Eutrophication and overfishing in temperate nearshore pelagic food

Eutrophication and overfishing in temperate nearshore pelagic food

Eutrophication and overfishing in temperate nearshore pelagic food

  • No tags were found...

You also want an ePaper? Increase the reach of your titles

YUMPU automatically turns print PDFs into web optimized ePapers that Google loves.

Vasas et al.: <strong>Eutrophication</strong> <strong>and</strong> <strong>overfish<strong>in</strong>g</strong> <strong>in</strong> <strong>food</strong> webs5RESULTS AND DISCUSSIONStructure of the generic <strong>food</strong> webBased on our literature review, 26 ‘trophic’ groups—19 tropho-species <strong>and</strong> 7 nutrient pools—were identifiedas relevant <strong>in</strong> <strong>temperate</strong> coastal ecosystems (Fig. 3,Table 1). The basic def<strong>in</strong>ition of tropho-species wasbased on their metabolism (autotrophic, heterotrophic)<strong>and</strong> size, s<strong>in</strong>ce these are the ma<strong>in</strong> determ<strong>in</strong>ants oftheir trophic roles. This classification was exp<strong>and</strong>ed,as organisms of similar size may differ <strong>in</strong> prey selectionor trophic fate.We def<strong>in</strong>ed 5 phytoplankton groups, based on theirbottom-up <strong>and</strong> top-down characteristics (Fig. 3). Theseare picoplankton PicoPl (e.g. Synechococcus spp.,Prochlorococcus spp., picoeukaryotes), autotrophic flagellatesAutNanFl (nano-sized phytoplankton belong<strong>in</strong>gto haptophytes, chrysophytes, cryptophytes, pras<strong>in</strong>ophytes),large autotrophic flagellates LAutFl (e.g.non-toxic d<strong>in</strong>oflagellates Ceratium spp.), diatoms Diat,<strong>and</strong> <strong>in</strong>edible bloom<strong>in</strong>g (HAB) algae InedAlg. The latterwas def<strong>in</strong>ed on the basis of the ‘loophole’ hypothesis(Bakun & Broad 2003), i.e. bloom<strong>in</strong>g species aredef<strong>in</strong>ed as those capable of escap<strong>in</strong>g predation controlsby zooplankton because of their size, shape ortoxicity (Irigoien et al. 2005). InedAlg thus <strong>in</strong>clude algaeform<strong>in</strong>g high biomass blooms (e.g. Phaeocystis globosacolonies) <strong>and</strong> toxic species (haptophytes, e.g. Prymnesiumparvum, Chrysochromul<strong>in</strong>a polylepis; raphidophytes,e.g. Heterosigma akashiwo; d<strong>in</strong>oflagellates,e.g. Alex<strong>and</strong>rium spp., Karenia brevis; cyanobacteria,e.g. Nodularia spumigena). Phytoplankton, on the otherh<strong>and</strong>, may rema<strong>in</strong> ungrazed if zooplankton is heavilycontrolled by predators (Daskalov 2002). The harmfuleffects of InedAlg <strong>and</strong> ungrazed edible phytoplanktonwill be discussed separately (see ‘Structural analysis:Consequences of human impacts’).The microbial network (Fig. 3) rests on the bacterialutilization of organic matter <strong>in</strong> the water column <strong>and</strong>the consumption of small auto- <strong>and</strong> heterotrophicgroups, generally one order of magnitude smaller thanthemselves (Sheldon et al. 1972). Free-liv<strong>in</strong>g bacteriaFreeBac utilize dissolved organic matter (DOM), whileNH4InedAlgVirInedAlgVirBacLDOMPicoPlFreeBacSDOMPO4Aut-NanoFlHet-NanoFlPOM-BacJellyfishLAutFlVirNocµZooPlPOMNO3SiDiatVirDiatNoctilucaMeso-ZooPlPlvFishBentFishPiscFishFig. 3. Generic structure of the <strong>pelagic</strong> <strong>food</strong> web. Circles represent trophic groups <strong>and</strong> arrows represent mass transfers betweentrophic groups. Acronyms def<strong>in</strong>ed <strong>in</strong> Table 1. Red: harmful groups; purple: viruses; dark green: l<strong>in</strong>ear <strong>food</strong> cha<strong>in</strong>; light green <strong>and</strong>light brown: microbial <strong>food</strong> web (light brown: bacteria); blue: <strong>in</strong>organic nutrients; brown: organic nutrients; black: exchange withthe sediment. Arrows have the same color as the recipient group

6Mar Ecol Prog Ser 336: 1–14, 2007bacteria attached to detrital particles POM-Bac hydrolyzeparticulate organic matter POM <strong>and</strong> release DOM<strong>in</strong>to the surround<strong>in</strong>g water. Both bacterial groups,along with picoplankton, support the growth of heterotrophicnanoflagellates HetNanoFl, which are <strong>in</strong> turnconsumed by microzooplankton µZooPl (ciliates, d<strong>in</strong>oflagellates,copepod nauplii <strong>and</strong> copepodits I-II), togetherwith AutNanFl (Fig. 3).The higher trophic levels <strong>in</strong>clude mesozooplanktonMesoZooPl (ma<strong>in</strong>ly copepods <strong>and</strong> copepodits III & IV)that graze on large phytoplankton (LAutFl <strong>and</strong> Diat)<strong>and</strong> µZooPl (Fig. 3). In eutrophicated coastal waters,MesoZooPl may be outnumbered by the omnivorousd<strong>in</strong>oflagellate Noctiluca that forms red-tide (occasionallygreen-tide) blooms, which significantly <strong>in</strong>fluencethe function<strong>in</strong>g of the ecosystem (e.g. Yılmaz et al.2005). When bloom<strong>in</strong>g, Noctiluca is toxic to fish becauseof its release of ammonium (Okaichi & Nishio1976). The unsaturated feed<strong>in</strong>g function determ<strong>in</strong>edfor Noctiluca when grow<strong>in</strong>g under laboratory conditionswith different prey (E. Breton pers. comm.), suggeststhat Noctiluca has a great potential to benefitfrom an <strong>in</strong>creased phytoplankton biomass <strong>in</strong> eutrophicatedwaters. Accord<strong>in</strong>gly, Noctiluca has been reportedas an important <strong>in</strong>dicator of anthropogenic <strong>in</strong>fluence(Daskalov 2003).The <strong>food</strong> requirements of top predators, like piscivorousfish species PiscFish, are fulfilled by planktivorousPlvFish <strong>and</strong> benthic-feed<strong>in</strong>g BentFish fish. PlvFish competefor MesoZooPl with Jellyfish (members of theCnidaria <strong>and</strong> Ctenophora), the third harmful trophicgroup (Fig. 3). Jellyfish are undesirable for humans,s<strong>in</strong>ce they compete with PlvFish <strong>and</strong>, be<strong>in</strong>g a trophicdead end, they do not transfer energy <strong>and</strong> nutrientstowards the top predators.At the base of the <strong>food</strong> web, viruses are responsiblefor much of the bacterial mortality <strong>and</strong> the decay ofphytoplankton blooms; their role <strong>in</strong> nutrient regenerationis thus far from negligible (Th<strong>in</strong>gstad et al. 1993).In this study we consider 4 host-specific groups ofviruses susceptible of <strong>in</strong>fest<strong>in</strong>g Diat, InedAlg, FreeBac<strong>and</strong> Noctiluca. Diat <strong>and</strong> InedAlg were chosen on thebasis of their ability to form huge transient blooms.Viruses <strong>in</strong>fest<strong>in</strong>g attached bacteria were not considereddue to the generally low number of their hosts (Azamet al. 1983, Becquevort et al. 1998). Despite a lack of literatureevidence, Noctiluca-specific viruses were<strong>in</strong>cluded <strong>in</strong> this study because of the observed highdensity <strong>and</strong> sudden collapse of Noctiluca blooms thatmight <strong>in</strong>dicate a viral attack (Beltrami & Carroll 1994).The generic <strong>food</strong> web <strong>in</strong>cluded 7 nutrient pools(Fig. 3). All 4 <strong>in</strong>organic nutrient pools (ammonium NH4,nitrate NO3, phosphate PO4 <strong>and</strong> silicic acid Si), whichsupport phytoplankton growth, exchange with the sediment,<strong>and</strong> NH4 <strong>and</strong> PO4 are rem<strong>in</strong>eralized by heterotrophiccomponents of the <strong>food</strong> web (FreeBac, POM-Bac, HetNanoFl, µZooPl, MesoZooPl, Noctiluca). Largerheterotrophic organisms (Jellyfish, PlvFish, BentFish <strong>and</strong>PiscFish) rem<strong>in</strong>eralize nutrients only to a negligibleextent, because of their relatively low biomass (Schneider1990, Hudson et al. 1999).The detrital organic matter is composed of dissolved(DOM) <strong>and</strong> particulate POM forms. Two pools of DOMare dist<strong>in</strong>guished on the basis of their biodegradability:labile LDOM <strong>and</strong> semi-labile SDOM (Fig. 3). Directexcretion by all phytoplankton groups flows to LDOM<strong>and</strong> is easily accessible for FreeBac. Other processes,namely overflow dur<strong>in</strong>g nutrient limitation from phytoplankton,stress lysis or viral lysis, egestion, sloppyfeed<strong>in</strong>g <strong>and</strong> fecal pellet production, contributes to all3 organic pools (LDOM, SDOM, POM).The structure of this generic <strong>pelagic</strong> <strong>food</strong> web of<strong>temperate</strong> coastal ecosystems is basically the same <strong>in</strong>different ecosystems, but the dom<strong>in</strong>ance of trophicgroups or pathways changes <strong>in</strong> l<strong>in</strong>e with environmentalconditions.Structural analysisRole of harmful speciesThe trophic role of the 3 harmful species (InedAlg,Noctiluca, Jellyfish) was determ<strong>in</strong>ed on the basis ofpairwise <strong>in</strong>teractions between the components of thegeneric <strong>food</strong> web (Table 2).InedAlg (Fig. 4a) has a strong negative effect on allphytoplankton groups, due to competition for <strong>in</strong>organicnutrients. On the other h<strong>and</strong>, InedAlg positively<strong>in</strong>fluences the lower <strong>food</strong> web (FreeBac, POM-Bac,HetNanoFl) through the release of organic matter afterviral <strong>and</strong> stress lysis, but unlike other large-sizedphytoplankters (LAutFl, Diat), it negatively affects thehigher <strong>food</strong> web (MesoZooPl, PlvFish, PiscFish; Fig. 4a).This result is supported by the low trophic efficiencyestimated for a Phaeocystis-dom<strong>in</strong>ated <strong>food</strong> web <strong>in</strong> theNorth Sea, <strong>and</strong> expla<strong>in</strong>ed by the important flow of primaryproducts throughout the bacterial loop (Rousseauet al. 2000).The role of Noctiluca <strong>in</strong> the web is ambiguous(Fig. 4b). It impacts MesoZooPl negatively, but 1 orderof magnitude less than InedAlg (Fig. 4a,b); Noctiluca<strong>and</strong> MesoZooPl compete, however, for the same prey(Diat). Thus, we expect that any <strong>in</strong>crease <strong>in</strong> Noctilucabiomass exerts a slightly negative effect on MesoZooPl<strong>and</strong>—as a consequence—on fishes. This result canpossibly be expla<strong>in</strong>ed with the <strong>in</strong>tensive <strong>and</strong> shortnutrient cycles at the very basis of the <strong>food</strong> web, <strong>in</strong>which Noctiluca is <strong>in</strong>volved. The direct nutrient catabolicrelease associated to Noctiluca growth, <strong>and</strong> the

Vasas et al.: <strong>Eutrophication</strong> <strong>and</strong> <strong>overfish<strong>in</strong>g</strong> <strong>in</strong> <strong>food</strong> webs 7Table 2. Pairwise <strong>in</strong>teractions between components of the generic <strong>food</strong> web, quantified as mixed trophic impacts (m ij values). See Table 1for abbreviationsTo PicoPl Aut LAutFl Diat InedAlg Free POM-Bac Het µZooPl Meso Noctiluca Jelly PlvFishFrom NanoFl Bac NanoFl ZooPl fishPicoPl –0.2570 –0.1208 –0.0689 –0.0393 –0.0608 –0.0292 –0.0672 –0.1758 –0.0397 –0.0122 –0.0070 –0.0122 –0.0091AutNanoFl –0.0818 –0.3272 –0.1070 –0.0460 –0.0693 –0.0402 –0.0594 –0.1743 –0.2347 –0.0145 –0.0276 –0.0145 –0.0109LAutFl –0.1388 –0.0058 –0.2130 –0.0641 –0.0762 –0.0079 –0.0288 –0.0373 –0.0958 –0.1115 –0.0278 –0.1115 –0.0836Diat –0.0899 –0.0118 –0.1180 –0.3770 –0.0276 –0.0495 –0.0532 –0.0530 –0.0487 –0.0811 –0.2635 –0.0811 –0.0608InedAlg –0.0930 –0.0674 –0.0557 –0.0388 –0.3052 –0.0413 –0.0915 –0.0194 –0.0061 –0.0179 –0.0234 –0.0179 –0.0134FreeBac –0.0438 –0.0106 –0.0309 –0.0178 –0.0344 –0.5940 –0.0123 –0.0896 –0.0352 –0.0149 –0.0281 –0.0149 –0.0112POM-Bac –0.0829 –0.0135 –0.0459 –0.0414 –0.0538 –0.0077 –0.2707 –0.1547 –0.0582 –0.0259 –0.0570 –0.0259 –0.0194HetNanoFl –0.4504 –0.0711 –0.0698 –0.0475 –0.0942 –0.0856 –0.1461 –0.4240 –0.1967 –0.0558 –0.0710 –0.0558 –0.0419µZooPl –0.3773 –0.4601 –0.0296 –0.0182 –0.0458 –0.0817 –0.1559 –0.3162 –0.4788 –0.0906 –0.0060 –0.0906 –0.0680MesoZooPl –0.0959 –0.2740 –0.3625 –0.0268 –0.0482 –0.0215 –0.0310 –0.1602 –0.2097 –0.5732 –0.0084 –0.4268 –0.3201Noctiluca –0.0512 –0.0315 –0.0480 –0.0718 –0.0348 –0.0479 –0.0691 –0.0049 –0.0149 –0.0016 –0.3038 –0.0016 –0.0012Jellyfish –0.0480 –0.1370 –0.1813 –0.0134 –0.0241 –0.0107 –0.0155 –0.0801 –0.1049 –0.2134 –0.0042 –0.2134 –0.1601PlvFish –0.0360 –0.1028 –0.1359 –0.0100 –0.0181 –0.0081 –0.0116 –0.0601 –0.0786 –0.1601 –0.0031 –0.1601 –0.3701BentFish –0.0120 –0.0343 –0.0453 –0.0033 –0.0060 –0.0027 –0.0039 –0.0200 –0.0262 –0.0534 –0.0010 –0.0534 –0.2100PiscFish –0.0240 –0.0685 –0.0906 –0.0067 –0.0121 –0.0054 –0.0078 –0.0401 –0.0524 –0.1067 –0.0021 –0.1067 –0.4200VirDiat –0.0086 –0.0014 –0.0332 –0.1226 –0.0155 –0.0258 –0.0599 –0.0121 –0.0193 –0.0125 –0.0212 –0.0125 –0.0094VirInedAlg –0.0216 –0.0263 –0.0281 –0.0150 –0.2216 –0.0219 –0.0400 –0.0163 –0.0116 –0.0097 –0.0237 –0.0097 –0.0073VirBac –0.0125 –0.0015 –0.0059 –0.0068 –0.0072 –0.1673 –0.0643 –0.0221 –0.0081 –0.0037 –0.0174 –0.0037 –0.0028VirNoc –0.0265 –0.0067 –0.0064 –0.0260 –0.0016 –0.0197 –0.0936 –0.0244 –0.0046 –0.0043 –0.2006 –0.0043 –0.0032LDOM –0.0219 –0.0053 –0.0155 –0.0089 –0.0172 –0.2030 –0.0062 –0.0448 –0.0176 –0.0075 –0.0140 –0.0075 –0.0056SDOM –0.0219 –0.0053 –0.0155 –0.0089 –0.0172 –0.2030 –0.0062 –0.0448 –0.0176 –0.0075 –0.0140 –0.0075 –0.0056POM –0.0573 –0.0292 –0.0698 –0.0055 –0.0712 –0.0162 –0.6947 –0.1522 –0.0657 –0.0251 –0.2911 –0.0251 –0.0188NH4 –0.1752 –0.1626 –0.1556 –0.0930 –0.1559 –0.0272 –0.0316 –0.0327 –0.0453 –0.0523 –0.0529 –0.0523 –0.0392PO4 –0.1752 –0.1626 –0.1556 –0.0930 –0.1559 –0.0272 –0.0316 –0.0327 –0.0453 –0.0523 –0.0529 –0.0523 –0.0392NO3 –0.1752 –0.1626 –0.1556 –0.0930 –0.1559 –0.0272 –0.0316 –0.0327 –0.0453 –0.0523 –0.0529 –0.0523 –0.0392Si –0.0225 –0.0030 –0.0295 –0.1558 –0.0069 –0.0124 –0.0133 –0.0133 –0.0122 –0.0203 –0.0659 –0.0203 –0.0152To –BentFish–PiscFish –VirDiat –Vir –VirBac –VirNoc –LDOM –SDOM –POM –NH4 –PO4 –NO3 –SiFromInedAlgPicoPl –0.0030 –0.0030 –0.0393 –0.0608 –0.0292 –0.0070 –0.0687 –0.0195 –0.0207 –0.0764 –0.0764 –0.0906 –0.0393AutNanoFl –0.0036 –0.0036 –0.0460 –0.0693 –0.0402 –0.0276 –0.0035 –0.0503 –0.0277 –0.0855 –0.0855 –0.1065 –0.0460LAutFl –0.0279 –0.0279 –0.0641 –0.0762 –0.0079 –0.0278 –0.0349 –0.0212 –0.0102 –0.1021 –0.1021 –0.1004 –0.0641Diat –0.0203 –0.0203 –0.6230 –0.0276 –0.0495 –0.2635 –0.0779 –0.1237 –0.0797 –0.0154 –0.0154 –0.0799 –0.6230InedAlg –0.0045 –0.0045 –0.0388 –0.6948 –0.0413 –0.0234 –0.0494 –0.0939 –0.1012 –0.0663 –0.0663 –0.0880 –0.0388FreeBac –0.0037 –0.0037 –0.0178 –0.0344 –0.4060 –0.0281 –0.3518 –0.3406 –0.0571 –0.0738 –0.0738 –0.0100 –0.0178POM-Bac –0.0065 –0.0065 –0.0414 –0.0538 –0.0077 –0.0570 –0.0295 –0.1020 –0.1934 –0.1147 –0.1147 –0.0143 –0.0414HetNanoFl –0.0140 –0.0140 –0.0475 –0.0942 –0.0856 –0.0710 –0.1407 –0.1785 –0.1419 –0.1574 –0.1574 –0.0620 –0.0475µZooPl –0.0227 –0.0227 –0.0182 –0.0458 –0.0817 –0.0060 –0.0506 –0.0205 –0.0022 –0.0867 –0.0867 –0.0097 –0.0182MesoZooPl –0.1067 –0.1067 –0.0268 –0.0482 –0.0215 –0.0084 –0.0393 –0.0565 –0.0491 –0.0802 –0.0802 –0.0326 –0.0268Noctiluca –0.0004 –0.0004 –0.0718 –0.0348 –0.0479 –0.6962 –0.0679 –0.0708 –0.0716 –0.0789 –0.0789 –0.0187 –0.0718Jellyfish –0.0534 –0.0534 –0.0134 –0.0241 –0.0107 –0.0042 –0.0196 –0.0282 –0.0246 –0.0401 –0.0401 –0.0163 –0.0134PlvFish –0.2100 –0.2100 –0.0100 –0.0181 –0.0081 –0.0031 –0.0147 –0.0212 –0.0184 –0.0301 –0.0301 –0.0122 –0.0100BentFish –0.2633 –0.2633 –0.0033 –0.0060 –0.0027 –0.0010 –0.0049 –0.0071 –0.0061 –0.0100 –0.0100 –0.0041 –0.0033PiscFish –0.5267 –0.4733 –0.0067 –0.0121 –0.0054 –0.0021 –0.0098 –0.0141 –0.0123 –0.0200 –0.0200 –0.0081 –0.0067VirDiat –0.0031 –0.0031 –0.1226 –0.0155 –0.0258 –0.0212 –0.0382 –0.0513 –0.0659 –0.0247 –0.0247 –0.0128 –0.1226VirInedAlg –0.0024 –0.0024 –0.0150 –0.2216 –0.0219 –0.0237 –0.0373 –0.0448 –0.0481 –0.0437 –0.0437 –0.0261 –0.0150VirBac –0.0009 –0.0009 –0.0068 –0.0072 –0.1673 –0.0174 –0.2297 –0.2464 –0.0533 –0.0153 –0.0153 –0.0018 –0.0068VirNoc –0.0011 –0.0011 –0.0260 –0.0016 –0.0197 –0.2006 –0.0311 –0.0525 –0.1057 –0.0047 –0.0047 –0.0030 –0.0260LDOM –0.0019 –0.0019 –0.0089 –0.0172 –0.2030 –0.0140 –0.1759 –0.1703 –0.0286 –0.0369 –0.0369 –0.0050 –0.0089SDOM –0.0019 –0.0019 –0.0089 –0.0172 –0.2030 –0.0140 –0.1759 –0.1703 –0.0286 –0.0369 –0.0369 –0.0050 –0.0089POM –0.0063 –0.0063 –0.0055 –0.0712 –0.0162 –0.2911 –0.0635 –0.1374 –0.2292 –0.1542 –0.1542 –0.0237 –0.0055NH4 –0.0131 –0.0131 –0.0930 –0.1559 –0.0272 –0.0529 –0.0693 –0.0449 –0.0479 –0.1139 –0.1139 –0.1485 –0.0930PO4 –0.0131 –0.0131 –0.0930 –0.1559 –0.0272 –0.0529 –0.0693 –0.0449 –0.0479 –0.1139 –0.1139 –0.1485 –0.0930NO3 –0.0131 –0.0131 –0.0930 –0.1559 –0.0272 –0.0529 –0.0693 –0.0449 –0.0479 –0.1139 –0.1139 –0.1485 –0.0930Si –0.0051 –0.0051 –0.1558 –0.0069 –0.0124 –0.0659 –0.0195 –0.0309 –0.0199 –0.0038 –0.0038 –0.0200 –0.1558

8Mar Ecol Prog Ser 336: 1–14, 20070.150.10a Inedible algae0.69480.050.00–0.05–0.10–0.15-0.30520.150.10b Noctiluca0.6962Mixed trophic impact0.050.00–0.05–0.10–0.15-0.30380.25c Jellyfish0.–0.05–0.10–0.15–0.20–0.25PicoPlAutNanoFlLAutFlDiatInedAlgFreeBacPOM-BacHetNanoFlµZooPlMesoZooPlNoctilucaJellyfishPlvFishBentFishPiscFishVirDiatVirInedAlgVirBacVirNocLDOMSDOMPOMNH4PO4NO3SiFig. 4. Mixed trophic impact of harmful tropho-species. Colors expla<strong>in</strong>ed <strong>in</strong> Fig. 3; see Table 1 for abbreviationsbacterial m<strong>in</strong>eralization of Noctiluca lysis products, cansupport diatom growth, but more importantly, otherphytoplankton groups as well. Such a promotion ofphytoplankton, comb<strong>in</strong>ed with the stimulation ofbacteria, is—through many pathways—beneficial tofishes. These longer pathways may at least partiallyreplace the diatom pathway, which is disrupted byNoctiluca. Hence, nutrient rem<strong>in</strong>eralization appears tobe the ma<strong>in</strong> trophic role of Noctiluca <strong>in</strong> the <strong>food</strong> web,as suggested for North Sea blooms by Schoemann etal. (1998).Jellyfish affect MesoZooPl more negatively thanfishes do, <strong>and</strong> as a consequence, the same applies tothe <strong>in</strong>organic <strong>and</strong> organic nutrient pools (Fig. 4c).Jellyfish may thus play a buffer role for nutrients, asrecently hypothesized for a coastal lagoon ecosystem

Vasas et al.: <strong>Eutrophication</strong> <strong>and</strong> <strong>overfish<strong>in</strong>g</strong> <strong>in</strong> <strong>food</strong> webs9(Fernández et al. 2005). In addition, Jellyfish are likelyto impede InedAlg <strong>and</strong> Noctiluca, prevent<strong>in</strong>g theirblooms by tak<strong>in</strong>g up <strong>and</strong> stor<strong>in</strong>g nutrients, <strong>and</strong> disrupt<strong>in</strong>gnutrient cycl<strong>in</strong>g <strong>in</strong> the water column. Thus, from ahuman perspective, Jellyfish could play a beneficialrole <strong>in</strong> eutrophicated <strong>and</strong> heavily overfished ecosystems.However, Jellyfish are more voracious predatorsof MesoZooPl than are PlvFish, both because of theirfeed<strong>in</strong>g characteristics <strong>and</strong> because they are not controlledby predators (Fig. 4c; cf. Fig. 6a). If Jellyfish outcompetePlvFish, the top-down cascade orig<strong>in</strong>at<strong>in</strong>gfrom the upper trophic level is re<strong>in</strong>forced <strong>and</strong> leads toa massive accumulation of large phytoplankton biomass(Diat <strong>and</strong> LAutFl), if nutrient concentrations arehigh enough (Daskalov 2003). At low nutrient concentrations,the 4-step trophic cha<strong>in</strong> AutNanoFl–µZooPl–MesoZooPl–Jellyfish prevails <strong>in</strong> the system <strong>and</strong> an <strong>in</strong>creasedlevel of jellyfish predation leads to a decrease<strong>in</strong> total phytoplankton biomass. In eutrophicatedwaters, however, large algae <strong>and</strong> the 3-step cha<strong>in</strong>Diat/LAutFl–MesoZooPl–Jellyfish are of greater importance,<strong>and</strong> the cascad<strong>in</strong>g effects of jellyfish predationon copepods lead to <strong>in</strong>creased total phytoplanktonbiomass (Stibor et al. 2004). Mass sedimentation ofungrazed phytoplankton biomass may result <strong>in</strong> hypoxiaor anoxia near the bottom (Cloern 2001). These <strong>and</strong> thestrong negative effects on fish <strong>and</strong> fisheries due toresource competition (see Shiganova 1998 for field evidencefrom the Black Sea) make jellyfish an undesiredgroup, from a human perspective.Consequences of human impactsHuman eutrophication <strong>and</strong> <strong>overfish<strong>in</strong>g</strong> affect the<strong>food</strong> web at several nodes. An <strong>in</strong>creased load<strong>in</strong>g of<strong>in</strong>organic (NH4, PO4, NO3) <strong>and</strong> organic nutrients(LDOM, SDOM, POM) disturbs the <strong>food</strong> web at the bottom,while fish<strong>in</strong>g pressure modifies top predators (Plv-Fish, PiscFish). In order to underst<strong>and</strong> how thesehuman impacts may affect the ecosystem, we haveanalyzed the role these groups play <strong>in</strong> the <strong>food</strong> web,with a focus on harmful tropho-species.Increased nutrient load. Nutrients NH4, PO4 <strong>and</strong>NO3 are beneficial to all tropho-species except Bent-Fish (s<strong>in</strong>ce it feeds on prey from outside the <strong>pelagic</strong>community; Fig. 5a). InedAlg <strong>and</strong> Jellyfish seem to befavored, compared to Diat <strong>and</strong> PlvFish (Fig. 5a). Thissuggests that an <strong>in</strong>crease <strong>in</strong> <strong>in</strong>organic nutrient <strong>in</strong>putwill enhance a disproportional biomass developmentof these undesired species. Noctiluca <strong>in</strong>directly benefitsfrom <strong>in</strong>organic N <strong>and</strong> P enrichment <strong>and</strong>, <strong>in</strong> turn,contributes to this pool with rem<strong>in</strong>eralization processesassociated with its metabolism. This process is a generalfeature of heterotrophic tropho-species, <strong>in</strong>clud<strong>in</strong>gMesoZooPl. The relative importance of these 2 nutrientcycles may lead to alternative stable states of theecosystem at high <strong>in</strong>organic nutrient levels: one associatedwith high MesoZooPl, <strong>and</strong> one with high Noctilucabiomass. The dom<strong>in</strong>ance of Noctiluca can be expla<strong>in</strong>edby the unexpected result that—even though bothgroups are direct competitors for Diat—MesoZooPlfavors Noctiluca growth through its contribution toPOM (Fig. 3), as reported by Kiørboe (2003).A confus<strong>in</strong>g result is that <strong>in</strong>organic N <strong>and</strong> P are <strong>in</strong>creas<strong>in</strong>glymore beneficial to small phytoplankton(Fig. 5a), s<strong>in</strong>ce every phytoplankton group supports itsheterotrophic grazer <strong>and</strong> the subsequent trophic levelsabove. Small phytoplankton organisms thus <strong>in</strong>directlypromote the grazers of their larger competitors. Thepattern <strong>in</strong> our model contradicts the general observationthat small phytoplankton is dom<strong>in</strong>ant <strong>in</strong> oligotrophicwaters, while eutrophicated waters are dom<strong>in</strong>atedby large phytoplankton. This may be an artifactresult<strong>in</strong>g from the simplicity of our model, s<strong>in</strong>cedynamical <strong>in</strong>formation is lost <strong>in</strong> structural networkanalyses. More specifically, the latter cannot accountfor time lags <strong>in</strong> the response of predators to changes <strong>in</strong>prey abundance. Even if the entire prey biomass isconsumed <strong>in</strong> the end, a predator respond<strong>in</strong>g with a significanttime lag to an <strong>in</strong>creased abundance of preywill allow the prey to develop <strong>in</strong> a way that mitigatesthe predator’s effects; this feature is not captured bystructural network analysis. The observed fact thatsmall predators respond faster to <strong>in</strong>creases <strong>in</strong> smallphytoplankters may counterbalance the advantagethat small algae have due to their high competitiveabilities for low nutrients (Fogg 1995) <strong>and</strong> their position<strong>in</strong> the <strong>food</strong> web. Further research is needed forunderst<strong>and</strong><strong>in</strong>g this phenomenon.All harmful groups (InedAlg, Noctiluca, Jellyfish) benefitmore from organic nutrient enrichment (LDOM,SDOM, POM) than their respective ‘desired’ competitor,Diat, MesoZooPl, PlvFish (Fig. 5b,c). Thus, a susta<strong>in</strong>ed<strong>in</strong>crease of organic matter may be responsiblefor the observed disproportional <strong>in</strong>crease <strong>in</strong> the biomassof the undesired groups. A marked differencebetween these groups is the role of s<strong>in</strong>k for organicmatter played by Jellyfish, while InedAlg <strong>and</strong> Noctilucaconstitute a source of organic matter throughout lysis(Table 1; Fig. 3). As a consequence, InedAlg, Noctiluca<strong>and</strong> DOM can <strong>in</strong>crease simultaneously <strong>and</strong> constitutean alternative stable state of the ecosystem.Consequences of <strong>overfish<strong>in</strong>g</strong>. Fish-driven trophiccascades may have large effects <strong>in</strong> ecosystems (Paceet al. 1999), <strong>and</strong> <strong>overfish<strong>in</strong>g</strong> largely disturbs the <strong>food</strong>web (fish<strong>in</strong>g down: Pauly et al. 1998). Accord<strong>in</strong>g toour calculations, PlvFish shows negative effects onJellyfish <strong>and</strong>, to a smaller extent, on InedAlg, Noctiluca<strong>and</strong> all nutrients (Fig. 6a), but it positively affects

10Mar Ecol Prog Ser 336: 1–14, 20070.–0.05–0.10–0.15a NutrientsMixed trophic impact0.–0.05–0.10–0.15b DOM0.20300.2030- 0.1759–0.17030.400.30c POM0.69470.200.100.00–0.10–0.20–0.30PicoPlAutNanoFlLAutFlDiatInedAlgFreeBacPOM-BacHetNanoFlµZooPlMesoZooPlNoctilucaJellyfishPlvFishBentFishPiscFishVirDiatVirInedAlgVirBacVirNocLDOMSDOMPOMNH4PO4NO3SiFig. 5. Mixed trophic impact of <strong>in</strong>organic <strong>and</strong> organic nutrients: (a) NH 4 , PO 4 , NO 3 ; (b) LDOM, SDOM; (c) POM. Colorsexpla<strong>in</strong>ed <strong>in</strong> Fig. 3; see Table 1 for abbreviationslarge phytoplankton (LAutFl <strong>and</strong> Diat). Therefore, Plv-Fish <strong>overfish<strong>in</strong>g</strong> would allow the development ofundesired groups (e.g. jellyfish blooms <strong>in</strong> the BlackSea: Gucu 2002, Lancelot et al. 2002), <strong>and</strong> <strong>in</strong>creasedconcentrations of nutrients <strong>in</strong> the water column. Theeffects of PlvFish <strong>overfish<strong>in</strong>g</strong> are, therefore, similar tothose subsequent to nutrient enrichment, <strong>and</strong> synergisticallysupport harmful species, which results <strong>in</strong> arapid degradation of the ecosystem. Because of thesimplified <strong>in</strong>teractions with<strong>in</strong> the fish community <strong>in</strong>our model, PiscFish exerts its effects entirely throughpredation of PlvFish; this group has, thus, oppositeeffects to PlvFish (Fig. 6b). PiscFish <strong>overfish<strong>in</strong>g</strong> canlead to blooms of Diat <strong>and</strong> LAutFl, which rema<strong>in</strong>ungrazed, because the predation pressure of PlvFishtends to suppress MesoZooPl (Daskalov 2002, Jordán

Vasas et al.: <strong>Eutrophication</strong> <strong>and</strong> <strong>overfish<strong>in</strong>g</strong> <strong>in</strong> <strong>food</strong> webs11Mixed trophic impact0.–0.05–0.10–0.15–0.20–0.25–0.300.150.10a PlvFishb PiscFish–0.37010.050.00–0.05–0.10–0.15–0.4200–0.5267–0.4733PicoPlAutNanoFlLAutFlDiatInedAlgFreeBacPOM-BacHetNanoFlµZooPlMesoZooPlNoctilucaJellyfishPlvFishBentFishPiscFishVirDiatVirInedAlgVirBacVirNocLDOMSDOMPOMNH4PO4NO3SiFig. 6. Mixed trophic impact of fish tropho-species. Colors expla<strong>in</strong>ed <strong>in</strong> Fig. 3. See Table 1 for abbreviations& Wyatt 2006), similarly to what is described abovefor jellyfish.In summary, <strong>overfish<strong>in</strong>g</strong> of PiscFish (under conditionsof nutrient enrichment) may lead to blooms of Diat<strong>and</strong> LAutFl that rema<strong>in</strong> ungrazed, but <strong>overfish<strong>in</strong>g</strong> ofPlvFish may support harmful species (InedAlg, Noctiluca,Jellyfish). Even <strong>in</strong> its simplicity, our analysis tentativelyexpla<strong>in</strong>s why the consequences of <strong>overfish<strong>in</strong>g</strong> <strong>in</strong>coastal seas were not visible for so long. Historically,<strong>overfish<strong>in</strong>g</strong> of larger PiscFish was the first step (Paulyet al. 1998), but the subsequent phytoplankton biomass<strong>in</strong>crease seemed to be related to the <strong>in</strong>crease <strong>in</strong> nutrientloads. However, after depletion of the larger Pisc-Fish, fisheries have turned towards the smaller, butnumerous PlvFish (e.g. anchovy). With time, the effectsof nutrient enrichment <strong>and</strong> <strong>overfish<strong>in</strong>g</strong> started todevelop <strong>in</strong> synergy, result<strong>in</strong>g <strong>in</strong> a very visible degradationof the ecosystem, characterized by HABs <strong>and</strong> jellyfishblooms. One remarkable example is the outburstof Mnemiopsis leidyi <strong>in</strong> the Black Sea after strong<strong>overfish<strong>in</strong>g</strong> of anchovy <strong>in</strong> 1988 (Shiganova 1998).Position<strong>in</strong>g of harmful speciesThe position of harmful species <strong>in</strong> the <strong>food</strong> web is farfrom r<strong>and</strong>om, as they disrupt the <strong>food</strong> web at eachbasic trophic level: InedAlg <strong>in</strong>creases the primary producers’biomass, Noctiluca that of primary consumers<strong>and</strong> Jellyfish to biomass of secondary consumers. Allthese species appear to benefit more from nutrientsthan their competitors, partly as a result of the absenceof predators. The <strong>in</strong>creas<strong>in</strong>g dom<strong>in</strong>ance of <strong>in</strong>edibleforms over edible ones <strong>in</strong> response to nutrient enrichmenthas been demonstrated both theoretically (e.g.Leibold 1996) <strong>and</strong> experimentally (e.g. Ste<strong>in</strong>er 2001),but other mechanisms are also <strong>in</strong>volved. Harmfulgroups are positioned <strong>in</strong> the network <strong>in</strong> a way thatenables them to exploit the most important bottom-upcontrollers of the <strong>food</strong> web (Table 3), accord<strong>in</strong>g to thebottom-up component of the keystone <strong>in</strong>dex (K b ). Themost important bottom-up controls are reflected by thehighest values of K b , which gives an approximation ofthe number of species that would disappear due to

12Mar Ecol Prog Ser 336: 1–14, 2007<strong>food</strong> shortage after the ext<strong>in</strong>ction of the given species.Accord<strong>in</strong>g our calculation of the <strong>in</strong>dex of Jordán et al.(1999), the most important groups are: the <strong>in</strong>organicnutrients NH3, PO4, NO3 (consumed by InedAlg); Diat<strong>and</strong> POM (consumed by Noctiluca), <strong>and</strong> MesoZooPl(consumed by Jellyfish). The crucial position of harmfulspecies <strong>in</strong> the <strong>food</strong> web expla<strong>in</strong>s their strong undesiredeffects <strong>in</strong> ecosystems.Use of qualitative structural analysis of coastalecosystemsS<strong>in</strong>ce the literature data required for the establishmentof the trophic web was scarce, the results of ourstructural network analysis are partly speculative.In addition, the qualitative structural approach failswhere dynamic features determ<strong>in</strong>e the relationshipsbetween trophic groups. Nevertheless, the agreementbetween our model results <strong>and</strong> the conclusions of elaboratecase studies supports the feasibility of the model<strong>and</strong> underscores the overwhelm<strong>in</strong>g importance of the<strong>food</strong> web structure <strong>in</strong> community dynamics.The effects of nutrient load<strong>in</strong>g <strong>and</strong> <strong>overfish<strong>in</strong>g</strong> onthe 3 harmful tropho-species <strong>and</strong> their <strong>in</strong>teractions aresummarized <strong>in</strong> Fig. 7. InedAlg blooms support themicrobial network <strong>and</strong> <strong>in</strong>hibit the transfer of nutrientsup the <strong>food</strong> web, <strong>in</strong>clud<strong>in</strong>g to commercially importantfish species (Fig. 7). The effect of Noctiluca on fishes isless detrimental, s<strong>in</strong>ce this d<strong>in</strong>oflagellate is <strong>in</strong>volved <strong>in</strong>short dynamic nutrient cycles at the base of the <strong>food</strong>web, <strong>and</strong> this cycl<strong>in</strong>g supports small phytoplankton<strong>and</strong> bacteria. The develop<strong>in</strong>g longer pathway fromm<strong>in</strong>ute producers to fishes may partially substitute theshort cha<strong>in</strong> from diatoms.In eutrophicated ecosystems, InedAlg <strong>and</strong> Noctilucablooms correspond to <strong>in</strong>creased total phytoplanktonbiomass, supported by positive relationships betweenelevated chlorophyll a levels, harmful blooms <strong>and</strong><strong>in</strong>creased nutrient load<strong>in</strong>g (Cloern 2001, Daskalov2003). The InedAlg biomass directly contributes to thechlorophyll level, while Noctiluca <strong>in</strong>directly supportsall non-diatom phytoplankton species (Fig. 4b) with its<strong>in</strong>tensive nutrient regeneration <strong>and</strong> <strong>in</strong>tensive feed<strong>in</strong>gon Diat. The shift from diatoms to non-siliceous algae<strong>in</strong> response to eutrophication has been repeatedlypo<strong>in</strong>ted out (e.g. Cloern 2001), but the possible contributionof Noctiluca blooms to this shift is new. InedAlg<strong>and</strong> Noctiluca are fundamentally <strong>in</strong>terrelated <strong>in</strong> coastalecosystems, with many mechanisms ensur<strong>in</strong>g the recycl<strong>in</strong>gof nutrients <strong>in</strong> the water column <strong>in</strong>stead ofexport<strong>in</strong>g them to fishes.On the other h<strong>and</strong>, InedAlg <strong>and</strong> Noctiluca <strong>in</strong>hibitJellyfish bloom<strong>in</strong>g (Fig. 7), because they reta<strong>in</strong> nutrients<strong>in</strong> the water column. Jellyfish is likely to act asa buffer <strong>in</strong> eutrophicated <strong>and</strong> overfished systems,s<strong>in</strong>ce it forms an efficient s<strong>in</strong>k of matter. As a consequence,Jellyfish <strong>in</strong>hibits InedAlg <strong>and</strong> Noctiluca as well(Fig. 7). At the same time, Jellyfish blooms lead to amassive biomass accumulation of large phytoplanktonbecause of the re<strong>in</strong>forced trophic cascade.Anthropogenic nutrient enrichment favors harmfultropho-species (Fig. 7) more than it benefits desiredgroups; this has far-reach<strong>in</strong>g effects, because harmfulspecies hold a key position <strong>in</strong> the <strong>food</strong> web by exploit-Fishery-PiscFishFishery-PlvFishTable 3. Bottom-up importance of each trophic group <strong>in</strong> thegeneric <strong>pelagic</strong> <strong>food</strong> web, calculated as the bottom-up componentof the keystone <strong>in</strong>dex (Jordán et al. 1999; cf. Fig. 2)JellyfishTrophic groupK bNH4, PO4, NO3 3.69Diat 3.17POM 2.69MesoZooPl 2.50FreeBac 1.69LDOM, SDOM 1.35LAutFl, µZooPl 1.17AutNanoFl, HetNanoFl 1.08Si 1.04InedAlg, Noctiluca 1.00PicoPl, POM-Bac 0.69PlvFish, BentFish 0.50Jellyfish, PiscFish, VirDiat, VirInedAlg, 0.00VirBac, VirNocNoctilucaIned-AlgNutrient load<strong>in</strong>gFig. 7. Diagram of relationships between harmful trophospecies<strong>and</strong> anthropogenic impacts. Solid arrows: positiveeffects; dashed arrows: negative effects; double-headed arrows:reciprocal relationship. Width of arrows is proportionalto the strength of the calculated trophic impacts

Vasas et al.: <strong>Eutrophication</strong> <strong>and</strong> <strong>overfish<strong>in</strong>g</strong> <strong>in</strong> <strong>food</strong> webs13<strong>in</strong>g the most important bottom-up controllers. Accord<strong>in</strong>gto our calculations, the trophic level at which <strong>overfish<strong>in</strong>g</strong>occurs is of crucial importance, as previouslysuggested by e.g. Pauly et al. (1998). The earlier<strong>overfish<strong>in</strong>g</strong> of PiscFish appears to susta<strong>in</strong> blooms ofdiatoms <strong>and</strong> other large algae that rema<strong>in</strong> ungrazed,while the present <strong>overfish<strong>in</strong>g</strong> of PlvFish supports HABspecies<strong>and</strong> jellies, act<strong>in</strong>g synergistically with nutrientenrichment.Calculations with modified versions of the webemployed <strong>in</strong> this study (without viruses, without harmfulgroups, version for the North Sea: V. Vasas et al.unpubl.) <strong>in</strong>dicate that the ma<strong>in</strong> conclusions <strong>and</strong> <strong>in</strong>teractionpathways are robust. Still, we emphasize thatthe results <strong>in</strong> this study are not meant as absolute numbers,but rather as characteristic constra<strong>in</strong>ts <strong>in</strong>herent tothe structure of the generic <strong>food</strong> web. The relativeimportance of these pathways may be quite different,depend<strong>in</strong>g on the environmental conditions of theecosystem, <strong>and</strong> the next step is a comparison of systemswith different structural properties. Moreover,the various roles of nutrients <strong>and</strong> the effects of unbalancednutrient enrichment could be exam<strong>in</strong>ed <strong>in</strong> thefuture, based on comparisons of the same web <strong>in</strong> termsof nitrogen, phosphorus <strong>and</strong> silica. Major changes toecosystem state often occur above certa<strong>in</strong> thresholds ofstress (Scheffer et al. 2001), <strong>and</strong> a search for the structuralcauses beh<strong>in</strong>d them is promis<strong>in</strong>g. Ecosystems thatshow threshold behavior are a great challenge to management,<strong>and</strong> the context described here will serve asa basis to study possible mechanisms of thresholds <strong>in</strong><strong>pelagic</strong> <strong>nearshore</strong> <strong>food</strong> webs.Acknowledgements. The authors thank 3 anonymous refereesfor constructive comments <strong>and</strong> suggestions. We aregrateful to W.C. Liu for technical help, T. Wyatt for commentson the manuscript, <strong>and</strong> K. Csepi for l<strong>in</strong>guistic help. This studyis a contribution to Stream 3 (Nutrient-driven thresholdsof environmental susta<strong>in</strong>ability) of the Integrated ProjectTHRESHOLDS (Thresholds of environmental susta<strong>in</strong>ability),funded by the European Commission (Global Change <strong>and</strong>Ecosystems) under contract 003933, <strong>and</strong> to the Belgianfederal policy project AMORE III. F.J. was supported bySociety <strong>in</strong> Science: The Branco Weiss Fellowship, ETH Zürich.LITERATURE CITEDArai MN (2001) Pelagic coelenterates <strong>and</strong> eutrophication: areview. Hydrobiologia 451:69–87Azam F, Cho BC (1987) Bacterial utilization of organic matter<strong>in</strong> the sea. In: Fletcher M, Gray TRG, Jones JG (eds)Ecology of microbial communities. Cambridge UniversityPress, Cambridge, p 261–281Azam F, Fenchel T, Field JG, Gray JS, Meyer-Reil LA,Th<strong>in</strong>gstad F (1983) The ecological role of water-columnmicrobes <strong>in</strong> the sea. Mar Ecol Prog Ser 10:257–263Bakun A, Broad K (2003) Environmental ‘loopholes’ <strong>and</strong>fish population dynamics: comparative pattern recognitionwith focus on El Niño effects <strong>in</strong> the Pacific. Fish Oceanogr12:458–473Becquevort S, Rousseau V, Lancelot C (1998) Major <strong>and</strong> comparableroles for free-liv<strong>in</strong>g <strong>and</strong> attached bacteria <strong>in</strong> thedegradation of Phaeocystis-derived organic matter <strong>in</strong>Belgian coastal waters of the North Sea. Aquat MicrobEcol 14:39–48Beltrami E, Carroll TO (1994) Model<strong>in</strong>g the role of viral disease<strong>in</strong> recurrent phytoplankton blooms. J Math Biol 32:857–863Billen G, Lancelot C, Meybeck M (1991) N, P <strong>and</strong> Si retentionalong the aquatic cont<strong>in</strong>uum from l<strong>and</strong> to ocean. In: MantouraRFC, Mart<strong>in</strong> JM, Wollast R (eds) Ocean marg<strong>in</strong>processes <strong>in</strong> global change, Dahlem Workshop Reports.Wiley, New York, p 19–44Buskey EJ (1995) Growth <strong>and</strong> biolum<strong>in</strong>escence of Noctilucasc<strong>in</strong>tillans on vary<strong>in</strong>g algal diets. J Plankton Res 17:29–40Brussaard CPD (2004) Viral control of phytoplankton populations—areview. J Eukaryot Microbiol 51:125–138Caron DA, Goldman JC (1990) Protozoan nutrient regeneration.In: Capriulo GM (ed) Ecology of mar<strong>in</strong>e protozoa.Oxford University Press, New York, p 283–306Cloern JE (2001) Our evolv<strong>in</strong>g conceptual model of thecoastal eutrophication problem. Mar Ecol Prog Ser 210:223–253Daskalov GM (2002) Overfish<strong>in</strong>g drives a trophic cascade <strong>in</strong>the Black Sea. Mar Ecol Prog Ser 225:53–63Daskalov GM (2003) Long-term changes <strong>in</strong> fish abundance<strong>and</strong> environmental <strong>in</strong>dices <strong>in</strong> the Black Sea. Mar EcolProg Ser 255:259–270Fernández JM, Selma MAE, Aymerich FR, Sáez MTP, FructuosoMFC (2005) Aquatic birds as bio<strong>in</strong>dicators of trophicchanges <strong>and</strong> ecosystem deterioration <strong>in</strong> the Mar Menorlagoon (SE Spa<strong>in</strong>). Hydrobiologia 550:221–235Fogg GE (1995) Some comments on picoplankton <strong>and</strong> its importance<strong>in</strong> the <strong>pelagic</strong> ecosystem. Aquat Microb Ecol 9:33–39Frangoulis C, Christou ED, Hecq JH (2005) Comparison ofmar<strong>in</strong>e copepod outfluxes: nature, rate, fate <strong>and</strong> role <strong>in</strong>the carbon <strong>and</strong> nitrogen cycles. Adv Mar Biol 47:253–309Fuhrman JA (1999) Mar<strong>in</strong>e viruses <strong>and</strong> their biogeochemical<strong>and</strong> ecological effects. Nature 399:541–548Fuhrman JA (2000) Impact of viruses on bacterial processes.In: Kirchman DL (ed) Microbial ecology of the oceans.Wiley, New York, p 327–350Glibert P, Pitcher G (eds) (2001) Global ecology <strong>and</strong> oceanographyof harmful algal blooms. GEOHAB Science Plan,SCOR & IOC, Baltimore/ParisGucu AC (2002) Can <strong>overfish<strong>in</strong>g</strong> be responsible for the succesfulestablishment of Mnemiopsis leidyi <strong>in</strong> the BlackSea? Estuar Coast Shelf Sci 54:439–451Hannon B (1973) The structure of ecosystems. J Theor Biol41:535–546Harary F (1961) Who eats whom? Gen Syst 6:41–44Harris RP, Irigoien X, Head RN, Rey C <strong>and</strong> 5 others (2000)Feed<strong>in</strong>g, growth <strong>and</strong> reproduction <strong>in</strong> the genus Calanus.ICES J Mar Sci 57:1708–1726Hart PJB, Reynolds JD (2002) H<strong>and</strong>book of fish biology <strong>and</strong>fisheries. Blackwell, OxfordHigashi M, Burns TP (eds) (1991) Theoretical studies ofecosystems—the network perspective. Cambridge UniversityPress, CambridgeHudson JJ, Taylor WD, Sch<strong>in</strong>dler DW (1999) Planktonic nutrientregeneration <strong>and</strong> cycl<strong>in</strong>g efficiency <strong>in</strong> <strong>temperate</strong>lakes. Nature 400:659–661Irigoien X, Flynn KJ, Harris P (2005) Phytoplankton blooms: a‘loophole’ <strong>in</strong> microzooplankton graz<strong>in</strong>g impact? J PlanktonRes 27:313–321

14Mar Ecol Prog Ser 336: 1–14, 2007Jordán F, Takács-Sánta A, Molnár I (1999) A reliability theoreticalquest for keystones. Oikos 86:453–462Jordán F, Wyatt T (2006) A graph theory exam<strong>in</strong>ation of theglobal spread<strong>in</strong>g hypothesis. Afr J Mar Sci 28:371–374Kiørboe T (2003) High turnover rates of copepod fecal pelletsdue to Noctiluca sc<strong>in</strong>tillans graz<strong>in</strong>g. Mar Ecol Prog Ser258:181–188Kiørboe T, Nielsen TG (1994) Regulation of zooplankton biomass<strong>and</strong> production <strong>in</strong> a <strong>temperate</strong>, coastal ecosystem. 1.Copepods. Limnol Oceonogr 39:493–507Kiørboe T, Titelman J (1998) Feed<strong>in</strong>g, prey selection <strong>and</strong> preyencounter mechanisms <strong>in</strong> the heterotrophic d<strong>in</strong>oflagellateNoctiluca sc<strong>in</strong>tillans. J Plankton Res 20:1615–1636Kirchman DL (2000) Uptake <strong>and</strong> regeneration of <strong>in</strong>organicnutrients by mar<strong>in</strong>e heterotrophic bacteria. In: KirchmanDL (ed) Microbial ecology of the oceans. Wiley, New York,p 261–288Lancelot C, Staneva J, Van Eeckhout D, Beckers JM, StanevE (2002) Modell<strong>in</strong>g the Danube-<strong>in</strong>fluenced north-westerncont<strong>in</strong>ental shelf of the Black Sea. II. Ecosystem responseto changes <strong>in</strong> nutrient delivery by the Danube River afterits damm<strong>in</strong>g <strong>in</strong> 1972. Estuar Coast Shelf Sci 54:473–499Leibold MA (1996) A graphical model of keystone predators<strong>in</strong> <strong>food</strong> webs: trophic regulation of abundance, <strong>in</strong>cidence,<strong>and</strong> diversity patterns <strong>in</strong> communities. Am Nat 147:784–812Margalef R (1991) Networks <strong>in</strong> ecology. In: Higashi M,Burns TP (eds) Theoretical studies of ecosystems—thenetwork perspective. Cambridge University Press, Cambridge,p 41–57Montani S, Pithakpol S, Tada K (1998) Nutrient regeneration<strong>in</strong> coastal seas by Noctiluca sc<strong>in</strong>tillans, a red tide-caus<strong>in</strong>gd<strong>in</strong>oflagellate. J Mar Biotechnol 6:224–228Nagata T (2000) Production mechanisms of dissolved organicmatter. In: Kirchman DL (ed) Microbial ecology of theoceans. Wiley, New York, p 128–160Okaichi T, Nishio S (1976) Identification of ammonia as thetoxic pr<strong>in</strong>ciple of red tide of Noctiluca miliaris. BullPlankton Soc Japan 23:25–30Pace ML, Cole JJ, Carpenter SR, Kitchell JF (1999) Trophiccascades revealed <strong>in</strong> diverse ecosystems. Trends Ecol Evol14:483–488Pauly D, Christensen V, Dalsgaard J, Froese R, Torres F Jr (1998)Fish<strong>in</strong>g down mar<strong>in</strong>e <strong>food</strong> webs. Science 279:860–863Power ME, Tilman D, Estes JA, Menge BA <strong>and</strong> 6 others (1996)Challenges <strong>in</strong> the quest for keystones. BioScience 46:609–620Purcell JE (1997) Pelagic cnidarians <strong>and</strong> ctenophores aspredators: selective predation, feed<strong>in</strong>g rates <strong>and</strong> effects onprey populations. Ann Inst Oceanogr Paris 73:125–137Rousseau V, Becquevort S, Parent JY, Gaspar<strong>in</strong>i S, Daro MH,Tackx M, Lancelot C (2000) Trophic efficiency of theplanktonic <strong>food</strong> web <strong>in</strong> a coastal ecosystem dom<strong>in</strong>ated byPhaeocystis colonies. J Sea Res 43:357–372Sarthou G, Timmermans KR, Bla<strong>in</strong> S, Tréguer P (2005)Growth physiology <strong>and</strong> fate of diatoms <strong>in</strong> the ocean: areview. J Sea Res 53:25–42Scheffer M, Carpenter S, Foley JA, Folke C, Walker B (2001)Catastrophic shifts <strong>in</strong> ecosystems. Nature 413:591–596Schneider G (1990) A comparison of carbon based ammoniaexcretion rates between gelat<strong>in</strong>ous <strong>and</strong> non-gelat<strong>in</strong>ousEditorial responsibility: Otto K<strong>in</strong>ne (Editor-<strong>in</strong>-Chief),Oldendorf/Luhe, Germanyzooplankton: implications <strong>and</strong> consequences. Mar Biol106:219 – 225Schoemann V, de Baar HJW, de Jong JTM, Lancelot C (1998)Effects of phytoplankton blooms on the cycl<strong>in</strong>g of manganese<strong>and</strong> iron <strong>in</strong> coastal waters. Limnol Oceanogr 43:1427–1441Schoemann V, Becquevort S, Stefels J, Rousseau V,Lancelot C (2005) Phaeocystis blooms <strong>in</strong> the globalocean <strong>and</strong> their controll<strong>in</strong>g mechanisms: a review. J SeaRes 53:43–66Sheldon RW, Prakash A, Sutcliffe Jr WH (1972) The sizedistribution of particles <strong>in</strong> the ocean. Limnol Oceanogr17:327–340Sherr EB, Sherr BF (2002) Significance of predation by protists<strong>in</strong> aquatic microbial <strong>food</strong> webs. Antonie Leeuwenhoek81:293–308Shiganova TA (1998) Invasion of the Black Sea by thectenophore Mnemiopsis leidyi <strong>and</strong> recent changes <strong>in</strong><strong>pelagic</strong> community structure. Fish Oceanogr 7:305–310Smith DC, Simon M, Alldredge AL, Azam F (1992) Intensehydrolytic enzyme activity on mar<strong>in</strong>e aggregates <strong>and</strong>implications for rapid particle dissolution. Nature 359:139–142Ste<strong>in</strong>er CF (2001) The effects of prey heterogeneity <strong>and</strong> consumeridentity on the limitation of trophic-level biomass.Ecology 82:2495–2506Stibor H, Vadste<strong>in</strong> O, Diehl S, Gelzleichter A <strong>and</strong> 10 others(2004) Copepods act as a switch between alternativetrophic cascades <strong>in</strong> mar<strong>in</strong>e <strong>pelagic</strong> <strong>food</strong> webs. Ecol Lett7:321–328Strom SL (2000) Bacterivory: <strong>in</strong>teractions between bacteria<strong>and</strong> their grazers. In: Kirchman DL (ed) Microbial ecologyof the oceans. Wiley, New York, p 351–386Strom SL (2002) Novel <strong>in</strong>teractions between phytoplankton<strong>and</strong> microzooplankton: their <strong>in</strong>fluence on the coupl<strong>in</strong>gbetween growth <strong>and</strong> graz<strong>in</strong>g rates <strong>in</strong> the sea. Hydrobiologia480:41–54Strom SL, Benner R, Ziegler S, Dagg MJ (1997) Planktonicgrazers are a potentially important source of mar<strong>in</strong>e dissolvedorganic carbon. Limnol Oceanogr 42:1364–1374Th<strong>in</strong>gstad TF, Heldal M, Bratbak G, Dundas I (1993) Areviruses important partners <strong>in</strong> <strong>pelagic</strong> <strong>food</strong> webs? TrendsEcol Evol 8:209–213Turner JT (2002) Zooplankton fecal pellets, mar<strong>in</strong>e snow <strong>and</strong>s<strong>in</strong>k<strong>in</strong>g phytoplankton blooms. Aquat Microb Ecol 27:57–102Turner JT, Roff JC (1993) Trophic levels <strong>and</strong> tropho-species <strong>in</strong>mar<strong>in</strong>e plankton: lessons from the microbial <strong>food</strong> web.Aquat Ecol 7:225–248Ulanowicz RE, Puccia CJ (1990) Mixed trophic impacts <strong>in</strong>ecosystems. Coenoses 5:7–16Vasas V, Jordán F (2006) Topological keystone species <strong>in</strong> ecological<strong>in</strong>teraction networks: consider<strong>in</strong>g l<strong>in</strong>k quality <strong>and</strong>non-trophic effects. Ecol Model 196:365–378Wilhelm SW, Suttle CA (1999) Viruses <strong>and</strong> nutrient cycles <strong>in</strong>the sea. BioScience 49:781–788Yılmaz IN, Okus E, Yüksek A (2005) Evidences for <strong>in</strong>fluenceof a heterotrophic d<strong>in</strong>oflagellate (Noctiluca sc<strong>in</strong>tillans) onzooplankton community structure <strong>in</strong> a highly stratifiedbas<strong>in</strong>. Estuar Coast Shelf Sci 64:475–485Submitted: July 21, 2006; Accepted: March 13, 2007Proofs received from author(s): April 18, 2007

Hooray! Your file is uploaded and ready to be published.

Saved successfully!

Ooh no, something went wrong!