Abstract
Nutrient enrichment is a major threat to subtidal macroalgal forests. Several studies have shown that nutrient inputs can enhance the ability of opportunistic algal species to acquire space freed by disturbance, at the expense of architecturally complex species that form forests. However, competition between canopy- and turf-forming macroalgae is not limited to the aftermath of disturbance. Canopy-forming macroalgae can provide suitable substratum for diverse epibiont assemblages, including both algae (epiphytes) and sessile invertebrates (epizoans). Despite evidence of enhanced epiphyte loading under eutrophic conditions, few experimental studies have assessed how nutrient enrichment influences the structure of epibiont assemblages on canopy-forming macroalgae at the edge versus inside forests. In oligotrophic waters of the NW Mediterranean, we experimentally tested the hypothesis that nutrient-driven proliferation of opportunistic epiphytic algae would affect the performance of the fucoid, Carpodesmia brachycarpa, and reduce the richness and abundance of the epizoan species they support. We predicted negative effects of nutrient enrichment to be greater at the edge than inside forests and on thalli that had recovered in cleared areas than on those within undisturbed canopy stands. Nutrient enrichment did not affect the photosynthetic efficiency and reproductive output of C. brachycarpa. By contrast, it enhanced herbivore consumption and decreased the cover and diversity of epizoans at forest edges, likely by stimulating the foraging activity of Arbacia lixula, the most abundant sea urchin in adjacent encrusting coralline barrens. Fertilization of areas inside forests had no effect on either C. brachycarpa or epibiont assemblages. Finally, nutrient enrichment effects did not vary between cleared and undisturbed areas. Our results show that moderate nutrient enrichment of oligotrophic waters does not necessarily cause the proliferation of epiphytes and, hence, a strengthening of their competitive effects on canopy-forming macroalgae. Nevertheless, enhanced herbivory damage to fertilized thalli at forest edges suggests that fragmentation could reduce the resilience of macroalgal forests and associated epibiont assemblages to nutrient enrichment.
Similar content being viewed by others
Avoid common mistakes on your manuscript.
Introduction
Coastal environments are under siege from human stressors (Halpern et al. 2008; Hoegh-Guldberg and Bruno 2010). Loss of foundation species (i.e. species that form or modify habitat) is of particular concern due to their key role in sustaining biodiversity and ecosystem functioning (Angelini et al. 2011; O’Leary et al. 2017; Gribben et al. 2019). Along temperate coasts worldwide, brown canopy-forming macroalgae, either Fucoids or Laminariales, are being progressively replaced by less complex, turf-forming species, impairing the functioning of shallow rocky reefs (Kautsky et al. 1986; Vogt and Schramm 1991; Bulleri and Benedetti-Cecchi 2006; Airoldi and Beck 2007; Gorman et al. 2009; Crowe et al. 2013; Strain et al. 2014; Krumhansl et al. 2016; Filbee-Dexter and Wernberg 2018).
Although there is substantial consensus over this state transition to be the result of cumulative effects of regional and global stressors (Estes and Palmisano 1974; Benedetti-Cecchi et al. 2001; Gorgula and Connell 2004; Airoldi and Beck 2007; Gorman et al. 2009; Smale and Wernberg 2013; Verges et al. 2014; Alestra and Schiel 2015; Ling et al. 2015; Wernberg et al. 2016; Bulleri et al. 2017), enhanced nutrient loading has been long identified among the primary drivers of macroalgal forest loss (Ballesteros et al. 1998; Benedetti-Cecchi et al. 2001; Gorgula and Connell 2004; Mangialajo et al. 2008; Gorman et al. 2009). Nonetheless, most of the evidence for nutrient-driven decline of macroalgal forests has been generated from eutrophic basins (e.g. the Skagerrak: Moy and Christie 2012; the Baltic Sea: Kautsky et al. 1986; Vogt and Schramm 1991; Havelange et al. 1997; Bergström et al. 2003; da Gama et al. 2008; the Adriatic Sea: Iveša et al. 2016; Strain et al. 2015), agricultural or urban catchments (Coleman et al. 2008; Mangialajo et al. 2008; Gorman et al. 2009) and, hence, it is not representative of temperate coasts characterized by lower nutrient status (Menge et al. 1999; Bulleri et al. 2012; Clausing et al. 2020).
In non-eutrophic basins, there is limited evidence for direct negative effects of moderate nutrient enrichment on canopy-forming macroalgae (Creed et al. 1997; Bokn et al. 2003; Steen and Rueness 2004; Steen and Scrosati 2004; Alestra and Schiel 2015; Chu et al. 2019; Tamburello et al. 2019). Brown macroalgae can, in fact, face seasonal nutrient limitation and benefit from nutrient inputs, especially when occurring as pulses (Schaffelke and Klumpp 1998) (Fig. 1). Increased nutritional value of plant tissue (i.e. lower C/N ratio) under elevated nutrient levels can stimulate canopy consumption by herbivores (Fig. 1) and, indeed, alter their behavior and foster their growth and reproduction (Hemmi and Jormalainen 2002, 2004; Kraufvelin et al. 2006; Valentine and Duffy 2006; Balata et al. 2010; Ghedini et al. 2015; Tuya et al. 2015; Ravaglioli et al. 2018). On the other hand, use of internal N stores, along with efficient external uptake, can provide a competitive advantage to complex macroalgae, such as Laminariales and Fucales, over ephemeral algal species (Pedersen and Borum 1997; Falkenberg et al. 2013; Kriegisch et al. 2019; Tamburello et al. 2019).
Several experimental studies have assessed the effects of nutrient enrichment on the ability of canopy-forming versus opportunistic species (either turfs or non-natives) to acquire space in the aftermath of disturbance (Gorgula and Connell 2004; Kraufvelin et al. 2010; Bulleri et al. 2012; Alestra and Schiel 2014; Carnell and Keough 2014; Piazzi and Ceccherelli 2017; Tamburello et al. 2019). By contrast, few studies (Russell et al. 2005; Werner et al. 2016) have experimentally investigated the effects of elevated nutrient levels on the interaction between canopy-formers and epibionts and these have exclusively focused on established canopy stands made of adult thalli. Thus, we know little of the structure of epibiont assemblages on canopy-forming macroalgae that have recruited and grown in disturbed areas, under enriched conditions.
In addition, most studies have focused on epiphytes, despite macroalgal canopies provide suitable substrata also for diverse assemblages of sessile invertebrates (Thornber et al. 2016; Teagle et al. 2017). As shown for epiphytes (D’Antonio 1985; Buschmann and Gómez 1993; Saier and Chapman 2004; Wahl 2008; Thornber et al. 2016), some epizoans, such as encrusting bryozoans, tunicates and sponges, can damage their macroalgal host by reducing light harvesting, nutrient uptake and reproductive output or promoting blade breakage from hydrodynamic forces (Dixon et al. 1981; Wong and Vercaemer 2012; Andersen et al. 2019). However, the effects of epibionts can be also positive. For instance, both epiphytes and epizoans can reduce host consumption by herbivores (Karez et al. 2000; Loffler et al. 2015). Sessile and mobile invertebrates can further sustain host growth through the provision of N-rich catabolites (Hepburn and Hurd 2005; Bracken et al. 2007; Hepburn et al. 2012; Peters et al. 2019). Thus, the net outcome of epibiosis is likely the result of a trade-off between negative and positive interactions (Thornber et al. 2016). Nutrient enrichment can alter such trade-offs by fostering the proliferation of opportunistic algae (e.g. the filamentous), at the expense of more complex algal forms (i.e. the foliose and corticated) and epizoans (Fig. 1).
Finally, the effects of nutrient enrichment on canopy-former epibionts can also vary according to the spatial configuration of canopy stands and, more specifically, among individuals at the edge versus inside forests (Fig. 1). Key features of both habitat-forming macrophytes (i.e. biomass, density, growth) and associated assemblages (diversity and relative abundances) can differ between forest edge and interior. In addition, thalli and epibiont assemblages at forest edges are exposed to different biotic (e.g. recruitment, grazing, predation) and abiotic (e.g. light, water flow, sedimentation, physical disturbance) conditions in comparison to those at the interior (Boström et al. 2006; Gaylord et al. 2007; Stewart et al. 2009; Arkema and Samhouri 2019).
In oligotrophic waters of the NW Mediterranean, we assessed how nutrient enrichment affects the photosynthetic efficiency, the reproductive output and herbivore damage in the fucoid, Carpodesmia brachycarpa, and the structure of the epibiont assemblage it supports. In particular, we tested the hypothesis that nutrient enrichment would facilitate the proliferation of opportunistic epiphytic algae at the expense of more complex algal forms and epizoans. We expected changes induced by nutrient enrichment to be greater at the edge than inside forests, since greater water motion can facilitate nutrient uptake (Ballesteros et al. 1998; Hurd 2000; Gaylord et al. 2007; Stewart et al. 2009). Since early life stages are generally more responsive to alterations in environmental conditions and resource availability, we predicted that nutrient-driven changes in the physiology of C. brachycarpa and associated epibiont assemblages would be greater for individuals that recruited in cleared areas and grew under enriched conditions than for adult specimens that were exposed to elevated nutrient levels when already fully developed.
Materials and methods
This study was carried out along the south-eastern coast of Capraia Island, in the Tuscan Archipelago (43.05° N, 9.85° E), between June 2014 and July 2016, within the framework of a broader project aimed to assess the mechanisms underlying shifts among alternative stable states on temperate rocky reefs. At depths between 2 and 8 m, the fucoid, Carpodesmia brachycarpa (J. Agardh) Orellana and Sansòn (previously Cystoseira brachycarpa), forms lush canopy stands that alternate with patches dominated by either encrusting corallines or algal mats made of foliose (Dictyota spp., Padina pavonica), filamentous (Sphacelariales), siphonous algae (Acetabularia acetabulum, Caulerpa cylindracea) and corticated Rhodophyta (e.g. Laurencia obtusa, Gastroclonium sp.) (Bulleri et al. 2017; Tamburello et al. 2019). Patches of habitat alternatives to macroalgal forests are produced by intensive grazing by sea urchins or disturbance due to hydrodynamic forces (Bulleri et al. 2018).
At 4–6 m depths, we randomly selected 8 boulders completely covered by C. brachycarpa canopies (hereafter referred to as forest habitat: FH) and 8 boulders over which urchins had formed barren patches (2–3 m2) within canopies (hereafter referred to as edge habitat: EH). All boulders were about ~ 15 m2 in surface area. Arbacia lixula was the dominant sea urchin in barren patches (mean density·m−2 ± SE = 3.344 ± 0.168), while Paracentrotus lividus densities were remarkably low (mean density·m−2 ± SE = 0.136 ± 0.024) (Tamburello et al. 2019). On each boulder, a 1.5 × 0.5 m area was marked, using epoxy putty, either inside the forest on FH boulders (> 1 m from the edge of the boulders) or at the edges between the forest and the barren on EH boulders. To assess how nutrient enrichment influences the physiology of newly established thalli and the structure of the epibiont assemblage they support, canopies were totally removed from marked areas in four FH and four EH, randomly chosen, boulders. Thus, there were 4 boulders for each combination of habitat (FH versus EH) and canopy treatment (Control versus Cleared).
Nutrients were elevated in 2 randomly identified boulders for each combination of habitat and canopy treatment, using slow-release fertilizer pellets (Osmocote, 6 months, 17:11:10 N:P:K) contained in plastic mesh bags (1 mm), a common method for elevating nutrient levels in seawater (Worm et al. 2000; Russell et al. 2005; Balata et al. 2010; Bulleri et al. 2012; Tuya et al. 2015; Ravaglioli et al. 2018). To achieve nutrient levels found in nearby urban areas, 8 bags, each containing 100 g of fertilizer, were fixed with plastic cables ties to steel hooks inserted in the rock within each area. Bags within an area were at least 30 cm apart and were replaced every 3 months to guarantee continuous nutrient release. At each of two times (June and November 2015), two seawater samples were taken ~ 3 cm above each fertilized area, using a 60 ml syringe (n = 16). Background nutrient levels in the area were assessed taking two water samples from each of six randomly chosen areas maintained at ambient nutrients, using the same method. These included also partial canopy removal areas that were generated within the framework of the broader project and not useful for the test of the hypotheses in this study (i.e. 30% and 70% canopy removal; see Tamburello et al. 2019 for details). Samples were immediately filtered (0.45 μm) and frozen prior to transport to the laboratory, where concentrations of nitrites (NO2), nitrates (NO3) and phosphates (PO4) were assessed by means of a continuous-flow AA3 Auto-Analyzer (Bran-Luebbe), following standard methods (Grasshoff et al. 1999). Although moderate, there was an increase in the concentration of NO3 and PO4 at both times of sampling and in that of NO2 at Time 1 (See Electronic Supplementary Material, ESM Fig. S1).
Measurements of nutrient levels from water samples collected nearby the releasing devices are generally highly variable in time and do not provide accurate estimates of mean concentrations achieved throughout the duration of an experiment (Russell et al. 2005; Bulleri et al. 2012). Thus, the weight of nutrient pellets in each bag was measured before deployment with a precision scale and, following retrieval from the field, after residual pellets were kept in a muffle oven for 28 h at 60 °C. The difference between the initial and final weight provides a more reliable estimate of daily rates of nutrient release (Carnell and Keough 2014). Across the duration of the experiment, the average daily release of N and P within each area was consistent among treatments (mean g day−1 ± SE; FH: canopy control, N = 0.392 ± 0.040, P = 0.254 ± 0.024; canopy removal, N = 0.421 ± 0.040, P = 0.272 ± 0.027; EH: canopy control, N = 0.38 ± 0.031, P = 0.247 ± 0.020; canopy removal, N = 0.400 ± 0.038, P = 0.259 ± 0.024).
Two years after the start of the experiment, C. brachycarpa had recovered in experimentally cleared areas, although to a greater extent under nutrient enrichment (Tamburello et al. 2019). Thus, five C. brachycarpa thalli were randomly identified in each of the areas assigned to a combination of habitat (FH versus EH), canopy (Control versus Cleared) and nutrient (Ambient versus Enhanced) treatments, for a total of 80 thalli. The length of thalli ranged between 8 and 24 cm, but the average length did not differ among experimental treatments (See Electronic Supplementary Material, ESM Table S1). Selected thalli were about 30 cm apart one from another and, in nutrient enriched areas, 20–30 cm apart from the nearest nutrient bag. For each thallus, in vivo chlorophyll fluorescence was measured on 3 randomly chosen branches with a pulse-amplitude-modulated (PAM) fluorometer (Diving-PAM, Walz). Effective quantum yield, an estimate of the photosynthetic efficiency of photosystem II (PSII) in light-adapted thalli, was measured in situ, between 11:00 a.m. and 14:00, by means of the saturating-light method on branches under ambient conditions. These thalli were then collected, sealed in transparent plastic bags and brought to the lab in an ice cooler, where they were preserved at − 20° C until further analyses.
The main consumers of C. brachycarpa in the Mediterranean are the sea urchins, P. lividus, and A. lixula, and the sparid fish, Sarpa salpa (Vergés et al. 2009; Agnetta et al. 2015). At our study site, urchins were absent inside C. brachycarpa stands and their grazing was, thus, limited to the boundary with barren areas. Thalli inside and at the edge of forests were exposed to herbivory by S. salpa (Vergés et al. 2009). To assess the effects of nutrient enrichment on herbivore consumption, we quantified the percentage of primary branches damaged in each thallus. In addition, since previous studies have shown that seawater nutrient levels influence the fecundity of brown seaweeds (Wahl 2008; O'Brien et al. 2013), the number of receptacles was counted on 5 randomly chosen primary fronds for each of four experimental thalli, under a dissecting microscope. The number of receptacles was standardized per frond surface area (i.e. expressed as density).
For each of the five experimental thalli, the abundance of algae and sessile animals was assessed on 5 randomly chosen primary branches. Species abundance was quantified as the surface occupied by the vertical projection of individuals of each species and expressed as a percent cover (Boudouresque 1971). Species were identified to the lowest taxonomic level possible, generally the genus or the species, except for encrusting corallines, Serpulidae, Foraminifera and Porifera.
Analysis of data
Replicate measures taken within thalli (3 for quantum yield and 5 for receptacle number and relative abundances of epibiont species) were averaged for analysis. The percentage of damaged fronds, effective quantum yield and number of receptacles were analyzed by means of ANOVAs, including the factors Habitat (fixed), Canopy treatment (fixed and crossed with Habitat), Nutrients (fixed and crossed with Habitat and Canopy treatment) and Boulder (random and nested within the other three factors).
The same four-factor design was used for multivariate and univariate analyses of epibionts. A four-factor PERMANOVA (Anderson 2001) on Bray–Curtis dissimilarities calculated on square-root transformed data was used to assess the response of the whole epibiont assemblage to the experimental conditions. Multivariate patterns were visualized using non-metric multidimensional scaling (nMDS). Multivariate analyses were performed using Primer 6 and PERMANOVA + (PRIMER-E 2008). Variations in total epibiont, epiphyte and epizoan cover and species richness, as well as variations in the relative abundance of the most abundant taxa, were analyzed by means of ANOVA. Pooling procedures were also used as recommended by Underwood (1997) to enhance the power of the statistical tests. More specifically, in the analyses of receptacle density and bryozoan abundance, the factor Boulder (Habitat × Canopy treatment × Nutrients) was not significant at P = 0.25 and was removed from the analyses, allowing the F tests for fixed factors and higher-order interactions to be carried out using the Residual term as the denominator. In all ANOVAs, homogeneity of variances was checked with Cochran’s C test and, when necessary, data were log-transformed. Student–Neuman–Keuls (SNK) tests were used for the ranking of the means.
Results
Nutrient enrichment did not influence the effective quantum yield or receptacle density in C. brachycarpa, while it increased the percentage of branches damaged by herbivores in thalli at forest edges (Fig. 2A–C, Table 1A–C). Receptacle density was significantly greater in thalli from cleared than canopy control areas (Fig. 2B, Table 1B).
C. brachycarpa supported a total of 102 epibiont taxa (Table S2). The structure of the epibiont assemblage differed between the edge and the inside of forests and between ambient and enriched nutrient levels (Fig. 3; Table 2). In the nMDS, symbols representing thalli exposed to nutrient enrichment are segregated from those maintained at ambient nutrient levels, while differences between habitats are not evident (Fig. 3). The high value of stress indicates considerable distortion in the two-dimensional representation of data.
The total cover of epibionts on C. brachycarpa was greater at the edge than inside the forest and decreased under nutrient enrichment, consistently between canopy treatments (Table 3, Fig. 4A). Nutrient enrichment significantly decreased the cover of epizoans on thalli at forest edges, but not on those inside the forest (Fig. 4C). By contrast, there was no effect of nutrient enrichment on epiphyte cover (Fig. 4B). Likewise, epizoan species richness decreased under nutrient enrichment, while there was no change in both total and epiphyte species richness (Table 3, Fig. 4D–F). Epizoan species richness was also greater on thalli in cleared than in control areas and inside the forest than at the edge of the forest (Fig. 4F).
None of the macroalgal groups, except for articulated corallines, responded to seawater fertilization (Table 4). This group decreased under enhanced nutrient levels, but cover values were generally very low, making these changes unlikely to be biologically meaningful (Fig. 5A). By contrast, nutrient enrichment decreased the cover of bryozoans on thalli at forest edges and that of hydrozoans on thalli from both habitats (Fig. 5B, C; Table 4). The analysis also indicated a significant effect of the interaction Habitat × Canopy treatment on the cover of hydrozoans, but the SNK tests did not show differences between means for any of the level comparisons. There was no effect of nutrient enrichment on sponges and serpulids, which covers on C. brachycarpa varied neither between cleared and control areas nor between the edge and inside of forests (Table 4).
Discussion
Nutrient enrichment had weak effects on the photosynthetic efficiency and reproductive output of the canopy-forming macroalga, C. brachycarpa. By contrast, it increased frond damage by herbivores at forest edges. Grazing by sea urchins is often intense at boundaries between barren patches and algal forests (Andrew 1994; Gagnon et al. 2004; Bulleri 2013). Greater water motion and light availability at forest edges may have facilitated nutrient uptake by macroalgae (Ballesteros et al. 1998; Hurd 2000; Stewart et al. 2009), enhancing their nutritional value and, hence, consumer pressure (Valentine and Duffy 2006; Balata et al. 2010; Prado et al. 2010b; Ghedini et al. 2015). P. lividus, a species actively feeding on Cystoseira, had very low densities in barrens on experimental boulders (i.e. 1.4 individuals ·10 m−2) and was unlikely to cause significant frond damage. Fertilization may have attracted A. lixula towards thalli at forest edges. This species has a limited ability to handle and consume intact Cystoseira and feeds mostly on encrusting algae and sessile invertebrates (Wangensteen et al. 2011; Agnetta et al. 2013, 2015).
Isotopic analyses have indeed shown that A. lixula occupies a higher trophic level than P. lividus and that it has, in some cases, a diet similar to that of a strict carnivore (Wangensteen et al. 2011). A. lixula attracted at forest edges, may have targeted epizoan preys on C. brachycarpa, halving their total cover and reducing their species richness. The decline of epizoans cannot be due to increased competition from epiphytes since their abundance, in contrast with our predictions, was not enhanced by nutrient enrichment.
This hypothesis would be supported by several lines of evidence: first, A. lixula was absent underneath intact canopies, explaining the lower damage of thalli inside the forest. Second, the abundance of sessile invertebrates, an important component of the diet of A. lixula, was very low in barren areas (i.e. total cover < 4%). Filter-feeders can benefit from nutrient enrichment via increased availability of plankton and organic particles. Such effects are common at sites exposed to sustained nutrient inputs (Gili and Coma 1998; Prado et al. 2010a; Rorig et al. 2017). Nutrients may have also enhanced the quality of epizoans as food. Stoichiometric theory assumes fixed elemental composition (i.e. homoestasis), but intraspecific variation in P content has been documented in some invertebrates and explained by dietary availability (Small and Pringle 2010). Although mostly limited to freshwater environments, there is evidence that the effects of nutrient enrichment on elemental compositions can propagate across trophic levels (Singer and Battin 2007; Small and Pringle 2010). Since foraging in invertebrate predators can be nutrient-specific (Mayntz et al. 2005), enhanced nutritional value (i.e. higher N and/or P content) of epizoans exposed to enrichment might have sustained predation by A. lixula.
Finally, as also documented in Cystoseira tamariscifolia (Otero Schmitt and Perez Cirera 1996), epizoans represented the dominant component of epibiont assemblages in the shaded, lower part of C. brachycarpa, while they were scant in the well-lit upper part, likely due to strong competition from macroalgae (Authors’ personal observation). Although A. lixula has a limited ability to bend down thalli and feed on apical fronds (Agnetta et al. 2015), it might be able to prey upon sessile invertebrates colonizing the cauloid and fronds closer to the bottom. Under these circumstances, frond damage would be a coincidental aspect of urchin foraging on epizoans, a phenomenon also termed as shared-doom (Dixon et al. 1981; Wahl and Hay 1995; da Gama et al. 2008).
Increased herbivore attraction to fertilized thalli at forest edges might also be the consequence of direct negative effects on epizoans. At ambient nutrient levels, thalli at forests edges supported a greater cover and diversity of epizoans than thalli inside forests. There are examples of epizoans deterring herbivory: the bryozoans, Lichenopora novae-zelandiae and Membranipora membranacea, reduced consumption of their host, respectively, Agarum fimbriatum and Saccharina latissimi, from herbivorous gastropods (Durante and Chia 1991; O'Brien et al. 2013). Likewise, along the coasts of Chile, consumption by the snail Tegula tridentata on the kelp, Lessonia trabeculata, colonized by hydroids was 3–4 times lower than on kelps without hydroids (González-Duarte et al. 2020). A decline of epizoans is very unlikely to have stimulated grazing by A. lixula on C. brachycarpa, but may have stimulated that by the fish, Sarpa salpa. This is a true herbivore (Havelange et al. 1997; Prado et al. 2010a) and may have preferentially browsed on fertilized thalli characterized by higher nutritional value (higher P and N content) and lower epizoan loading. Heavy consumption of Posidonia oceanica plants within fertilized patches inside seagrass beds and preferential feeding on Cystoseira branches bearing reproductive structures, suggests active selection of more nutritional plant tissues by S. salpa (Gianni et al. 2017; Ravaglioli et al. 2018). In addition, fertilized thalli may have lower levels of defensive compounds, such as phenolics (Ilvessalo and Tuomi 1989; Yates and Peckol 1993; Pavia and Toth 2000; Ravaglioli et al. 2018). Nonetheless, we did not observe more intense grazing on thalli in cleared areas, despite they supported higher numbers of receptacles. In addition, S. salpa is highly mobile and should have caused comparable damage to fertilized thalli both at the edge and inside forests.
Rapid recovery of canopies in areas cleared within forests (i.e. not subjected to urchin grazing) and exposed to nutrient addition (Tamburello et al. 2019), further suggests a weak grazing pressure by S. salpa. Thus, the hypothesis of enhanced frond damage at forest edges due to increased herbivory from S. salpa does not seem to be supported by our data. For the same reason, enhanced consumption by fish is unlikely to explain the weak response of epiphytes to fertilization both inside and at the edge of forests. This does not exclude trophic compensation of nutrient effects by meso-grazers (e.g. gastropods and amphipods) living within C. brachycarpa canopies (Piazzi et al. 2018). For example, the gastropod herbivore, Turbo undulatus, could absorb positive effects of nutrient enrichment, maintaining algal turf growth under check (Ghedini et al. 2015). Alternatively, greater nutrient uptake efficiency of C. brachycarpa may have limited the proliferation of weedy species either composing turfs (Tamburello et al. 2019) or growing as epiphytes (this study). In oligotrophic waters, low or moderate nutrient inputs can advantage complex, slow-growing macroalgae, such as Fucales, over ephemeral species (Pedersen and Borum 1997).
Ammonium excretion by sessile invertebrates can represent an important source of nitrogen for macroalgae during shortage periods (e.g. in summer) (Hurd et al. 1994; Hepburn and Hurd 2005; Bracken et al. 2007; Hepburn et al. 2012). Independently from the underpinning mechanisms, nutrient enrichment caused a decrease in the cover of sessile invertebrates on the lower part of thalli of C. brachycarpa. Such a decline did not influence the photosynthetic activity or the development of reproductive structures, as Carpodesmia can efficiently take up N in the form of nitrates (Epiardlahaye 1988). In general, brown seaweeds can use ammonium and nitrates simultaneously and the uptake of one form does not influence the uptake of the other (Haines and Wheeler 1978). Thus, decreased abundance of the animal component of the epibiont assemblages during events of nutrient release should not limit the productivity of brown seaweed stands.
There were no differences in the response to nutrient enrichment between C. brachycarpa within established stands and those that recolonized cleared areas during the study (i.e. 2 years). Elevation of nutrient levels has been found to reduce invertebrate settlement, likely through the alteration of biofilm chemical cues (Lawes et al. 2018). Our data indicate that nutrients did not influence the recruitment of sessile invertebrates on C. brachycarpa or that the alterations caused at the earlier stages of epibiont colonization were not long-lasting. Under these circumstances, the effects of nutrient enrichment on the structure of the epibiont assemblage supported by C. brachycarpa would not change when fertilization occurs simultaneously with acute events of mechanical disturbance. Interestingly, thalli in cleared areas had more receptacles, suggesting that reduced competition for light could foster the reproduction (Dayton et al. 1992; Viejo and Åberg 2001). Increased reproductive output might be key for the recovery of C. brachycarpa stands after disturbances and this process appears not to be altered by nutrient enrichment.
Our results suggest that fragmentation of macroalgal forests, increasing the perimeter to area ratio, could exacerbate nutrient effects on C. brachycarpa and its epibionts by increasing herbivore damage. Such indirect effects of nutrient enrichment are likely dependent upon the composition of the herbivore assemblage. The extent of the damage suffered by C. brachycarpa could be expected to be greater when macroalgal forests are adjacent to barren areas supporting higher densities of P. lividus. Indeed, at high densities, this species is able to completely eliminate erect macroalgae, forming barren grounds (Agnetta et al. 2015). Sparse densities of this species on shallow rocky reefs around the island, can be explained by a strengthening of predatory control in response to the establishment of partially or fully protected areas (Bulleri et al. 2018). Similarly, reduced densities and/or foraging efficiency of S. salpa due to predation may explain why there was not an increase in consumption rates on C. brachycarpa and its epiphytes in fertilized areas. Re-establishment of lost predatory control through fishery management is recognized as a valid strategy for mitigating the effects of nutrient inputs on habitat-forming macrophytes (Östman et al. 2016). Our study suggests that reducing the intensity and frequency of mechanical disturbances fragmenting macroalgal forests could further enhance their resistance and resilience to nutrient loading. Controlling disturbances linked with climate change, such as sea storms, requires a transnational and long-term effort. By contrast, targeting localized disturbances, such as those due to boat anchoring and fishing gear, might be a more viable strategy in the short-term. In particular, it may sustain the persistence of macroalgal forest in the face of nutrient enrichment in systems characterized by weak top-down control (e.g. outside MPAs).
In summary, our experiment shows that moderate nutrient enrichment of oligotrophic waters does not necessarily cause the proliferation of opportunistic epiphytes and, hence, a strengthening of their competitive effects on canopy-forming macroalgae. In particular, thalli inside forests appear little susceptible to either direct or indirect effects of nutrient enrichment. Our results reinforce the findings of previous experimental studies suggesting that nutrient enrichment can reduce the resilience of Mediterranean macroalgal forests to other disturbances, but it is unlikely, per se, to cause a shift towards a less productive state dominated by algal turfs (Piazzi and Ceccherelli 2017; Tamburello et al. 2019; Kraufvelin et al. 2020). It is worth noting that the net effects of seawater enrichment on canopy-forming macroalgae can vary according to the intensity and temporal regime (i.e. chronic versus acute) of nutrient inputs, their natural concentration in the receiving water body and composition of the herbivore assemblage (Russell et al. 2005; Bulleri et al. 2012; Tuya et al. 2015; Östman et al. 2016; Ravaglioli et al. 2018). This brings two main caveats: (i) caution should be used in generalizing the results of single-site studies—such as ours—to broader areas; (ii) strategies for mitigating the impact of nutrient enrichment on marine macrophytes should be tailored regionally, on biotic and abiotic features of targeted ecosystems.
Availability of data and material
The datasets generated and analysed during the current study are available from the corresponding author on reasonable request.
References
Agnetta D, Bonaviri C, Badalamenti F, Scianna C, Vizzini S, Gianguzza P (2013) Functional traits of two co-occurring sea urchins across a barren/forest patch system. J Sea Res 76:170–177. https://doi.org/10.1016/j.seares.2012.08.009
Agnetta D, Badalamenti F, Ceccherelli G, Di Trapani F, Bonaviri C, Gianguzza P (2015) Role of two co-occurring Mediterranean sea urchins in the formation of barren from Cystoseira canopy. Est Coast Shelf Sci 152:73–77. https://doi.org/10.1016/j.ecss.2014.11.023
Airoldi L, Beck MW (2007) Loss, status and trends for coastal marine habitats of Europe. In: Gibson RN, Atkinson RJA, Gordon JDM (eds) Oceanogr Mar Biol, vol 45, pp 345–405
Alestra T, Schiel DR (2014) Effects of opportunistic algae on the early life history of a habitat-forming fucoid: influence of temperature, nutrient enrichment and grazing pressure. Mar Ecol Prog Ser 508:105–115
Alestra T, Schiel DR (2015) Impacts of local and global stressors in intertidal habitats: Influence of altered nutrient, sediment and temperature levels on the early life history of three habitat-forming macroalgae. J Exp Mar Biol Ecol 468:29–36. https://doi.org/10.1016/j.jembe.2015.03.017
Andersen GS, Moy FE, Christie H (2019) In a squeeze: epibiosis may affect the distribution of kelp forests. Ecol Evol 9:2883–2897. https://doi.org/10.1002/ece3.4967
Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Aust Ecol 26:32–46. https://doi.org/10.1111/j.1442-9993.2001.01070.pp.x
Andrew NL (1994) Survival of kelp adjacent to areas grazed by sea urchins in New South Wales, Australia. Aust J Ecol 19:466–472. https://doi.org/10.1111/j.1442-9993.1994.tb00513.x
Angelini C, Altieri AH, Silliman BR, Bertness MD (2011) Interactions among foundation species and their consequences for community organization, biodiversity, and conservation. Bioscience 61:782–789. https://doi.org/10.1525/bio.2011.61.10.8
Arkema KK, Samhouri JF (2019) Living on the edge: variation in the abundance and demography of a kelp forest epibiont. Diversity 11:120. https://doi.org/10.3390/d11080120
Balata D, Piazzi L, Nesti U, Bulleri F, Bertocci I (2010) Effects of enhanced loads of nutrients on epiphytes on leaves and rhizomes of Posidonia oceanica. J Sea Res 63:173–179. https://doi.org/10.1016/j.seares.2009.12.001
Ballesteros E, Sala E, Garrabou J, Zabala M (1998) Community structure and frond size distribution of a deep water stand of Cystoseira spinosa (Phaeophyta) in the northwestern Mediterranean. Eur J Phycol 33:121–128. https://doi.org/10.1017/s0967026298001541
Benedetti-Cecchi L, Pannacciulli F, Bulleri F, Moschella PS, Airoldi L, Relini G, Cinelli F (2001) Predicting the consequences of anthropogenic disturbance: large-scale effects of loss of canopy algae on rocky shores. Mar Ecol Prog Ser 214:137–150. https://doi.org/10.3354/meps214137
Bergström L, Berger R, Kautsky L (2003) Negative direct effects of nutrient enrichment on the establishment of Fucus vesiculosus in the Baltic Sea. Eur J Phycol 38:41–46. https://doi.org/10.1080/0967026031000096236
Bokn TL, Duarte CM, Pedersen MF, Marbá N, Moy FE, Barron C, Bjerkeng B, Borum J, Christie H, Engelbert S, Fotel FL, Hoell EE, Karez R, Kersting K, Kraufvelin P, Lindblad C, Olsen M, Sanderud KA, Sommer U, Sørensen K (2003) The response of experimental rocky shore communities to nutrient additions. Ecosystems 6:577–594. https://doi.org/10.1007/s10021-002-0108-6
Boström C, Jackson EL, Simenstad CA (2006) Seagrass landscapes and their effects on associated fauna: a review. Estuar Coastal Shelf Sci 68:383–403. https://doi.org/10.1016/j.ecss.2006.01.026
Boudouresque CF (1971) Méthodes d’étude qualitative et quantitative du benthos (en particulier du phytobenthos). Tethys 3:79–104
Bracken MES, Gonzalez-Dorantes CA, Stachowicz JJ (2007) Whole-community mutualism: associated invertebrates facilitate a dominant habitat-forming seaweed. Ecology 88:2211–2219. https://doi.org/10.1890/06-0881.1
Bulleri F (2013) Grazing by sea urchins at the margins of barren patches on Mediterranean rocky reefs. Mar Biol 160:2493–2501. https://doi.org/10.1007/s00227-013-2244-2
Bulleri F, Benedetti-Cecchi L (2006) Mechanisms of recovery and resilience of different components of mosaics of habitats on shallow rocky reefs. Oecologia 149:482–492. https://doi.org/10.1007/s00442-006-0459-3
Bulleri F, Russell BD, Connell SD (2012) Context-dependency in the effects of nutrient loading and consumers on the availability of space in marine rocky environments. PLoS ONE 7:e33825. https://doi.org/10.1371/journal.pone.0033825
Bulleri F, Benedetti-Cecchi L, Ceccherelli G, Tamburello L (2017) A few is enough: a low cover of a non-native seaweed reduces the resilience of Mediterranean macroalgal stands to disturbances of varying extent. Biol Invasions 19:2291–2305. https://doi.org/10.1007/s10530-017-1442-0
Bulleri F, Cucco A, Dal Bello M, Maggi E, Ravaglioli C, Benedetti-Cecchi L (2018) The role of wave-exposure and human impacts in regulating the distribution of alternative habitats on NW Mediterranean rocky reefs. Est Coast Shelf Sci 201:114–122. https://doi.org/10.1016/j.ecss.2016.02.013
Buschmann AH, Gómez P (1993) Interaction mechanisms between Gracilaria chilensis (Rhodophyta) and epiphytes. Hydrobiologia 260:345–351. https://doi.org/10.1007/bf00049039
Cadenasso ML, Pickett STA, Weathers KC, Jones CG (2003) A framework for a theory of ecological boundaries. Bioscience 53:750–758
Carnell PE, Keough MJ (2014) Spatially variable synergistic effects of disturbance and additional nutrients on kelp recruitment and recovery. Oecologia 175:409–416. https://doi.org/10.1007/s00442-014-2907-9
Chu Y, Liu Y, Li J, Gong Q (2019) Effects of elevated pCO2 and nutrient enrichment on the growth, photosynthesis, and biochemical compositions of the brown alga Saccharina japonica (Laminariaceae, Phaeophyta). PeerJ 7:e8040. https://doi.org/10.7717/peerj.8040
Clausing RJ, Phillips NE, Fong P (2020) Environmental context shapes the long-term role of nutrients in driving producer community trajectories in a top–down dominated marine ecosystem. J Ecol. https://doi.org/10.1111/1365-2745.13405
Coleman MA, Kelaher BP, Steinberg PD, Millar AJK (2008) Absence of a large brown macroalga on urbanized rocky reefs aronud Sydney, Australia, and evidence for historical decline. J Phycol 44:897–901
Creed JC, Norton TA, Kain JM (1997) Intraspecific competition in Fucus serratus germlings: the interaction of light, nutrients and density. J Exp Mar Biol Ecol 212:211–223. https://doi.org/10.1016/s0022-0981(96)02748-7
Crowe TP, Cusson M, Bulleri F, Davoult D, Arenas F, Aspden R, Benedetti-Cecchi L, Bevilacqua S, Davidson I, Defew E, Fraschetti S, Gollety C, Griffin JN, Herkül K, Kotta J, Migne A, Molis M, Nicol SK, Noel L, Pinto IS, Valdivia N, Vaselli S, Jenkins SR (2013) Large-scale variation in combined impacts of canopy loss and disturbance on community structure and ecosystem functioning. PLoS ONE 8:e66238. https://doi.org/10.1371/journal.pone.0066238
da Gama BAP, de A Santos RP, Pereira RC (2008) The effect of epibionts on the susceptibility of the red seaweed Cryptonemia seminervis to herbivory and fouling. Biofouling 24:209–218. https://doi.org/10.1080/08927010802041253
D’Antonio C (1985) Epiphytes on the rocky intertidal red alga RhodomelaLarix (Turner) C. Agardh: negative effects on the host and food for herbivores? J Exp Mar Biol Ecol 86:197–218. https://doi.org/10.1016/0022-0981(85)90103-0
Dayton PK, Tegner MJ, Parnell PE, Edwards PB (1992) Temporal and spatial patterns of disturbance and recovery in a kelp forest community. Ecol Monogr 62:421–445. https://doi.org/10.2307/2937118
Dixon J, Schroeter SC, Kastendiek J (1981) Effects of the encrusing bryozoan, Membranipora membranacea, on the loss of blades and fronds by the giant kelp, Macrocystis pyrifera (Laminariales). J Phycol 17:341–345. https://doi.org/10.1111/j.1529-8817.1981.tb00860.x
Durante KM, Chia FS (1991) Epiphytism on Agarum fimbriatum —can herbivore preference explain distributions of epiphytic bryozoans? Mar Ecol Prog Ser 77:279–287. https://doi.org/10.3354/meps077279
Epiardlahaye M (1988) Effects of ammonium, nitrate and phosphate on the growth of Cystoseira stricta (Phaeophyta, fucales) cuttings in culture. Cryptogamie Algol 9:211–229
Estes JA, Palmisano JF (1974) Sea otters—their role in structuring nearshore communities. Science 185:1058–1060. https://doi.org/10.1126/science.185.4156.1058
Falkenberg LJ, Russell BD, Connell SD (2013) Contrasting resource limitations of marine primary producers: implications for competitive interactions under enriched CO2 and nutrient regimes. Oecologia 172:575–583. https://doi.org/10.1007/s00442-012-2507-5
Filbee-Dexter K, Wernberg T (2018) Rise of turfs: a new battlefront for globally declining kelp forests. Bioscience 68:64–76. https://doi.org/10.1093/biosci/bix147
Gagnon P, Himmelman JH, Johnson LE (2004) Temporal variation in community interfaces: kelp-bed boundary dynamics adjacent to persistent urchin barrens. Mar Biol 144:1191–1203. https://doi.org/10.1007/s00227-003-1270-x
Gaylord B, Rosman JH, Reed DC, Koseff JR, Fram J, MacIntyre S, Arkema K, McDonald C, Brzezinski MA, Largier JL, Monismith SG, Raimondi PT, Mardian B (2007) Spatial patterns of flow and their modification within and around a giant kelp forest. Limnol Oceanogr 52:1838–1852
Ghedini G, Russell BD, Connell SD (2015) Trophic compensation reinforces resistance: herbivory absorbs the increasing effects of multiple disturbances. Ecol Lett 18:182–187. https://doi.org/10.1111/ele.12405
Gianni F, Bartolini F, Pey A, Laurent M, Martins GM, Airoldi L, Mangialajo L (2017) Threats to large brown algal forests in temperate seas: the overlooked role of native herbivorous fish. Sci Rep 7:6012. https://doi.org/10.1038/s41598-017-06394-7
Gili J-M, Coma R (1998) Benthic suspension feeders: their paramount role in littoral marine food webs. Trends Ecol Evol 13:316–321. https://doi.org/10.1016/S0169-5347(98)01365-2
González-Duarte MM, Megina C, Subida MD (2020) Anti-herbivory protection by mutualism in marine ecosystems: the case of kelps and hydroids. Est Coast Shelf Sci 235:106578. https://doi.org/10.1016/j.ecss.2019.106578
Gorgula SK, Connell SD (2004) Expansive covers of turf-forming algae on human-dominated coast: the relative effects of increasing nutrient and sediment loads. Mar Biol 145:613–619. https://doi.org/10.1007/s00227-004-1335-5
Gorman D, Russell BD, Connell SD (2009) Land-to-sea connectivity: linking human-derived terrestrial subsidies to subtidal habitat change on open rocky coasts. Ecol Appl 19:1114–1126. https://doi.org/10.1890/08-0831.1
Grasshoff K, Ehrhardt M, Kremling K, Anderson L (1999) Methods of seawater analysis. Wiley, Weinheim, p 600
Gribben PE, Angelini C, Altieri AH, Bishop MJ, Thomsen MS, Bulleri F (2019) Facilitation cascades in marine ecosystems: A synthesis and future directions. Oceanogr Mar Biol 57:27–168
Haines KC, Wheeler PA (1978) Ammonium and nitrate uptake by the marine macrophytes Hypnea musciformis (Rhodophyta) and Macrocystis pyrifera (Phaeophyta). J Phycol 14:319–324. https://doi.org/10.1111/j.1529-8817.1978.tb00305.x
Halpern BS, Walbridge S, Selkoe KA, Kappel CV, Micheli F, D’Agrosa C, Bruno JF, Casey KS, Ebert C, Fox HE, Fujita R, Heinemann D, Lenihan HS, Madin EMP, Perry MT, Selig ER, Spalding M, Steneck R, Watson R (2008) A global map of human impact on marine ecosystems. Science 319:948–952. https://doi.org/10.1126/science.1149345
Havelange S, Lepoint G, Dauby P, Bouquegneau J-M (1997) Feeding of the sparid fish Sarpa salpa in a seagrass ecosystem: diet and carbon flux. Mar Ecol 18:289–297. https://doi.org/10.1111/j.1439-0485.1997.tb00443.x
Hemmi A, Jormalainen V (2002) Nutrient enhancement increases performance of a marine herbivore via quality of its food alga. Ecology 83:1052–1064
Hemmi A, Jormalainen V (2004) Genetic and environmental variation in performance of a marine isopod: effects of eutrophication. Oecologia 140:302–311
Hepburn CD, Hurd CL (2005) Conditional mutualism between the giant kelp Macrocystis pyrifera and colonial epifauna. Mar Ecol Prog Ser 302:37–48
Hepburn CD, Frew RD, Hurd CL (2012) Uptake and transport of nitrogen derived from sessile epifauna in the giant kelp Macrocystis pyrifera. Aquatic Biol 14:121–128. https://doi.org/10.3354/ab00382
Hoegh-Guldberg O, Bruno JF (2010) The impact of climate change on the world’s marine ecosystems. Science 328:1523–1528. https://doi.org/10.1126/science.1189930
Hurd CL (2000) Water motion, marine macroalgal physiology, and reproduction. J Phycol 36:453–472. https://doi.org/10.1046/j.1529-8817.2000.99139.x
Hurd CL, Durante KM, Chia FS, Harrison PJ (1994) Effect of bryozoan colonization on inorganic nitrogen acquisition by the kelps Agarum fimbriatum and Macrocystis integrifolia. Mar Biol 121:167–173. https://doi.org/10.1007/bf00349486
Ilvessalo H, Tuomi J (1989) Nutrient availability and accumulation of phenolic compounds in the brown alga Fucus vesiculosus. Mar Biol 101:15–119
Iveša L, Djakovac T, Devescovi M (2016) Long-term fluctuations in Cystoseira populations along the west Istrian Coast (Croatia) related to eutrophication patterns in the northern Adriatic Sea. Mar Poll Bull 106:162–173. https://doi.org/10.1016/j.marpolbul.2016.03.010
Karez R, Engelbert S, Sommer U (2000) “Co-consumption” and “protective coating”: two new proposed effects of epiphytes on their macroalgal hosts in mesograzer-epiphyte-host interactions. Mar Ecol Prog Ser 205:85–93. https://doi.org/10.3354/meps205085
Kautsky N, Kautsky H, Kautsky U, Waern M (1986) Decreased depth penetration of Fucus vesiculosus L. since the 1940s indicates eutrophication in the Baltic Sea. Mar Ecol Prog Ser 28:1–8
Kraufvelin P, Salovius S, Christie H, Moy FE, Karez R, Pedersen MF (2006) Eutrophication-induced changes in benthic algae affect the behaviour and fitness of the marine amphipod Gammarus locusta. Aquat Bot 84:199–209
Kraufvelin P, Lindholm A, Pedersen MF, Kirkerud LA, Bonsdorff E (2010) Biomass, diversity and production of rocky shore macroalgae at two nutrient enrichment and wave action levels. Mar Biol 157:29–47
Kraufvelin P, Christie H, Gitmark JK (2020) Top-down release of mesopredatory fish is a weaker structuring driver of temperate rocky shore communities than bottom-up nutrient enrichment. Mar Biol 167:49
Kriegisch N, Reeves SE, Johnson CR, Ling SD (2019) Top-down sea urchin overgrazing overwhelms bottom-up stimulation of kelp beds despite sediment enhancement. J Exp Mar Biol Ecol 514:48–58. https://doi.org/10.1016/j.jembe.2019.03.012
Krumhansl KA, Okamoto DK, Rassweiler A, Novak M, Bolton JJ, Cavanaugh KC, Connell SD, Johnson CR, Konar B, Ling SD, Micheli F, Norderhaug KM, Perez-Matus A, Sousa-Pintol I, Reed DC, Salomon AK, Shears NT, Wernberg T, Anderson RJ, Barrett NS, Buschmanns AH, Carr MH, Caselle JE, Derrien-Courtel S, Edgar GJ, Edwards M, Estes JA, Goodwin C, Kenner MC, Kushner DJ, Moy FE, Nunn J, Stenecka RS, Vaquez J, Watson J, Witmand JD, Byrnes JEK (2016) Global patterns of kelp forest change over the past half-century. Proc Natl Acad Sci USA 113:13785–13790. https://doi.org/10.1073/pnas.1606102113
Lawes JC, Clark GF, Johnston EL (2018) Disentangling settlement responses to nutrient-rich contaminants: elevated nutrients impact marine invertebrate recruitment via water-borne and substrate-bound cues. Sci Total Environ 645:984–992. https://doi.org/10.1016/j.scitotenv.2018.07.234
Ling SD, Scheibling RE, Rassweiler A, Johnson CR, Shears N, Connell SD, Salomon AK, Norderhaug KM, Perez-Matus A, Hernandez JC, Clemente S, Blamey LK, Hereu B, Ballesteros E, Sala E, Garrabou J, Cebrian E, Zabala M, Fujita D, Johnson LE (2015) Global regime shift dynamics of catastrophic sea urchin overgrazing. Philos T R Soc B 370:20130269. https://doi.org/10.1098/rstb.2013.0269
Loffler Z, Bellwood DR, Hoey AS (2015) Associations among coral reef macroalgae influence feeding by herbivorous fishes. Coral Reefs 34:51–55. https://doi.org/10.1007/s00338-014-1236-0
Mangialajo L, Chiantore M, Cattaneo-Vietti R (2008) Loss of fucoid algae along a gradient of urbanisation, and structure of benthic assemblages. Mar Ecol Prog Ser 358:63–74. https://doi.org/10.3354/meps07400
Mayntz D, Raubenheimer D, Salomon M, Toft S, Simpson SJ (2005) Nutrient-specific foraging in invertebrate predators. Science 307:111–113. https://doi.org/10.1126/science.1105493
Menge BA, Daley BA, Lubchenco J, Sanford E, Dahlhoff E, Halpin PM, Hudson G, Burnaford JL (1999) Top-down and bottom-up regulation of New Zealand rocky intertidal communities. Ecol Monogr 69:297–330
Moy FE, Christie H (2012) Large-scale shift from sugar kelp (Saccharina latissima) to ephemeral algae along the south and west coast of Norway. Mar Biol Res 8:309–321. https://doi.org/10.1080/17451000.2011.637561
O’Brien JM, Krumhansl KA, Scheibling RE (2013) Invasive bryozoan alters interaction between a native grazer and its algal food. J Mar Biol Ass UK 93:1393–1400. https://doi.org/10.1017/s0025315412001683
O’Leary JK, Micheli F, Airoldi L, Boch C, De Leo G, Elahi R, Ferretti F, Graham NAJ, Litvin SY, Low NH, Lummis S, Nickols KJ, Wong J (2017) The resilience of marine ecosystems to climatic disturbances. Bioscience 67:208–220. https://doi.org/10.1093/biosci/biw161
Östman Ö, Eklöf J, Eriksson BK, Olsson J, Moksnes P-O, Bergström U (2016) Top-down control as important as nutrient enrichment for eutrophication effects in North Atlantic coastal ecosystems. J Appl Ecol 53:1138–1147. https://doi.org/10.1111/1365-2664.12654
Otero Schmitt J, Perez Cirera JL (1996) Epiphytism on Cystoseira (Fucales, Phaeophyta) from the Atlantic coast of Northwest Spain. Bot Mar 39:445–465. https://doi.org/10.1515/botm.1996.39.1-6.445
Pavia H, Toth GB (2000) Influence of light and nitrogen on the phlorotannin content of the brown seaweeds Ascophyllum nodosum and Fucus vesiculosus. Hydrobiologia 440:299–305
Pedesen MF, Borum J (1997) Nutrient control of estuarine macroalgae: growth strategy and the balance between nitrogen requirements and uptake. Mar Ecol Prog Ser 161:155–163
Peters JR, Reed DC, Burkepile DE (2019) Climate and fishing drive regime shifts in consumer-mediated nutrient cycling in kelp forests. Glob Change Biol 25:3179–3192. https://doi.org/10.1111/gcb.14706
Piazzi L, Ceccherelli G (2017) Concomitance of oligotrophy and low grazing pressure is essential for the resilience of Mediterranean subtidal forests. Mar Poll Bull 123:197–204. https://doi.org/10.1016/j.marpolbul.2017.08.061
Piazzi L, Bonaviri C, Castelli A, Ceccherelli G, Costa G, Curini-Galletti M, Langeneck J, Manconi R, Montefalcone M, Pipitone C, Rosso A, Pinna S (2018) Biodiversity in canopy-forming algae: structure and spatial variability of the Mediterranean Cystoseira assemblages. Estuar Coast Shelf Sci 207:132–141. https://doi.org/10.1016/j.ecss.2018.04.001
Prado P, Alcoverro T, Romero J (2010a) Influence of nutrients in the feeding ecology of seagrass (Posidonia oceanica L.) consumers: a stable isotopes approach. Mar Biol 157:715–724. https://doi.org/10.1007/s00227-009-1355-2
Prado P, Romero J, Alcoverro T (2010b) Nutrient status, plant availability and seasonal forcing mediate fish herbivory in temperate seagrass beds. Mar Ecol Prog Ser 409:229–239. https://doi.org/10.3354/meps08585
PRIMER-E (2008) PERMANOVA and PRIMER 6. PRIMER-E, Lutton
Ravaglioli C, Capocchi A, Fontanini D, Mori G, Nuccio C, Bulleri F (2018) Macro-grazer herbivory regulates seagrass response to pulse and press nutrient loading. Mar Environ Res 136:54–61. https://doi.org/10.1016/j.marenvres.2018.02.019
Rorig LR, Ottonelli M, Itokazu AG, Maraschin M, Lins JVH, Abreu PCV, De Almeida MTR, Ramlov F, D’Oca M, Ramalho LV, Diehl FL, Horta JPA, Pereira J (2017) Blooms of bryozoans and epibenthic diatoms in an urbanized sandy Beach (Balneario Camboriu—SC —Brazil): dynamics, possible causes and biomass characterization. Braz J Oceanogr 65:678–694. https://doi.org/10.1590/s1679-87592017116106504
Russell BD, Elsdon TS, Gillanders BM, Connell SD (2005) Nutrients increase epiphyte loads: broad-scale observations and an experimental assessment. Mar Biol 147:551–558. https://doi.org/10.1007/s00227-005-1571-3
Saier B, Chapman AS (2004) Crusts of the alien bryozoan Membranipora membranacea can negatively impact spore output from native kelps (Laminaria longicruris). Bot Mar 47:265–271. https://doi.org/10.1515/bot.2004.031
Schaffelke B, Klumpp DW (1998) Short-term nutrient pulses enhance growth and photosynthesis of the coral reef macroalga Sargassum baccularia. Mar Ecol Prog Ser 170:95–105. https://doi.org/10.3354/meps170095
Singer GA, Battin TJ (2007) Anthropogenic subsidies alter stream consumer-resource stoichiometry, biodiversity, and food chains. Ecol Appl 17:376–389. https://doi.org/10.1890/06-0229
Smale DA, Wernberg T (2013) Extreme climatic event drives range contraction of a habitat-forming species. Philos T R Soc B 280:20122829. https://doi.org/10.1098/rspb.2012.2829
Small GE, Pringle CM (2010) Deviation from strict homeostasis across multiple trophic levels in an invertebrate consumer assemblage exposed to high chronic phosphorus enrichment in a Neotropical stream. Oecologia 162:581–590. https://doi.org/10.1007/s00442-009-1489-4
Steen H, Rueness J (2004) Comparison of survival and growth in germlings of six fucoid species (Fucales, Phaeophyceae) at two different temperature and nutrient levels. Sarsia 89:175–183. https://doi.org/10.1080/00364820410005818
Steen H, Scrosati R (2004) Intraspecific competition in Fucus serratus and F. evanescens (Phaeophyceae : Fucales) germlings: effects of settlement density, nutrient concentration, and temperature. Mar Biol 144:61–70. https://doi.org/10.1007/s00227-003-1175-8
Stewart HL, Fram JP, Reed DC, Williams DL, Brzezinski MA, MacIntyre S, Gaylord B (2009) Differences in growth, morphology and tissue carbon and nitrogen of Macrocystis pyrifera within and at the outer edge of a giant kelp forest in California, USA. Mar Ecol Prog Ser 375:101–112
Strain EMA, Thomson RJ, Micheli F, Mancuso FP, Airoldi L (2014) Identifying the interacting roles of stressors in driving the global loss of canopy-forming to mat-forming algae in marine ecosystems. Glob Change Biol 20:3300–3312. https://doi.org/10.1111/gcb.12619
Strain EMA, van Belzen J, van Dalen J, Bouma TJ, Airoldi L (2015) Management of local stressors can improve the resilience of marine canopy algae to global stressors. PLoS ONE 10:e0120837. https://doi.org/10.1371/journal.pone.0120837
Tamburello L, Ravaglioli C, Mori G, Nuccio C, Bulleri F (2019) Enhanced nutrient loading and herbivory do not depress the resilience of subtidal canopy forests in Mediterranean oligotrophic waters. Mar Environ Res 149:7–17. https://doi.org/10.1016/j.marenvres.2019.05.015
Teagle H, Hawkins SJ, Moore PJ, Smale DA (2017) The role of kelp species as biogenic habitat formers in coastal marine ecosystems. J Exp Mar Biol Ecol 492:81–98. https://doi.org/10.1016/j.jembe.2017.01.017
Thornber C, Jones E, Thomsen M (2016) Epibiont-marine macrophyte assemblages. In: Ólafsson E (ed) Marine macrophytes as foundation species. CRC Press, Boca Raton, pp 43–65
Tuya F, Betancor S, Viera-Rodríguez MA, Guedes R, Riera R, Haroun R, Espino F (2015) Effect of chronic versus pulse perturbations on a marine ecosystem: integration of functional responses across organization levels. Ecosystems 18:1455–1471. https://doi.org/10.1007/s10021-015-9911-8
Underwood AJ (1997) Experiments in ecology: their logical design and interpretation using analysis of variance. Cambridge University Press, Cambridge
Valentine JF, Duffy JE (2006) The central role of grazing in seagrass ecology. In: Larkum WD, Orth RJ, Duarte C (eds) Seagrasses: biology, ecology and conservation. Springer, Dordrecht, pp 63–501
Vergés A, Alcoverro T, Ballesteros E (2009) Role of fish herbivory in structuring the vertical distribution of canopy algae Cystoseira spp. in the Mediterranean Sea. Mar Ecol Prog Ser 375:1–11
Verges A, Tomas F, Cebrian E, Ballesteros E, Kizilkaya Z, Dendrinos P, Karamanlidis AA, Spiegel D, Sala E (2014) Tropical rabbitfish and the deforestation of a warming temperate sea. J Ecol 102:1518–1527. https://doi.org/10.1111/1365-2745.12324
Viejo RM, Åberg P (2001) Effects of density on the vital rates of a modular seaweed. Mar Ecol Prog Ser 221:105–115. https://doi.org/10.3354/meps221105
Vogt H, Schramm W (1991) Conspicuous decline of Fucus in Kiel Bay (Western Baltic): what are the causes? Mar Ecol Prog Ser 69:189–194
Wahl M (2008) Ecological lever and interface ecology: epibiosis modulates the interactions between host and environment. Biofouling 24:427–438. https://doi.org/10.1080/08927010802339772
Wahl M, Hay ME (1995) Associational resistance and shared doom: effects of epibiosis on herbivory. Oecologia 102:329–340. https://doi.org/10.1007/bf00329800
Wangensteen OS, Turon X, Garcia-Cisneros A, Recasens M, Romero J, Palacin C (2011) A wolf in sheep’s clothing: carnivory in dominant sea urchins in the Mediterranean. Mar Ecol Prog Ser 441:117–128. https://doi.org/10.3354/meps09359
Wernberg T, Bennett S, Babcock RC, de Bettignies T, Cure K, Depczynski M, Dufois F, Fromont J, Fulton CJ, Hovey RK, Harvey ES, Holmes TH, Kendrick GA, Radford B, Santana-Garcon J, Saunders BJ, Smale DA, Thomsen MS, Tuckett CA, Tuya F, Vanderklift MA, Wilson S (2016) Climate-driven regime shift of a temperate marine ecosystem. Science 353:169–172. https://doi.org/10.1126/science.aad8745
Werner FJ, Graiff A, Matthiessen B (2016) Even moderate nutrient enrichment negatively adds up to global climate change effects on a habitat-forming seaweed system. Limnol Oceanogr 61:1891–1899. https://doi.org/10.1002/lno.10342
Wong MC, Vercaemer B (2012) Effects of invasive colonial tunicates and a native sponge on the growth, survival, and light attenuation of eelgrass (Zostera marina). Aquat Invasions 7:315–326
Worm B, Lotze HK, Bostrom C, Engkvist R, Labanauskas V, Sommer U (1999) Marine diversity shift linked to interactions among grazers, nutrients and propagule banks. Mar Ecol Prog Ser 185:309–314. https://doi.org/10.3354/meps185309
Worm B, Reusch TBH, Lotze HK (2000) In situ nutrient enrichment: methods for marine benthic ecology. Int Rev Hydrobiol 85:359–375. https://doi.org/10.1002/(sici)1522-632(200004)85:2/3%3c359::aid-iroh359%3e3.0.co;2-i
Yates JL, Peckol P (1993) Effects of nutrient availability and herbivory on polyphenolics in the seaweed Fucus Versiculosus. Ecology 74:1757–1766
Acknowledgements
We sincerely thank E. Biagi, G.R. Lombardo, E. Re and N. Niktoreh for help in the lab, one anonymous reviewer, Prof. V. Jormalainen and the Associate Editor P. Kraufvelin for providing insightful comments on an earlier drafts.
Funding
Open access funding provided by Università di Pisa within the CRUI-CARE Agreement. This project was funded by the Italian Ministry for Education, University and Research (MIUR), under the call FIRB 2012, through the project HI-BEF (Unveiling hidden relationships between biodiversity and ecosystem functioning in Mediterranean rocky reefs (protocol RBFR 12RXWL).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Responsible Editor: P. Kraufvelin.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Reviewed by V. Jormalainen and an undisclosed expert.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
About this article
Cite this article
Bulleri, F., Pardi, G., Tamburello, L. et al. Nutrient enrichment stimulates herbivory and alters epibiont assemblages at the edge but not inside subtidal macroalgal forests. Mar Biol 167, 181 (2020). https://doi.org/10.1007/s00227-020-03789-5
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00227-020-03789-5