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Marine ecology progress series 340:163

MARINE ECOLOGY PROGRESS SERIES
Vol. 340: 163–171, 2007
Published June 18
Mar Ecol Prog Ser
Changes in South African rocky intertidal
invertebrate community structure associated with
the invasion of the mussel Mytilus galloprovincialis
Tamara B. Robinson1, 2,*, George M. Branch1, Charles L. Griffiths1, 2,
Anesh Govender1, Philip A. R. Hockey3
1Marine Biology Research Institute, Zoology Department, University of Cape Town, Private Bag X 03,
Rondebosch 7701, South Africa
2Centre of Invasion Biology, Zoology Department, University of Cape Town, Private Bag X 03,
Rondebosch 7701, South Africa
3DST/NRF Centre of Excellence at the Percy FitzPatrick Institute, University of Cape Town, Private Bag X 03,
Rondebosch 7701, South Africa
ABSTRACT: Since the establishment of the alien mussel Mytilus galloprovincialis in South Africa,several authors have studied its interactions with individual indigenous species. However, thebroader implications of this invasion on the intertidal zone remain undocumented. This paper analy-ses the impacts of this mussel on the rocky-shore invertebrate community structure at Marcus Islandon the west coast of South Africa. The effects of the invasion were linked to 3 key elements and werenot consistently spread across the intertidal zone, but were focused within the mid-to-low shore.
Firstly, physical stress in the mid-intertidal zones was ameliorated by the presence of M. galloprovin-cialis beds. Secondly, habitat complexity was increased where M. galloprovincialis replaced barerock or less complex secondary habitat. Thirdly, habitat became less patchy as mussel beds blan-keted the shore. Consequently, invertebrate density and species richness increased substantially, andcommunity composition changed significantly in the mid-shore. Lower on the shore, significantchanges in invertebrate community structure were driven by a switch from mono-layered beds of thesmall indigenous mussel Aulacomya ater to multilayered beds of M. galloprovincialis, despite nochange in total species richness.
KEY WORDS: Alien mussel · Community structure · Marine invasions · Mytilus galloprovincialis ·Rocky shores Resale or republication not permitted without written consent of the publisher the impacts of alien species on the biological structureof the communities they invade.
The spread of alien species is altering the composi- One alien species that has received substantial atten- tion of marine communities on a global scale (Ruiz et tion at the level of species-specific effects is the mytilid al. 1999, Mack et al. 2000, Grosholz 2002) and has mussel Mytilus galloprovincialis along the South been identified as a major threat to biodiversity (Occhi- African coast. As the most abundant and widespread pinti-Ambrogi & Savini 2003). Many studies have con- invasive marine species in this region (Robinson et al.
sidered direct interactions between alien and indige- 2005), M. galloprovincialis has partially displaced the nous species (Berman & Carlton 1991, Byers 2000, local mussels Choromytilus meridionalis and Aula- Byrnes & Witman 2003, Bachelet et al. 2004, Le Pape et comya ater along the west coast (Hockey & Van Erkom al. 2004), but relatively little attention has been paid to Schurink 1992), while exhibiting spatial segregation Inter-Research 2007 · www.int-res.com Mar Ecol Prog Ser 340: 163–171, 2007 with the indigenous mussel Perna perna on the south present in low numbers) and again in 2001, by which coast (Robinson et al. 2005). As a consequence of the time M. galloprovincialis was well established and had rapid growth rate, high fecundity and desiccation toler- invaded much of the South African coast (Robinson et ance of this invasive mussel (Van Erkom Schurink & al. 2005). In 1980, 7 intertidal zones were identified Griffiths 1990, Hockey & Van Erkom Schurink 1992), its and sampled. They were (in descending order of tidal arrival resulted in a net upshore shift in the zonation of intertidal mussel beds. Due to extremely high recruit- (1) The Porphyra zone, consisting of patchy beds of ment rates (up to 20 000 recruits m–2; Harris et al. 1998), the alga Porphyra capensis.
M. galloprovincialis presently dominates primary rock (2) The Ulva zone, characterised by mixed beds of the surfaces at the expense of various competitively inferior algae Ulva capensis and Ulva (=Enteromorpha) linza.
limpet species (Branch & Steffani 2004). By excluding (3) The Granularis zone, dominated by the limpet the limpet Scutellastra granularis from open rock, M. galloprovincialis has reduced the number of individ- (4) The algal turf zone, covered by a moss-like red al- uals that occur directly on rock, although at the same gal community dominated by Caulacanthus ustulatus. time it offers the potential of increasing overall S. gran- (5) The Gigartina zone, characterised by the algae ularis density by providing a favourable settlement and Gigartina radula and Pterosiphonia cloiophylla. recruitment substratum for juveniles (Griffiths et al.
(6) The Aulacomya zone, dominated by the ribbed 1992, Hockey & Van Erkom Schurink 1992). A second mussel Aulacomya ater. limpet species, Scutellastra argenvillei, has also been (7) The Choromytilus zone, comprising beds of the significantly affected by this invasion, although the black mussel Choromytilus meridionalis. strength of the interaction between these 2 species is In 1980, 10 to 16 quadrats, each of 0.01 m2, were mediated by wave action (Steffani & Branch 2003a,b).
selected randomly in each zone from within areas of On exposed shores, M. galloprovincialis outcompetes 100% algal or mussel cover. These quadrats were S. argenvillei and dominates the primary substratum, cleared, and all mobile and sessile invertebrates while, on semi-exposed shores, the mussel is relatively >1 mm in size were counted and identified to species scarce and S. argenvillei maintains dominance in open level. In the Granularis zone, where invertebrates tend rock space (Steffani & Branch 2003a,b).
to be large and sparsely distributed, animals were Besides the biological role of mussels on rocky shores, counted in situ in 27 quadrats of 0.5 m2.
they also form an important biotic substratum (Seed & In 2001, the same survey protocol was used, with 2 Suchanek 1992). Mussel beds impact surrounding exceptions. Firstly, Mytilus galloprovincialis had over- community structure as the highly complex configura- run most of the Granularis zone, making it inappropri- tion of mussel matrices offers a multitude of micro- ate to employ the 0.5 m2 quadrats previously used to habitats, which ameliorate fluctuating environmental sample this zone, and 0.01 m2 quadrats were cleared.
conditions and provide protection from predation Secondly, 7 samples were taken per zone. These were (Gosselin & Chia 1995). The physical presence of the randomly, horizontally interspersed between the 1980 mussel shells also constitutes a suitable hard substratum samples. To ensure equivalent areas were analysed for settlement and development of co-occurring species.
in 1980 and 2001, in each zone a randomly selected Despite substantial work on the ecological impacts of subset of 7 samples from 1980 was compared with the Mytilus galloprovincialis and the known role of mus- 7 samples taken in 2001. All calculations, except those sels as biotic substratum, the impact of this invasion on of rarefaction curves, were conducted using the ran- the intertidal community has not been considered. In dom sub-sample.
an effort to elucidate community impacts of such inva- Prior to univariate analyses, data were tested for nor- sions, this study characterises changes in intertidal in- mality using the Kolmogorov-Smirnov 1-sample test vertebrate community composition following invasion and for homogeneity of variances using Levene's test.
of South African rocky shores by M. galloprovincialis.
All univariate analyses were conducted using STATIS-TICA for Windows (Version 6), StatSoft Inc. (2004),with α set at 0.05.
MATERIALS AND METHODS
Densities per square metre of mussels and other invertebrates were compared before and after the This study took place on the southern shores of Mar- Mytilus galloprovincialis invasion (1980 versus 2001) cus Island in Saldanha Bay (33° 02.59' S, 17° 58.26' E) using the Mann-Whitney U-test. Each intertidal zone on the west coast of South Africa. The distribution and was considered separately.
abundance of intertidal invertebrates was recorded in To estimate the sufficiency of our sample size and 1980, before the invasion of Mytilus galloprovincialis compare species richness between times in the respec- was recognised (although this species may have been tive zones, sample-based rarefaction curves (Gotelli & Robinson et al.: Changes in community structure associated with an exotic mussel Colwell 2001) and the incidence-based richness esti-mate Chao 2 (Chao 1987) were calculated using theprogramme EstimateS (Colwell 2005).
Community composition (based on numerical abun- dance) was analysed separately for each intertidalzone using multivariate techniques in the PRIMERsoftware package (Plymouth Marine Laboratory)and non-standardised, fourth-root transformed data.
ANOSIM was employed to detect significant changesin community structure between 1980 and 2001. SIM-PER resolved which species were responsible for thesechanges. Non-metric multidimensional scaling wasused to generate graphic illustrations of the differencesbetween the 1980 and 2001 communities in each zone.
In 2001, only 6 of the original 7 intertidal zones could be detected. The algal turf zone could no longer be dis-tinguished and thus could not be resampled. Despitethe exclusion of this zone from the following analyses,it should be noted that the disappearance of a zone initself represents a major change in community struc-ture. As the vertical heights of the respective zoneswere not recorded in 1980, it was not possible to deter-mine if this zone had become dominated by Mytilusgalloprovincialis, or if it had been incorporated into thezones previously occurring above or below it.
Fig. 1. Mean densities (+ SD) of the various mussel species The densities of the various mussel species in each recorded per square metre in each intertidal zone on Marcus zone in 1980 and 2001 are shown in Fig. 1. In 1980, Island in 1980 and 2001. Mytilus galloprovincialis may have Choromytilus meridionalis occurred at relatively low been present in low numbers in the 1980 survey, but unde- densities of 2000 to 5000 m–2 across most of the shore, tected due to misidentification (n.s.: no significant difference in overall mussel densities between years; *p < 0.05; **p < 0.01) except in the Granularis zone and in the algal-domi-nated zones higher on the shore. The smaller Aulacomyaater attained much higher densities, but was confined tothe lower intertidal zone. In 2001, Mytilus gallopro- were substantial and significant increases in inverte- vincialis was recorded in all sampling zones, with the ex- brate density (p < 0.01), whereas decreases occurred in ception of the Porphyra zone, and dominated 4 out of 5 of the Gigartina and Aulacomya zones (respectively, p < these zones, reaching densities of 2000 to 10 000 m–2. In 0.05 and p < 0.01). The increases reflected invasion by the mid-shore Ulva and Granularis zones, the M. gallo- Mytilus galloprovincialis of zones that previously sup- provincialis invasion increased the total number of mus- ported few mussels. The reduction in invertebrate den- sels present, but did not replace those present prior to its sity in the Gigartina zone was a result of the disappear- invasion. This was, however, not the case in the Aula- ance of a single gastropod species (Aetoniella nigra), comya and Choromytilus zones, where the invasion which was common in 1980. The decline in the Aula- markedly decreased the densities of indigenous mussel comya zone reflected a shift from the typically smaller species, particularly A. ater. By 2001, there had been a but abundant Aulacomya ater to larger but less dense shift in the distribution and abundance of mussels from M. galloprovincialis and a reduction in crustacean num- the Aulacomya zone to higher up the shore, with all bers. Except in the Porphyra and Aulacomya zones, zones except the Aulacomya zone showing an increase there was a dramatic increase in the density of mussels in overall mussel density (Fig. 1).
between 1980 and 2001. The most striking increase In the Porphyra and Choromytilus zones there were no occurred in the Granularis zone, where mussels were significant differences in the overall densities of inverte- absent in 1980, but, in 2001, occurred at a density of brates between 1980 and 2001 (Mann-Whitney U-tests, 2660 individuals m–2 (4012 SD). In contrast, there was a p < 0.05; Fig. 2). In the Ulva and Granularis zones there marked decrease in density of mussels in the Aulacomya Mar Ecol Prog Ser 340: 163–171, 2007 capensis. In the Gigartina zone, the small gastropodsAetoniella nigra and Tricolia neritina contributed themost to the 93.7% dissimilarity between years. Both spe-cies were abundant in 1980 (mean densities of 14 771 m–2[6107 SD] and 5729 m–2 [2758 SD], respectively), butwere absent in 2001. Within the Aulacomya zone, Aula-comya ater, which decreased dramatically between 1980and 2001, contributed most to the 96.8% dissimilarity be-tween the pre- and post-invasion communities. Similarly,community differences in the Choromytilus zone wereexplained primarily by the replacement of Choromytilusmeridionalis by M. galloprovincialis. The role of mussels as dominant species affecting community structure of benthic intertidal habitats iswell established (Petraitis 1995, Tokeshi & Romero1995, Enderlein & Wahl 2004, Miyamoto & Noda 2004).
Mussels play a regulating role in community structurein 3 ways. Firstly, through their monopolisation of pri-mary rock space (Ruiz Sebastián et al. 2002, Steffani &Branch 2003b), secondly, by providing secondary habi-tat in the form of a 3-dimensional matrix (which pro-vides habitat for other species and may enhance theirrecruitment; Crooks & Khim 1999, Miyamoto & Noda2004), and thirdly, through their biological activities Fig. 2. Mean densities (+ SD) of invertebrates recorded per (e.g. by filter-feeding they remove large quantities of square metre in each zone on Marcus Island in 1980 and 2001,coded by major taxonomic groups. Note the difference in the particulate matter and plankton from near-shore scales of the y-axes in the 2 data sets (n.s.: no significant waters, reducing larval settlement of some associated difference in invertebrate density between years; *p < 0.05; species; Tsuchiya & Nishihira 1986, Asmus & Asmus 1991). The structural complexity of mussel beds pro-vides a multitude of microhabitats that ameliorate fluc- zone. In particular, A. ater decreased from 18 529 tuating environmental conditions and offer protection (5905 SD) to 514 (367 SD) individuals m–2.
from predation (Dumas & Witman 1993). Thus, it is not Sample-based rarefaction curves reached a plateau surprising that the intertidal fauna on Marcus Island only in the Porphyra zone in 2001 (Fig. 3). Chao 2 esti- changed considerably following the arrival of the inva- mates of total species richness showed a significant sive mussel Mytilus galloprovincialis.
decline in the Porphyra zone in 2001, with increases in As invasions by marine alien species are to a large the Ulva and Granularis zones (based on the lack of extent unpredictable, it is exceptionally difficult to overlapping confidence intervals; Fig. 4). No signifi- assess the impact of these species through replicated cant changes in total species richness were detected in experimental manipulations. As such, this study makes the 3 zones lowest on the shore.
use of data collected at a single point in time in 1980 The communities in all 6 zones changed significantly (prior to the invasion of Mytilus galloprovincialis) in between 1980 and 2001, even when the contribution order to make comparisons with post-invasion commu- made by Mytilus galloprovincialis was excluded nities. This pre-invasion data, however, has limitations (ANOSIM, p < 0.01; Fig. 5). In the Porphyra zone, 90% of that govern the extent of the current comparison.
the average difference between these 2 groups was Firstly, no data on the algal component of the intertidal accounted for by a decrease in the abundance of 1 spe- community were collected. Secondly, no measure of cies, the isopod Exosphaeroma varicolor. Over the same biomass was made for any species. Thirdly, no assess- period, the Ulva and Granularis zones, respectively, had ment was made of open rock space, and, lastly, a small average community dissimilarities of 86.4 and 99.8%.
number of samples were collected. In order to assess In both zones, this difference was explained primarily the adequacy of our sample size, rarefied species accu- by increased densities of the nudibranch Onchidella mulation curves were constructed. Only in the Por- Robinson et al.: Changes in community structure associated with an exotic mussel Fig. 3. Sample-based rarefaction species curves with 95% confidence intervals for all sampling zones in 1980 (s) and 2001 (d) phyra zone in 2001 was an asymptote reached, indicat- changes solely to the invasion of M. galloprovincialis.
ing that the sampling effort was too low to fully charac- Nonetheless, inter-annual changes of species richness terise species composition. However, the Chao 2 inci- and abundance within the benthic communities of dence-based richness estimate is still considered an Saldanha Bay (in which Marcus Island is located) are appropriate measure of total diversity as it usually known to be minimal (Jackson & McGibbon 1991), and requires ca. 50% of species to be sampled (Colwell & it is likely that a similar pattern applies to intertidal Coddington 1994). As no long-term continuous moni- toring has taken place on Marcus Island, it is not possi- The Mytilus galloprovincialis invasion affected the ble to unequivocally ascribe the observed community indigenous mussels Aulacomya ater and Choromytilus Mar Ecol Prog Ser 340: 163–171, 2007 stocks and often occupies heavily silted and sandyareas among rocks (T. B. Robinson pers. obs.), bothhabitats rarely occupied by M. galloprovincialis alongthe South African coast. Due to the presence of theserefuges, it is highly unlikely that C. meridionalis willbe driven to local extinction by the appearance ofM. galloprovincialis.
The change in community structure in the Porphyra zone is unlikely to be a consequence of the musselinvasion, as Mytilus galloprovincialis does not occurthis high on the shore. Crustacea and insect larvaedominated in both 1980 and 2001, and minor changesin abundance of these taxa probably result from sea-sonal variation in abundance of the dominant alga Por-phyra capensis (Griffin et al. 1999).
Prior to the arrival of Mytilus galloprovincialis, both the Ulva and Granularis zones were patchy environ-ments, comprising mainly bare rock interspersed withpatches of algae and large limpets. These zones weretherefore spatially simple habitats in which physicalstress would have played an important role in deter-mining biological assemblages. However, followingthe mussel invasion, the patchy mosaic of bare rock,algae and limpets was transformed to a less patchy butstructurally more complex mussel matrix. Reducedpatchiness in the Granularis zone is reflected in thereduction in sample variability from 1980 to 2001(Fig. 5). Thus, the physical stresses previously typicalof these zones were ameliorated, and the nature of thehabitat in these zones was dramatically altered. Thisaccounts for the massive increase in invertebrate den-sity, total species richness, as well as the changes in Fig. 4. Chao 2 estimates (+ 95% confidence intervals) for all community composition recorded in these zones.
sampling zones on Marcus Island in 1980 and 2001 (n.s.: no sig-nificant difference based on overlapping confidence intervals) In the Gigartina zone, the density of mussels remained unaltered, despite changes in the speciescomposition (Fig. 1). However, unlike the indigenous meridionalis in several ways. In the low-shore (Aula- mussels, Mytilus galloprovincialis develops multi-lay- comya zone), the density of A. ater decreased by ered beds (Hockey & Van Erkom Schurink 1992, almost 2 orders of magnitude as this slow-growing McQuaid & Phillips 2000). Consequently, the invasion species was outcompeted by M. galloprovincialis.
has resulted in an increase in structural complexity in There was also a decrease in the overall density of this zone. Despite this change, total species richness mussels in this zone, as the small A. ater has been remained unaltered. This is in line with findings by largely replaced by the larger M. galloprovincialis. In Hammond (2001) who recorded no difference in infau- the high- to mid-shore, densities of A. ater increased nal species diversity between indigenous mussels and dramatically as protection provided by M. galloprovin- M. galloprovincialis. The substantial decrease in the cialis beds enabled this species to survive high on the invertebrate density was due to extreme reductions in shore, from where it was precluded previously by the number of gastropods Aetoniella nigra and Tricolia virtue of its intolerance to desiccation (Van Erkom neritina, although it remains unclear whether these Schurink & Griffiths 1990), although it was still numer- decreases are a consequence of natural variation, or ically far subordinate. The most striking impact of the reflect changes induced by the arrival of M. gallo- M. galloprovincialis invasion was the total replace- ment of C. meridionalis in both the Aulacomya and Because the Aulacomya zone was previously charac- Choromytilus zones and, to a lesser extent in the terised by the presence of mussel beds, the invasion of Gigartina zone (Fig. 1). It should, however, be noted Mytilus galloprovincialis is unlikely to have altered the that C. meridionalis still thrives in substantial subtidal uniformity of the habitat in this zone to any great Robinson et al.: Changes in community structure associated with an exotic mussel Fig. 5. Non-metric multidimensional scaling of species abundance (fourth-root transformed) for all 6 sampling zones (a) to (f) in 1980 (s) and 2001 (d), excluding the contribution made by Mytilus galloprovincialis extent. However, Aulacomya ater decreased consider- be a consequence of its relatively slow growth rate ably in density between 1980 and 2001 (from 18 529 (Hockey & Van Erkom Schurink 1992, Van Erkom to 514 individuals m–2), while M. galloprovincialis Schurink & Griffiths 1993).
conversely increased. The switch from mono-layered The Choromytilus zone was originally characterised beds of small mussels to multilayered beds of large by substantial beds of this indigenous mussel. The ar- mussels resulted in a significant reduction in the over- rival of Mytilus galloprovincialis, thus, did not replace all density of mussels present in this zone. Van Erkom the type of habitat present, but altered it from a single- Schurink & Griffiths (1990) reported a density of layered mussel bed, typical of Choromytilus meridion- 10 000 A. ater m–2 in this zone at Marcus Island. Thus, alis, to a multi-layered mussel matrix associated with it would appear that A. ater has decreased progres- M. galloprovincialis (Griffiths et al. 1992). As a result, sively in abundance at Marcus Island since the arrival no change was recorded in total species richness. The of M. galloprovincialis. The poor competitive ability of fact that M. galloprovincialis reached its highest densi- A. ater (relative to M. galloprovincialis) is thought to ties in this lower-most zone is unexpected, as the den- Mar Ecol Prog Ser 340: 163–171, 2007 sity of this species on South African shores is generally cies (Carcinus maenas (L.) & Cancer irroratus Say). J Exp accepted to be maximal in the mid-intertidal zone (Van Mar Biol Ecol 169:89–101 Enderlein P, Wahl M (2004) Dominance of blue mussels ver- Erkom Schurink & Griffiths 1990).
sus consumer-mediated enhancement of benthic diversity.
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cies. Aquaculture 109:257–273 Editorial responsibility: Steven Morgan (Contributing Editor), Submitted: May 3, 2006; Accepted: December 1, 2006 Bodega Bay, California, USA Proofs received from author(s): May 28, 2007

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