You are on page 1of 6

J. Mar. Biol. Ass. U.K.

(2006), 86, 417^421 Printed in the United Kingdom

The bioengineer Perumytilus purpuratus (Mollusca: Bivalvia) in central Chile: biodiversity, habitat structural complexity and environmental heterogeneity
Luis Prado* and Juan Carlos Castilla*O
gicas, *Center for Advanced Study of Ecology and Biodiversity, Facultad de Ciencias Biolo lica de Chile, Casilla 114-D, Santiago, Chile. Ponticia Universidad Cato O Corresponding author, e-mail:

The mussel Perumytilus purpuratus is distributed from Ecuador to the Strait of Magellan on the Pacic coast; and also extends along the Atlantic coast up to La Lober| a, Argentina. The species forms dense three-dimensional matrices which constitute a microhabitat for a wide variety of organisms. Here we test the hypothesis that factors determining habitat structural complexity and environmental heterogeneity of Perumytilus matrices have signicant eects on the associated macrofaunal community. In total we found 92 invertebrate taxa in P. purpuratus matrices. The number of layers (stratication) in the matrix had a signicant eect on evenness: the greater the stratication, the lower the evenness index. Sediment retention by matrices in sheltered sectors had a signicant eect on evenness: greater sediment retention resulted in lower evenness. Sediment retention also determined signicant dierences in macrofaunal assemblages. In matrices without sediment retention, mussel layering and the presence of algae on the shells of P. purpuratus determined signicant macrofaunal dierences. As a dominant competitor, P. purpuratus plays a major role in intertidal rocky shores where it is present, structuring communities and determining local biodiversity.

Ecosystem engineer species (Jones et al., 1994) modulate the availability of resources for other species and may change the physical structure, complexity and heterogeneity of the environment. Autogenic engineers provide habitat for other species, playing an important role in the structure of associated communities. An example is the small mussel (maximum shell length 40 mm) Perumytilus purpuratus (Lamarck, 1819), which inhabits the midintertidal rocky shores in the south-eastern Pacic from Ecuador (2800S 77830W), down the west coast of South America to Cape Horn and round into the South Atlantic, as far north as La Lober| a, Argentina (41880 S 638100 W) (Zagal & Hermosilla, 2001; L. Prado personal observations). This species forms dense three-dimensional matrices (Alvarado & Castilla, 1996) constituting a microhabitat which reduces desiccation during low tides and increases protection against the mechanical eects of waves. The existence of an elevated number of invertebrates and macroalgae (the latter settling on mussel valves) has been shown to occur in P. purpuratus matrices (De Amesti, 1994). Studies have addressed the eect of mussel habitat structural complexity: (e.g. depth of mussel matrix, macroalgae attached to shells, sand retention) or size of the patch area, and environmental heterogeneity (wave exposure, tidal height) on mussel associated fauna. For example, the area of mussel patches has been positively correlated with species richness (Tsuchiya & Nishihira, 1985); the retention of sediment has been correlated with increases in the diversity of mussel associated macrofauna (Gibbons, 1988). Also, tidal height has a
Journal of the Marine Biological Association of the United Kingdom (2006)

signicant eect on mussel matrix species richness: those located at higher intertidal levels show lower species richness than those at lower levels (Suchanek, 1980). Despite the potential importance of these factors in structuring macrofaunal communities associated with mussels, there are no studies which have simultaneously considered the inuence of mussel habitat complexity and environmental heterogeneity on structuring associated communities. In this paper we test the hypothesis that species richness, evenness and faunal assemblages of macrofauna associated with matrices of Perumytilus purpuratus vary signicantly with mussel habitat complexity (number of layers in the matrix, sediment retention, the presence/absence of algae attached to mussel shells), or environmental heterogeneity (wave exposure).


Sampling location, wave exposure and mussel matrices

The Bay of Punta de Tralca (32835S 71870W, Figure 1) has extensive Perumytilus purpuratus intertidal matrices. During September 2002 we randomly sampled these matrices considering the following variables: (1) wave exposure and mussel sediment retention. We selected two sampling sectors inside the bay and one sector outside, each sector was 200 m of coastline (Figure 1): Sector 1 (Punta de Tralca center of the bay, PT-C); Sector 2 (Southern Area, outside of the bay, SA); Sector 3 (Punta de Tralca headland, PT-H). They presented notable dierences: Sector 1 consists of rocks on a gravel-sandy beach where mussel matrices continuously trap sediment. In


L. Prado and J.C. Castilla

Biodiversity, complexity and heterogeneity in Perumytilus purpuratus Following taxonomic identication, sediment samples were dried for 72 h at 508C and weighed using a digital scale (0.01g precision). Specimens were determined to the lowest taxonomic level possible.
Statistical analyses

Figure 1. Sampling sectors in Punta de Tralca, central Chile.

contrast, Sectors 2 and 3 are located in and around massive rock platforms where sediment retention is minimal. (2) Stratication of the mussel matrices. Stratication was determined using two protocols: (a) a specially designed mussel matrix-depth instrument in the eld. The device was a 177.5 cm high-density plastic L-shaped ruler attached to a scale graduated in millimetres and a sti, 3.5 mm diameter, wire (Prado, 2004). For each quadrat the wire was inserted six times into the mussel matrix and the depth was recorded using a millimetre scale. Matrices were classied as monolayered (around 2 cm depth) and multilayered (around 3.5 cm depth); (b) using a theoretical mussel depth approximation, based on mussel sizes (Guin ez & Castilla, 1999). (3) Algal cover (mainly Gelidium, Centroceras, ulvoids) attached to the valves of P. purpuratus. Mussel matrices were classied as present (fully covered) or absent (uncovered) with algae. Five replicates per treatment were used.
Exposure and estimation of maximum wave velocity

We evaluated signicant dierences using three-way analysis of variance (ANOVA), considering mussel matrix layering (L), the presence/absence of algae (A) and wave exposure-sediment (E). Response variables were: species richness (R) and evenness (J). We used SAS 6.3 software, with PROC MIXED for maximum likelihood calculations and PROC GLM adjusted for least squares, Minitab 12.1. Assumptions for homogeneity of variance (Levenes test) and normality (Kolmogorov ^Smirnov test) were checked for prior to analyses; we used Log (x+1) transformation when necessary. T o analyse dierences in faunal assemblages of the community associated with P. purpuratus we used non-metric multidimensional scaling (n-MDS) and non-parametric multivariate analyses of variance (np-MANOVA) (Anderson, 2001). Using the SIMPER algorithm (Clarke, 1993) we evaluated the main species determining assemblage dierences.

Characterization of the sampling sectors

T o characterize wave exposure in each of the sampling sectors, we measured maximum wave velocity (VMAX, Castilla et al., 1998) for ve days: 6 and 20 November and 19^21 December 2002. Each time we used 15 dynamometers (Bell & Denny, 1994) in each sector and considered the maximum value recorded by each dynamometer during the sampling period, calculating the average VMAX for each sector.
Mussel and macrofaunal sampling

Average maximum wave velocity (VMAX) in Sectors 1, 2 and 3 were 9.52, 10.99 and 11.07 (m s71) respectively (Figure 2A). Sector 1 had the lowest wave exposure (sheltered) and was signicantly dierent (three-way ANOVA, P50.05) from Sectors 2 and 3, which did not dier signicantly from each other. The amount of sediment trapped inside the matrices showed signicant dierences: mussels in Sector 1 trapped large amounts of sediment, varying between 87 and 268 g per sample. Sectors 2 and 3 trapped less that 1g of sediment (Figure 2B).
Habitat structural complexity of mussel matrices

The fauna associated with mussels was sampled using a wire quadrat of 225 cm2 (1515 cm). This size represented the minimum area necessary to accurately sample the fauna associated with Perumytilus matrices (Prado, 2004). Mussel associated invertebrates and macro algae attached to mussel valves were collected using a metallic scraper and a hand vacuum collector (enhancing collection of n motile individuals). Samples were transported to Estacio Costera de Investigaciones Marinas (ECIM), Las Cruces, lica de Chile, and stored at Ponticia Universidad Cato 7208C. The macrofauna (larger than 300 microns) was sorted manually and stored in 70% alcohol. Macroalgae were stored in vials at 7208C. The sediment was collected and stored in plastic ziplock bags, in 70% alcohol.
Journal of the Marine Biological Association of the United Kingdom (2006)

According to eld determinations, depth of monolayered and multilayered mussel matrices varied between 2.02 ( 0.1) cm and 3.56 ( 0.1) cm, respectively. The dierence between mono and multilayered depth matrices among the sectors was signicant (three-way ANOVA, P50.01). On the other hand, the theoretical number of layers (Guin ez & Castilla, 1999) varied between 0.97 and 1.47 for monolayered and multilayered matrices, respectively. In this case there was a signicant dierence for

Figure 2. (A) Maximum wave velocity (VMAX); and (B) amount of sediment retained in mussel beds in the three sampling sectors of Punta de Tralca. Bars represent averages and the lines above, standard error.

Biodiversity, complexity and heterogeneity in Perumytilus purpuratus

L. Prado and J.C. Castilla


Table 1. List of macrofauna associated with matrices of Perumytilus purpuratus in Punta de Tralca, central Chile.
CNIDARIA Phymactis clematis Anthothoe chilensis NEMERTEA Lineus atrocaeruleus Amphiporus nelsoni ANNELLIDA Perinereis falklandica Pseudonereis gallapaguensis Polychaeta n.i. Nereididae non det. (juv.) Cirratulidae non det. Halosydna patagonica Halosydna sp. Arabella cincta Lumbrineris magalhaensis Boccardia tricuspa Oligochaeta non det. T erebella sp. Eulalia sp. T yposyllis magdalena T yposyllis lidentata T yposyllis sp. Marphysa aenea NEMATODA Nematoda non det. MOLLUSCA Brachidontes granulata Semimytilus algosus Aulacomya atra Lasaea petitiana Veneridae non det. Entodesma cuneata Scurria ceciliana Scurria variabilis Scurria plana Scurria zebrina Scurria araucana Fissurella crassa Fissurella maxima Fissurella cumingi T egula atra Prissogaster niger Tricolia umbilicata Dendropoma sp. Calyptraea trochiformis Caecum chilensis Nodilittonina araucana Eatoniella nigra Eatoniella glomerosa Acanthina monodon Concholepas concholepas Siphonaria lessoni Onchidiella marginata Acanthopleura echinata Chiton granosus Chiton barnesi Polyplacophora non det. Chaetopleura benaventei Chaetopleura peruviana T onicia sp. Callistochiton viviparus ARTHROPODA Jehlius cirratus Balanus laevis Notochthamalus scabrosus Balanus osculus Acanthocyclus gayi Acanthocyclus hassleri Paraxanthus barbiger Cyclograpsus cinereus Allopetrolisthes punctatus Allopetrolisthes spinifrons Petrolisthes tuberculatus Petrolisthes laevigatus Petrolisthes angulosus Hyale hirtipalma Hyale media Hyale grandicornis Hyale sp. (juv.) Antias dimorphis Janiridae non det. Jaeropsis bidens Isocladus calcarea Exosphaeroma lanceolata Cymodocella foveolata Dynamenella acuticauda Dynamenella eatoni Tanaidacea non det. Harpacticoida sp. 1 Harpacticoida sp. 2 Harpacticoida sp. 3 Picnogonida sp. 1 Chironomidae sp. 1 Acari sp. 1 Araneae sp. 1 ECHINODERMATA Patiria chilensis T etrapygus niger

the interaction between Sector and Layer (three-way ANOVA, P50.05), mostly due to low values for multilayered matrices in the sheltered sector. A monotonic positive relationship between the depth (D) of Perumytilus purpuratus matrices (eld data) and the theoretical number of layers (La) was observed: La 0.2797+0.3398 D (r2 0.517, P50.001). Table 2. ANOVAs comparing species richness and evenness of macrofauna in mussel matrices of Perumytilus purpuratus in Punta de Tralca, central Chile.
(A) Species richness df Sector S Layer L Algae A S*L S*A L*A S*L*A Error Total 2 1 1 2 2 1 2 48 59 MS 0.0346 0.0122 0.0002 0.0193 0.0014 0.0000 0.0135 0.0112 F 3.09 1.09 0.02 1.72 0.12 0.00 1.20 P 0.054 0.302 0.888 0.190 0.887 0.980 0.309 (B) Evenness MS 0.006710 0.007676 0.001715 0.000230 0.002893 0.000002 0.000825 0.001018 F 6.59 7.54 1.69 0.23 2.84 0.00 0.81 P 0.003 0.008 0.200 0.799 0.068 0.962 0.451

Figure 3. (A) Species richness; (B) evenness; and (C) non-metric multidimensional scaling (n-MDS) for Perumytilus purpuratus matrices in Punta de Tralca. Bars represent averages and the lines above, standard error. In MDS, circles represent monolayer and squares, multilayer; white represent with algae and black, without algae. Sectors are indicated inside each symbol.
Journal of the Marine Biological Association of the United Kingdom (2006)


L. Prado and J.C. Castilla

Biodiversity, complexity and heterogeneity in Perumytilus purpuratus

Table 3. NP-MANOVAs for the macrofaunal assemblages in mussel matrices of Perumytilus purpuratus among sampling sector in Punta de Tralca, central Chile (data transformed with Log(x+1)).
Sector 1 df Layer L Algae A L A Residual Total 1 1 1 16 19 MS 3635.8064 4855.6613 1431.5733 2920.4885 F 1.2449 1.6626 0.4902 P 0.2510 0.0850 0.9280 MS 5233.0401 8048.5499 1523.4483 1477.6822 Sector 2 F 3.5414 5.4467 1.0310 P 0.003 0.001 0.388 MS 4569.5827 5086.7923 2243.1699 2102.7684 Sector 3 F 2.1731 2.4191 1.0668 P 0.031 0.017 0.388

Macrofauna associated with Perumytilus purpuratus matrices

Species richness (R). In total we found 92 invertebrate taxa, belonging to seven phyla. The most common taxa were: Arthropoda (N 33), Mollusca (N 35) and Annelida (N 17) (Table 1). In Sector 1 the number of taxa ranged between 16 and 20 (mean 18); in Sector 2 between 19 and 22 (mean 20); in Sector 3 between 19 and 22 (mean 20), both for monolayered and multilayered mussel matrices (Figure 3A). There were no significant dierences caused by any of the factors tested (threeway ANOVA, P40.05, Table 2A). Evenness (J). The evenness index (J) ranged between 0.39 and 0.63 (Figure 3B). There was a signicant eect associated with Sector and Layer (three-way ANOVA, P50.01, Table 2B). Sector 1, with the lowest J, and diered signicantly (three-way ANOVA, P50.05), from Sectors 2 and 3, which did not dier signicantly from each other (Tukey ^ Kramer posthoc comparisons, P50.05). Multivariate analyses. The n-MDS (Figure 3C) showed three main groups (stress 0.06), which were signicantly dierent (P50.05). Sector 1 had 52.94% dissimilarity with Sector 2 (np-MANOVA, P50.05). The main taxa determining the dierences were: Cirratulidae, Brachidontes granulata, Hyale sp., Phymactis clematis, Lasaea petitiana, Jehlius cirratus, Harpacticoid sp., Hyale grandicornis, Onchidiella marginata, Hyale hirtipalma, Siphonaria lessoni, T egula atra, Harpacticoid sp. 1, Perinereis falklandica and Balanus osculus. Polychaetes and bivalves were the most commonly found organisms in Sector 1 (sheltered with elevated sediment trapped inside the mussel matrix), while in Sector 2 the most represented taxa were amphipods, anemones and gastropods. Furthermore, Sector 1 had 51.08% dissimilarity with Sector 3 (np-MANOVA, P50.05). The main taxa determining this dierence were: Balanus osculus, Cirratulidae, Harpacticoid sp. 2, Hyale sp., Harpacticoid sp. 1, Onchidiella marginata, Hyale hirtipalma, Perinereis falklandica, Phymactis clematis,T egula atra,T yposyllis magdalena, Hyale grandicornis and Lasaea petitiana. Polychaetes were the most represented group in Sector 1, while in Sector 3 amphipods and anemones were the most common taxa. Sector 2 had 40.67% dissimilarity with Sector 3 (np-MANOVA, P50.05). The main taxa determining this dierence were: Brachidontes granulata, Balanus osculus, Harpacticoid sp. 2, Harpacticoid sp.1, Jehliuscirratus, Lassaeapetitiana, Siphonaria lessoni, Chiton granosus, Jaeropsis bidens, Antias dimorphis, Hyale grandicornis and Harpacticoid sp. 3.
Journal of the Marine Biological Association of the United Kingdom (2006)

Regarding faunal assemblages inside each sampling sector, there were no signicant eects for stratication and algae on mussel valves within Sector 1 (P40.05, np-MANOVA, Table 3). In contrast, Sectors 2 and 3 showed signicant eects for both factors (P50.05, np-MANOVA, Table 3).

We found a total of 92 invertebrate taxa associated with Perumytilus purpuratus matrices in the Punta de Tralca Bay, central Chile, which is higher than values reported from previous studies conducted on intertidal mussels (Perumytilus, Semimytilus and Brachidontes) in South America (De Amesti, 1994; Thiel & Ullrich, 2002; Adami et al., 2004). One notable nding is that the full diversity of taxa is present both in Perumytilus mono- and multilayer matrices ( i.e. same species richness). A similar value of species richness was found in northern Chile, associated with another bioengineer, the tunicate Pyura preaputialis (Cerda & Castilla, 2001), which forms thick (approximately 20^30 cm) and extensive intertidal matrices. The most abundant genera found in P. purpuratus matrices were Lasaea, Brachidontes, Hyale, T yposyllis and Pseudonereis, which belong to the same family or genus as the most abundant taxa associated with other mussels around the world (Seed, 1996). This suggests that worldwide the fauna associated with aggregated rocky intertidal mussels appear to converge into iso-communities. Mussel habitat structural complexity and environmental heterogeneity strongly inuence the structure of the communities associated with mussels (Tsuchiya & Nishihira, 1985). In this study, the number of layers (stratication) showed a signicant eect on species evenness (Table 2): greater stratication in mussel matrices corresponded to lower values of evenness in the associated community; meaning that some species became dominant. In the same vein, greater mussel stratication in sectors without sedimentation also determined a signicant dierence in faunal assemblages (Table 3). In previous studies of fauna associated with mussel matrices, habitat structural complexity was associated with biomass, area and the average length of mussels (Tsuchiya & Nishihira, 1985, 1986; Vallarino et al., 2002; Adami et al., 2004). Nevertheless, these attributes did not always exhibit signicant correlations with species diversity. In our study, we found that sediment retention was an important part of the habitat structural complexity in P. purpuratus matrices, being responsible for the greatest dierences in diversity

Biodiversity, complexity and heterogeneity in Perumytilus purpuratus indices and composition of faunal assemblages associated with them. This is in concordance with McQuaid & Dower, 1990, who demonstrated an increase in species richness in rocky shore environments regularly inundated with sand. In our study, a third potential attribute determining mussel habitat structural complexity was the algae attached to the mussel shells. In fact, in rocky shore sectors not aected by sedimentation (Sectors 2 and 3), the presence of algae showed a signicant eect on macrofaunal assemblages (Table 3). No eect was found in Sector 1, where sedimentation in mussel matrices is a crucial biodiversity attribute. Our study has revealed several species diversity patterns linked with mussel habitat structural complexity and environmental heterogeneity (wave exposure) aecting the assemblage of species associated with the autogenic bioengineer Perumytilus purpuratus, providing insight into the processes structuring the mussel-associated community and local biodiversity.
s We appreciate the collaboration of Professor Nicola s Caro, Gioconda Peralta, Ricardo Rozbaczylo and Andre nica Ortiz and Guin ez, Brendan Kelaher, Sara Kimberlin, Vero Justine Holls. Also acknowledge suggestions by two anonymous referees. This study was part of the thesis for Marine Biology degree by L. Prado and it was supported by the FONDAPCASEB (FONDECYT-CONICYT 1501-0001, Project no. 6, to J.C. Castilla).

L. Prado and J.C. Castilla


pez, J., 2004. Spatial and temporal Adami, M., Tablado, A. & Lo variability in intertidal assemblages dominated by the mussel Brachidontes rodriguezii (dOrbignyi, 1846). Hydrobiologia, 520, 49^59. Alvarado, J. & Castilla, J., 1996. Tridimensional matrices of Perumytilus purpuratus on intertidal platforms with varying wave forces in central Chile. Marine Ecology Progress Series, 133, 135^141. Anderson, M., 2001. A new method for non-parametric multivariate analysis of variance. Austral Ecology, 26, 32^46. Bell, E. & Denny, M., 1994. Quantifying wave exposure: a simple device for recording maximum water velocity and results of its use at several eld sites. Journal of Experimental Marine Biology and Ecology, 191, 9^29. Castilla, J., Steinmiller, D. & Pacheco, C., 1998. Quantifying wave exposure daily and hourly on the intertidal rocky shore of central Chile. Revista Chilena de Historia Natural, 71, 19^25. Cerda, M. & Castilla, J., 2001. Diversidad y biomasa de macroinvertebrados en matrices intermareales del tunicado Pyura preaputialis (Heller, 1878) en la bah| a de Antofagasta. Revista Chilena de Historia Natural, 74, 841^853. Clarke, K., 1993. Non-parametric multivariate analyses of changes in community structure. Australian Journal of Ecology, 18, 117^143. De Amesti, P., 1994. Importancia del banco de Perumytilus purpur bitat atus (Lamarck, 1819) (Mollusca: Bivalvia: Mytilidae) como ha temporal para macroinvertebrados marinos mo viles que lo utilizan en sus primeras etapas de vida. Marine Biology thesis, Universidad lica del Norte, Coquimbo, Chile. Cato

Gibbons, M., 1988. The impact of sediment acumulations, relative habitat complexity and elevation on rocky shore meiofauna. Journal of Experimental Marine Biology and Ecology, 122, 225^241. Guin ez, R. & Castilla, J., 1999. A tridimensional self-thinning model for multilayered intertidal mussels. American Naturalist, 154, 341^357. Jones, C.G., Lawton, J.H. & Shachak, M., 1994. Organisms as ecosystem engineers. Oikos, 69, 373^386. Lintas, C. & Seed, R., 1994. Spatial variation in the fauna associated with the Mytilus edulis on a wave-exposed rocky shore. Journal of Molluscan Studies, 60, 165^174. McQuaid, C. & Dower, K., 1990. Enhancement of habitat heterogenity and species richness on rocky shores inundated by sand. Oecologia, 84, 142^144. Peake, A. & Quinn, G., 1993. T emporal variation in species-area curves for invertebrates in clumps of an intertidal mussel. Ecography, 16, 269^277. Pielou, E.C., 1974. Mathematical ecology. New Y ork: Wiley. Prado, L., 2004. Diversidad de invertebrados marinos asociada al chorito maico, Perumytilus purpuratus (Lamarck, 1819) en Chile central. Marine Biology thesis, Universidad de Valpara| so, Valpara| so, Chile. Seed, R., 1996. Patterns of biodiversity in the macro-invertebrate fauna associated with mussel patches on rocky shores. Journal of the Marine Biological Association of the United Kingdom, 76, 203^210. Sokal, R. & Rohlf, F., 1989. Biometry. San Francisco: W.H. Freeman. Suchanek, T., 1980. Diversity in natural and articial mussel bed communities of Mytilus californianus. American Zooologist, 20, 807. 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. Hedgol Marine Research, 56, 21^30. Tsuchiya, M. & Nishihira, M., 1985. Islands of Mytilus as habitat for small intertidal animals: eect of island size on community structure. Marine Ecology Progress Series, 25, 71^81. Tsuchiya, M. & Nishihira, M., 1986. Islands of Mytilus as habitat for small intertidal animals: eect of Mytilus age structure on the species composition of the associated fauna and community organization. Marine Ecology Progress Series, 31, 171^178. Vallarino, E., Rivero, M., Gravina, M. & El| as, R., 2002. Las respuesta al impacto cloacal a nivel comunitario en los bancos ntico sodoccidental, y el uso intermareales de mit| lidos del Atla n de contaminadel | ndice de Shannon para la determinacio n. Revista Biolog|a Marina y Oceanograf|a, 37, 25^33. cio Zagal, C. & Hermosilla, C., 2001. Gu| a de invertebrados Marinos del n ed. Santiago de Chile: Litoral Valdiviano, primera edicio Quebecor World Chile S.A.

Submitted 9 September 2005. Accepted 26 January 2006.

Journal of the Marine Biological Association of the United Kingdom (2006)

Reproduced with permission of the copyright owner. Further reproduction prohibited without permission.