Context-dependent consequences of Marenzelleria spp. (Spionidae: Polychaeta) invasion for nutrient cycling in the Northern Baltic Sea

Oceanologia (2015) 57, 342—348 Available online at www.sciencedirect.com ScienceDirect j o u r n a l h o m e p a g e : w w w. e l s e v i e r. c o m / l o c a t e / o c e a n o ORIGINAL RESEARCH ARTICLE Context-dependent consequences of Marenzelleria spp. (Spionidae: Polychaeta) invasion for nutrient cycling in the Northern Baltic Sea§ Alexey Maximov a,*, Erik Bonsdorff b, Tatjana Eremina c, Laura Kauppi d, Alf Norkko d, Joanna Norkko d a Zoological Institute Russian Academy of Sciences, St. Petersburg, Russia Environmental and Marine Biology, Faculty of Science and Engineering, Åbo Akademi University, Åbo, Finland c Russian State Hydrometeorological University, St. Petersburg, Russia d Tvärminne Zoological Station, University of Helsinki, Hanko, Finland b Received 12 January 2015; accepted 17 June 2015 Available online 14 July 2015 KEYWORDS Bioturbation; Bioirrigation; Nutrient fluxes; Macrozoobenthos; Non-indigenous species Summary Marenzelleria spp. are among the most successful non-native benthic species in the Baltic Sea. These burrowing polychaetes dig deeper than most native Baltic species, performing previously lacking ecosystem functions. We examine evidence from experiments, field sampling and modelling that the introduction of Marenzelleria spp. affects nutrient cycling and biogeochemical processes at the sediment—water interface. Over longer time scales, bioirrigation by Marenzelleria spp. has the potential to increase phosphorus retention in bottom deposits because of deeper oxygen penetration into sediments and formation of a deeper oxidized layer. In contrast, nitrogen fluxes from the sediment increase. As a consequence of a decline of the phosphate concentration and/or rising nitrogen/phosphorus ratio, some Northern Baltic ecosystems may experience improvement of the environment because of mitigation of eutrophication and harmful cyanobacteria blooms. Although it is difficult to unambiguously estimate the ecosystem-level consequences of invasion, in many cases it could be considered as positive due to increased structural and functional diversity. The long-term interactions with the native § The present study was supported by BONUS project COCOA, Russian Foundation for Basic Research (grant 14-04-91721), Russian Geographical Society (grant 13-05-41464) and Government Target Project N82014/166 of the Ministry of Education and Science of the Russian Federation. * Corresponding author at: Zoological Institute Russian Academy of Sciences, Universitetskaya nab. 1, 199034 St. Petersburg, Russia. Tel.: +7 8123281311; fax: +7 8123282941. E-mail address: (A. Maximov). Peer review under the responsibility of Institute of Oceanology of the Polish Academy of Sciences. http://dx.doi.org/10.1016/j.oceano.2015.06.002 0078-3234/# 2015 Institute of Oceanology of the Polish Academy of Sciences. Production and hosting by Elsevier Sp. z o.o. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). Context-depended consequences of Marenzelleria spp. (Spionidae: Polychaeta) invasion 343 fauna still remain unknown, however, and in this paper we highlight the major knowledge gaps. # 2015 Institute of Oceanology of the Polish Academy of Sciences. Production and hosting by Elsevier Sp. z o.o. This is an open access article under the CC BY-NC-ND license (http:// creativecommons.org/licenses/by-nc-nd/4.0/). 1. Introduction Annelid worms are well known habitat modifiers. In terrestrial ecosystems, the key role of earthworms was first recognized by Darwin (1881). He stated “It may be doubted whether there are many other animals which have played so important a part in the history of the world. . .” (Darwin, 1881). The earthworms function as ecosystem engineers by modifying the physical, chemical and biological characteristics of soil (Straube et al., 2009). In marine sediments, analogical roles are played by polychaete worms. Through bioturbation and bioirrigation they affect the physical structure of sediments and exchange processes at the sediment— water interface (Berke, 2010; Kristensen et al., 2012; Meysman et al., 2006; Quintana et al., 2011). Although experimental studies of the effects of burrowing animals on marine sediment biogeochemistry are numerous (e.g. Caliman et al., 2011; Hedman et al., 2011; Karlson et al., 2007b; Norling et al., 2007), ecosystem-level biogeochemical consequences of this activity still remain poorly understood. A recent largescale invasion of bioturbating polychaetes of the genus Marenzelleria to the species-poor benthic communities of the Northern Baltic Sea (Maximov, 2011; Norkko and Jaale, 2008; Villnäs and Norkko, 2011) has provided the opportunity to study the role of worm-induced processes in the ecosystem. Marenzelleria spp. are among the most successful nonnative benthic species in the Baltic Sea during recent decades. They first appeared in 1985 and quickly colonized the entire sea, occupying a dominant position in the zoobenthos (Ezhova et al., 2005; Kauppi et al., 2015; Villnäs and Norkko, 2011; Zettler et al., 2002). Initially the introduced polychaetes were identified as the North American Marenzelleria viridis (Verrill). During the subsequent revision of the genus the polychaetes from the eastern Baltic Sea were described as a different species, namely Marenzelleria neglecta, also originating from North America (Sikorski and Bick, 2004). In the mid-2000s the occurrence of three sibling Marenzelleria species in the Baltic Sea was confirmed by molecular methods: M. viridis, M. neglecta and M. arctia (Chamberlin) (Bastrop and Blank, 2006; Blank et al., 2008). The last species was known earlier only from the Arctic Basin (Sikorski and Buzhinskaya, 1998). According to recent studies, polychaetes dominating in the deep open areas of northern Baltic Sea belong to M. arctia (Kauppi et al., 2015). The native benthic macrofauna of the Northern Baltic Sea is low in diversity and thus strongly dominated by a few key species. Examples of the most common sediment-dwelling invertebrate species in the area are the bivalve Macoma balthica, and the crustaceans Monoporeia affinis, Pontoporeia femorata and Saduria entomon (Bonsdorff, 2006; Elmgren, 1984; Villnäs and Norkko, 2011). Polychaete worms in the Northern Baltic Sea are, as a rule, not abundant with a complete absence of large burrowing forms. In this paper we provide an overview of evidence from experiments, field sampling and modelling that the introduction of Marenzelleria spp. affects sediment-water fluxes and nutrient cycling in a region that was previously practically devoid of worms. Here we discuss patterns emerging from reviewed studies on direct worm-induced effects on nutrient fluxes, highlighting perspectives for future research and important implications of the Marenzelleria spp. invasion for ecosystem services and management. 2. Experimental studies A substantial amount of experimental data about the influence of Marenze (...truncated)