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Habitat structure is more important than nutrient supply in modifying mussel bed assemblage in an upwelling area of the Peruvian coast

Abstract

Upwelling intensity modifies coastal primary production and influences individual traits of habitat-forming species. Along the Peruvian coast, beds of the mytilid Perumytilus purpuratus provide structurally complex habitats that harbour many organisms. We predict that in the nutrient-rich system of Central Peru, the modification of structural complexity would have stronger effects on the Perumytilus community than nutrient addition. We experimentally examined the effects of nutrient addition on the Perumytilus-dominated assemblage and we evaluated the potential effect of varying shell size on the Perumytilus-dominated assemblage. Nutrient addition to the mussel bed with slow-release fertilizers caused no changes in the total macro- and microalgal biomass and did not affect abundances or composition of the assemblage. To explore the effect of structural complexity on the Perumytilus assemblage, we manipulated mussel size with experimental bags containing small and large individuals. Predators, grazers and mobile organisms were more abundant among smaller mussels, with smaller gap volume, whereas the barnacle Jehlius cirratus was more abundant on larger mussels. In conclusion, point-source nutrient addition to the mussel bed did not enhance primary production. However, the modification of structural characteristics related to mussel size induced changes in the faunal assemblage. Thus, it seems that in this nutrient-rich system, nutrient enhancement would not significantly affect Perumytilus and its assemblage, whereas structural habitat seems to play an important role in shaping this community.

Introduction

Nutrient enrichment of surface waters as a result of the upwelling of deeper oceanic water has been well documented for several shores around the world (e.g. Bosman et al. 1987). On rocky shores, this nutrient enhancement may produce variation at lower trophic levels (bottom–up effect, Menge 1992) by (1) influencing the growth of sessile filter-feeders, which depends on the input of plankton and particulate matter or (2) modifying directly algal productivity (Wieters 2005). Several studies from coastal upwelling areas (Bustamante 1995; Menge et al. 1997, 1999) support the predictions of the bottom–up theory that high offshore production (e.g. high phytoplankton concentration) increases onshore production by enhancing food supply to filter-feeders, leading to improved survival, increased reproductive output and higher growth rates (Blanchette et al. 2007).

In benthic systems, biogenic habitats are often generated by dominant competitors, that is, species that monopolize the primary substratum, and establish a secondary substratum for smaller organisms (e.g. Bruno et al. 2003). Along the Chilean coast, Wieters (2005) has demonstrated how coastal upwelling may influence the individual traits of such facilitators, modifying the environment and determining the degree to which other species benefit, involving thus important consequences for community regulation. In intertidal rocky shores, mytilids create a 3-dimensional structure that consists of three major components: the mussel matrix, an assemblage of associated organisms and accumulated detritus (Suchanek 1985). These structures facilitate colonization by certain organisms (Suchanek 1978, 1985), which would either decrease in density or altogether disappear if mytilids did not exist on the rocky substratum (Tokeshi and Romero 2000). Ecosystem engineering (i.e. the creation, modification and maintenance of habitats by organisms, Jones et al. 1994) by mussels modifies their local environment (e.g. McKindsey and Bourget 2001) by mitigating desiccation stress (Helmuth 1998), buffering hydrodynamic forces (Bertness et al. 2006; O’Donnell 2008), providing refugia against predators (Borthagaray and Carranza 2007) and providing energy for the associated community (Norling and Kautsky 2007). Furthermore, by modifying heterogeneity and structural complexity (i.e. variation in habitat structure attributable to the absolute abundance of individual structural components, Beck 2000), shell size seems to play an important role influencing community structure of the assemblage associated with mussel beds (Tsuchiya and Nishihira 1986). For instance, larger shells usually support more individuals of a given fouling species and a greater richness of fouling species than smaller ones (see Gutiérrez et al. 2003).

The mytilid Perumytilus purpuratus (Lamarck, 1819; hereafter Perumytilus) inhabits the mid intertidal rocky shores in the south-eastern Pacific from Ecuador (2°00′ S 77°30′ W), down the west coast of South America to Cape Horn, and in the South Atlantic as far north as La Lobería, Argentina (41°8′ S 63°10′ W, Prado and Castilla 2006). The matrices that form Perumytilus harbour a great number of invertebrates and macroalgae (Alvarado and Castilla 1996; Prado and Castilla 2006). Previous studies suggest that on rocky shores, Perumytilus matrices primarily provide structural protection to the associated community, mainly composed of suspension-feeding organisms (Thiel and Ullrich 2002), while they trap sediment, affecting the composition of faunal assemblages and reducing evenness as sediment retention increases (Prado and Castilla 2006). Thus, Perumytilus can be considered a bioengineer playing a key role in structuring communities and determining local biodiversity on rocky shores of the south-eastern Pacific.

Despite the importance of biogenic habitats in structuring intertidal assemblages, it is not clear yet how their positive effects are related to other structuring processes in benthic communities (e.g. disturbance, predation, competition, primary production; Valdivia and Thiel 2006). Open, upwelling-dominated coastlines are thought to be less susceptible to the effects of additional nitrogen because of the large amount of nitrogen supplied by coastal upwelling (see Nielsen 2003). Moreover, previous studies have reported weaker responses to nutrient addition of primary and secondary producers as background nutrient increases (e.g. Posey et al. 2006; Teichberg et al. 2008), while along the Peruvian coast, upwelled nutrients may overwhelm the effects of anthropogenic inputs on the structure of intertidal communities (Firstater et al. 2010). On the other hand, since on rocky shores Perumytilus mainly provides structurally complex habitats, changes in structural complexity would affect the associated community regardless of the system productivity. Thus, we predict that in a nutrient-rich system, nutrient enhancement would have a minor effect on the assemblage associated with Perumytilus, whereas modification of mussel shell size would have larger effects on the Perumytilus assemblage. In this study, we experimentally examined in a nutrient-rich system, the effects of nutrient addition on the Perumytilus assemblage and we evaluated the potential effect of varying shell size on the Perumytilus assemblage.

Materials and methods

Study site

The study was performed on the rocky shore areas located south of Ancón Bay (11°46′ S, 77°11′ W; Fig. 1), on the Peruvian central coast. This area, subjected to a semidiurnal tidal cycle with an average amplitude of 0.54 m (Dirección de Hidrografía y Navegación 2006), is part of the Peruvian coastal upwelling ecosystem and is located within a main upwelling centre, receiving waters with high nutrient concentrations, low oxygen content and experiencing frequent phytoplanktonic blooms (Tarazona et al. 2003). In Ancón Bay, Perumytilus is commonly found in rock crevices of the upper-mid intertidal zone, forming dense beds in the mid zone, with an associated community that comprises up to 87 species (Paredes and Tarazona 1980).

Fig. 1
figure 1

Map of the area of Ancón Bay, indicating the study site (open circle)

Effects of nutrient supply on the assemblage of Perumytilus beds and microphytobenthic Chl-a

The responses to nutrient addition of the mussel-associated community and the microphytobenthic Chl-a on mussel shells were examined in a short-term field experiment in which nutrient level was manipulated. The experiment was conducted between April and June 2008. This timescale was considered appropriate since previous studies on the effects of nutrients on macroalgae, periphyton and mussel communities have detected significant responses after 2 months or less of continuous nutrient enrichment (e.g. Worm and Sommer 2000; Hillebrand and Kahlert 2001; Valdivia and Thiel 2006). Twenty plots (ten replicates per treatment: nutrient addition and control) were distributed in the mid intertidal zone, over a mussel bed of approximately 200 m2. Each plot consisted of a 10 × 10 cm area fully covered with mussels. Two small areas at the upper and lower edge of each plot (parallel to shoreline) were cleared from mussels in order to introduce fertilizer bags. The fertilizer bags (20 × 3 cm nylon bags with 1-mm mesh size) contained 60 g slow-release fertilizer (Multicote, Schultz Company, USA) with nitrogen (18%), phosphate (6%) and potassium (12%). This amount of fertilizer has been demonstrated to enhance nutrient availability over a wide range of nutrient background concentrations (Worm et al. 2000). The bags in experimental controls were filled with inert stones (for details, see Valdivia and Thiel 2006), and all bags were fixed to the rock with stainless screws. Unfortunately, due to methodological constraints in obtaining a reliable measure of nutrients from the plots, we could not directly assess the nutrient release in the mussel bed. However, slow-release fertilizer pellets increase nutrients in sediments and water column, remaining largely unaffected by wave exposure (see Worm et al. 2000 for review of enrichment methods).

At the end of the experiment, the mussels and the associated organisms were removed from the plots by scraping, taking care to collect all mobile fauna, and stored frozen in plastic bags. Samples were then sieved through a 1-mm mesh, and all organisms were identified to the lowest possible taxonomic level (usually genus or species). The invertebrates were counted, and dry mass of algae was determined by drying at 80°C to constant weight. Algal species were grouped into functional groups (foliose, corticated and thinly corticated) following Steneck and Dethier (1994). Faunal organisms were also classified according to their feeding habits (grazers, suspension-feeders, deposit-feeders and predators/scavengers) and mobility (sessile and mobile). This was done on the basis of morphological characteristics of specimens and available literature (see Valdivia and Thiel 2006).

Univariate and multivariate statistical analyses were performed to test the effects of nutrient addition on mussel assemblage. Separate t-tests were performed to analyse differences in mussel densities, total algal biomass, algal functional groups, total abundance of invertebrates, feeding guilds and mobility groups. Homogeneity of variances could not be achieved by any transformation for deposit-feeder data; therefore, raw data were analysed with the more conservative value of α = 0.01 (see Connell and Glasby 1999). Two separate sets of multivariate analyses were performed, one for macrofauna with abundance data and the other for algae with biomass data. Based on Bray-Curtis similarity matrices on fourth root-transformed data (Clarke and Warwick 2001), two one-way analyses of similarities (ANOSIMs) were performed (Clarke 1993). In addition, the percentage contributions of each taxon to patterns of dissimilarity between treatments were calculated (Clarke 1993), and taxa contributing to at least 10% of the dissimilarity were considered important differentiators (Bulleri 2005). The abundances of these taxa were then analysed by means of separate t-tests (Zar 1999).

Chl-a content, an indicator of total microalgal load, that provides an important food resource for grazers on exposed rocky shores (Thompson et al. 2004; Armitage et al. 2006), was measured on the mussel shells following an adaptation of the method proposed by Thompson et al. (1999). For this, two mussels (~25-mm shell length) were selected from each sample, cleaned from all visible macroalgae, dissected and soft tissue carefully removed from their valves. One empty valve from each individual was then placed in a single container with 100% ethanol. After 7 h of pigment extraction, Chl-a biomass was determined with a spectrophotometer. After extraction, digital pictures of the shells were taken and their 2-dimensional surface areas were measured with image analyser software (ImageJ 1.4). Averaged content of Chl-a was then expressed as µg cm−2. Differences in Chl-a biomass between treatments were evaluated with a t-test.

Effects of mussel size on the assemblage

To test the effect of Perumytilus size on the community structure, a transplant experiment with small (shell length 6–17 mm) and large (shell length > 30 mm) mussels was performed in May 2007. These size ranges were chosen to represent the natural size variability in the study area determined on the basis of the size frequency distribution plot. Mussels were cleaned of epifauna and groups of ~50 small and ~6 large mussels, respectively, were placed in net bags (10-mm mesh) occupying a standardized total volume of ~30 cm3. Bags were placed in two 6-l buckets filled with seawater for 1 day to stimulate attachment of byssal threads between mussels. Twelve bags of each treatment were then randomly fastened to a patch of bare rock in the mid intertidal zone with stainless screws. After 80 days, in August 2007, all organisms were removed from bags. They were identified to the lowest possible taxonomic level, counted, including epibiont barnacles, and classified as described previously. Macroalgae were not quantified because they settled mainly on net bags. As many mussels disappeared from several bags, analyses were restricted to those with more than 20 small (n = 7) and at least 4 large mussels (n = 7).

The amount of interstitial space (i.e. the available space among mussels, see Bartholomew et al. 2000) and total sample volume was estimated. Retrieved mussels (4–6 large and 24–64 small mussels, see “Results”) were cleaned and placed in jars (120 mm height × 60 mm diameter), crowded as they occur in natural beds. Inside the jars, large mussels were mono or two layered, whereas small mussels were four to seven layered. Then, jars were filled with water until all mussels were covered. Gap volume within mussels was then estimated as the total volume of water added. Finally, individual shell areas were estimated based on calculation for the area of an ellipse (with shell length and width as major and minor axes, respectively). Differences in total sample volume, gap volume and total shell area between small and large mussels were examined with t-tests. Homoscedasticity could not be achieved for total sample volume and shell area data. For these variables, raw data were therefore analysed with α = 0.01 (see above).

Two sets of analyses on abundance data, one standardized per cm2 of the total sample shell area and another standardized per cm3 of gap volume, were used to explore the differences in species composition between mussel sizes. Multivariate analyses were performed as described previously and the abundances of the most important differentiators (species that contribute at least 10% of the dissimilarity) were analysed by means of separate t-tests. Additionally, the differences in total abundance, feeding guilds and mobility groups of invertebrates were examined with separate t-tests. Abundance data of Semimytilus algosus (Gould, 1850), Jehlius cirratus (Darwin, 1854), grazers, suspension-feeders, mobile and sessile organisms, and total abundance were transformed to X0.25 to meet t-test assumptions. Univariate analysis on deposit-feeders data was not performed because these were only found in one sample of each treatment.

The use of replicate experimental sites, taking into account the spatial variability in the responses of organisms (Chapman 2000), would have ensured the generality of our results; however, constraints of feasibility and appropriate access to similar areas prevented us from using replicate sites. Consequently, our inferences are restricted to the studied area.

Results

Effects of nutrient supply on the assemblage of Perumytilus beds and microphytobenthic Chl-a

Twenty-six taxa were found in the Perumytilus bed (Table 1). Mussel density (mean = 89.3 individuals per 100 cm2, SD = 32.4) was not different between nutrient addition and control plots (t = −1.18, df = 17, P = 0.25). There were no differences in total algal biomass, total abundance of invertebrates and abundances of the feeding groups between treatments (Table 2; Figs. 2, 3).

Table 1 Invertebrates associated with Perumytilus purpuratus during nutrient addition and transplant experiments
Table 2 Results of t-tests on algal total biomass, invertebrates’ total abundance and functional groups of Perumytilus purpuratus assemblage in mussel bed fertilization experiment
Fig. 2
figure 2

Effect of nutrient addition on total biomass of different algal functional groups of Perumytilus purpuratus bed assemblages (median; box, 25th to 75th percentiles; whiskers, 5th to 95th percentiles)

Fig. 3
figure 3

Effect of nutrient addition on total abundance, faunal feeding guilds and mobility groups of Perumytilus purpuratus bed assemblages (median; box, 25th to 75th percentiles; whiskers, 5th to 95th percentiles)

Analysis of similarities for algae and invertebrates did not reveal differences in the species composition between treatments (ANOSIM global R = −0.03 and −0.02 for algae and invertebrates, respectively, P = 0.6 for both). Finally, there were no differences in Chl-a biomass on mussel surface between nutrient addition (mean = 0.39 µg cm−2, SD = 0.28) and controls (mean = 0.23 µg cm−2, SD = 0.18; t = −1.46, df = 17, P = 0.16).

Effects of mussel size on the assemblage

Total sample volume did not differ between treatments (t = −0.3, df = 12, P = 0.77), ranging from 17.3 to 25.9 cm3 for large mussels (4–6 retrieved mussels) and from 11.3 to 34.5 cm3 for small mussels (24–64 retrieved mussels). Gaps within large mussels were more than threefold larger than within small mussels (t = −8.54, df = 12, P < 0.001). However, there were no differences between total shell areas (t = −0.1, df = 12, P = 0.92).

A total of 14 invertebrates species were found in transplants (Table 1). The analysis of similarity (ANOSIM) revealed significant differences between mussel size treatments when comparing structure of faunal assemblages per cm2 of total shell area (R = 0.196, P = 0.01); moreover, these differences increased when comparing structure per cm3 of gap (R = 0.348, P = 0.001).

The barnacle Jehlius cirratus, Semimytilus algosus recruits and the sessile polychaete Phragmatopoma moerchi (Kinberg, 1867) contributed most to the differences between treatments, accounting for 23.3, 14.8 and 11.6% of the dissimilarity by cm2 of total shell area, and 17.6, 17.8 and 10% by cm3 of gap, respectively. The polychaete Pseudonereis gallapagensis (Kinberg, 1866) was also an important differentiator when analysing gaps (10.7% of the dissimilarity).

When analysing abundances per cm2 of total shell area, density of Jehlius cirratus was higher on large mussels, but no further difference was detected by univariate tests (Table 3; Fig. 4). When considering abundances per cm3 of gap, Pseudonereis gallapagensis was the only species with higher abundance in samples with small mussels. With respect to functional groups, predators, grazers and mobile organisms were also more abundant among small mussels. On the other hand, the abundances of Semimytilus algosus recruits, Jehlius cirratus, suspension-feeders, sessile and total abundance did not vary between treatments (Table 3; Fig. 4).

Table 3 Results of t-tests on most important differentiators and functional groups in mussel transplant experiment
Fig. 4
figure 4

Effect of Perumytilus purpuratus size on total abundance, feeding guilds and mobility groups of associated fauna, standardized by a cm2 of total shell area and b cm3 of gap (median; box, 25th to 75th percentiles; whiskers, 5th to 95th percentiles). Letters denote significant differences (α < 0.05)

Discussion

Effects of nutrient supply on the assemblage of Perumytilus beds and microphytobenthic Chl-a

The extent to which the ecosystem engineering effects of habitat-forming organisms may depend on environmental conditions remains largely unexplored (Wright and Jones 2006; Menge et al. 2008). The results of our experimental nutrient addition to the Perumytilus bed agree with previous studies, finding no response of microalgal biomass and only weak response of the macrofaunal abundance to local nutrient enrichment in areas with high levels of background nutrients (Posey et al. 2006; Valdivia and Thiel 2006). It is likely that local nutrient enrichment alone may be insufficient in stimulating structural changes in exposed rocky shore communities (Bokn et al. 2003; Thompson et al. 2004).

Nutrient addition did not result in increased microphytobenthos on the surface of Perumytilus shells, which may be due to several reasons. Nitrogen availability and herbivores have strong and antagonistic effects on microalgal biomass, species composition and diversity (Hillebrand et al. 2000). Since grazers could freely enter our fertilized plots, it is possible that their effect might have prevented biofilm growth. Since nutrient addition increases food quality and thereby attract grazers (Worm and Sommer 2000), a higher abundance of grazers would be expected in enriched plots; however, abundances were similar between treatments. This could be due to the high mobility of grazers that allow them to quickly move within the mussel bed (Valdivia and Thiel 2006). Moreover, a meta-analysis on experiments with periphyton (Hillebrand 2002) has shown that even in high-productivity areas, grazing pressure increases with increasing nitrogen availability. Thus, enrichment would lead to increased microalgal biomass (bottom–up effect), but grazers would also remove more biomass in enriched nutrient plots (top–down effect, Sommer 1999; Hillebrand et al. 2000). The exclusion of grazers combined with our nutrient enrichment treatment would have provided a valuable insight into the relative strength of bottom–up and top–down control on biofilm; however, the use of cumbersome devices to manipulate mobile grazers in the mussel bed would have probably distorted natural conditions as well (see Parker et al. 1993).

Regarding the associated fauna, the abundance of single species or feeding groups remained unaffected by nutrient addition. Up to 92 associated species were registered in the Perumytilus beds of the Peruvian and Chilean shores (Paredes and Tarazona 1980, Prado and Castilla 2006). In this study, the number of taxa reported (26) is thought to be underestimated since some groups, such as the polychaete Syllis or the limpet Scurria, may contain at least 3 and 4 species, respectively, which could not be distinguished (see Tokeshi and Romero 1995). Nevertheless, the results of our analyses are still valid for interpretation since they were based on the abundances of feeding groups. Invertebrate assemblages associated with Perumytilus beds were dominated by sessile suspension-feeders (barnacles and anemones), followed by grazers (chitons and limpets) and other groups. Thus, as suggested for assemblages of mussel beds from the Chilean shore (Thiel and Ullrich 2002), most organisms obtain their feeding resources from the water column rather than from materials deposited on or by the mussels, using mussel shells as structural support.

Effects of mussel size on the assemblage

There were no changes in the species composition related to mussel size. However, differences in densities of single species and feeding groups were observed when analysing densities both per area and interstitial volume of small and large mussels. All species that differed between mussel sizes were sessile. The barnacle Jehlius cirratus was more abundant per unit area among large mussels, and the tube-building polychaete Phragmatopoma moerchi was restricted to large mussels, although the total shell surface areas of small and large mussels were similar. The microtopography and chemical properties of the shell surface are important factors controlling the settlement of epibionts on mytilids (Bers et al. 2010); however, it is possible that larvae that actively explore the substratum before settling, such as barnacle cyprids, selected the larger and continuous surface of large mussels reducing, thus, the risk of overgrowing the substratum organisms (i.e. the mussel) and inducing further the settling of conspecifics (Thompson et al. 1998; Wahl 2009).

Differences in the structure of the associated community increased when analysing abundances per unit volume of interstitial space. At this level, Jehlius cirratus, Semimytilus algosus recruits and Phragmatopoma moerchi were also identified as differentiators between differently sized mussels. Moreover, the polychaete Pseudonereis gallapagensis, a large free-ranging predator, contributed to distinguish between treatments and was more abundant among small mussels. Even though there was more interstitial space among large mussels, more grazers, predators and mobile organisms per unit volume were also found in small mussel gaps. The internal structure of mussel interstitial space, filled with sediment, byssal threads and shell fragment favours occupancy by a variety of small animals through creation of several microhabitats (Tsuchiya and Nishihira 1985, 1986). Our measures of interstitial volume did not take into account these components; however, we can speculate about an enhancement of habitat complexity within small mussels compared with larger ones. Habitat complexity can have strong effects on the local distributions of some intertidal organisms (Beck 2000). In transplants, smaller and denser mussels constituted a more complex matrix, which could provide a more suitable environment, reducing desiccation and improving protection for mobile fauna that can actively select their habitat (Tsuchiya and Nishihira 1986).

In our transplant experiment, the total sample volumes were similar; thus, differences in mussel size entailed differences in density. An increase in almost threefold shell length represented a reduction of about 8.5-fold in the number of mussels per unit volume. Similar relationships between size and density have been observed when sampling natural patches per unit area (Tsuchiya and Nishihira 1986). Therefore, it is not surprising to find variation in macroinvertebrate densities that are often positively related to mussel densities (e.g. Vaughn and Spooner 2006). Moreover, since interactions at the population level, playing an important role in the space regulation in the Perumytilus bed, are highly density dependent (e.g. self-thinning, Guiñez and Castilla 1999), an additional transplant experiment varying mussel size and keeping density constant would have allowed us to decouple both structural elements, adding some valuable insight into mechanisms underlying space occupancy.

Coastal upwelling, by altering the primary production over the large scale, may control trait-dependent habitat modification and regulate the relative importance of facilitation in marine rocky intertidal communities (Wieters 2005). In Ancón Bay, local nutrient addition did not result in the enhancement of primary production or changes in the community structure of the Perumytilus bed, but differences in mussel size led to variation in habitat structure which was reflected in the lower densities of many associated organisms among larger mussels. Present results suggest that in upwelling areas, where nutrient would not be a limiting factor, local nutrient enhancement would not significantly affect Perumytilus and its assemblage, whereas biologically generated structural habitat seems to play an important role in shaping this community. However, since this study was conducted at a single site, further experiments spanning larger spatial scales are necessary to determine the generality of these findings within nutrient-rich areas, while consumer manipulation would also elucidate the role of grazing in controlling primary production.

References

  • Alvarado JL, Castilla JC (1996) Tridimensional matrices of mussels Perumytilus purpuratus on intertidal platforms with varying wave forces in central Chile. Mar Ecol Prog Ser 133:135–141

    Article  Google Scholar 

  • Armitage AR, Frankovich TA, Fourqurean JW (2006) Variable responses within epiphytic and benthic microalgal communities to nutrient enrichment. Hydrobiologia 569:423–435

    Article  CAS  Google Scholar 

  • Bartholomew A, Diaz RJ, Cicchetti G (2000) New dimensionless indices of structural habitat complexity: predicted and actual effects on a predator’s foraging success. Mar Ecol Prog Ser 206:45–58

    Article  Google Scholar 

  • Beck MW (2000) Separating the elements of habitat structure: independent effects of habitat complexity and structural components on rocky intertidal gastropods. J Exp Mar Biol Ecol 249:29–49

    Article  PubMed  Google Scholar 

  • Bers AV, Díaz ER, da Gama BAP, Vieira-Silva F, Dobretsov S, Valdivia N, Thiel M, Scardino AJ, McQuaid CD, Sudgen HE, Thomason JC, Wahl M (2010) Relevance of mytilid shell microtopographies for fouling defence–a global comparison. Biofouling 26:367–377

    Article  Google Scholar 

  • Bertness MD, Crain CM, Silliman BR, Bazterrica MC, Reyna MV, Hidalgo F, Farina JK (2006) The community structure of western Atlantic Patagonian rocky shores. Ecol Monogr 76:439–460

    Article  Google Scholar 

  • Blanchette CA, Helmuth B, Gaines SD (2007) Spatial patterns of growth in the mussel, Mytilus californianus, across a major oceanographic and biogeographic boundary at Point Conception, California, USA. J Exp Mar Biol Ecol 340:126–148

    Article  Google Scholar 

  • Bokn TL, Duarte CM, Pedersen MF, Marba N, Moy FE et al (2003) The response of experimental rocky shore communities to nutrient additions. Ecosystems 6:577–594

    Article  CAS  Google Scholar 

  • Borthagaray AI, Carranza A (2007) Mussels as ecosystem engineers: their contribution to species richness in a rocky littoral community. Acta Oecol 31:243–250

    Article  Google Scholar 

  • Bosman AL, Hockey PAR, Siegfried WR (1987) The influence of coastal upwelling on the functional structure of rocky intertidal communities. Oecologia 72:226–232

    Article  Google Scholar 

  • Bruno JF, Stachowicz JJ, Bertness MD (2003) Inclusion of facilitation into ecological theory. Trends Ecol Evol 18:119–125

    Article  Google Scholar 

  • Bulleri F (2005) Experimental evaluation of early patterns of colonisation of space on rocky shores and seawalls. Mar Environ Res 60:355–374

    Article  PubMed  CAS  Google Scholar 

  • Bustamante RH, Branch GM, Eekhout S, Robertson B, Zoutendyk P et al (1995) Gradients of intertidal primary productivity around the coast of South Africa and their relationships with consumer biomass. Oecologia 102:189–201

    Article  Google Scholar 

  • Chapman MG (2000) Poor design of behavioural experiments gets poor results: examples from intertidal habitats. J Exp Mar Biol Ecol 250:77–95

    Article  PubMed  Google Scholar 

  • Clarke KR (1993) Non-parametric multivariate analysis of changes in community structures. Aust J Ecol 18:117–143

    Article  Google Scholar 

  • Clarke KR, Warwick RM (2001) Change in marine communities: an approach to statistical analysis and interpretation, 2nd edn. PRIMER-E, Plymouth

    Google Scholar 

  • Connell SD, Glasby TM (1999) Do urban structures influence local abundance and diversity of subtidal epibiota? A case study from Sydney Harbour, Australia. Mar Environ Res 47:373–387

    Article  CAS  Google Scholar 

  • Dirección de Hidrografía y Navegación (2006) Tabla de mareas 2006. Puertos de la costa del Perú, Océano Pacífico—América del Sur. Ministerio de Defensa, Marina de Guerra del Perú, República del Perú

  • Firstater FN, Hidalgo FJ, Lomovasky BJ, Tarazona J, Flores G, Iribarne OO (2010) Coastal upwelling may overwhelm the effect of sewage discharges in rocky intertidal communities of the Peruvian coast. Mar Freshw Res 61:309–319

    Article  CAS  Google Scholar 

  • Guiñez R, Castilla JC (1999) A tridimensional self-thinning model for multilayered intertidal mussels. Am Nat 154:341–357

    Article  PubMed  Google Scholar 

  • Gutiérrez JL, Jones CG, Strayer DL, Iribarne OO (2003) Mollusks as ecosystem engineers: the role of shell production in aquatic habitats. Oikos 101:79–90

    Article  Google Scholar 

  • Helmuth BST (1998) Intertidal mussel microclimates: predicting the body temperature of a sessile invertebrate. Ecol Monogr 68:51–74

    Article  Google Scholar 

  • Hillebrand H (2002) Top-down versus bottom-up control of autotrophic biomass: a meta-analysis on experiments with periphyton. J N Am Benthol Soc 21:349–369

    Article  Google Scholar 

  • Hillebrand H, Kahlert M (2001) Effect of grazing and nutrient supply on periphyton biomass and nutrient stoichiometry in habitats of different productivity. Limnol Oceanogr 46:1881–1898

    Article  CAS  Google Scholar 

  • Hillebrand H, Worm B, Lotze HK (2000) Marine microbenthic community structure regulated by nitrogen loading and grazing pressure. Mar Ecol Prog Ser 204:27–38

    Article  CAS  Google Scholar 

  • Jones CG, Lawton JH, Shachak M (1994) Organisms as ecosystem engineers. Oikos 69:373–386

    Article  Google Scholar 

  • Mc Kindsey CW, Bourget E (2001) Diversity of a northern rocky intertidal community: the influence of body size and succession. Ecology 82:3462–3478

    Article  Google Scholar 

  • Menge BA (1992) Community regulation: under what conditions are bottom-up factors important on rocky shores? Ecology 73:755–765

    Article  Google Scholar 

  • Menge BA, Daley BA, Wheeler PA, Dahlhoff E, Sanford E, Strub PT (1997) Benthic-pelagic links and rocky intertidal communities: bottom-up effects on top-down control? Proc Natl Acad Sci USA 94:14530–14535

    Article  PubMed  CAS  Google Scholar 

  • Menge BA, Daley BA, Lubchenco J, Sanford E, Dahlhoff E et al (1999) Top-down and bottom-up regulation of New Zealand rocky intertidal communities. Ecol Monogr 69:297–330

    Article  Google Scholar 

  • Menge BA, Chan F, Lubchenco J (2008) Response of a rocky intertidal ecosystem engineer and community dominant to climate change. Ecol Lett 11:151–162

    PubMed  Google Scholar 

  • Nielsen KJ (2003) Nutrient loading and consumers: agents of change in open-coast macrophyte assemblages. Proc Natl Acad Sci USA 100:7660–7665

    Article  PubMed  CAS  Google Scholar 

  • Norling P, Kautsky N (2007) Structural and functional effects of Mytilus edulis on diversity of associated species and ecosystem functioning. Mar Ecol Prog Ser 351:163–175

    Article  Google Scholar 

  • O’Donnell MJ (2008) Reduction of wave forces within bare patches in mussel beds. Mar Ecol Prog Ser 362:157–167

    Article  Google Scholar 

  • Paredes C, Tarazona J (1980) Las comunidades de mitílidos del mediolitoral rocoso del Departamento de Lima. Rev Peru Biol 2:59–71

    Google Scholar 

  • Parker T, Johnson C, Chapman ARO (1993) Gammarid amphipods and littorinid snails have significant but different effects on algal succession in littoral fringe tidepools. Ophelia 38:69–88

    Google Scholar 

  • Posey MH, Alphin TD, Cahoon L (2006) Benthic community responses to nutrient enrichment and predator exclusion: influence of background nutrient concentrations and interactive effects. J Exp Mar Biol Ecol 330:105–118

    Article  CAS  Google Scholar 

  • Prado L, Castilla JC (2006) The bioengineer Perumytilus purpuratus (Mollusca:Bivalvia) in Central Chile: biodiversity, habitat structural complexity and environmental heterogeneity. J Mar Biol Ass UK 86:417–421

    Article  Google Scholar 

  • Sommer U (1999) The susceptibility of benthic microalgae to periwinkle (Littorina littorea, Gastropoda) grazing in laboratory experiments. Aqua Bot 63:11–21

    Article  Google Scholar 

  • Steneck RS, Dethier MN (1994) A functional group approach to the structure of algal-dominated communities. Oikos 69:476–498

    Article  Google Scholar 

  • Suchanek TH (1978) The ecology of Mytilus edulis L in exposed rocky intertidal communities. J Exp Mar Biol Ecol 31:105–120

    Article  Google Scholar 

  • Suchanek TH (1985) Mussels and their role in structuring rocky shore communities. In: Moore PG, Seed R (eds) The ecology of rocky coasts. Hodder & Stoughton, London, pp 70–96

    Google Scholar 

  • Tarazona J, Gutiérrez D, Paredes C, Indacochea A (2003) Overview and challenges of marine biodiversity research in Peru. Gayana 67:206–231

    Google Scholar 

  • Teichberg M, Fox SE, Aguila C, Olsen YS, Valiela I (2008) Macroalgal responses to experimental nutrient enrichment in shallow coastal waters: growth, internal nutrient pools, and isotopic signatures. Mar Ecol Prog Ser 368:117–126

    Article  CAS  Google Scholar 

  • Thiel M, Ullrich N (2002) Hard rock versus soft bottom: the fauna associated with intertidal mussel beds on hard bottoms along the coast of Chile, and considerations on the functional role of mussel beds. Helgol Mar Res 56:21–30

    Article  Google Scholar 

  • Thompson RC, Norton TA, Hawkins SJ (1998) The influence of epilithic microbial films on the settlement of Semibalanus balanoides cyprids–a comparison between laboratory and field experiments. Hydrobiologia 375(376):203–216

    Article  Google Scholar 

  • Thompson RC, Tobin ML, Hawkins SJ, Norton TA (1999) Problems in extraction and spectrophotometric determination in chlorophyll from epilithic microbial biofilms: towards a standard method. J Mar Biol Ass UK 79:551–558

    Article  CAS  Google Scholar 

  • Thompson RC, Norton TA, Hawkins SJ (2004) Physical stress and biological control regulate the producer-consumer balance in intertidal biofilms. Ecology 85:1372–1382

    Article  Google Scholar 

  • Tokeshi M, Romero L (1995) Filling a gap: dynamics of space occupancy on a mussel-dominated subtropical rocky shore. Mar Ecol Prog Ser 119:167–176

    Article  Google Scholar 

  • Tokeshi M, Romero L (2000) Spatial overlap and coexistence in a mussel-associated polychaete assemblage on a South American rocky shore. Mar Ecol 21:247–261

    Article  Google Scholar 

  • Tsuchiya M, Nishihira M (1985) Islands of Mytilus as a habitat for small intertidal animals: effect of island size on community structure. Mar Ecol Prog Ser 25:75–85

    Article  Google Scholar 

  • Tsuchiya M, Nishihira M (1986) Islands of Mytilus edulis as a habitat for small intertidal animals: effect of Mytilus age structure on the species composition of the associated fauna and community organization. Mar Ecol Prog Ser 31:171–178

    Article  Google Scholar 

  • Valdivia N, Thiel M (2006) Effects of point-source nutrient addition and mussel removal on epibiotic assemblages in Perumytilus purpuratus beds. J Sea Res 56:271–283

    Article  Google Scholar 

  • Vaughn CC, Spooner DE (2006) Unionid mussels influence macroinvertebrate assemblage structure in streams. J N Am Benthol Soc 25:691–700

    Article  Google Scholar 

  • Wahl M (2009) Epibiosis: ecology, effects and defences. In: Wahl M (ed) Marine hard bottom communities. Patterns, dynamics, diversity, and changes. Ecological studies 206. Springer, Berlin, pp 61–69

    Google Scholar 

  • Wieters EA (2005) Upwelling control of positive interactions over mesoscales: a new link between bottom-up and top-down processes on rocky shores. Mar Ecol Prog Ser 301:43–54

    Article  Google Scholar 

  • Worm B, Sommer U (2000) Rapid direct and indirect effects of a single nutrient pulse in a seaweed-epiphyte-grazer system. Mar Ecol Prog Ser 202:283–288

    Article  Google Scholar 

  • Worm B, Reusch TBH, Lotze HK (2000) In situ nutrient enrichment: methods for marine benthic ecology. Internat Rev Hydrobiol 85:359–375

    Article  CAS  Google Scholar 

  • Wright JP, Jones CG (2006) The concept of organisms as ecosystem engineers ten years on: progress, limitations, and challenges. Bioscience 56:203–209

    Article  Google Scholar 

  • Zar JH (1999) Biostatistical analysis, 2nd edn. Prentice Hall, New Jersey

    Google Scholar 

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Acknowledgments

We thank Dr. J. Tarazona for laboratory resources, P. Gallegos, C. Paredes and A. Gamarra for collaborating in species identification and for their remarks, and three anonymous referees for their careful reviews of the manuscript and important suggestions. F. N. F. is particularly indebted to G. Caille for his guidance and encouragement. This study was conducted and financed in the framework of the EU-project CENSOR (Climate variability and El Niño Southern Oscillation: Implications for natural resources and management, contract 511071) and is CENSOR publication No. 0382.

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Correspondence to Fausto N. Firstater.

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Communicated by Martin Thiel.

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Firstater, F.N., Hidalgo, F.J., Lomovasky, B.J. et al. Habitat structure is more important than nutrient supply in modifying mussel bed assemblage in an upwelling area of the Peruvian coast. Helgol Mar Res 65, 187–196 (2011). https://doi.org/10.1007/s10152-010-0214-3

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