Elsevier

Journal of Marine Systems

Volume 168, April 2017, Pages 31-37
Journal of Marine Systems

Following the flow of ornithogenic nutrients through the Arctic marine coastal food webs

https://doi.org/10.1016/j.jmarsys.2016.12.006Get rights and content

Highlights

  • Arctic colonial seabirds supply coastal communities with allochtonous nutrients.

  • Most probably, phytoplankton assimilate ornithogenic nutrients in the sea initially.

  • Seabird-derived nutrients do not supply food chains based on benthic producers.

  • Ornithogenic subsidies are not a major nutrient source for marine organisms.

Abstract

Arctic colonial seabirds are recognized as effective fertilizers of terrestrial ecosystems by delivering marine-origin nutrients to the vicinities of their nesting sites. A proportion of this ornithogenic matter is then thought to return to the sea and, concentrated within a smaller area, locally provides additional nutrients for the nearshore marine communities. The aim of this study was to assess the presence and impact of local ornithogenic enrichment on two important elements of the Arctic coastal food web: (1) the planktonic pathway originating in the surface water, and (2) the benthic pathway based on benthic primary production. We sampled two areas in Isfjorden (Spitsbergen): one located below a coastal mixed breeding colony of guillemots and kittiwakes, and a control area not influenced by the colony. Slightly higher nitrogen stable isotope ratios (δ15N) were found in particulate organic matter suspended in the surface water (POM), sedimentary organic matter (SOM) from outside the zone of dense kelp forest, and the predatory/scavenging whelks Buccinum sp. collected below the seabird colony (the components recognized as following the planktonic path). In contrast, no ornithogenic isotopic enrichment was detected in the herbivorous gastropod Margarites helicinus or in SOM from the kelp zone (benthic path). The data are compatible with those obtained from the same location a year before, showing δ15N enrichment in predatory/scavenging hermit crabs Pagurus pubescens below the seabird, and no such changes in kelps Saccharina latissima or their presumed consumers, sea urchins Strongylocentrotus droebachiensis (Zmudczyńska-Skarbek et al., 2015a). The results suggest that, in the conditions of periodic, short-term pulses of ornithogenic nutrient inputs to the local marine environment, which typify the short High Arctic summer, planktonic organisms are the initial organisms to incorporate these nutrients before transfer to the benthic food web via pelagic–benthic coupling. However, the supply of ornithogenic resources alone is insufficient to support benthic producers and the trophic pathways based on them. Overall, the ornithogenic subsidies are not a major nutrient source for marine organisms from below the seabird colony.

Introduction

In Arctic shelf seas, light conditions and availability of macronutrients are highly seasonal, presenting several constraints to the organisms living there (Michel, 2013). Nitrogen and phosphorus concentrations in seawater are high during the winter months but become fully depleted in summer due to the dense phytoplankton blooms that form during spring. At the same time, photosynthetic carbon fixation is possible only with sunlight, which in central Spitsbergen is available from mid-February to late October, with the period of the midnight sun lasting from late April to late August. The phytoplankton bloom and the influx of melt water from the land during late spring and summer both contribute to water turbidity, further modulating nutrient levels and the photosynthetic capacity of other producers such as macroalgae (Aguilera et al., 2002, Wiencke et al., 2010). Thus, the strong seasonality typical of the High Arctic determines the potential food sources available to benthic communities, including the direct primary production of benthic micro- and macroalgae, the partial transfer of pelagic suspended particulate organic matter (POM) and sea ice algae via sympagic-pelagic–benthic coupling, sedimentary organic matter (SOM), and terrestrial deposits from river discharge and coastal erosion (Iken et al., 2005, Kędra et al., 2012, Renaud et al., 2008, Renaud et al., 2015, Søreide et al., 2013). Seabirds nesting in dense coastal colonies are assumed to play additional but largely unquantified role providing nutrients back to the marine pelagic and benthic environments (Young et al., 2011 and references therein), and are potentially of great importance as they are at their peak during the otherwise nutrient-limited part of the year in the summer months.

Seabirds are widely recognized as key elements of Arctic ecosystems. One important feature of their biology is their reliance on marine resources for feeding, while then releasing many of these nutrients where they nest on land, often on coastal terraces and sea-facing mountain slopes and cliffs, where many species form large breeding colonies during the summer months. Due to the transport and deposition of marine-derived organic matter, primarily in the form of guano, nutrient-poor soil in the vicinity of their colonies is fertilized. This stimulates primary and secondary production, and has considerable influence on species composition and biomass across the multiple trophic levels of the local terrestrial ecosystem (e.g. Eurola and Hakala, 1977, Jakubas et al., 2008, Zawierucha et al., 2016, Zmudczyńska et al., 2012, Zmudczyńska-Skarbek et al., 2015b, Zmudczyńska-Skarbek et al., 2013, Zwolicki et al., 2016).

Although researchers have been aware of the potential of guano input to influence marine environments for many years (e.g. Leentvaar, 1967), there remains a dearth of knowledge about the fate of ornithogenic nutrients which, if not assimilated on the land, may return to the sea through leaching, runoff or volatilization, and also direct deposition of faeces just offshore from the colony (but see Kolb et al., 2010, Lindeboom, 1984, Staunton Smith and Johnson, 1995, Wainright et al., 1998). In recent years, interest in ornithogenic enrichment of the marine ecosystem has increased although published studies are limited to a very few, mostly temperate, locations (Gagnon et al., 2013, Kolb et al., 2010, Methratta, 2004, Signa et al., 2012, Vizzini et al., 2016). It is hypothesised that nutrients originating from vast areas of seabird oceanic feeding grounds may be concentrated in relatively small coastal areas, and constitute there an important resource for marine primary producers and consumers (a ‘bottom-up effect’, sensu Young et al., 2011).

The role of seabirds in delivering nutrients to the spatially limited marine littoral zone beneath their colonies is particularly poorly investigated in the often-inaccessible polar regions. It has been suggested, however, that the consequences of enrichment of marine ecosystems may not be as apparent as on land due to water movements such as waves, tides and bottom currents leading to nutrient dispersion (Young et al., 2011). The limited data currently available from the Arctic are inconsistent, partly because of different regions and physical and temporal scales of the studies available. Thus, some earlier works described increased levels of nutrients and enhanced productivity of phyto- and zooplankton near seabird colonies on the coasts of the Russian Arctic (Novaya Zemlya and Murmansk Coast; Golovkin, 1967, Golovkin and Garkavaya, 1975, Zelickman and Golovkin, 1972). Wainright et al. (1998) also reported well-defined enrichment of δ15N and δ13C (i.e. stable isotopes proxies for estimating the influence of seabirds on the ecosystem) in marine phytoplankton, kelp and some zooplankton near seabird colonies in the region of the exceptionally productive Bering Sea shelf. However, these authors also suggested that, at a wider scale, the ornithogenic nutrient supplies were relatively small and possibly insignificant for these organisms' overall requirements.

Our initial studies of seabird influence on coastal benthic communities at Spitsbergen (Zmudczyńska-Skarbek et al., 2015a) gave evidence of seabirds locally fertilizing elements of marine food chains based on phytoplankton, but were not conclusive. Furthermore, since the surface water food web components may sediment to the bottom (as phyto-detritus, plankton carcasses, fecal pellets, molts and marine snow), they might then enter the benthic ecosystem (a phenomenon known as pelagic–benthic coupling; Iken et al., 2005, Renaud et al., 2011, Renaud et al., 2008, Søreide et al., 2013, Tamelander et al., 2006). However, in our initial study, no ornithogenic enrichment of large benthic producers, macroalgae, or their assumed primary consumers was found (Zmudczyńska-Skarbek et al., 2015a).

To examine the importance of pelagic–benthic coupling in transferring ornithogenic matter into the benthic food web, the present study investigated a greater range of elements of the nearshore community, and focused on POM and SOM. POM suspended near the surface can serve as a surrogate for phytoplankton, and the starting point in the transfer of ornithogenic components to the seafloor where it may be assimilated by filter-feeding organisms. SOM, consisting of the remains of POM and benthic organisms together with products of their metabolism, is a food source for benthic detritivores and scavengers.

This study complemented the results obtained initially (Zmudczyńska-Skarbek et al., 2015a), and aimed to assess the presence of local ornithogenic nutrient enrichment on two key elements of the High Arctic coastal food web on Spitsbergen: (1) the planktonic pathway originating in the surface water, and (2) the benthic pathway based on benthic primary production. We hypothesised that the planktonic path would show stronger evidence of dependence on nutrient input from seabirds nesting in the immediate vicinity, while the benthic path would show lower or no such benefit. We integrate new data with the preliminary information presented by Zmudczyńska-Skarbek et al. (2015a) in order to give a more thorough assessment of the flow of ornithogenic nutrients into and through the coastal pelagic and benthic food webs.

Section snippets

Study area

The study was conducted on the south-east coast of Isfjorden, the largest fjord on the west coast of Spitsbergen (Svalbard Archipelago, Fig. 1) in early August 2014, when seabirds and their chicks were still present in their colonies. Isfjorden is 170 km long and up to 24 km wide, and includes four side-fjords. About 55% of its area is shallower than 100 m (Nilsen et al., 2008). Its hydrology is shaped by periodic inflow of relatively warm and nutrient-rich Atlantic water from the West Spitsbergen

Nitrogen enrichment of the benthic food web

POM suspended in the surface water showed slightly higher nitrogen stable isotope ratios below the seabird colony as compared with the CONTROL area both close to and far from the shore (POM-close: 5.01‰ vs. 4.49‰, POM-far: 4.25‰ vs. 3.55‰, respectively) although the differences were not statistically significant (p = 0.393 in both comparisons; Table 1; Fig. 2). Similarly, a tendency towards higher POM δ15N close to the coast versus far from it was observed both in the SEABIRD (t = 2.39, p = 0.175)

Planktonic pathway

Previous studies from polar (Golovkin and Garkavaya, 1975, Treasure et al., 2015) and temperate regions (Methratta, 2004, Signa et al., 2012) have confirmed that phytoplankton receive and assimilate ornithogenic nutrients in the vicinity of seabird colonies, which was reflected by increased biomass of producers and elevated nitrogen isotopic signal (higher 15N enrichment, closer to the source of guano; Wainright et al., 1998, Vizzini et al., 2016). This study identified similar patterns,

Conclusions

Green oases of lush vegetation growing around seabird colonies, surrounded by large expanses of inhospitable and often barren land, characterise High Arctic landscapes (e.g. Eurola and Hakala, 1977, Zmudczyńska-Skarbek et al., 2013). Seabirds are recognized as effective fertilizers of the terrestrial ecosystem, delivering marine-derived nutrients to the vicinities of their nesting areas (Mulder et al., 2011, Stempniewicz et al., 2007, Wainright et al., 1998, Zwolicki et al., 2013, Zwolicki et

Acknowledgements

We thank Dr. Gilles Lepoint and Dr. Nicolas Sturaro (Laboratory of Oceanology, University of Liège, Belgium) for performing the isotopic analyses, Prof. Peter Convey (British Antarctic Survey, UK) for consultation and linguistic improvement, and the many colleagues that have contributed to our discussions. This study was supported by the Faculty of Biology, University of Gdańsk to KZS (grant nos. 538-L120-B082-13, 538-L120-B605-14 and 538-L120-B949-15).

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