Freshwater Biology (2014) 59, 2009–2023
doi:10.1111/fwb.12403
Environmentally-mediated consumer control of algal proliferation in Florida springs DINA M. LIEBOWITZ*, MATTHEW J. COHEN†, JAMES B. HEFFERNAN‡, LAWRENCE V. KORHNAK† AND THOMAS K. FRAZER* *School of Natural Resources and Environment, University of Florida, Gainesville, FL, U.S.A. † School of Forest Resources and Conservation, University of Florida, Gainesville, FL, U.S.A. ‡ Nicholas School of the Environment, Duke University, Durham, NC, U.S.A.
SUMMARY 1. Reduced grazing can lead to increases in autotroph biomass and changes in taxonomic composition similar to those associated with nutrient enrichment. In Florida’s iconic spring ecosystems, algal proliferation has become widespread, yet the causes remain unclear. 2. We tested three linked hypotheses: (i) loss of top-down grazer control explains algae proliferation, a change often attributed to nitrate enrichment; (ii) grazer control is mediated by dissolved oxygen (DO) concentration; and (iii) an algal-dominated state may persist if biomass exceeds a critical level beyond which grazers can no longer constrain accumulation. 3. We tested these hypotheses using hierarchically nested benthic surveys of algal, vascular plant and gastropod biomasses along with physicochemical measurements in eleven springs spanning gradients in nitrogen enrichment, algal cover and DO. 4. We observed a significant and temporally consistent negative association between algal and gastropod biomasses (R2 = 0.38), with gastropods displaying the strongest explanatory power in multivariate prediction models that explained 45% of algal variation in the best fitted model. 5. A modest but significant positive bivariate association was observed between gastropod biomass and DO (R2 = 0.23); a multivariate model including temperature, velocity, canopy cover, submerged aquatic vegetation and conductivity explained 56% of gastropod variation. 6. Residuals from a linear relationship between gastropod and algal biomasses were strongly bimodal above a threshold grazer biomass of 20 g dry weight m 2 (c. 235 snails m 2) suggesting alternative states of high and low algal abundance. 7. These observations support the hypothesis that gastropods have the potential to control benthic algae in Florida’s springs, identify DO as a partial explanation for variation in grazer abundance and imply potentially important hysteretic behaviour in top-down algal control. Keywords: algae blooms, Elimia spp., hypoxia, hysteresis, top-down control
Introduction Broad-scale shifts in aquatic autotroph composition and abundance, particularly the proliferation of nuisance algae, are increasingly common and often result in substantial ecological and economic damage. The attempts to understand the causes of these changes have focused attention on a large and well-studied suite of potential drivers, including changes in nutrient concentration and stoichiometry (Dodds, 2006; Elser et al., 2007; Hillebrand et al., 2007), consumer biomass (Carpenter et al., 1995;
Hillebrand, 2009; Poore et al., 2012), light availability (Odum, 1956; Hillebrand, 2005), water velocity and hydrology (Hoyer, Frazer & Notestein, 2004; Riseng, Wiley & Stevenson, 2004) and their myriad interactions. Nutrient enrichment generally receives the majority of management attention, as this stressor is frequently identified as the most amenable to intervention. However, changes in autotrophic assemblages can be multicausal (Hillebrand, 2002; Gruner et al., 2008), and aquatic herbivores have been shown to exert comparable, or even dominant, control on autotroph biomass,
Correspondence: Dina M. Liebowitz, 217 Eucalyptus Avenue, Santa Cruz, CA 95060, U.S.A. E-mail:
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and they can strongly influence the structure and function of aquatic ecosystems (Heck & Valentine, 2007; Gruner et al., 2008; Baum & Worm, 2009; Estes et al., 2011). The impacts of herbivore grazing depend on a variety of factors, from grazer abundance and health, to autotroph growth rates and palatability. Models of both press and pulse disturbances suggest that declines in herbivore populations can induce a switch from a low algae system to a resilient algal-dominated system if high algal biomass or older algal growth forms become sufficiently resistant to grazing (Scheffer et al., 2008). Empirical studies support this mechanism, indicating that as algae accumulate, unpalatable algal growth forms or species can limit grazer control, so that even if grazer densities increase, they can no longer decrease algal density (Gliwicz, 1990; van de Koppel et al., 1996; Gragnani, Scheffer & Rinaldi, 1999; Van Alstyne et al., 1999; Lotze & Worm, 2000). This can lead to hysteretic behaviour, in which a system does not return to its original state at the same rate in which it changed, even if the original conditions are restored, through the development of alternative algal states in response to positive feedbacks (van de Koppel et al., 2001; Scheffer & Carpenter, 2003). The implication is that over some range of conditions, a response variable (in this case algal density) can occupy two configurations at the same level of a control variable (grazer density), resulting in bimodal distributions of observed values, or of their residuals after accounting for other factors (van de Koppel et al., 2001). However, if algae do not become unpalatable or inaccessible, algal biomass can be reduced by additional grazer growth or consumption rates (Lamberti et al., 1987; Suding & Hobbs, 2009). Identifying the role of grazers in controlling algae, and differentiating hysteretic behaviour in algal biomass from nonlinear but monotonic behaviour, has important restoration implications. Aquatic grazers are suffering severe declines and extinctions worldwide, due to a broad suite of stressors including hydrological modification, habitat loss, declining water quality and quantity, invasive species and potential interactions (Brown, Lang & Perez, 2008a; Lysne et al., 2008). Low dissolved oxygen (DO) is a particularly serious and widespread environmental stressor that can cause mortality directly through suffocation or indirectly through reduced feeding rates and resulting starvation, reduced fecundity and behavioural changes that increase predation vulnerability (Diaz, 2001; Wu, 2002; Cheung et al., 2008). The combined effects of grazer sensitivity to low DO and the presence of algal escape densities may allow low-DO conditions to have cascading effects on algal biomass that may persist, even
after grazer populations and DO conditions have recovered (Scheffer et al., 2008). Examining the role of environmental factors such as DO on grazers, and the potential loss of grazer control of nuisance algal blooms, helps us both to explore the potential for alternative stable states in systems where those patterns have previously not been considered, as well as to broaden management attention and considerations for ecosystem restoration. North Florida has the highest density of large freshwater springs in the world (Scott et al., 2004); they provide significant economic value to the state (Bonn, 2004) and represent important sites for studying ecosystem energetics and trophic dynamics (e.g. Odum, 1956, 1957). However, widespread nuisance filamentous algal blooms and the decline of submerged aquatic vegetation (SAV) have impacted habitat quality, human health and aesthetics. Increases in nitrate (NO3 ) concentration have been widely implicated as the causal agent, and management attention has overwhelmingly focused on nutrient reduction and related remediation (Stevenson, Pinowska & Wang, 2004; Brown et al., 2008b), yet several lines of evidence suggest that loss of top-down control also merits consideration (Heffernan et al., 2010). Consumer regulation of algae in these systems has only recently been explored (Dormsjo, 2008; Liebowitz, 2013), and no systematic investigations of top-down controls have been undertaken. Low concentration of dissolved oxygen (DO) is one of many stressors that can affect springs, but the effect of increasing incidence of hypoxia in Florida’s springs (Heffernan et al., 2010) on Florida’s freshwater gastropods is poorly understood (Hanley & Ultsch, 1999). Recently, Dormsjo (2008) and Liebowitz (2013) found high Elimia spp. mortality and potential sublethal effects under hypoxic conditions in both field and laboratory studies. Although gastropod densities are poorly characterised in Florida’s springs, pleurocerids can reach ‘extraordinary levels’ (Walsh, 2001), up to 579 g m 2 damp weight (DuToit, 1979), suggesting a potentially strong role in controlling algal biomass. Pleurocerids are heavy-shelled snails with low dispersal rates (Brown et al., 2008a) that limit repopulation, which suggests potentially persistent effects of even transient hypoxia and provides a plausible example of how these spring ecosystems could develop hysteretic patterns. We therefore used the Florida springs as systems to investigate how environmental variation, especially in DO, can mediate consumer control of algal proliferation. We posed three hypotheses about algal accumulation in spring ecosystems. First, we hypothesised that gastropod © 2014 John Wiley & Sons Ltd, Freshwater Biology, 59, 2009–2023
Consumer control of algae in Florida springs grazing has the potential to control algal accumulation in Florida’s springs. Second, we hypothesised that dissolved oxygen influences grazer abundance, and third, that feedbacks between algal accumulation and grazing can create stable high and low algal states. These hypotheses led to three linked predictions: (i) gastropod and algal biomasses are negatively associated; (ii) DO concentrations and gastropod densities are positively associated; and (iii) above a gastropod density threshold, alternative states cause algal biomass to be bimodal (either high or low); below this threshold, algal biomass will be uniformly high.
Methods Study site selection We used existing data on biological, chemical and physical attributes of Florida springs (Scott et al., 2004; Stevenson et al., 2004) to create three binary groupings: (i) high versus low nitrate concentration (breakpoint at 0.35 mg L 1, corresponding to recently adopted numeric nutrient criterion; Obreza et al., 2011); (ii) high versus low DO concentration at the vent (source) of the spring (using a 2 mg L 1 hypoxia threshold; Diaz, 2001); and (iii) high versus low algal abundance with a breakpoint at 50% cover following Stevenson et al. (2004) for most springs (or qualitative high versus low following Scott et al. (2004) if quantitative data were lacking). One spring was selected from each of the resulting 8 groups (Table 1), after further screening sites based on spring run length >200 m before confluence with another water body (to allow examination of within-system longitudinal DO variation) and excluding springs with tidal or salinity influences. In addition, we obtained measurements in three springs from the Ichetucknee complex to further populate the sample of low-DO systems. At each location, we measured physical, chemical and biotic variables (e.g. flow velocity, pH, macrophyte abundance) as potential predictors of herbivore and algal abundance. Nitrate and DO associations with algae are interpreted with caution because the sampling design intentionally crossed these with algal abundance.
Field sampling design and protocols We employed a hierarchical sampling design to document variation among and within springs, and along longitudinal gradients in DO and nitrate concentration. Surveys were conducted in each of the eleven springs during three separate time periods to allow detection of © 2014 John Wiley & Sons Ltd, Freshwater Biology, 59, 2009–2023
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temporal effects; sampling rotation one was conducted from 15 December 2008 to 27 February 2009; sampling rotation two was from 27 March to 3 August 2009; and sampling rotation three was from 13 August to 9 November 2009. At each spring, we selected three ‘sites’: Site 1 was at the spring vent; Site 2 was 100 m downstream; and the location of Site 3 depended on the DO profiles. In high-DO springs, Site 3 was 200 m downstream from the vent. In low-DO springs, Site 3 was sufficiently downstream to ensure enough distance for reaeration, so that DO levels exceeded 2 mg L 1 even at the trough of diel variation (see Heffernan & Cohen, 2010). This was measured using a multiparameter sonde (YSI 6920, Yellow Springs Instruments, Yellow Springs, OH, U.S.A.) taking hourly measurements over a 4- to 6day period prior to the selection of the sites. At each site, we established two line transects spanning from bank to bank perpendicular to the river (transects were parallel to each other and 10 m apart), with three sampling points evenly spaced along each line transect, giving a total of six sampling points per site. At each point, we used a 0.25 m2 quadrat to estimate benthic cover of filamentous algae and submerged aquatic vegetation (SAV), using a 5-step Braun–Blanquet scale (Braun-Blanquet, 1932) (1 = 0–5%, 2 = 6–25%, 3 = 26– 50%, 4 = 51–75%, 5 = 76–100%). We estimated light penetration through the canopy using a densiometer (Lemmon, 1956; calibrated so higher values indicate more light), surface flow velocity using the float method (Hauer & Lamberti, 2006), and DO, water temperature, specific conductance and pH using a multiparameter sonde. At each site, we also collected a 500-mL water sample into an acid-washed polyethylene bottle that was acidified to pH 2.0 using hydrochloric acid and stored below 4 °C until analysis. Water samples were filtered using a 0.45-lm glass fibre filter and analysed within 28 days for nitrate (EPA method 353.2) and orthophosphate (EPA method 365.1). We sampled vegetation and large invertebrates at each sampling point using a Hess-type invertebrate sampler with a circular footprint of 0.086 m2. The sampler was modified with a larger mesh size (c. 1 mm) to facilitate sampling in flocculent and diverse substrates, and a mesh cap over the top of the sampler to keep animals from escaping in deeper water. After inserting the sampler 1–2 cm into the sediment to create a seal, vegetation was clipped at the sediment–water interface and guided into the mesh bag attached to the downstream side of the sampler. The sediment was subsequently agitated to collect remaining invertebrates and algae, a process considered complete when three consecutive sweeps with a
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Table 1 Categorisation of 32 previously studied springs into eight groups, through crossing binary divisions of high versus low NO3 , dissolved oxygen (DO), and Algae% cover (measured at the spring vent in autumn 2003; Stevenson et al., 2004). The ‘# Springs’ columns show how many of the 32 springs fall within each category. One spring from each category was selected, and its attributes are described under the ‘Sampled spring’ column. Three additional low DO springs were sampled
High N (>0.35 mg L 1)
Low N (50% cover)
Low algae (2 mg L 1)
6
Blue Hole (BH) NO3 = 0.66 mg L 1 DO = 2.1 mg L 1 Algae% Cover = 87
6
Gilchrist Blue (GB) NO3 = 1.7 mg L 1 DO = 4.0 mg L 1 Qualitative low
Low DO (2 mg L 1)
3
Fern Hammock (FH) NO3 = 0.12 mg L 1 DO = 6.0 mg L 1 Algae% Cover = 54
5
Cypress (CP) NO3 = 0.3 mg L 1 DO = 5.2 mg L 1 Algae% Cover = 0
Low DO (
