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Eutrophication and Overfishing in Temperate Nearshore Pelagic Food Webs: a Network Perspective

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Eutrophication and Overfishing in Temperate Nearshore Pelagic Food Webs: a Network Perspective MARINE ECOLOGY PROGRESS SERIES Vol. 336: 1–14, 2007 Published April 27 Mar Ecol Prog Ser OPENPEN ACCESSCCESS FEATURE ARTICLE Eutrophication and overfishing in temperate nearshore pelagic food webs: a network perspective Vera Vasas1, 4,*, Christiane Lancelot1, Véronique Rousseau1, Ferenc Jordán2, 3 1Ecologie des Systèmes Aquatiques, Université Libre de Bruxelles, Campus Plaine CP 221, Boulevard du Triomphe, 1050 Bruxelles, Belgium 2Collegium Budapest, Institute for Advanced Study, Szentháromság u. 2, 1014 Budapest, Hungary 3Animal Ecology Research Group, Hungarian Academy of Sciences, Hungarian Natural History Museum, Ludovika t. 2, 1083 Budapest, Hungary 4Present address: Department of Plant Taxonomy and Ecology, Eötvös Loránd University, Pázmány Péter s. 1/C, 1117 Budapest, Hungary ABSTRACT: We investigated the effects of human activ- ities on the pelagic food web structure of nearshore marine ecosystems. Their generic structure was estab- lished on the basis of literature review and analyzed by qualitative structural network analysis. Two main issues were addressed: (1) the role of species capable of forming harmful algal blooms (HABs) and red tides (Noctiluca spp.), as well as the role of jellyfish, in eutrophicated sys- tems; (2) the contribution of human influences on food webs, focusing on bottom-up (increased nutrient loading) and top-down (overfishing) effects. Results suggest that HAB-forming species and Noctiluca stimulate the micro- bial network, but reduce higher trophic levels such as commercially important fish species. Jellyfish act as a Eutrophication and overfishing are threatening marine coas- buffer in eutrophicated and overfished systems, as they tal communities worldwide. Visible consequences are harmful retain nutrients from the water column, but their blooms algal blooms and jellyfish outbreaks. The analysis of the pela- gic food web structure by Vasas et al. (diagrammatically idea- lead to a massive accumulation of large phytoplankton lized above) helps us to understand the mechanisms by which organisms. Anthropogenic nutrient enrichment favors eutrophication and overfishing can generate ecosystem shifts. undesirable species because of their specific position in Illustration: Sándor Snepp; background from Google Earth™ the food web, and this crucial position may explain their far-reaching effects. Finally, while it appears that over- fishing of piscivorous fishes inhibited HABs and sup- ported blooms of diatoms and other large algae in the past, the present-day loss of planktivorous fishes acts syn- INTRODUCTION ergistically with nutrient enrichment in promoting HAB species, Noctiluca and jellyfish. These fundamental con- Coastal waters receive large amounts of anthropo- straints, which are inherent in the generic structure of genic nutrients from domestic and industrial effluents pelagic food webs, thus largely determine community and agricultural runoff. Effects of coastal eutrophica- dynamics in marine coastal ecosystems. tion are discernible at all trophic levels (Cloern 2001) KEY WORDS: Food web · Eutrophication · Overfishing · and appear as direct and indirect qualitative changes Network analysis · Coastal ecosystem · Indirect effects · in pelagic food webs, e.g. proliferation of harmful algal Harmful algal blooms · Gelatinous plankton blooms (HABs), extinction of species at higher trophic levels, and reduced yields of harvestable fishes and Resale or republication not permitted without written consent of the publisher invertebrates. These alterations of the food web struc- *Email: [email protected] © Inter-Research 2007 · www.int-res.com 2 Mar Ecol Prog Ser 336: 1–14, 2007 ture are primarily caused by an excessive input of which human perturbations (nutrient loading from the anthropogenic nutrients having altered N:P:Si ratios bottom up, and overfishing from the top down) might (excess of N and P) in comparison with natural aquatic influence their blooms. This analysis discriminates systems (Billen et al. 1991). between inedible HAB-forming and other algae, be- High-biomass blooms of harmful species at different cause the method only allows the separation of groups trophic levels are one response of the coastal system to on the basis of trophic position; we note, however, that nutrient enrichment. In temperate coastal waters, 3 many innocuous species also bloom, and that edible groups with different trophic positions are considered HAB species may exist. as harmful and as indicators of eutrophication: photo- synthetic algae that form HABs (Glibert & Pitcher 2001), the red-tide ichthyotoxic dinoflagellate Nocti- METHODS luca spp. (Okaichi & Nishio 1976, Daskalov 2002), and jellyfish (e.g. Arai 2001); the jellyfish are considered Network construction. Trophic groups specific to dead ends in the food web. Autotrophic and hetero- the generic pelagic food web and the relationships trophic HAB species are separated in the analysis, between them were identified based on literature because they occupy different trophic levels. review (references in Table 1). Trophic groups were Recent field studies (Daskalov 2002, Gucu 2002, defined on the basis of their trophic functions in the Lancelot et al. 2002) and theoretical evidence (Jordán ecosystem. They represent both tropho-species, i.e. & Wyatt 2006) show links between HABs, jellyfish groups of species that have the same set of predators blooms and overfishing, confirming the observation and prey, and nutrient pools. A tropho-species may be that multiple stressors operate in natural communities either a taxonomically homogeneous or a distant group (Cloern 2001). The existence of trophic cascades, i.e. of of species (Turner & Roff 1993). In some cases different far-reaching top-down effects of predators in aquatic life stages or toxic/non-toxic forms of the same species ecosystems, imply that fisheries actively modify the may belong to different tropho-species. ecosystem, rather than being merely beneficiaries of A trophic relationship between 2 tropho-species was sea resources (Pace et al. 1999). only considered if it represents an important prey– The worldwide problems of increased nutrient load- predator interaction. The importance of the interaction ing and overfishing call for generic and holistic ap- and the contribution of each trophic group to differ- proaches to assess their combined effect, and struc- ent nutrient pools were based on a literature survey tural analysis of trophic networks is a useful tool for (Table 1) and field data (Rousseau et al. 2000). The investigating their causes and consequences. Relation- food web model is thus qualitative, as it is based on ships between parts and the whole can be investigated the existence of the main relationships, rather than on from a network perspective (Higashi & Burns 1991); in actual diet or flow information. this study, we studied changes at the level of the whole Structural network analysis. We used a slightly system that are due to isolated modification of its com- modified version of the mixed trophic impacts method ponents. To identify principal mechanisms underlying (Ulanowicz & Puccia 1990, Vasas & Jordán 2006), the global degradation of coastal ecosystems, we ana- which calculates direct and indirect trophic interac- lyzed the topological structure of a generic pelagic tions from trophic flow data. In the original method, the food web. In this approach, only the very primary dietary coefficient (gij) is the effect of prey i on preda- information of ‘who eats whom’ is considered, hence tor j and represents the actual proportion of i within the giving information about the basic organization of the diet of j. For this network analysis we only considered system. Such simple models are not able to describe the presence/absence of prey–predator interactions the dynamical behavior of a given system, but they (e.g. Fig. 1, where i = A, B, C), and we assume that give information about the core functions determining each prey has the same effect on a given predator; thus its behavior (e.g. Vasas & Jordán 2006). g = 1͞D (1) The present model can be applied to all temperate ij j,in coastal water ecosystems with only minor local modifi- where Dj,in is the number of prey tropho-species of j cations. Special attention was given to highlighting the (called indegree). Similarly, the negative effect of preda- most typical relationships between nutrients and tor i (Fig. 1, where i = D, E) on its prey j (fij) is measured organisms, and to understanding the role and position by the fraction of net output consumed by predator i: of harmful eutrophication-indicator species in the net- f = 1͞D (2) work. To achieve this objective, we quantified the role ij j,out of the 3 selected harmful groups (inedible blooming where Dj,out (called outdegree) is the number of algae, Noctiluca spp., jellyfish) according to their posi- predators of j and non-predatory mortality factors tions in the food web, and we explored the extent to (stress-induced lysis or sedimentation). Net output had Vasas et al.: Eutrophication and overfishing in food webs 3 Table 1. Tropho-species: code, size, input and output of matter. Recent reviews are cited where possible. LDOM: labile dissolved organic matter; SDOM: semi-labile DOM; POM: particulate organic matter Code Trophic group Size (μm) Input Output Sourcea PicoPl Pico- <2 NH4, NO3, PO4 Grazed by HetNanoFl 19, 21 phytoplankton Release of LDOM 15 AutNanoFl Autotrophic 2 to 20 NH4, NO3, PO4 Grazed by µZooPl 19, 22 nanoplankton Release of LDOM 15 LAutFl Large autotrophic 20 to 200 NH4,
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