Journal of Marine Systems 144 (2015) 48–56

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Journal of Marine Systems

j ourna l homepage: www.e lsev ie r .com/ locate / jmarsys

An assessment of seabird influence on Arctic coastalbenthic communities

Katarzyna Zmudczyńska-Skarbek a,⁎, Piotr Balazy b, Piotr Kuklinski b,c

a University of Gdańsk, Department of Vertebrate Ecology and Zoology, Wita Stwosza 59, 80-308 Gdańsk, Polandb Polish Academy of Sciences, Institute of Oceanology, Marine Ecology Department, PowstańcówWarszawy 55, 81-712 Sopot, Polandc Natural History Museum, Department of Life Sciences, Cromwell Road, London SW7 5BD, United Kingdom

⁎ Corresponding author. Tel./fax: +48 585236141.E-mail address: biozmud@ug.edu.pl (K. Zmudczyńska

http://dx.doi.org/10.1016/j.jmarsys.2014.11.0130924-7963/© 2014 Elsevier B.V. All rights reserved.

a b s t r a c t

a r t i c l e i n f o

Article history:Received 25 April 2014Received in revised form 21 November 2014Accepted 24 November 2014Available online 29 November 2014

Keywords:BenthosGuanoNutrientsSeabirdsSpitsbergenStable isotopes

It is well recognized that seabirds, particularly those nesting in coastal colonies, can provide significant nutrientenrichment to Arctic terrestrial ecosystems. However, little is known about the fate of bird-derived nutrients thatreturn to themarine environment and potentially concentrate below the colonies. To attempt to assess the influ-ence of this potential nutrient enrichment of the coastal benthic community, samples of macroalgae, sea urchins(mainly algivores), and hermit crabs (scavengers)were collected at two Arctic localities (Spitsbergen), (1) belowa mixed colony of guillemots and kittiwakes, and (2) in an adjacent geomorphologically similar location notinfluenced by the seabird colony. A much higher nitrogen stable isotope ratio (δ15N) and total nitrogen contentwere 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 period in macroalgaein late winter/early spring, when there is little or no runoff from the land, and/or ornithogenic nutrients beingdirectly incorporated by phytoplankton. Sea urchins showed higher δ15N and total N in the control site compar-ing to the colony-influenced area, suggesting differential food sources in their diet and a role of scavenging/carnivory on higher trophic levels there. Opportunistically feeding hermit crabs showed δ15N and total N enrich-ment below the seabird colony, suggesting dependence on detritus derived from food chains originating frompelagic producers. Our results indicate that seabirds in the Arctic may fertilize coastal benthic communitiesthrough pelagic–benthic coupling, while having no direct impact on bottom primary production.

© 2014 Elsevier B.V. All rights reserved.

1. Introduction

Arctic terrestrial ecosystems typically reach their greatest levels ofdevelopment close to the coast, and are otherwise characterized byvery low primary production. A range of factors, including short grow-ing season, low temperatures and liquid water availability, presence ofpermafrost, and chronic nutrient deficiency underlie this lowproductiv-ity (Callaghan, 2001). In parallel, low levels of nutrients such as nitrogenand phosphorus lead to low productivity in the upper layers of theArctic deep open seas (Thomas et al., 2008). However, locally intenseproduction occurs at the outflow of Atlantic and Pacific waters, andthe Siberian and North American rivers as a result of relatively highnutrient inputs (Dunton et al., 2006; Fichot et al., 2013; Thomas et al.,2008). Additionally intense nutrient influx takes place near the sea icemargin and over the continental shelf due to vertical mixing of watermasses (Bluhm and Gradinger, 2008; Hunt and Megrey, 2005;Sakshaug, 2004; Wassmann et al., 2006). In the latter situation, nutri-ents from the bottom water and sediments are thereby brought to thesurface and made available for use by phytoplankton. The bulk organic

-Skarbek).

matter they produce forms the base of the local food chain. Such highlyproductive locations also concentrate representatives of higher trophiclevels, such as zooplankton,fish andmarine birds andmammals feedingthere. Within relatively shallow areas, any primary production that isnot utilized in the pelagic zone, sinks through the water column,ultimately supporting benthic communities (a phenomenon calledpelagic–benthic coupling; Iken et al., 2005; Renaud et al., 2008, 2011;Søreide et al., 2013; Tamelander et al., 2006).

Seabirds play an important role in Arctic ecosystems. Thesehomoeothermic organisms feed on marine resources over vast areasof the pelagic zone, but necessarily breed and moult on land, often incolonies of several hundred thousand individuals. During their repro-ductive season seabirds effectively transport huge amounts of organicmatter, produced in the marine environment, to the nutrient-poorland (e.g. Stempniewicz, 2005). Deposition on land is mainly in theform of guano, but also as feathers, egg shells and carcasses (Bokhorstet al., 2007; BosmanandHockey, 1986; Polis et al., 1997). These depositscontain allochthonous biogenic nutrients which significantly fertilizethe soil, stimulating characteristic lush vegetation growth around thecolonies in Arctic locations such as Svalbard (Anderson and Polis, 1999;Mulder et al., 2011; Zmudczyńska et al., 2008; Zmudczyńska-Skarbeket al., 2013; Zwolicki et al., 2013). However, ornithogenic nutrients not

49K. Zmudczyńska-Skarbek et al. / Journal of Marine Systems 144 (2015) 48–56

incorporated into the terrestrial ecosystem can return through runoffand leaching to the sea. Therefore, seabirds can potentially exert notonly awell-known ‘top-down effect’ onmarine ecosystem, as consumersof plankton and fish, but they can also have a ‘bottom-up effect’ throughthe concentration of nutrients from vast marine feeding areas into therelatively small coastal area immediately adjacent to a colony, whichmay constitute a locally important resource for marine producers andsubsequent consumers (Young et al., 2011).

There are four differentways in which nutrients derived from guanomay 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 nestingareas; this is encouraged when the nesting slope is steep, the colony islarge and dense, there is little vegetation (thus plants do not assimilatethe excess nutrients), and/or there is heavy rainfall (Kolb et al., 2010;Staunton Smith and Johnson, 1995); (iii) nutrients derived fromguano are leached into ground water and then disperse into the seaduring tidal oscillation (Staunton Smith and Johnson, 1995); and (iv)ammonia volatilized from guano (from uric acid) dissolves in rain andis deposited into the sea (Lindeboom, 1984). Regardless of the mecha-nism of transfer, there is a high probability of nutrient accumulationclose to the colony area, and therefore of enhancement of primary andsecondary production in this littoral zone, as is seen in the adjacentterrestrial ecosystems (Ellis, 2005; Jakubas et al., 2008; Kolb et al.,2010). However, this enhancement may not be as apparent in themarine system as it is on land. In the terrestrial environment, nutrientsmay be stored in soil and available for use by microbial and plantcommunities over a longer period (Anderson and Polis, 1999). In thesea, waves and currents effectively mix the water, leading to nutrientdispersion and flushing out (Young et al., 2011), therefore being avail-able to support marine producers on the local scale for a shorter period.

In contrast with terrestrial and freshwater environments, the influ-ence of seabirds on marine systems through the local concentration ofnutrients has not been thoroughly studied (Mulder et al., 2011 andreferences therein), particularly in the polar regions. Existing studiesare difficult to compare as they have considered various marinesystems, such as the Baltic (Kolb et al., 2010) and Mediterranean Seas(Gagnon et al., 2013), regions with low or no tidal fluctuation, andunder weak wave or current influence, and more open and shelf seasthat freely exchange with surrounding oceans (Wainright et al., 1998).Other studies describe tidal pools and coastal lagoons (Bosman andHockey, 1986; Loder et al., 1996; Methratta, 2004; Palomo et al., 1999;Wootton, 1991), nutrient-rich (Bedard et al., 1980; Tatur, 2002) oroligotrophic (Lapointe et al., 1992) waters, and areas that differ in theintensity of seabird impact primarily through colony size (Kolb et al.,2010; Signa et al., 2012). Response variables examined have includednutrient content inwater column and/or sediments, abundance, quality,condition and/or behaviour of marine producers and consumers and,most recently, studies have started to address stable isotope levels insuspended and sedimented organic matter and in marine producers(Gagnon et al., 2013; Kolb et al., 2010; Signa et al., 2012).

To date, there have been few studies of seabird impact on themarinelittoral zone in theHighArctic. Earlier studies (Golovkin, 1967; Golovkinand Garkavaya, 1975; Zelickman and Golovkin, 1972) described highwater nutrient content andhigh productivity of phyto- and zooplanktonin the vicinity of seabird colonies on the coast of the Russian Arctic(Novaya Zemlya, Murmansk Coast). Wainright et al. (1998) document-ed a well-defined enrichment in both 15N and 13C in marine phyto-plankton, kelp and some zooplankton near seabird colonies on thePribilof Islands. They suggested, however, that the ornithogenic nutrientsupplement was relatively small and insignificant in the context ofthese producers' overall requirements. Similar conclusions weredrawn by Kurle et al. (2008) in a study of rocky intertidal communitystructure at the Aleutian Islands. However, both the latter areas aresituated in or in close proximity to the Bering Sea shelf, an area that isrecognized as oneof themost nutrient-rich andmost productivemarine

habitats in theworld (Hunt andMegrey, 2005; Sakshaug, 2004), regard-less of the seabird impact.

The study area of the current investigation, Spitsbergen, is located inthe High Arctic (76°–80° N), at the north-west edge of the relativelyproductive Barents Sea shelf (Hunt and Megrey, 2005; Sakshaug,2004). Its benthic communities are well described (e.g. Balazy andKuklinski, 2013; Kędra et al., 2012; McMahon et al., 2006; Renaudet al., 2011) but, as yet, the role of ornithogenic nutrients in their foodweb structure and functioning has not been considered. Nitrogen stableisotope ratio (15N/14N) is themost commonly used proxy for estimatingthe influence of seabirds on the ecosystem (e.g. Gillies et al., 2012; Kolbet al., 2010). Higher measured δ15N values in the vicinity of a seabirdcolony result from the isotopic fractionation of N occurring, first, withprogress through the food web (seabirds are the top predators), andsecond, when ammonia volatilizes from guano (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 introphic ecology as different food sources, such asmacroalgae and pelag-ic, sediment and sea ice particulate organic matter (POM), as well asterrestrial supplies, have distinct δ13C values, and carbon shows muchlower fractionation than nitrogen (Barrett et al., 2005; Budge 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 localornithogenic nutrient enrichment on the coastal benthic communitiesof Spitsbergen. Two hypotheses were addressed:

(1) that the nitrogen stable isotope ratios (δ15N) in benthicproducers and consumers are expected to be higher in the imme-diate vicinity of a large seabird colony.

(2) the impact of ornithogenic nutrient enrichment close to a seabirdcolony is less pronounced in the marine than the terrestrialecosystem.

As a complementary tool to δ15N we measured the carbon stableisotope ratios (δ13C) in all the samples. This parameter reflects theisotopic 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-eastcoast of Isfjorden (west Spitsbergen, Svalbard, Fig. 1), the largest fjordon the west coast of Spitsbergen. Seabirds and their chicks were stillpresent in their colonies at this time. Isfjorden is 170 km long, up to24 km wide and includes four side-fjords. About 55% of the Isfjordensystem is shallower than 100 m (Nilsen et al., 2008). The fjord has nodistinct sill at its entrance, which enables inflow of relatively warmand nutrient-rich Atlantic water from the West Spitsbergen Current (abranch of the Gulf Stream), and to a lesser extent cold and nutrient-poor Arctic water from the East Spitsbergen Current from the ArcticOcean (Loeng, 1991). In late spring and summer, the hydrology ofIsfjorden is also influenced by surface waters derived from glacial meltand river runoff (Nilsen et al., 2008).

Samples were collected nearshore both from the marine environ-ment (benthic macroalgae and invertebrates) and from the land(plants), at two localities (Fig. 1):

(1) SEABIRD area (78°12′N 15°14′E) — below a mixed colony ofBrunnich's guillemots (Uria lomvia) and kittiwakes (Rissatridactyla) situated on Fuglefjella cliff at about 200 m a.s.l. Theslope beneath the colony is exposed to the north-west and hasan inclination of ca. 50°. The very luxuriant vegetation develop-ing on this slope below the colony is composed mainly of Oxyriadigyna, Cerastium arcticum, Alopecurus borealis and Poa alpina v.vivipara.

CONTROL

SEABIRD

Isfjorden

Longyearbyen

Svalbard

ColeselvaHollendarelva

Adventelva

Grondalselva

1

1

2

2

3

3

Fig. 1. Study areas with sampling sites located at sea (empty rectangles), and three sites on land (empty circles). Isfjorden, Svalbard.

50 K. Zmudczyńska-Skarbek et al. / Journal of Marine Systems 144 (2015) 48–56

The sea bottom in this location is primarily composed of hardbedrock. Beaches and the shallowest depths (0–2 m) consist ofpebbles, cobbles and boulders. Due to the tidal and wave distur-bance, and ice scour this shallowest zone is almost devoid of life.Deeper parts (2–15 m) include steep (30°–45°) rocky shelvesand mixed boulder fields, giving substrata for dense kelp forests(Laminaria spp., Saccharina latissima, Alaria esculenta) and a veryrich epibenthic community. Coralline algae, sedentary poly-chaetes, barnacles, bryozoans, cnidarians (Urticina crassicornis,Hormathia nodosa, Cribrinopsis sp.), ascidians (Halocynthia sp.)and sponges are well represented. Common benthic predatoryand scavenging fauna include hermit crabs (Pagurus pubescens),spider crabs (Hyas araneus), shrimps (Lebbeus polaris, Eualusgaimardii, Sclerocrangon boreas), starfish (Crossaster papposus,Henricia sp.) and bottom-dwelling fish (e.g. Myoxocephalusscorpius). At a 15–20 m depth the bottom flattens out (10°–15°slope), descending towards the fjord axis. The epibenthic grazingechinoid Strongylocentrotus droebachiensis, although also foundat shallower depths, occurs here in large densities.

(2) CONTROL area (78°11′N 14°74′E) — Nordhallet area, ca. 10 kmfrom the seabird colony towards the fjord mouth. The landwardgeomorphology is much less steeply inclined (ca. 5°) than that ofthe SEABIRD location while the immediate coastal area is almostflat. Vegetation is dominated bymosses,Carex sp. and Salix polaris,with smaller contributions by herbs such as Polygonum viviparumand O. digyna (the latter inland from the coast). The seabed zona-tion is similar to that of the SEABIRD area. The beach, and theshallowest (0–2 m) and deeper (2–20 m) areas include a similarmix of rocky substrata, but those at the greater depth are partlyoverlain by mud. The inclination of the seabed is lower (15°–30°)and includes no sharp changes in gradient. As above, dense kelpforests are present down to a 10–15mdepth. Epibenthos howeveris not as species rich at the CONTROL site as at the SEABIRD and noactiniarians were found there.

2.2. Sampling protocol

2.2.1. LandAt each study location, 10 samples of the aboveground vegetation

were harvested at each of the three sites at different distances fromthe seashore (Fig. 1). At each site, samples were obtained a few metresapart, and equidistant from the shore.

− At the SEABIRD area we collected a total of 30 samples of O. digynafrom sites located (1) 50 m from the colony (to avoid guanopotentially covering the plants) and 170 m from the seashore,(2) 60 m below site 1, and (3) a further 60 m from the colony and50 m from the shore (to avoid direct sea spray influence).

− Since O. digynawas very rare in the CONTROL area and then only atdistances greater than 300 m from the seashore, we doubled all thedistances used previously. Hence, we collected samples (N= 10) ofthis plant at site 1— 340m away from the shore. At sites close to theshore another species of the family Polygonaceae was sampled,P. 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).

2.2.2. Sea bottomAt 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 theshore, at three points situated equidistantly to the shore, each separatedby ca. 20 m from the other. Thus, both at the SEABIRD and CONTROLareas we sampled 30 individuals of each of: benthic producers —

brown algae S. latissima, their principal consumers — sea urchinsS. droebachiensis (Wessels et al., 2006), and scavenging/predatoryhermit crabs P. pubescens (Hazlett, 1981; Lancaster, 1988). The speciesselected represented the largest and most abundant taxa of the giventrophic 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 forall dry mass measures). Brown algae were also cleaned mechanicallyand then washed with tap water to remove epibionts. Each individualwas divided into two sub-samples representing a lamina (blade, a fewcm2 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 for1 day to expel food remnants in their digestive systems. Whole individ-uals of hermit crabs and all the internal body parts carefully (manually)extracted from the exoskeleton of sea urchins were dried. Each hermitcrab individual was weighed with a precision of 0.01 g. Dry sampleswere ground with a vibrating mill (LMW-S, Testchem). A small amountof each sample (2–3 mg, weighed with a microbalance, precision0.01 mg) was packed into a tin capsule.

Nitrogen and carbon stable isotope ratios were determined in acontinuous flow elemental analyser (MicroVario, Elementar,Germany) coupled with an IRMS mass spectrometer (Isoprime100,Isoprime, UK) at the University of Liège, Belgium. Results wereexpressed in the conventional δ15N and δ13C notations, according tothe equation:

δX ¼ Rsample=Rstandard–1� �

� 1000 ‰ð Þ;

where Rsample was the stable isotope ratio 15N/14N or 13C/12C in theanalysed sample, and Rstandard was the stable isotope ratio 15N/14N or

51K. Zmudczyńska-Skarbek et al. / Journal of Marine Systems 144 (2015) 48–56

13C/12C (respectively) in the reference material, i.e. atmospheric N2 fornitrogen and PeeDee belemnite for carbon (Kelly, 2000). Since wefocused primarily on δ15N we did not chemically decarbonate ordelipidate the samples due to the possible influence of both these proce-dures on nitrogen isotope fractionation (Carabel et al., 2006; Guerinet al., 2013; Post et al., 2007).

Total nitrogen and carbon contents (%) were also measured in everysample during the isotopic analyses.

2.4. Statistical analyses

Due to the non-normal distributions of data in many groups tested(Shapiro–Wilk test, P b 0.05) and a relatively low number of terrestrialplant 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 the first and third quartiles were calcu-lated to describe data distributions. To test for differences in eachparameter between the study areas the Mann–Whitney test was used.Z statistic was given when the number of samples in each of the groupscompared was higher than 20, and U statistic when the number waslower than 20 at least in one group. To control the familywise errorrate after multiple comparisons of the terrestrial plant parametersbetween sites we used the Bonferroni correction and a significancelevel of α = 0.05/15 = 0.0033. Means and standard deviations arealso presented to enable comparison of our resultswith those presentedby other authors. Data were processed using STATISTICA 10.0 (StatSoft,Inc. Team, 2011).

3. Results

3.1. Terrestrial ecosystem

At both study areas, the nitrogen stable isotope ratios of terrestrialplants differed depending on the distance from the seashore (andconcurrently from the colony in case of the SEABIRD area). In theSEABIRD area where all samples were represented by O. digyna, thehighest average values of δ15N were recorded closest to the colony (site1, Me = 32.44‰), significantly lower at site 2 (25.73‰), and loweragain (though statistically insignificant from site 2) at site 3 (22.57‰;Table 1). δ15N of plants collected in the CONTROL area showed a similarpattern (Me = 5.98, −1.94, and −3.00‰, respectively, for sites 1, 2,and 3), noting that P. viviparumwas sampled at sites 2 and 3. The differ-ence between these two sites in the CONTROL area was only ca. 1‰while in the SEABIRD area it was about 3‰ between sites 2 and 3.

Carbon stable isotope ratio of terrestrial plants was lowest in closeproximity to the seabird colony (site 1, Me = −30.26‰), significantlyhigher (less negative) at site 2 (−29.71‰), and intermediate (but notsignificantly different from the other sites) at site 3 (−29.96‰;Table 1). In the CONTROL area, plant δ13C values were highest of all atsite 1 (−28.79‰), and similar to each other and to all the SEABIRDsites at sites 2 and 3 (−30.20 and −30.06‰, respectively).

Total plant nitrogen contentwas the highest close to the colony (site1,Me=4.25%), intermediate close to the shore (site 3: 3.77%), and low-est on the mid-slope (site 2: 3.45%) in the SEABIRD area, but thesevalues were not statistically significantly different from each other

Table 1Median values of δ15N, δ13C (‰), total nitrogen and carbon content (%) inplants collected at diffeletters indicate significantly different values within each parameter (Mann–Whitney test with

SEABIRD

1 (N = 9) O. digyna 2 (N = 11) O. digyna 3 (N = 10) O. digyna

δ15N 32.44a 25.73b 22.57b

Total N 4.25a 3.45ac 3.77a

δ13C −30.26a −29.71b −29.96ab

Total C 40.88a 40.41a 40.13a

(Table 1). In the CONTROL area, considerably higher plant nitrogencontent values were recorded at site 2 (3.28%) and site 3 (3.38%;P. viviparum) than at site 1 (2.78%, O. digyna).

Total plant carbon content showed a similar level across all the threesites 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 areawere significantly higher than total C at site 1 of the CONTROL area(36.10%), but lower than the control sites 2 (44.40%) and 3 (45.00%).

Due to differences in the nitrogen and carbon isotope ratios, andtotal C andN contents between the two plant species (possibly irrespec-tive of the seabird fertilization but, for instance, resulting from differentpotential to nutrient absorption or resource partitioning; Kjelland andChapin, 1992), we excluded P. viviparum samples from further analyses(including them did not change the direction or the significance of thestatistical differences described below in δ15N, δ13C, and total N; datanot shown). Clear differences were found both in the nitrogen isotopicratio and total nitrogen content between O. digyna specimens growingbelow the colony and those from the control area (P b 0.001 in bothcases; Fig. 1). On average, δ15N was five times greater in the SEABIRDarea (MeS = 25.21‰) compared to the CONTROL (5.98‰), and therewas a ca. 1% increase of total N values (3.96% vs. 2.78%). The lowestvalue of O. digyna δ15N signature recorded in the SEABIRD area was20.40‰ while the highest among the samples in the CONTROL was9.14‰. The values of the total N content in the SEABIRD area rangedfrom 3 to 5% whereas those in the CONTROL area were 2.4 to 3.6%.

Carbon stable isotope ratio was ~1‰ lower while the total Ccontent was 4% higher in O. digyna collected in the SEABIRD area(δ13C: −29.94‰, total C: 40.31%) than in samples from the CONTROLarea (δ13C: −28.79‰, total C: 36.01%), and both the differences werehighly significant (P b 0.001; Fig. 2).

3.2. Marine ecosystem

There were no statistical differences in δ15N between brown algaesampled 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 theSEABIRD than in the CONTROL area (MeS = 5.10‰ vs. MeC = 5.51‰,P = 0.001) while hermit crabs showed the opposite pattern (MeS =8.49‰ vs. MeC = 8.12‰, P b 0.001). Since hermit crab individualswere 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 b 0.001), we additionallycompared only specimens of similar biomass, ranging from 0.05 to0.2 g DM (NS = 11, NC = 15). We obtained similar results, with δ15Nbeing higher in the SEABIRD area than in the CONTROL (Mann–Whitneytest, U = 43.00, P = 0.042).

Total N content in algal blades was significantly higher close tothe colony as compared to the CONTROL area (MeS = 1.18% vs.MeC = 0.93%, P b 0.001) while in the stipes it was similar across thesites (MeS = 1.26% vs. MeC = 1.18%, P = 0.371). Similarly to the δ15Npattern, total N in sea urchins was lower in the SEABIRD than in theCONTROL area (MeS = 3.31% vs. MeC = 4.00%, P b 0.001). There wasno statistical difference in hermit crab total N content between the

rent distances from the seashore on both study areas (cf.Materials andmethods). DifferentBonferroni correction, P b 0.0033).

CONTROL

1 (N = 10) O. digyna 2 (N = 10) P. viviparum 3 (N = 10) P. viviparum

5.98c −1.94d −3.00d

2.78b 3.28bc 3.38bc

−28.79c −30.20ab −30.06ab

36.10b 44.40c 45.00c

ControlColony0

5

10

15

20

25

30

35

40

δ15N

(‰)

Z=4.67, P<0.001

ControlColony

0

1

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8

9

10

ControlColony

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Colony Control

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9

10

Z=-3.20, P<0.01

Colony Control

0

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9

10

Z=4.47, P<0.001

ControlColony0

1

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8

Tot

al N

con

tent

(%

)

Z=4.08, P<0.001

ControlColony0

1

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8Z=3.93, P<0.001

ControlColony0

1

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Colony Control0

1

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8Z=-3.78, P<0.001

Colony Control0

1

2

3

4

5

6

7

8

Terrestrial plant Alga-stipe Sea urchin Hermit crabAlga-lamina

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 Saccharinalatissima, sea urchins Strongylocentrotus droebachiensis, and hermit crabs Pagurus pubescens on the SEABIRD and CONTROL areas. Significant differences between the areas marked witharrows (Mann–Whitney test). Note different scales of the vertical axis of δ15N signature in terrestrial plants.

52 K. Zmudczyńska-Skarbek et al. / Journal of Marine Systems 144 (2015) 48–56

two sites (MeS = 6.50% vs. MeC = 6.13%, P = 0.251), and it was validalso when specimens of similar biomass were compared (P = 0.350).

Stable carbon isotope ratios were significantly lower in the SEABIRDarea 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 b 0.001) and in hermit crab bodies(MeS = −20.30‰ vs. MeC = −18.16‰, P b 0.001; the difference isstill significant when hermit crabs of similar size were compared: 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 con-tent was lower 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 b 0.001), but was higher in hermit crabs (MeS =36.41% vs. MeC = 32.00%, P = 0.001; there were no differences whencrabs of similar size were compared, P = 0.177).

4. Discussion

It is well known that seabirds can play an important role in shapingterrestrial habitats close to their breeding colonies (Anderson and Polis,1999; Mulder et al., 2011 and refs. therein; Zwolicki et al., 2013). Thisrole is especially important in nutrient-poor polar regions, where thevicinities of seabird colonies provide exceptional green oases amongvast areas vegetated only by lichens, mosses and tiny dwarf shrubs (e.g.Stempniewicz, 2005; Zmudczyńska et al., 2009; Zmudczyńska-Skarbeket al., 2013). The rich plant community below the colony studied hereprovides a classic example of this lush ornithogenic tundra (‘bird-cliffvegetation’ as described by Rønning, 1996). Our finding of five timeshigher δ15N values in this vegetation comparedwith vegetation growing

away from ornithogenic influence confirms the importance of marine-derived nutrient transfer into the terrestrial ecosystem.

Most aspects of seabird influence on the terrestrial ecosystem exhib-it a gradual change with distance from the colony (Leishman and Wild,2001; Odasz, 1994; Ryan andWatkins, 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 (Kolb et al., 2010; Lindeboom, 1984; StauntonSmith and Johnson, 1995). In the SEABIRD area, δ15N in plant tissuesalso gradually decreased with distance from the colony. However,even in the most distant site and only 50 m from the sea shore, theaverage nitrogen isotopic ratio was 22.6‰, almost four times higherthan at the CONTROL area (Table 1). This indicates that bulk nutrientsthat may reach the marine ecosystem continued to be available. Whilemost seabird colonies are situated close to the coast, little is knownabout the fate of colony-derived nutrients that enter the sea. Opportu-nistic observations in Isfjorden are suggestive of differences betweenareas close to seabird colonies and those not influenced, exemplifiedby the bigger size of hermit crab individuals found at the SEABIRDarea comparing with those at the CONTROL area.

The use of stable isotope analyses that integrate dietary informationover long periods of time in the study of trophic interactions is wellestablished (Hobson and Welch, 1992; Kelly, 2000; Michener andLajtha, 2007). A range of studies in terrestrial, freshwater and marineecosystems (e.g. Mulder et al., 2011 and refs. therein) have clearlydemonstrated that a distinct isotopic signal of δ15N (and in manycases also δ13C) separates organisms supplied by seabird-derived nutri-ents from those using different food sources, such as atmospheric nitro-gen fixation, windblown material or precipitation on land, andinflowing water masses, coastal erosion or river discharge to the sea.

ControlColony-32

-30

-28

-26

-24

-22

-20

-18

-16

-14

δ13C

(‰)

U=7.00, P<0.001

ControlColony-32

-30

-28

-26

-24

-22

-20

-18

-16

-14

Z=-2.87, P<0.01

ControlColony-32

-30

-28

-26

-24

-22

-20

-18

-16

-14

Z=-4.93, P<0.001

Colony Control-32

-30

-28

-26

-24

-22

-20

-18

-16

-14

Colony Control-32

-30

-28

-26

-24

-22

-20

-18

-16

-14

Z=-5.50, P<0.001

ControlColony16

20

24

28

32

36

40

44

Tot

al C

con

tent

(%

)

Z=4.17, P<0.001

ControlColony16

20

24

28

32

36

40

44

Z=-2.49, P<0.05

ControlColony16

20

24

28

32

36

40

44

Z=-2.14, P<0.05

Colony Control16

20

24

28

32

36

40

44

Z=-5.09, P<0.001

Colony Control16

20

24

28

32

36

40

44

Z=3.25, P<0.01

Terrestrial plant Alga-stipe Sea urchin Hermit crabAlga-lamina

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 Saccharinalatissima, sea urchins Strongylocentrotus droebachiensis, and hermit crabs Pagurus pubescens on the SEABIRD and CONTROL areas. Significant differences between the areas marked witharrows (Mann–Whitney test).

53K. Zmudczyńska-Skarbek et al. / Journal of Marine Systems 144 (2015) 48–56

Therefore, our initial expectationwas for a similar distinction to be pres-ent in benthic organisms of the shallow littoral zone below a seabirdcolony. However, as well as the considerable dilution and dispersioncaused by waves and currents, benthic primary producers can exploitother nutrient sources, such as from rich deep water masses broughtup to the shelf, from material sinking from the euphotic zone(sympagic–pelagic–benthic coupling), and from rivers, melting glaciersand snow (Iken et al., 2005; Kędra et al., 2012; Renaud et al., 2008).All these factors, together with the frequent omnivory seen amongconsumers, may influence the isotopic signal in the sea.

Consistent with previous studies, terrestrial plants growing belowthe colony showed much higher δ15N, total nitrogen and carbon con-tents, though a bit lower δ13C, compared with the control area.S. latissima showed similar differences in the case of δ13C of both itsblades and stipes, and the total N content of the former. However, nodifferences in δ15N were apparent in kelp collected in the two areas.As well as the factors mentioned above, this observationmay be relatedto the strong seasonality of the local climate, with short periods of lightand nutrient availability for marine producers. In the Arctic, the highestnutrient levels are noted during winter (when there is limited or norunoff from the land), and they then decrease rapidly after sea icebreak-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 conditionsworsen again since meltwater carrying sediment from land enters thewater column and the phytoplankton bloom develops (Wiencke et al.,2010). Dunton (1985) observed that in Stefansson Sound, AlaskanBeaufort 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) occurringfrom late April to late July. This way the kelp effectively optimisedlight 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 sunnormally returns to Isfjorden in the middle of February, and from theend of April it operates for 24 h a day there (Elverland, 2009). Hence,S. latissima growth pattern from our study areas may resemble morethose from lower latitudes, such as Great Britain coast or NarragansettBay, USA, where it achieved the maximum growth rate from Februaryto June and from January to May (respectively; refs given by Dunton,1985). At that time in Isfjorden, seabirds have not yet or just startedlaying eggs (in late May/early June, Kovacs, 2005), therefore their totalguano input was still small and diminished by vernal development ofterrestrial vegetation before entering the sea. It is also possible thatornithogenic nutrients entering the water column in mid-summermay be taken up by phytoplankton, as reported by Methratta (2004)in the Gulf of Maine, USA. If so, a seabird-driven phytoplankton bloomcould then reduce light availability and further inhibit growth of benthicmacroalgae, effectively reducing any dependence of the macroalgae onornithogenic nutrients.

The sea urchin S. droebachiensis is considered an omnivore, poten-tially including algae, invertebrates and microbes in its diet, althoughprimarily grazing on macroalgae (Scheibling and Hatcher, 2007).In the typical Arctic benthic food web of Kongsfjorden (west Spitsber-gen), S. droebachiensis and the amphipod Gammarellus homari arethe only consumers of fresh macroalgae. Of 19 macroalgal species

Table2

Mea

n±

SDof

stab

leisotop

eva

lues

(‰)of

particulateorga

nicmatter(POM),alga

ean

dinve

rteb

ratescolle

cted

withinthestud

yarea

andarou

ndSv

alba

rd.V

alue

sin

bold

—in

thevicinity

ofaseab

irdco

lony

.

Area,

depth

PelagicPO

MSe

dimen

tPO

MSa

ccha

rina

latissim

aStrong

ylocen

trotus

sp.

Pagu

ruspu

bescen

sRe

f.

nδ1

5N

δ13C

nδ1

5N

δ13C

nδ1

5N

δ13C

nδ1

5N

δ13C

nδ1

5N

δ13C

Isfjorde

n,be

low

Fuglefjella

5–15

m30

4.02

±0.92

−22

.23±

1.06

305.14

±0.48

−17

.97±

1.58

308.57

±0.35

−20

.15±

1.28

A

Isfjorde

n,be

low

Nordh

allet

5−15

m28

3.94

±2.09

−20

.83±

0.97

305.53

±0.36

−18

.47±

1.08

308.12

±0.30

−18

.08±

0.98

A

Isfjorde

n,Adv

entfjorden

0–14

m5

3.3±

0.85

−22

.6±

0.81

3B

Isfjorde

nmou

th1–

25m

3–5

4.2±

0.28

−25

.8±

0.23

35

4.5±

0.40

5−

15.7

±1.95

3,5

67.1±

0.41

−14

.5±

0.53

3B

Isfjorde

n12

0–42

2m

20.00

±0.57

−24

.60±

0.14

37

4.9±

0.98

−22

.81±

1.93

1,3

96.44

4,5

−16

.523

,4,5

110

.1−

14.8

3B

Kon

gsfjorde

n,closeto

Kon

gsbree

n0–

15m

30.5±

0.06

−29

.48±

1.06

1−

0.74

−23

.31

C

Kon

gsfjorde

n,closeto

Ny-Ålesu

nd0–

15m

2−

1.81

±0.58

−30

.05±

0.09

10.56

−24

.00

16.70

−19

.97

C

Kon

gsfjorde

n,closeto

Ny-Ålesu

nd32

9m

19.91

,2

−17

.91,2

D

BarentsSe

aMargina

lIce

Zone

213–

343m

45.60

±1.93

1,2

−24

.78±

1.43

1,2

18.21

,2

−17

.81,2

111

.81,2

−18

.71,2

E

Refs:A

—Th

isstud

y,B—

Løkk

en(201

3),C

—Kęd

raet

al.(20

12),D—

Rena

udet

al.(20

11),E—

Tamelan

deret

al.(20

06).

1Samples

chem

ically

decarbon

ized

priorto

analysis.

2Samples

chem

ically

delip

idated

priorto

analysis.

3δ1

3Cva

lues

mathe

matically

norm

alized

forlip

idconten

tcorrection

.4

Value

scalculated

from

thegive

nmeanva

lues

forgrou

psof

samples.

5Onlygo

nads

analysed

.

54 K. Zmudczyńska-Skarbek et al. / Journal of Marine Systems 144 (2015) 48–56

experimentally offered to sea urchins, S. latissima (and especially itsblades) was the most preferred food in a multi-choice assay, and wasalso consumed at the highest rate in a no-choice assay (Wessels et al.,2006). Our isotopic results are not consistentwith S. droebachiensis pref-erentially grazing on S. latissima within the study areas. The sea urchinδ15N was lower in the SEABIRD than the CONTROL area, whereas Nisotopic signatures in both parts of the brown alga were similar acrossthe two sites. The opposite pattern was seen with the carbon isotoperatios, which were significantly lower in S. latissima growing belowthe seabird colony than away from it, but comparable in sea urchinbodies from the two sites. It is worth to notice that the total nitrogencontent in S. latissima blades was significantly lower in the CONTROLas compared with the SEABIRD area. Some studies demonstrate thatanimal tissues become enriched with 15N following nutritional stress,e.g. caused by reduced nutrient intake (Adams and Sterner, 2000) orfasting during breeding (Hobson et al., 1993) as a consequence ofrecycling of body nitrogen. Hence, nitrogen-poor diet might be respon-sible for the sea urchin δ15N increase in the CONTROL area. Howeverother authors, like Oelbermann and Scheu (2002) have found the oppo-site — δ15N of predator bodies increased with higher N content of theirprey. They also argue that in thefield it is unlikely that generalist feederssurvive for a long time on diets of very low quality.

Most likely, local sea urchins supplemented their diet by alternativefood sources which had different N and C isotopic signals thanS. latissima. From among several macroalgae species consumed withdifferent rates by sea urchins in the experiment led by Wessels et al.(2006), Løkken (2013) gives stable isotope data of six sampled in theIsfjorden mouth. The analysed macroalgae showed either higher orlower 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 consumerisotopic signal. Yet there is no matching sea urchin data to confirm it.There is also lots of evidence that S. droebachiensis may optimise itsenergy and nutrition requirements through selective feeding on thebest food accessible within that available within a habitat (Scheiblingand Hatcher, 2007). Below depth range of algae occurrence, where thefood resources are insufficient, S. droebachiensis switches to carnivory,scavenging, and even cannibalism when starving (Himmelman andSteele, 1971; Renaud et al., 2011). More research on the diet of localpopulations of sea urchins is needed, for instance to verify if theincreased values of δ15N and total N content in the CONTROL areamight 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 andsympagic origin. This feeding strategy means that they are particularlywell adapted to living in harsh, unpredictable environments and it isthought that nutrient availability has rarely been a limiting factor forthese decapods (Lancaster, 1988). Our results suggest that the hermitcrab P. pubescens shows evidence of ornithogenic nutrient influence,with their nitrogen stable isotope ratio being significantly higherbelow the colony than at the control site. All the four parameters studied(N and C stable isotope ratios and total contents) in hermit crabsshowed the same pattern of differences between the SEABIRD andCONTROL areas as in the case of terrestrial plants, while the patternwas different comparing with the kelp and sea urchins. This may indi-cate the seabird-derived enrichment of at least some of the producersof the food chains that hermit crabs based on, at least partially, such asbenthic microalgae and/or phytoplankton. One of the challenges forfuture research is to measure the proportion of food originating in thepelagic zone in the hermit crab diet, since pelagic organic matter maybe supported by the ornithogenic nutrients to a relatively large extent(Methratta, 2004; Signa et al., 2012), and then may sink and enter thebottom food chains through pelagic–benthic coupling (Renaud et al.,2008; Søreide et al., 2013; Tamelander et al., 2006).

Comparing our results with other published isotopic data frombenthic food chain elements from Svalbard (Table 2), levels of nitrogen

55K. Zmudczyńska-Skarbek et al. / Journal of Marine Systems 144 (2015) 48–56

stable isotopes in S. latissima and both the benthic consumers obtainedfrom similar to those of the current study were lower than in either ofour two study areas. However, δ15N values of both Strongylocentrotussp. and P. pubescens were highly enriched when collected from muchdeeper sites, most likely indicating a higher proportion of animal tissuesin their diet. As yet, no isotopic studies have described the entire localfood chain, it remains unclear which parts of this food web area areinfluenced by the input of ornithogenic nutrients.

Our results indicate that the influence of seabirds on the coastalbenthic environment in the Arctic, while detectable, is less than whathas been observed in the terrestrial ecosystem. However, it remainsunclear which elements of the seabed community are positively andnegatively influenced by seabird fertilization. Even though sufficientsample sizes of each species studiedwere collected to reduce variabilityamong replicates, each species demonstrated a different pattern ofisotopic variability between the two study areas. Further studies arenecessary to fully understand the influence of ornithogenic nutrientson the benthic community, including both absolute and relative abun-dances, and isotopic analyses across the food web, and from nutrientsfrom the water column throughout the year.

Acknowledgements

We thank Dr. Gilles Lepoint (Laboratory of Oceanology, University ofLiège, Belgium) for the isotopic analyses and Prof. Peter Convey (BritishAntarctic Survey, UK) for the consultation and linguistic improvement.Many colleagues have contributed to our discussions. This study wassupported by the Faculty of Biology, University of Gdańsk to KZS(Grant No. 538-L120-B082-13) and the Polish National Science Centreto PK (Grant No. 2011/03/B/NZ8/02872) and PB (DEC-2011/01/N/NZ8/04493). We also acknowledge the Antoni Dębski Scholarshipgranted by the Polish Society of Hyperbaric Medicine and Technology(PTMiTH) to PB. The study was performed under the permission ofthe Governor of Svalbard.

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