) – 120 m from site 1 and 220 m from the shore, and (3) – 100 m from the shore (N = 20 samples in total).

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SEA BOTTOM – At each study location, samples of benthic organisms were collected with the use of SCUBA diving at a depth of 5–15 m, ca. 50 m from the shore, at three points situated equidistantly to the shore, each separated by ca. 20 m from the other. Thus, both at the SEABIRD and the CONTROL area we sampled 30 individuals of each of: benthic producers – brown algae Saccharina latissima, their principal consumers – sea urchins Strongylocentrotus droebachiensis (Wessels et al., 2006), and scavenging/predatory hermit crabs Pagurus pubescens (Hazlett, 1981; Lancaster, 1988). The species selected represented the largest and most abundant taxa of the given trophic group at both sites.

2.3. Stable isotope analyses After collection terrestrial plants were cleaned by hand and oven-dried at 60°C to a constant mass (the same conditions were used for all dry mass measures). Brown algae were also cleaned mechanically and then washed

ACCEPTED MANUSCRIPT with tap water to remove epibionts. Each individual was divided into two sub-samples representing a lamina (blade, a few cm2 cut from the distal area) and a stipe (3–5 cm cut from the middle), and then dried. Benthic invertebrates were left in clean salt water for 1 day to expel food remnants in their digestive systems. Whole

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individuals of hermit crabs and all the internal body parts carefully (manually) extracted from the exoskeleton of

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sea urchins were dried. Each hermit crab individual was weighed with a precision 0.01 g. Dry samples were

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ground with a vibrating mill (LMW-S, Testchem). A small amount of each sample (2–3 mg, weighed with a microbalance, precision 0.01 mg) was packed into a tin capsule.

Nitrogen and carbon stable isotope ratios were determined in continuous flow elemental analyser (MicroVario,

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Elementar, Germany) coupled with an IRMS mass spectrometer (Isoprime100, Isoprime, UK) at the University of Liège, Belgium. Results were expressed in the conventional δ15N and δ13C notation, according to the equation:

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δX = (Rsample / Rstandard – 1) × 1,000 (‰);

where Rsample was the stable isotope ratio 15N/14N or 13C/12C in the analysed sample, and Rstandard was the stable isotope ratio 15N/14N or 13C/12C (respectively) in the reference material, i.e. atmospheric N2 for nitrogen and

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PeeDee belemnite for carbon (Kelly 2000). Since we focused primarily on δ15N we did not chemically

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decarbonate or delipidate the samples due to the possible influence of both these procedures on nitrogen isotope fractionation (Carabel et al. 2006, Post et al. 2007, Guerrin et al. 2013).

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Total nitrogen and carbon content (%) was also measured in every sample during the isotopic analyses.

2.4. Statistical analyses

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Due to the non-normal distributions of data in many groups tested (Shapiro-Wilk test, P < 0.05) and a relatively low number of terrestrial plant samples collected from each of the three sites on land, non-parametric analyses were used. Medians (MeS in the SEABIRD area, MeC in the CONTROL area) and first and third quartiles were calculated to describe data distributions. To test for differences in each parameter between the study areas the Mann-Whitney test was used. Z statistic was given when the number of samples in each of the groups compared was higher than 20, and U statistic when the number was lower than 20 at least in one group. To control the familywise error rate after multiple comparisons of the terrestrial plant parameters between sites we used the Bonferroni correction and a significance level of α = 0.05/15 = 0.0033. Means and standard deviations are also presented to enable comparison of our results with those presented by other authors. Data were processed using STATISTICA 10.0 (StatSoft, Inc., 2011).

ACCEPTED MANUSCRIPT 3. Results 3.1. Terrestrial ecosystem At both study areas, nitrogen stable isotope ratios of terrestrial plants differed depending on the distance from the

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seashore (and concurrently from the colony in case of the SEABIRD area). In the SEABIRD area where all

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samples were represented by Oxyria digyna, the highest average values of δ15N were recorded closest to the

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colony (site 1, Me = 32.44‰), significantly lower at site 2 (25.73‰), and lower again (though statistically insignificant from site 2) at site 3 (22.57‰; Table 1). δ15N of plants collected in the CONTROL area showed similar pattern (Me = 5.98, –1.94, and –3.00‰, respectively, for sites 1, 2, and 3), noting that Polygonum

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viviparum was sampled at sites 2 and 3. The difference between these two sites in the CONTROL area was only ca. 1‰ while in the SEABIRD area it was about 3‰ between site 2 and 3.

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Carbon stable isotope ratio of terrestrial plants was lowest in close proximity to the seabird colony (site 1, Me = –30.26‰), significantly higher (less negative) at site 2 (–29.71‰), and intermediate (but not significantly different from the other sites) at site 3 (–29.96‰; Table 1). In the CONTROL area, plant δ13C values were

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and –30.06‰, respectively).

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highest of all at site 1 (–28.79‰), and similar to each other and to all the SEABIRD sites at sites 2 and 3 (–30.20

Total plant nitrogen content was the highest close to the colony (site 1, Me = 4.25%), intermediate close to the

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shore (site 3: 3.77%), and lowest on the mid-slope (site 2: 3.45%) in the SEABIRD area, but these values were not statistically significantly different from each other (Table 1). In the CONTROL area, considerably higher plant nitrogen content values were recorded at site 2 (3.28%) and site 3 (3.38%; P. viviparum) than at site 1

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(2.78%, O. digyna).

Total plant carbon content showed similar level across all the three sites of the SEABIRD area (site 1, Me = 40.88%; site 2, 40.41%; site 3, 40.13%; Table 1). All three average total C values in the SEABIRD area were significantly higher than total C at site 1 of the CONTROL area (36.10 %), but lower than the control site 2 (44.40 %) and 3 (45.00 %). Due to differences in nitrogen and carbon isotope ratio, and total C and N content between the two plant species (possibly irrespective of the seabird fertilization but, for instance, resulting from different potential to nutrient absorption or resource partitioning; Kjelland and Chapin, 1992), we excluded P. viviparum samples from further analyses (including them did not change the direction or the significance of the statistical differences described below in δ15N, δ13C, and total N; data not shown). Clear differences were found both in nitrogen isotopic ratio and total nitrogen content between O. digyna specimens growing below the colony and those from the control

ACCEPTED MANUSCRIPT area (P < 0.001 in both cases; Fig. 1). On average, δ15N was five times greater in the SEABIRD area (MeS = 25.21‰) compared to the CONTROL (5.98‰), and there was a ca. 1% increase of total N values (3.96% vs. 2.78%). The lowest value of O. digyna δ15N signature recorded in the SEABIRD area was 20.40‰ while the

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ranged from 3 to 5% whereas those in the CONTROL area were 2.4 to 3.6%.

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highest among the samples in the CONTROL was 9.14‰. The values of total N content in the SEABIRD area

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Carbon stable isotope ratio was ~1‰ lower while total C content was 4% higher in O. digyna collected in the SEABIRD area (δ13C: –29.94‰, total C: 40.31%) than in samples from the CONTROL area (δ13C: –28.79‰,

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total C: 36.01%), and both the differences were highly significant (P < 0.001; Fig. 2).

3.2. Marine ecosystem

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There were no statistical differences in δ15N between brown algae sampled at either study site (lamina: MeS = 2.62‰ vs. MeC = 3.09‰, P = 0.462; stipe: MeS = 4.92‰ vs. MeC = 5.00‰, P = 0.464; Fig. 2). Sea urchin δ15N signature had significantly lower values in the SEABIRD than in the CONTROL area (MeS = 5.10‰ vs. MeC =

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5.51‰, P = 0.001) while hermit crabs showed the opposite pattern (MeS = 8.49‰ vs. MeC = 8.12‰, P < 0.001).

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Since hermit crab individuals were bigger in the SEABIRD area (median ind. dry mass = 0.22 g, max. 1.23 g) than those in the CONTROL (Me = 0.06 g DM, max. 0.46 g; Mann-Whitney test: Z = 4.96, P < 0.001), we

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additionally compared only specimens of similar biomass, ranging from 0.05 to 0.2 g DM (N S = 11, NC = 15). We obtained similar results, with δ15N being higher in the SEABIRD area than in the CONTROL (MannWhitney test, U = 43.00, P = 0.042).

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Total N content in algal blades was significantly higher close to the colony as compared to the CONTROL area (MeS = 1.18% vs. MeC = 0.93%, P < 0.001) while in the stipes it was similar across the sites (MeS = 1.26% vs. MeC = 1.18%, P = 0.371). Similarly to δ15N pattern, total N in sea urchins was lower in the SEABIRD than in the CONTROL area (MeS = 3.31% vs. MeC = 4.00%, P < 0.001). There was no statistical difference in hermit crab total N content between the two sites (MeS = 6.50% vs. MeC = 6.13%, P = 0.251), and it was valid also when specimens of similar biomass were compared (P = 0.350). Stable carbon isotope ratios were significantly lower in the SEABIRD area than in the CONTROL area in both parts of S. latissima (lamina: MeS = –20.62‰ vs. MeC = –19.70‰, P = 0.004; stipe: MeS = –23.49‰ vs. MeC = – 21.90‰, P < 0.001) and in hermit crab bodies (MeS = –20.30‰ vs. MeC = –18.16‰, P < 0.001; the difference still significant when compared hermit crabs of similar size: U = 23.00, P = 0.002). δ13C of sea urchins was similar across the two areas (MeS = –17.99‰ vs. MeC = –18.46‰, P = 0.126; Fig. 3). Total C content was lower

ACCEPTED MANUSCRIPT below the colony than in the CONTROL area in algae (lamina: MeS = 21.92% vs. MeC = 25.83%, stipe, P = 0.013: MeS = 22.10% vs. MeC = 23.09%, P = 0.033) and sea urchins (MeS = 24.74% vs. MeC = 29.36%, P < 0.001), but was higher in hermit crabs (Me S = 36.41% vs. MeC = 32.00%, P = 0.001; no differences when crabs

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of similar size compared, P = 0.177).

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4. Discussion

It is well known that seabirds can play an important role in shaping terrestrial habitats close to their breeding colonies (Anderson and Polis, 1999; Mulder et al., 2011 and refs. therein; Zwolicki et al., 2013). This role is

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especially important in nutrient-poor polar regions, where the vicinities of seabird colonies provide exceptional green oases among vast areas vegetated only by lichens, mosses and tiny dwarf shrubs (e.g. Stempniewicz, 2005;

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Zmudczyńska et al., 2009; Zmudczyńska-Skarbek et al., 2013). The rich plant community below the colony studied here provides a classic example of this lush ornithogenic tundra (‘bird-cliff vegetation’ as described by Rønning, 1996). Our finding of five times higher δ15N values in this vegetation compared with vegetation

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growing away from ornithogenic influence confirms the importance of marine-derived nutrient transfer into the

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terrestrial ecosystem.

Most aspects of seabird influence on the terrestrial ecosystem exhibit a gradual change with distance from the

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colony (Leishman and Wild, 2001; Odasz, 1994; Ryan and Watkins, 1989; Zmudczyńska et al., 2012). This results from a combination of diminishing guano supplies (Zwolicki et al., 2013), nutrients being taken up by plants, volatilization, runoff, and/or leaching (Lindeboom, 1984; Kolb et al., 2010; Staunton Smith and Johnson,

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1995). In the SEABIRD area, δ15N in plant tissues also gradually decreased with distance from the colony. However, even in the most distant site and only 50 m from the sea shore, the average nitrogen isotopic ratio was 22.6‰, almost four times higher than at the CONTROL area (Table 1). This indicates that bulk nutrients that may reach the marine ecosystem continued to be available. While most seabird colonies are situated close to the coast, little is known about the fate of colony-derived nutrients that enter the sea. Opportunistic observations in Isfjorden are suggestive of differences between areas close to seabird colonies and those not influenced, exemplified by the bigger size of hermit crab individuals found at the SEABIRD area comparing with those at the CONTROL area. The use of stable isotope analyses that integrate dietary information over long periods of time in the study of trophic interactions is well established (Hobson and Welch, 1992; Kelly, 2000; Michener and Lajtha, 2007). A range of studies in terrestrial, freshwater and marine ecosystems (e.g. Mulder et al., 2011 and refs. therein) have

ACCEPTED MANUSCRIPT clearly demonstrated that a distinct isotopic signal of δ15N (and in many cases also δ13C) separates organisms supplied by seabird-derived nutrients from those using different food sources, such as atmospheric nitrogen fixation, wind blown material or precipitation on land, and inflowing water masses, coastal erosion or river

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discharge to the sea. Therefore, our initial expectation was for a similar distinction to be present in benthic

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organisms of the shallow littoral zone below a seabird colony. However, as well as the considerable dilution and

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dispersion caused by waves and currents, benthic primary producers can exploit other nutrient sources, such as from rich deep water masses brought up to the shelf, from material sinking from the euphotic zone (sympagicpelagic-benthic coupling), and from rivers, melting glaciers and snow (Iken et al., 2005; Kędra et al., 2012;

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Renaud et al. 2008). All these factors, together with the frequent omnivory seen among consumers, may influence the isotopic signal in the sea.

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Consistent with previous studies, terrestrial plants growing below the colony showed much higher δ15N, total nitrogen and carbon contents, though a bit lower δ13C, compared with the control area. Saccharina latissima showed similar differences in case of δ13C of both its blades and stipes, and total N content of the former.

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However, no differences in δ15N were apparent in kelp collected in the two areas. As well as the factors

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mentioned above, this observation may be related to the strong seasonality of the local climate, with short periods of light and nutrient availability for marine producers. In the Arctic, the highest nutrient levels are noted

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during winter (when there is limited or no runoff from the land), and they then decrease rapidly after sea ice break-up, as light starts to penetrate deeply into the water column, and conditions for photosynthesis become favourable (Aguilera et al., 2002). Subsequently, during summer and autumn, light conditions worsen again

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since meltwater carrying sediment from land enters the water column and the phytoplankton bloom develops (Wienke et al., 2011). Dunton et al. (1985) observed that in Stefansson Sound, Alaskan Beaufort Sea (70°N), S. latissima completed nearly all of its annual growth during the period between sea ice break-up and late June/early July, with its highest growth rate (4.7 mm per day) occurring from late April to late July. This way the kelp effectively optimised light and nutrient conditions in the water (Aguilera et al., 2002). However, there was no sea ice forming in Isfjorden during the last (2012/2013) and previous winters (pers. observation), while the sun normally returns to Isfjorden in the middle of February, and from the end of April it operates for 24 hours a day there (Elverland, 2009). Hence, S. latissima growth pattern from our study areas may resemble more those from lower latitudes, such as Great Britain coast or Narragansett Bay, USA, where it achieved the maximum growth rate from February to June and from January to May (respectively; refs given by Dunton et al., 1985). At that time in Isfjorden, seabirds have not yet or just started laying eggs (in late May/early June, Kovacs, 2005),

ACCEPTED MANUSCRIPT therefore their total guano input was still small and diminished by vernal development of terrestrial vegetation before entering the sea. It is also possible that ornithogenic nutrients entering the water column in mid-summer may be taken up by phytoplankton, as reported by Mehratta (2004) in the Gulf of Maine, USA. If so, a seabird-

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driven phytoplankton bloom could then reduce light availability and further inhibit growth of benthic

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macroalgae, effectively reducing any dependence of the macroalgae on ornithogenic nutrients.

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The sea urchin Strongylocentrotus droebachiensis is considered an omnivore, potentially including algae, invertebrates and microbes in its diet, although primarily grazing on macroalgae (Scheibling and Hatcher, 2007). In the typical Arctic benthic food web of Kongsfjorden (west Spitsbergen), S. droebachiensis and the amphipod

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Gammarellus homari are the only consumers of fresh macroalgae. Of 19 macroalgal species experimentally offered to sea urchins, Saccharina latissima (and especially its blades) was the most preferred food in a multi-

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choice assay, and was also consumed at the highest rate in a no-choice assay (Wessels et al., 2006). Our isotopic results are not consistent with S. droebachiensis preferentially grazing on S. latissima within the study areas. The sea urchin δ15N was lower in the SEABIRD than the CONTROL area, whereas N isotopic signatures in both

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parts of the brown alga were similar across the two sites. The opposite pattern was seen with carbon isotope

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ratios, which were significantly lower in S. latissima growing below the seabird colony than away from it, but comparable in sea urchin bodies from the two sites. It is worth to notice that total nitrogen content in S. latissima

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blades was significantly lower in the CONTROL as compared with the SEABIRD area. Some studies demonstrate that animal tissues become enriched with 15N following nutritional stress, e.g. caused by reduced nutrient intake (Adams and Sterner, 2000) or fasting during breeding (Hobson et al., 2003) as a consequence of

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recycling of body nitrogen. Hence, nitrogen-poor diet might be responsible for the sea urchin δ15N increase in the CONTROL area. However other authors, like Oelbermann and Scheu (2002) have found the opposite – δ15N of predator bodies increased with higher N content of their prey. They also argue that in the field it is unlikely that generalist feeders survive for a long time on diets of very low quality. Most likely, local sea urchins supplemented their diet by alternative food sources which had different N and C isotopic signals than S. latissima. From among several macroalgae species consumed with different rate by sea urchins in the experiment led by Wessels et al. (2006), Løkken (2013) gives stable isotope data of six sampled in Isfjorden mouth. The analysed macroalgae showed either higher or lower isotopic values (δ15N: from 2.2 to 5.2‰, δ13C: –36.9 to –18.3‰) comparing to S. latissima found in the same area (δ15N: 3.3‰, δ13C: –22.6‰), what could inevitably influence the consumer isotopic signal. Yet there is no matching sea urchins data to confirm it. There is also lots of evidence that S. droebachiensis may optimize its energy and nutrition

ACCEPTED MANUSCRIPT requirements through selective feeding on the best food accessible within that available within a habitat (Scheibling and Hatcher, 2007). Below depth range of algae occurrence, where the food resources are insufficient, S. droebachiensis switches to carnivory, scavenging, and even cannibalism when starving

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(Himmelman and Steele, 1971; Renaud et al., 2011). More research on the diet of local populations of sea

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urchins is needed, for instance to verify if the increased values of δ15N and total N content in the CONTROL

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area might result from assimilating food of animal origin there.

Hermit crabs are highly opportunistic omnivorous feeders (Hazlett, 1981) and their diet may include detritus of benthic, pelagic and sympagic origin. This feeding strategy means they are particularly well adapted to living in

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harsh, unpredictable environments and it is thought that nutrient availability has rarely been a limiting factor for these decapods (Lancaster, 1988). Our results suggest that the hermit crab Pagurus pubescens shows evidence of

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ornithogenic nutrient influence, with their nitrogen stable isotope ratio being significantly higher below the colony than at the control site. All four parameters studied (N and C stable isotope ratios and total contents) in hermit crabs showed the same pattern of differences between the SEABIRD and the CONTROL area as in case

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of terrestrial plants, while the pattern was different comparing with the kelp and sea urchins. This may indicate

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the seabird-derived enrichment of at least some of the producers of the food chains that hermit crabs based on, at least partially, such as benthic microalgae and/or phytoplankton. One of the challenges for future research is to

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measure the proportion of food originating in pelagic zone in the hermit crab diet, since pelagic organic matter may be supported by the ornithogenic nutrients to a relatively large extent (Mehratta, 2004; Signa et al., 2012), and then sink and enter the bottom food chains through pelagic-benthic coupling (Renaud et al., 2008; Søreide et

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al., 2013; Tamelander et al., 2006).

Comparing our results with other published isotopic data from benthic food chain elements from Svalbard (Table 2), levels of nitrogen stable isotopes in S. latissima and both the benthic consumers obtained from similar to those of the current study were lower than in either of our two study areas. However, δ15N values of both Strongylocentrotus sp. and P. pubescens were highly enriched when collected from much deeper sites, most likely indicating a higher proportion of animal tissues in their diet. As yet, no isotopic studies have described the entire local food chain, it remains unclear which parts of this food web area are influenced by the input of ornithogenic nutrients. Our results indicate that the influence of seabirds on the coastal benthic environment in the Arctic, while detectable, is less than has been observed in the terrestrial ecosystem. However, it remains unclear which elements of the seabed community are positively and which negatively influenced by seabird fertilization. Even

ACCEPTED MANUSCRIPT though sufficient sample sizes of each species studied were collected to reduce variability among replicates, each species demonstrated a different pattern of isotopic variability between the two study areas. Further studies are necessary to fully understand the influence of ornithogenic nutrients on the benthic community, including both

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absolute and relative abundances, and isotopic analyses across the food web, and from nutrients from the water

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column throughout the year.

Acknowledgements

We thank Dr. Gilles Lepoint (Laboratory of Oceanology, University of Liège, Belgium) for the isotopic analyses

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and Prof. Peter Convey (British Antarctic Survey, UK) for consultation and linguistic improvement. Many colleagues have contributed to our discussions. This study was supported by the Faculty of Biology, University

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of Gdańsk to KZS (Grant No. 538-L120-B082-13) and the Polish National Science Centre to PK (Grant No. 2011/03/B/NZ8/02872) and PB (DEC-2011/01/N/NZ8/04493). We also acknowledge the Antoni Dębski Scholarship granted by the Polish Society of Hyperbaric Medicine and Technology (PTMiTH) to PB. The study

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was performed under the permission of the Governor of Svalbard.

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Figure captions

Fig. 1 Study areas with sampling sites located at sea (empty rectangulars), and three sites on land (empty

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circles). Isfjorden, Svalbard.

Fig. 2 Median (horizontal line), quartile values (box), and non-outliers range (whiskers) of δ15N and total nitrogen content in terrestrial plants Oxyria digyna, brown algae Saccharina latissima, sea urchins

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Strongylocentrotus droebachiensis, and hermit crabs Pagurus pubescens on the SEABIRD and CONTROL area.

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Significant differences between the areas marked with arrows (Mann-Whitney test). Note different scale of the vertical axis of δ15N signature in terrestrial plants.

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Fig. 3 Median (horizontal line), quartile values (box), and non-outliers range (whiskers) of δ13C and total carbon content in terrestrial plants Oxyria digyna, brown algae Saccharina latissima, sea urchins Strongylocentrotus droebachiensis, and hermit crabs Pagurus pubescens on the SEABIRD and CONTROL area. Significant

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differences between the areas marked with arrows (Mann-Whitney test).

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Figure 1

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Figure 2

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Figure 3

ACCEPTED MANUSCRIPT Table 1 Median values of δ15N, δ13C (‰), total nitrogen and carbon content (%) in plants collected at different distances from the seashore on both study areas (cf. Materials and methods). Different letters indicate significantly different values within each parameter (Mann-Whitney test with Bonferroni correction, P <

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0.0033).

2 (N = 10)

3 (N = 10)

O. digyna

O. digyna

P. viviparum

P. viviparum

32.44a

25.73b

22.57b

5.98c

–1.94d

–3.00d

4.25a

3.45ac

3.77a

2.78b

3.28bc

3.38bc

–30.26a

–29.71b

–29.96ab

–28.79c

–30.20ab

–30.06ab

40.88a

40.41a

40.13a

36.10b

44.40c

45.00c

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O. digyna

1 (N = 10)

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O. digyna

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Total C

3 (N = 10)

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δ13C

2 (N = 11)

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Total N

1 (N = 9)

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δ15N

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SEABIRD

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Table 2 Mean ±SD of stable isotope values (‰) of particulate organic matter (POM), algae and invertebrates collected within the study area and around Svalbard. Values bold

depth

n

δ13C

n

δ15N

Saccharina latissima

δ13C

n

δ15N

δ13C

30 4.02±0.92

–22.23±1.06

30

5.14±0.48

–17.97±1.58

30 8.57±0.35 –20.15±1.28

A

28 3.94±2.09

–20.83±0.97

30

5.53±0.36

–18.47±1.08

30 8.12±0.30 –18.08±0.98

A

5

–22.6±0.813

n

δ15N

δ13C

Ref.

US

Isfjorden, below

MA N

Fuglefjella 5–15 m Isfjorden, below

TE D

Nordhallet 5–15 m

CE P

Isfjorden, Adventfjorden

AC

0–14 m Isfjorden mouth 1–25 m

Pagurus pubescens

δ13C

n

δ15N

Strongylocentrotus sp.

IP

δ15N

Sediment POM

CR

Pelagic POM

Area,

T

– in the vicinity of a seabird colony.

3–5

4.2±0.28

–25.8±0.233

2

0.00±0.57

–24.60±0.143

7

4.9±0.98

–22.81±1.931, 3

3

0.5±0.06

–29.48±1.06

1

–0.74

–23.31

3.3±0.85

B

5

4.5±0.405

–15.7±1.953, 5

6

9

6.444,5

–16.523, 4, 5

1

7.1±0.41 –14.5±0.533

B

Isfjorden 120–422 m

10.1

–14.83

B

Kongsfjorden, close to Kongsbreen 0–15 m

C

ACCEPTED MANUSCRIPT

Kongsfjorden, close

2

–1.81±0.58

–30.05±0.09

1

0.56

–24.00

6.70

–19.97

US

to Ny-Alesund 329 m

MA N

Barents Sea Marginal Ice Zone 5.60±1.931, 2 –24.78±1.431, 2

TE D

4

1

9.91, 2

–17.91, 2

1

8.21, 2

–17.81, 2

D

1

11.81, 2

–18.71, 2

Refs: A – This study, B – Løkken 2013, C – Kędra et al. 2012, D – Renaud et al. 2011, E – Tamelander et al. 2006 1

C

CR

Kongsfjorden, close

213–343 m

1

IP

0–15 m

T

to Ny-Alesund

– samples chemically decarbonized prior to analysis, 2 – samples chemically delipidated prior to analysis, 3 – δ13C values mathematically normalized for lipid content correction, 4 – values

AC

CE P

calculated from the given mean values for groups of samples, 5 – only gonads analysed

E

ACCEPTED MANUSCRIPT Highlights 

In the Arctic, ornithogenic nutrients are not fully used on land and may be also available for the nearshore marine organisms. Benthic macroalgae do not show clear ornithogenic nutrient enrichment.



Sea urchins’ diet is highly differentiated and may comprise of higher-quality food of animal origin.



Hermit crabs are influenced by seabirds possibly through pelagic-benthic coupling.



Seabird influence on coastal benthic environment is less pronounced than on land.

AC

CE P

TE

D

MA

NU

SC R

IP

T

