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Above- and below-ground vertebrate herbivory may each favour a different subordinate species in an aquatic plant community

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Above- and below-ground vertebrate herbivory may each favour a different subordinate species in an aquatic plant community
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  Oecologia (2010) 162:199–208DOI 10.1007/s00442-009-1450-6  1 3 COMMUNITY ECOLOGY - ORIGINAL PAPER Above- and below-ground vertebrate herbivory may each favour a di V  erent subordinate species in an aquatic plant community Bert Hidding · Bart A. Nolet · Thijs de Boer · Peter P. de Vries · Marcel Klaassen Received: 9 November 2008 / Accepted: 11 August 2009 / Published online: 10 September 2009 ©  The Author(s) 2009. This article is published with open access at Springerlink.com Abstract At least two distinct trade-o V  s are thought tofacilitate higher diversity in productive plant communitiesunder herbivory. Higher investment in defence andenhanced colonization potential may both correlate withdecreased competitive ability in plants. Herbivory may thuspromote coexistence of plant species exhibiting divergentlife history strategies. How di V  erent seasonally tied herbi-vore assemblages simultaneously a V  ect plant communitycomposition and diversity is, however, largely unknown.Two contrasting types of herbivory can be distinguished inthe aquatic vegetation of the shallow lake Lauwersmeer. Insummer, predominantly above-ground tissues are eaten,whereas in winter, waterfowl forage on below-ground plantpropagules. In a 4-year exclosure study we experimentallyseparated above-ground herbivory by waterfowl and large W sh in summer from below-ground herbivory by Bewick’sswans in winter. We measured the individual and combinede V  ects of both herbivory periods on the composition of thethree-species aquatic plant community. Herbivory e V  ectsizes varied considerably from year to year. In 2years her-bivore exclusion in summer reinforced dominance of Pota-mogeton pectinatus  with a concomitant decrease in Potamogeton pusillus , whereas no strong, unequivocale V  ect was observed in the other 2years. Winter exclusion,on the other hand, had a negative e V  ect on  Zannichellia palustris , but the e V  ect size di V  ered considerably betweenyears. We suggest that the colonization ability of  Z. palus-tris  may have enabled this species to be more abundantafter reduction of P. pectinatus  tuber densities by swans.Evenness decreased due to herbivore exclusion in summer.We conclude that seasonally tied above- and below-groundherbivory may each stimulate di V  erent components of amacrophyte community as they each favoured a di V  erentsubordinate plant species. Keywords Aquatic macrophytes · Waterfowl · Tubers · Competition colonization trade-o V   · Bare patch formation Introduction The e V  ect of herbivores on plant community diversity canhave one of two outcomes. Generalist herbivores have beenassociated with decreased plant diversity in settings charac-terised by low productivity, where few species are tolerantor resistant to consumption (Ol V   and Ritchie 1998; Proulxand Mazumder 1998; Bakker etal. 2006). In contrast, her- bivory has been found to positively a V  ect diversity in pro-ductive grassland systems (Summerhayes 1941; Noy-Meiretal. 1989; Bakker etal. 2006), but also in disparate marine habitats such as the rocky intertidal (Lubchenco 1978). Herbivore-mediated increases in plant diversity havebeen explained in terms of two trade-o V  s. Firstly, a trade-o V   may exist between plant defence and competitive ability(Lubchenco 1978; Gleeson and Wilson 1986), allowing both defensive and more palatable competitive species tocoexist under herbivory. A second trade-o V   that may pro-mote diversity is a shift in the balance between colonizationand mortality (Ol V   and Ritchie 1998). This trade-o V   maycome into e V  ect when herbivory results in open patches.Anegative correlation between a plant’s ability to compete Communicated by Scott Collins.B. Hidding ( & ) · B. A. Nolet · T. de Boer · P. P. de Vries · M. KlaassenDepartment of Plant-Animal Interactions, Centre for Limnology, Netherlands Institute of Ecology, Rijksstraatweg 6, 3631 AC Nieuwersluis, The Netherlandse-mail: b.hidding@nioo.knaw.nl  200Oecologia (2010) 162:199–208  1 3 for resources and its capacity to colonize these openpatches may allow a great number of species to coexist(Tilman 1994).Few studies have addressed the formation of barepatches by herbivores explicitly; however, it seems thattheir formation depends, at least in part, on the identity of the herbivore (Ol V   and Ritchie 1998; Bakker etal. 2006). Ingrassland systems, rabbits (Bakker and Ol V   2003), prairiedogs (Coppock etal. 1983), picas (Bagchi etal. 2006) and bisons (Collins and Barber 1985) were all reported to pro-mote species diversity through the creation of bare patches.Collins and Barber (1985) also suspected additive diversitye V  ects of grazing and bare patch formation through bisonwallowing. For such animals however, grazing and wallow-ing are unavoidably entangled.Freshwater wetlands provide an excellent opportunity toinvestigate the separate e V  ects of bare patch formation andabove-ground grazing. Many of these systems in temperateclimates experience foraging on above-ground biomass bywaterfowl (Jupp and Spence 1977; Lauridsen etal. 1993; Søndergaard etal. 1996; Van Donk and Otte 1996) and W sh(Prejs 1984; Van Donk and Otte 1996) during the warmer months. In winter, however, after die-o V   of the above-ground plant parts, tubers and roots of aquatic plants areconsumed by migratory waterfowl (Anderson and Low1976; Beekman etal. 1991; Nolet etal. 2001; Sponberg and Lodge 2005). These birds, most notably swans and canvas-backs, may e V  ectively deplete entire patches, as propagulesand with them individual ramets are consumed. This resultsin a mosaic of patches varying widely in the density of tubers remaining (Klaassen and Nolet 2008). Conversely,summer grazing frequently results in stem breakage (Schut-ten etal. 2005), leaving individual plants damaged, butalive. These di V  erent modes of herbivory may each a V  ectthe suitability of species traits along di V  erent trade-o V  s,potentially resulting in additive e V  ects in terms of speciescomposition.To date, studies on the e V  ects of vertebrate herbivory oncommunity composition in aquatic systems have focusedon waterfowl herbivory on above-ground tissues. Thesestudies report a reduction in the seemingly most palatablemacrophyte species in control plots relative to exclosureplots, and no e V  ect or an increase in less-preferred speciesinside the exclosures (Van Donk and Otte 1996; Santamaria2002; Rodriguez-Villafane etal. 2007; Van de Haterd and Ter Heerdt 2007). In contrast, community compositione V  ects of below-ground herbivory in shallow lakes haveseldom been studied (but see LaMontagne etal. 2003), although remarkable and counterintuitive e V  ects of Bewick’s swans foraging on fennel pondweed ( Potamog-eton pectinatus ) tubers were found in Lake KrankesjöninSweden (Sandsten and Klaassen 2008). While the P.pectinatus  tubers were most eaten by swans, competingperfoliate pondweed ( Potamogeton perfoliatus ) was virtu-ally wiped out by the sediment disturbances caused by theswans. As a result, the relationship between Bewick’sswans and fennel pondweed represents a case of ecologicalmutualism (Sandsten and Klaassen 2008).The in X uence of below-ground herbivory by Bewick’sswans may be such that antagonistic coevolution has led toecological mutualism (De Mazancourt etal. 2001). On theother hand, as herbivory on below-ground propagulesresults in bare patches, good colonizers may pro W t at theexpense of dispersal-limited dominant resource competi-tors, resulting in an increase in plant diversity. In parallel,herbivory by waterfowl and W sh on above-ground tissues of aquatic macrophytes may compare to the positive diversitye V  ect of herbivores as observed in grasslands and rockyintertidal communities, i.e. to the disadvantage of the palat-able, productive species.In a 4-year exclosure study, we combined exclusion of above-ground herbivores in summer (ducks, coots, muteswans and large W sh) and below-ground foraging byBewick’s swans in winter in a full factorial design. Wethereby simultaneously considered the possible changesthat both above-ground and below-ground herbivory mayhave on the species composition and evenness of a macro-phyte community over multiple years. We considered theevenness component of diversity since changes in speciesnumber are trivial in this species-poor community. Wetested the following hypotheses: (1a) Bewick’s swansfacilitated growth of their food source fennel pondweed bydamaging and burying turions and seeds of competitors(ecological mutualism), or alternatively, (1b) foragingBewick’s swans promoted community evenness by allevi-ating interspeci W c competition through local removal of  P.pectinatus  tubers, which created opportunities for colo-nizers; (2) selective foraging of mute swans, coots andducks on the competitively dominant macrophyte speciesin summer facilitated subordinates and hence endorsedevenness. Materials and methods Experimental siteExclosure experiments were carried out in theBabbelaar, a branch of the shallow lake Lauwersmeer(The Netherlands), that is closed to the public (2,100ha,53°22  N, 06°13  E). The lake is eutrophic to hypertro-phic with a mean concentration of total N of 3.4mgl ¡ 1 and total P of 0.28mgl ¡ 1  (mean of monthly measure-ments made October 2003–October 2007 covering theexperimental period; data provided by the Noorderzijlvestwater board).  Oecologia (2010) 162:199–208201  1 3 The Lauwersmeer is a former bay of the Wadden Seathat has become a freshwater lake since its embankment in1969. The water level of the lake is strictly managed bymeans of sluice drainage to achieve the target level (-93cmrelative to the Amsterdam ordnance datum). From the early1970s onwards the lake was gradually colonised by fennelpondweed ( Potamogeton pectinatus  L.). At the time thereported study started, fennel pondweed could be foundalong the whole Lauwersmeer shoreline. In the Babbelaar, P. pectinatus  dominates, yet it is likely to be more dispersallimited than the two other submersed macrophyte speciesthat were present, as it propagates mostly by means of sub-terranean tubers positioned at relatively short distancesfrom the maternal plant. Lesser pondweed ( Potamogeton pusillus  L.), propagates mostly through turions formedabove ground (Barrat-Segretain and Bornette 2000),whereas horned pondweed (  Zannichellia palustris  L.)reproduces mainly through seeds (Van Vierssen 1982).Since the mid 1970s, high numbers of Bewick’s swansannually visit the lake on their autumn migration (Prop andvan Eerden 1981). The birds usually arrive in the Lauwers-meer area in October and forage on the tubers of fennelpondweed (Beekman etal. 1991; Nolet etal. 2001). The total time spent on tuber foraging in the Lauwersmeer istypically short, and numbers quickly drop after 2–4weeksof massive swan presence as a W xed giving-up density of pondweed tubers is attained (Nolet etal. 2006). In the autumns (2003–2006) preceding above-ground sampling insummer, 4,000, 5,500, 2,800 and 1,200 swan-days (=thesum of daily swan counts) were recorded in the Babbelaar,respectively (Nolet etal. 2006, A.Gyimesi and B.A.Nolet, unpublished data).In summer, the macrophyte beds in the Lauwersmeerare exploited mainly by coot ( Fulica atra  L.), mallard(  Anas platyrhynchos  L.), gadwall (  Anas strepera  L.), com-mon teal (  Anas crecca  L.) and mute swan ( Cygnus olor  Gmelin). In summer, birds were counted on a monthlybasis covering the whole Lauwersmeer [data from the Sta-atsbosbeheer (state forestry service)]. Bird numbersincreased from May to August in a similar way in eachyear of the study. Numbers steadily increased from around1,200 coots and ducks in May numbers to § 17,000 inAugust (Fig.1). Mute swan numbers were more stableover these months, X uctuating between 400 and 1,100individuals. Fish community data had been collected in2000 (Kroes and Riemersma 2001). Bream (  Abramisbrama  L.) was the most abundant W sh in biomass but thisspecies is not herbivorous. Roach (  Rutilus rutilus  L.) andcarp [ Cyprinus carpio  (L.)] were the most abundant facul-tative herbivores. The density of roach was estimated at22kgha ¡ 1 . Carp was estimated at 58kgha ¡ 1  while rudd[ Scardinius erythrophthalmus  (L.)] density was low at1.5kgha ¡ 1  (Kroes and Riemersma 2001).Experimental designIn early October 2003, prior to the arrival of Bewick’sswans, eight 12 £ 12-m exclosure blocks were establishedin the Babbelaar (Fig.2). Exclosure blocks were dividedinto four 6 £ 6-m plots, each receiving one of four treat-ments: a summer exclosure preventing the consumption of above-ground parts by birds (s), a winter exclosure prevent-ing tuber-digging waterfowl from disrupting the sediment(w), a year-round exclosure, which was a combination of both treatments (s+w), and a control plot (c), which wasopen year round (Fig.2). Treatments were randomlyassigned to the four plots within a block. For the summertreatment a 6 £ 6-m cage was made, constructed of wooden poles and mesh wire (mesh size 5cm). The cageswere topped with bird netting. Each year, the cages wereerected in March and removed at the end of September. Ascages in winter would possibly be vulnerable to forcesexerted by ice, the winter treatment instead consisted of mesh wire placed on the sediment surface. The mesh wirewas kept in place with short bamboo sticks from late Sep-tember until March. We established two sets of four blocks, Fig.1 Number of birds observed each month over the summer on theLauwersmeer, the Netherlands: a  ducks and coots, b  mute swans( Cygnus olor   Gmelin). Ducks and coots include coots ( Fulica atra  L.),gadwalls (  Anas strepera  L.), mallards (  Anas platyrhynchos  L.), andcommon teal (  Anas crecca  L.). Data for swans are reported separatelybecause they are more than an order of magnitude heavier than ducksand coots. Note  scales  are di V  erent on  y-axes 05000100001500020000050010001500 2004200520062007 (a)(b) Ducks and cootsMute swans May June July August Bird countBird count  202Oecologia (2010) 162:199–208  1 3 which were 180m apart. Within each set of blocks the dis-tance between the centres of the blocks was 40m. A slightgradient in water depth existed with decreasing water depthfrom block 1 (62 § 2cm SD relative to target level) toblock 8 (35 § 2cm SD; Hidding etal. 2009).SamplingAll sampling was done inside an area of 4.5 £ 4.5m withinthe 6 £ 6-m treatment plots in order to minimize edgee V  ects. This area in turn was divided into 36 squares of 75 £ 75cm. Above-ground material to be sorted to specieslevel was sampled in mid June and 5weeks later, in midJuly. On each of these occasions one of the 36 squares wassampled. Assignment of sampling squares to samplingoccasions was done at random, with the restriction thateach sampling square was visited only once. Material wassampled by placing a 50-cm-diameter core over the vegeta-tion. Plants were then harvested by hand at the sedimentsurface and sorted to species level in the laboratory. Thesamples were dried at 60°C for 72h and subsequentlyweighed. The density of fennel pondweed tubers wasassessed both at the end of September and in March by col-lecting twelve 7-cm-diameter, 35-cm-deep cores of sedi-ment, more or less evenly spaced inside each treatmentplot. The cores were sieved in the W eld at mesh size 3mm.Tubers were pooled for each plot, dried, and weighed.Statistical analysisThe e V  ect of exclosure treatments and covariates on speciesabove-ground biomass, species proportions and evennesswas assessed in a linear mixed e V  ect model using the nlmepackage in R (Pinheiro and Bates 2000). Biomass data werenormalised using a cube-root transformation, whereas spe-cies proportions were arcsine transformed. Evenness wasestimated using the (untransformed) Shannon evennessindex [  H    /ln( S  ); Shannon and Weaver 1963; Pielou 1966]. In the experimental design, winter treatment, summer treat-ment and year were W xed factors. The factor month of sam-pling was nested within year. This was done since samplingdates among years may correspond to di V  erent stages in theplant’s phenology, making months unique representativesof a given year. Secondly, months represent repetitive mea-surements at a di V  erent scale than years. Block was a ran-dom factor within which summer exclusion, winterexclusion and year were crossed. As the two covariatesblock depth and sediment silt content were not independent(simple regression F  1, 30 =7.95, P <0.01) with sandier sed-iment in the shallower blocks, a composite abiotic parame-ter was calculated using a reduced major axis regression.Three di V  erent models were constructed containing thethree di V  erent covariates and their interactions with the W xed categorical factors. The covariates were either waterdepth, sediment silt content or a composite abiotic variable.The log-likelihood of the di V  erent models was calculatedunder W xed  df   and the model with the highest log-likelihoodwas chosen for further analysis, in e V  ect including a singlecovariate. The number of relevant interactions was esti-mated by W tting the data with a full model, one with three-way interactions, a model with two-way interactions and amodel without interactions using maximum likelihood(ML) estimation. A likelihood ratio test at  =0.05 wasused to decide whether including higher interaction levelsreturned a better W t, as is appropriate for hierarchicallynested models (Hilborn and Mangel 1997). ANOVAs were then applied to the selected model including block as ran-dom factor using a restricted ML estimation method. Afterdetermination of the interaction levels the signi W cance of the random factor block was determined using a likelihoodratio test comparing the W t of the models with block asrandom factor and models without the variable block. Thesigni W cance threshold (  ) was Bonferroni adjusted for the F  -tests by dividing 0.05 by 3, the number of species simul-taneously studied (new  =0.017). Results Model selection yielded the best W t for models includingwater depth as covariate rather than sediment silt content ora composite abiotic parameter. This was true for allresponse variables. Also, in all cases only two-way interac-tions were signi W cant according to likelihood ratio tests oninteraction levels. The predictor variable year was alwayshighly signi W cant (Table1) indicating variability amongyears for above-ground plant biomass of the three consid-ered species (Fig.3). In addition, the three plant speciesresponded di V  erently within years resulting in variable pro-portional di V  erences between species (Fig.4). However, Fig.2 Diagram of the experimental treatment layout established inthe Lauwersmeer. The two treatments indicated by  shading  were sep-arated in time, and treatment plots were randomly assigned withinblocks. The summer treatment ( light grey ) ran from March until Sep-tember and the winter treatment ( dark grey ) from September untilMarch. c  Control plot, s  summer exclosure, w  winter exclosure, s+w year-round exclosure 6 m1.5 m12 m12 mSWC S + W   O e  c  ol   o gi   a  (  2  0 1  0  )  1  6 2  : 1  9  9 –2  0  8 2  0  3   1  3 Table1 Mixed e V  ect linear model results for biomass and proportion of species plus the Shannon evenness index (  E   )Main e V  ects and two-way interactions are included. Signi W cance of the random variable plot was assessed through elimination and comparison of the goodness of W t using a likelihood ratio (  LR )test. Signi W cant e V  ects are indicated in  bold d.w.  Dry weightlme modelBlock (random)SummerWinterYearWater depthSummer £ WinterSummer £ YearSummer £ DepthWinter £ YearWinter £ DepthYear £ DepthMonth/Year  df  1 df  1,2261,2263,2261,2261,2263,2261,2263,2261,2263,2264,226 Potamogeton pectinatus  d.w.LR<0.001 F  412.8333.06110.1292.4061.3586.8890.0061.1220.0182.86716.197 3 q d.w. (g) P >0.999 P <0.001 0.082 <0.001 0.1220.245 <0.001 0.9380.3410.8940.037 <0.001 P. pectinatus  %LR0.162 F  36.9554.87722.5718.2580.9489.3305.3961.0830.8064.8401.899Arcsine q (fraction) P 0.688 P <0.001 0.028 <0.0010.004 0.331 <0.001 0.0210.3570.370 0.003 0.112 Potamogeton pusillus  d.w.LR0.094 F  35.2244.20816.3038.3055.6935.76832.0710.3390.4358.61935.971 3 q d.w. (g) P 0.759 P <0.001 0.041 <0.0010.004 0.018 0.001<0.001 0.7970.510 <0.001<0.001 P. pusillus  %LR0.001 F  31.3543.02521.6366.2852.0337.8576.3621.1760.5096.1103.258Arcsine q (fraction) P 0.975 P <0.001 0.083 <0.0010.013 0.155 <0.0010.012 0.3200.477 <0.0010.013  Zannichellia palustris  d.w..LR<0.001 F  0.22416.74633.68148.1802.3175.03417.0361.7491.1030.6345.984 3 q d.w. (g) P >0.999 P 0.637 <0.001<0.001<0.001 0.129 0.002<0.001 0.1580.2950.594 <0.001  Z. palustris  %LR<0.001 F  26.4517.1738.50729.9620.3834.4140.0230.6800.5512.5145.170Arcsine q (fraction) P >0.999 P <0.0010.008<0.001<0.001 0.536 0.005 0.8800.5650.4590.059 0.001 EvennessLR<0.001 F  22.9550.2525.04113.7182.2813.4056.2650.5750.3832.7883.715  E   P >0.999 P <0.001 0.617 0.002<0.001 0.1320.019 0.013 0.6320.5370.042 0.006
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