An Invasive Polychaete Species Found in Living Marine Stromatolites

Aquatic Invasions (2016) Volume 11, Issue 3: 257–266 DOI: http://dx.doi.org/10.3391/ai.2016.11.3.04 Open Access

Research Article

An invasive polychaete species found in living marine stromatolites

Nelson A.F. Miranda1,*, Elena K. Kupriyanova2, Gavin M. Rishworth1, Nasreen Peer1, Thomas G. Bornman3,4, Matthew S. Bird1 and Renzo Perissinotto1 1DST/NRF Research Chair in Shallow Water Ecosystems, Nelson Mandela Metropolitan University, Port Elizabeth 6031, South Africa 2Australian Museum Research Institute, Australian Museum, 1 William Street, Sydney, NSW 2010 Australia 3South African Environmental Observation Network, Elwandle Coastal Node, Port Elizabeth, South Africa 4Coastal and Marine Research Institute, Department of Botany, Nelson Mandela Metropolitan University, Port Elizabeth, South Africa *Corresponding author E-mail: [email protected]

Received: 15 January 2016 / Accepted: 28 April 2016 / Published online: 14 May 2016 Handling editor: Elisabeth Cook

Abstract

This study represents the first report of an invasive species associated with modern, living stromatolites. The presence and potential impacts of the reef-forming tubeworm Ficopomatus enigmaticus (Fauvel, 1923) in unique stromatolite ecosystems of South Africa are addressed. Data on F. enigmaticus populations and a suite of environmental variables were collected on a monthly basis in 2014, at three sites along the Eastern Cape coast. Results are interpreted in terms of known environmental tolerance, reproductive strategy and environmental impacts of F. enigmaticus around the world. A combination of variables influenced the F. enigmaticus populations, particularly temperature and the availability of substrates for settlement. Low water temperatures (< 20°C) in winter appeared to limit the species growth and reproduction. Small populations of adult individuals were however able to persist all year round in habitats that exhibit favourable environmental conditions. These stromatolite pools appear to function as unique ecosystems that provide refuge for estuarine species, thus acting as stepping stones facilitating the dispersal and range expansion of estuarine fauna along the coast, including invasive species. Key words: tubeworm, settlement, temperature, tolerance, stepping stones, refuge, range expansion

Introduction Perissinotto et al. 2014) is therefore of interest because they appear to provide refugia and may function as During the last two decades, marine invasive species stepping stones for invasive species. Stromatolites have been reported from virtually every coastal (layered microbialites) are formed through the ecosystem worldwide (Ruiz et al. 1997; Bax et al. deposition of calcium carbonate and the trapping of 2003; Gallardo et al. 2016). A number of drivers act sediment by microalgae, predominantly cyanobacteria either singularly or synergistically (Lau and Schultheis and diatoms (Reid et al. 2000; Bosak et al. 2013). 2015) to prompt an invasion. Such drivers include Marine, living, stromatolites are rare and considered disturbance, propagule pressure, human-mediated to be partial analogues (Riding 2011) of those transport, low biotic and abiotic resistance, and shifting ancient microbialites that dominated shallow Archean climate regimes (Blackburn et al. 2015; Bellard et al. and Proterozoic oceans (Grotzinger and Knoll 1999; 2016; Penk et al. 2016). Refugia or stepping-stones Riding 2011). The stromatolites discovered in South can affect spread by allowing organisms to utilise Africa are similar in structure but less extensive and smaller, sometimes unfavourable (Apte et al. 2000), marine-influenced compared to those found in habitats to expand their distribution from, and to, south-western Australia (Forbes et al. 2010) and preferred environments. Northern Ireland (Cooper et al. 2013). They are The recent discovery of an extensive network of formed at the intersection of fresh, carbonate-rich, peritidal stromatolite pools along the South African groundwater discharge and the upper subtidal coastline (Smith et al. 2005; Smith et al. 2011; marine zone (Perissinotto et al. 2014).

257 N.A.F. Miranda et al.

Figure 1. Map of the study area showing the sampling locations on the south coast of South Africa (A, B and C) as well as the location of all coastal freshwater seeps in the surrounding area from Cape Recife to Oyster Bay (black dots; 540 in total). Two stromatolite pools uninvaded by F. enigmaticus were sampled at site A, three invaded pools were sampled at site B, one invaded and two uninvaded pools were sampled at site C. Adapted from Perissinotto et al. (2014).

South African stromatolites host a wide variety of substrates, including artificial structures, and has had freshwater, estuarine, and marine organisms that major impacts on the ecology of systems it invaded appear to alternate their dominance in response to in Argentina and South Africa (Obenat and Pezzani vertical mixing and the balance between freshwater 1994; Schwindt and Iribarne 2000; Bianchi and Morri and seawater inputs (Perissinotto et al. 2014). Among 2001; Schwindt et al. 2001; Schwindt et al. 2004a; these species is the invasive estuarine tubeworm Schwindt et al. 2004b; Dittmann et al. 2009; McQuaid Ficopomatus enigmaticus (Fauvel, 1923). The species and Griffiths 2014). is suspected to originate from temperate regions of This study represents the first report of an the Indian Ocean, but geographic origin is still invasive species associated with living stromatolites. uncertain and a matter of debate (reviewed by Modern stromatolites along the South African coast Dittmann et al. 2009). The species was first recorded are characterised by highly variable environmental in South Africa (as Mercierella enigmatica) in the conditions with frequent and extreme fluctuations 1950’s (Day 1951) and is thought to have been associated with regular spring tidal over-topping and introduced by ship fouling from southern or western flushing with freshwater from groundwater (Perissinotto Australia (Mead et al. 2011a). Presently, most estuaries in South Africa are colonised by this alien species et al. 2014). This high variability creates a unique (Day 1981; Plisko and Griffiths 2011), and it is suspected habitat suited only to those species able to tolerate that stromatolite pools act as stepping-stones in the extreme environmental fluctuations. Our goal was to spread of this species across estuarine systems that examine the presence and potential impacts of the are often located far apart from each other. This reef-forming tubeworm F. enigmaticus in stromatolite serpulid tubeworm is considered to be a highly invasive ecosystems. This was done by assessing population ecosystem engineer that has colonised many abundance patterns and growth rates of the tubeworm subtropical and temperate areas of the world (ten in stromatolite pools to determine the most important Hove and Weerdenburg 1978; Day 1981; Fornos et environmental variables correlated to tubeworm al. 1997; Bianchi and Morri 2001; Mead et al. 2011b; populations by comparing invaded and uninvaded Pernet et al. 2016). It builds large reefs on hard habitats in terms of environmental variables.

258 Invasive polychaete in marine stromatolites

Table 1. Stromatolite pools sampled on the south coast of South Africa. Eight pools were surveyed in total: four invaded and four uninvaded by Ficopomatus enigmaticus.

Pools Pool number Site Status 1 A Uninvaded by F. enigmaticus Three upper pools (sensu Perissinotto et al. 2014) contained stromatolite structures and were located nearest 2 B Invaded by F. enigmaticus to freshwater seepage points. 3 C Uninvaded by F. enigmaticus

Three middle pools contained the most stromatolite 4 A Uninvaded by F. enigmaticus accretion and are considered typical barrage pools 5 B Invaded by F. enigmaticus (Perissinotto et al. 2014). They were located between seepage points and the subtidal zone. 6 C Uninvaded by F. enigmaticus

Two additional pools were situated nearer to seepage 7 B Invaded by F. enigmaticus points than the subtidal zone. These contained stromatolite structures, and relatively high numbers of live F. enigmaticus as well as empty tubes attached to 8 C Invaded by F. enigmaticus boulders.

recorded hourly temperature and salinity data. Methods Additional information that influences all pools was Study sites and sample collection also collected for the study area. Rainfall, as measured by the South African Weather Services at the Port Samples were collected in 2014 during the first Elizabeth International Airport (~ 9 km from Site B), extensive survey of the three barrage pool sites influences freshwater input to all the pools. Swell reported by Perissinotto et al. (2014). Collection sites height, as modelled by Windguru (http://www.windguru.cz) were located west of Cape Recife (site A, 34º02′42.13″S, for Port Elizabeth, was considered an indicator of 25º34′07.50″E), at Schoenmakerskop (site B, 34º02′ environmental energy as the pools are regularly over- 28.23″S, 25º32′18.60″E), and east of Seaview (site C, topped by saltwater during spring high tides and 34º01′03.16″S, 25º21′56.48″E) along the South African storm surges. Inshore ocean surface temperature was coastline in the vicinity of Port Elizabeth (Figure 1). measured using Onset Hobo® U22-001 underwater Sampling was conducted at lowest low-tide during temperature recorders (Onset, Cape Cod, Massa- the first spring tidal phase of each month during chusetts, USA) deployed at depths < 1 m below mean each season (autumn: Mar – May; winter: Jun – Aug; spring low water. Ficopomatus enigmaticus are spring: Sep – Nov; summer: Dec – Feb). suspension feeders known to filter large volumes of The current study focused on middle and upper water (Davies et al. 1989), hence potentially affecting pools in sites A, B, and C (see Perissinotto et al. total suspended solids (TSS), particulate organic 2014), as well as two additional pools, one at site B matter (POM) and chlorophyll-a (chl-a) concentra- and one at site C (Figure 1, Table 1). All pools in tions. Water samples were collected monthly from this study were located between the subtidal pools to determine TSS (mg.l-1), POM (mg.l-1) and waterline and landward groundwater seepage. Lower chl-a (mg.m-3). Water was filtered through pre- pools (sensu Perissinotto et al. 2014) were closest to combusted and pre-weighed Whatman GF/F filters. the subtidal, had the least stromatolite growth, and Filters with retained materials were oven dried (60°C always contained marine organisms with no trace of for 48 h) and weighed with a digital balance (0.01 mg) F. enigmaticus. Therefore, lower pools were not to determine TSS (total dry mass) and then combus- included in this study. ted (450°C for 4 h) and weighed again to determine A YSI 6600-V2 multiprobe system (YSI POM (organic component). For water-column chl-a Incorporated, Yellow Springs, Ohio, USA) was used analyses, water was filtered through a GF/F filter. to measure physico-chemical parameters in all pools: To extract pigments, filters with retained material temperature (°C), salinity, depth (m), pH, turbidity were placed in 8 ml of 90% acetone solution for 48 h (NTU), and dissolved oxygen (DO, mg.l-1). Star Oddi in darkness at 4°C. Fluorescence was measured using DST CT (http://www.star-oddi.com) probes were deployed a Turner 10-AU narrow-band system (Turner Designs, in crevices at the bottom of each middle pool and Sunnyvale, California, USA).

259 N.A.F. Miranda et al.

The availability of substrates suitable for colonisation by F. enigmaticus was estimated every month. Objects larger than 500 cm3 (such as bottles, cans, tree trunks, and other debris) were regarded as substrates on which F. enigmaticus could settle (Schwindt and Iribarne 2000; Schwindt et al. 2004a) and were counted in each pool. Algal mats can cover hard substrates and effectively create a physical barrier to larval settlement (Norkko and Bonsdorff 1996). Therefore, to calculate the total (algae-free) area potentially available for the settlement of F. enigmaticus during this study, the total hard substrate area of each pool was measured and the percentage benthic algal cover was estimated based on photo-quadrats. A 12 megapixel digital camera was positioned 1.5 m over a 1 × 1 m PVC quadrat, which was placed on the water surface and aligned according to landmarks. The entire water surface of pools was photographed every month in this way. All pools were searched for traces of tubeworms every month. The number of live F. enigmaticus individuals was counted in each pool, and the length Figure 2. Ficopomatus enigmaticus tubeworms on colloform of their calcareous tubes was measured with Vernier formations in a stromatolite pool along the south coast of South callipers (to the nearest 0.01 mm). Tube growth Africa (a), ventral view (b), dorsal view (c) and operculum (d) of (increase in length, mm) was also tracked for each extracted specimen. Photographs by N.A.F. Miranda. live individual worm found. Photographs were used to confirm the identity of individuals as each Non-parametric permutational MANOVA displayed distinct settlement locations and tube (PERMANOVA, Anderson et al. 2008) was used to shapes. Measurements were repeated every 30 days test for differences in the measured environmental and used to determine tube length increases of variables. In this regard, a three-way PERMANOVA individual worms. Average monthly tube growth rate design tested for differences between pools uninvaded (increase in length) was then calculated for invaded and invaded (UI) by F. enigmaticus (fixed term, 2 pools. To determine dry mass (biomass), worms (5 levels), pools (random factor nested in UI, 8 levels) individuals per pool) were separated from their and seasons (fixed factor, four levels). The tubes, oven dried (60°C for 48 h) and individually resemblance matrix was based on Euclidean distance. weighed to the nearest 0.01 mg. Statistical significance was tested using 9999 permutations of residuals under a reduced model. Statistical analyses Distance-based linear modelling (DISTLM, Legendre and Anderson, 1999; McArdle and Anderson, 2001; General linear models (GLM) with quasi-Poisson Anderson et al. 2008) was used to perform permuta- distribution (season, four levels: autumn, winter, spring, tional regression (9999 random permutations) to test summer; status, two levels: invaded and uninvaded) for linear relationships between F. enigmaticus were run for each environmental variable (TSS, abundance (response) and the above-mentioned POM, chl-a, temperature, salinity, depth, pH, environmental variables (predictors). The response turbidity, dissolved oxygen, potential available area variable (F. enigmaticus abundance) was first for settlement, potential substrates for settlement), converted to a Euclidean distance matrix. A step- followed by Tukey’s post-hoc testing to determine if wise selection procedure was used, incorporating the there were significant differences between invaded corrected Akaike Information Criterion (AICc) and uninvaded pools in each season. ANOVA (Burnham and Anderson 2002) as the selection followed by Tukey’s post-hoc test was used to criterion to measure the relative goodness of fit for determine if there were differences between seasons each model. The final subset of environmental in log(x+1) transformed F. enigmaticus tube growth variables that provided maximum parsimony data. In both cases, all model assumptions were met. (according to the AICc criterion) is presented. The a These analyses were done using the statistical priori significance level (α) for all multivariate tests software R, version 2.15.1. was set at 0.01.

260 Invasive polychaete in marine stromatolites

Figure 3. Rainfall, ocean temperature and swell height data collected in the study area (a-c); selected environmental variables (water temperature, salinity, available potential area for settlement and pool depth) collected from four stromatolite pools invaded by F. enigmaticus (red solid line) and four uninvaded pools (blue dashed line) (d-g); monthly F. enigmaticus tube growth in invaded pools (h) and number of F. enigmaticus individuals (abundance) per invaded pool (i). Data were collected in 2014 and are presented as monthly means (± SD).

Results (Table S1). During summer, the average increase in The highest mean TSS and POM values were recorded tube length reached 6.86 mm per 30 days (Figure 3). during summer (supplementary material Table S1). However, there were no significant differences in The lowest mean TSS was recorded during spring. tube growth between seasons (ANOVA, P > 0.05). The lowest mean POM, highest mean turbidity and Individuals had an average dry mass of 0.23 ± 0.04 highest mean chl-a were recorded during autumn. mg, tube length of 21.45 ± 2.16 mm, and reached a Temperature was lowest in winter and highest in biomass of up to 94.35 mg dry mass per invaded pool summer (Table S1, Figure 3). In general, all pools (or 23.59 mg. m-2). After a mass-mortality event at the were colder and saltier in autumn and winter and end of January 2014 (coinciding with a red tide in warmer and fresher in spring and summer. Mean DO the Algoa Bay area and the lowest DO readings ranged between 8 and 12 mg.l-1 and mean pH was recorded in the study), no live F. enigmaticus approximately 8 in all pools. While both invaded and individuals were recorded in 3 of the invaded pools uninvaded pools had areas potentially available for (site C additional pool, site B upper and additional settlement throughout the year (Table S1, Figure 3), pool) from February to August. However, a few these were significantly smaller only in uninvaded large individuals (average biomass 0.75 ± 0.02 mg and pools during winter. tube length 27.86 ± 0.47 mm) persisted in a single The density of F. enigmaticus was greatest in spring, pool (middle pool, site B) during autumn and winter reaching mean (± SE) values of 14.6 ± 13.0 ind.m-2 (total dry mass: 7.47 mg or 0.62 mg.m-2).

261 N.A.F. Miranda et al.

Table 2. PERMANOVA test for differences in abiotic variables across F. enigmaticus invaded and uninvaded stromatolite pools (IU, fixed factor), pools (random factor nested in IU) and seasons (fixed factor). The degrees of freedom, df; sum of squares, SS; means squared, MS; pseudo – F statistic; and probability level based on 9999 random permutations, P(perm), are presented. Significant factors are in bold (α = 0.01). Data were collected in Eastern Cape stromatolite pools in 2014. Source df SS MS Pseudo-F P(perm) IU 1 39.382 39.4 0.606 0.778 Seasons 3 227.44 75.8 8.440 0.001 Pools (IU) 6 390.07 65.0 8.488 0.001 IU × Seasons 3 21.214 7.1 0.787 0.754 Pools(IU) × Seasons 18 161.69 9.0 1.173 0.093 Residuals 64 490.2 7.7 0.606 0.778 Total 95 1330

Table 3. Distance-based linear regression model of F. enigmaticus abundance (response) against environmental variables (predictors) measured in Eastern Cape stromatolite pools in 2014 (A). Sequential tests for stepwise model (R2 = 0.26), and percentage of multivariate variation explained by individual axes are presented (B). The most parsimonious model included number of potential substrates for settlement, “Substrates”; stromatolite pool water temperature, “Temp”; and available potential area for settlement, “Area”. A: Model summary Variable AICc SS (trace) Pseudo - F P Prop. Cumul. res. df Substrates 626.40 7869.0 11.80 < 0.01 0.111 0.111 94 Temp (°C) 620.95 4761.9 7.64 < 0.01 0.068 0.179 93 Area (m2) 613.57 5488.6 9.63 < 0.01 0.078 0.257 92

B: Variation explained by axes Axis Individual Cumulative Individual Cumulative % explained variation of fitted model % explained variation of total variation 1 98.21 98.21 25.21 25.21 2 1.79 100 0.46 25.67

Mean ocean surface temperature was lowest in while swell height was lower and ocean temperature spring and highest in summer (January and February) was higher in the study area (Figure 4). The stepwise (Figure 3). Mean swell height increased in autumn AICc analysis showed that F. enigmaticus abundance and peaked in winter, with this peak coinciding exhibited a significant relationship with pool tempera- with an increase in mean salinity recorded in all ture, number of substrates, and area potentially pools in winter while the highest salinities were available for settlement (Table 3). However, this recorded in invaded pools (Table S1, Figure 3). three variable model only explained 26% of the total There was a clear recruitment event at the onset of variation in F. enigmaticus abundance data. spring (August/September), during which 95 ± 49 individuals were recorded per invaded pool (Table Discussion S1; Figure 3). This coincided with an increase in mean rainfall (> 50 mm) and a drop in mean swell Ficopomatus enigmaticus is not an obligate reef height at the end of winter (mean swell height builder (Bianchi and Morri 2001) and occurs indivi- remained at approximately 3 m from August to dually or in small aggregations in the South African December). stromatolite pools, often attached to rocks, directly Significant differences in stromatolite pool abiotic on stromatolites (Figure 2), or on any other available data were detected between seasons and pools (Table substrates. Availability of settlement substrates and 2). No significant differences in abiotic conditions were water temperature appear to be the most important detected, however, between invaded and uninvaded variables controlling the persistence of F. enigmaticus pools. There were differences among seasons and F. in stromatolite pools. Overall, environmental variables enigmaticus presence was greater in spring when explained a low percentage of the variation in F. temperature, TSS, and POM were higher in the pools, enigmaticus abundance (Table 3). This is expected

262 Invasive polychaete in marine stromatolites for a habitat generalist with wide environmental tolerance. However, Schwindt et al. (2004a) argued that habitats favoured by F. enigmaticus populations are very similar in their physical, chemical, and biological characteristics throughout the world. These authors also suggested that the most important variables that affect the spread of this species in invaded habitats may be salinity, nutrients (i.e., TSS, POM and chl-a), and environmental energy (e.g., current speed, or swell height as proxy). The TSS, POM and chl-a values measured in the current study correspond with the lowest recorded by Schwindt et al. (2004a) and therefore may partially explain the relatively small population size observed in stromatolite pools. The use of estuaries and intermittent water bodies as stepping stones for aquatic organisms is well- documented (Burridge et al. 2004; Reynolds et al. 2014; Tulbure et al. 2014). These environments facilitate spread, recruitment, and invasion of organisms by providing food (O’Sullivan et al. 2014), a favourable environment during a shift or an unfavourable time period (Hannah et al. 2014), and reducing the distance between suitable habitats for organisms with a mobile life stage (Gaines and Bertness 1992). Perhaps not all these factors are necessary. For example, habitats with unstable environmental characteristics, such as stromatolite pools, still appear to create suitable stepping stones for habitat generalists such as the estuarine tubeworm. Ficopomatus enigmaticus exhibits gregarious larval settlement, which is strongly affected by the ability of the larvae to recognise adults of their own species (Bianchi and Morri 1996), the nature of the Figure 4. PCA showing differences in abiotic data collected during 2014 from four invaded and four uninvaded stromatolite settlement substrate, and water flow velocity pools. The PCA is presented with labels for the different seasons (Kupriyanova et al. 2001). Due to their position and (a) and presence/absence of F. enigmaticus (b). The first two axes physical structure, stromatolite pools maintain explain 37.4% of the total variance (PC1 = 22% and PC2 = 15.4%). relatively constant water levels throughout the year and appear to provide a degree of shelter against strong currents that would disrupt larval settlement. conditions that would have been lethal to F. enigma- In agreement with Thorp (1994), the shallow depth ticus, even though it is tolerant to low dissolved of invaded pools led to the development of elevated oxygen (Dittmann et al. 2009). temperatures during the reproductive period of F. Despite its wide salinity and temperature tolerance enigmaticus within the stromatolites, thereby range, environmental conditions do influence growth enhancing larval and adult growth. Indeed, invaded rates of F. enigmaticus (Bianchi and Morri, 1996). pools may reach higher temperatures than uninvaded Rates of tube length growth vary widely (reviewed pools and the ocean, during which time worm in Dittmann et al. 2009). In this study, the fastest F. growth could escalate. Furthermore, when over 95% enigmaticus growth rates and greatest abundances of the population died in invaded pools in February were recorded in stromatolite pools during a mass 2014, a small portion of the population survived and recruitment event at the onset of Austral spring. persisted during the entire study period in certain However, tube growth was also not significantly stromatolite pools, which acted as refuges for F. different between seasons. Furthermore, the presence enigmaticus. The cause of the demise of F. of empty tubes in some pools suggests that worms enigmaticus in February is not certain, but was have survived in greater numbers in the past. Post- possibly linked to a harmful algal bloom prevailing settlement growth of F. enigmaticus juveniles is in the area at that time. Red tides can cause hypoxic very fast and particularly affected by salinity and

263 N.A.F. Miranda et al. temperature (Dittmann et al. 2009, and references worms settle on brittle stromatolite deposits. therein). Once individuals settle, they can grow to However, they may persist for long enough to attract maturity lengths of 6–10 mm in a few weeks, other worms and spawn. High rates of predation by although this may vary regionally. However, crabs and molluscs, combined with increased competition temperatures exceeding 20ºC and salinities of 10–30 for food and space with other benthic organisms, may appear to be optimal for F. enigmaticus growth explain the absence of F. enigmaticus in lower pools (Tebble 1953). Ficopomatus enigmaticus is sensitive (excluded from analyses in this study). Although to reductions in temperature (Kupriyanova et al. only environmental variables were considered in this 2001) and, as with most invertebrates, embryonic and study, biotic factors are also important and should be larval development time increases with decreasing addressed in future studies. temperatures (Kupriyanova et al. 2001). The minimum The filter-feeding ability of F. enigmaticus is temperature value for spawning can vary among remarkable, as it can affect whole ecosystems by populations and is reported to range from 10 to 17°C removing large amounts of particulate matter from (Dittmann et al. 2009). During the current study, the water column, thus affecting primary production average temperatures as low as 14.5°C were recorded by removing phytoplankton, potentially ameliorating in the ocean in spring, while invaded stromatolite eutrophication, and decreasing overall turbidity pools had average temperatures > 20°C, which seem (Davies et al. 1989; Bruschetti et al. 2008). to be more favourable for growth and reproduction. However, the F. enigmaticus population densities in Ficopomatus enigmaticus larvae are passively stromatolite pools are much lower than those in distributed by water currents (Kupriyanova et al. estuaries and lagoons where they form reefs. Based 2001), and the source of the spawning event that on clearance rate estimates of 8.59 ml.mg−1 dry mass resulted in the early spring recruitment in stromatolite of worm h−1 (Davies et al. 1989), worms in the pools is uncertain. Perhaps the increase in temperature current study filtered a maximum of 19 L of water in pools, reduction in swell height, and steady per pool per day. Although turbidity, TSS, POM, rainfall created the required conditions for successful and chl-a were marginally lower in some invaded spawning. The source of the larvae may have been pools compared to uninvaded pools, it remains the persisting population of large adult worms in the inconclusive whether the feeding of F. enigmaticus stromatolite pools. Alternatively, F. enigmaticus had a significant effect in stromatolite pools. could be introduced through shipping and mariculture Wasson et al. (2001) indicated that F. enigmaticus (Glasby et al. 2007), attached to debris coming from and other invasive species can make use of suitable adjacent estuaries with larger populations, and even estuarine habitats as “stepping stones”. Interestingly, attached to large mobile organisms, such as turtles invasive species can be transferred via stepping stone and crabs. Although only one period of spawning habitats with potentially unfavourable environmental and settlement was observed in the current study, conditions (Apte et al. 2000). Land-use changes in more periods are possible since different populations the past few decades have resulted in the exhibit variability in settlement periods and introduction of more artificial structures in aquatic reproductive activity seems to be timed to fit the environments and increased dumping of waste, preferred local conditions (Dittmann et al. 2009). especially buoyant plastic, into coastal waters, both As suggested by Hill (1967) for the closely related of which have been linked to global increases in the Ficopomatus uschakovi (Pillai, 1960), F. enigmaticus spread and biomass of F. enigmaticus (Schwindt et may have different salinity optima for survival, growth, al. 2004b; McQuaid and Griffiths 2014) and other and reproduction. The implication is that salinity invasive aquatic species (Airoldi et al. 2015; Mesel fluctuations may be critical for the successful et al. 2015). According to Saura et al. (2013), the reproduction and development of Ficopomatus capacity of species to exploit stepping stones (Tebble 1953). Fluctuations in temperature and depends on species-specific life-history traits. This salinity may also exclude competitors and predators study shows that F. enigmaticus is capable of using of F. enigmaticus, allowing them to recruit. Deeper small freshwater seepage areas along the South pools are more stable in terms of temperature, but African coastline. Havel et al. (2005) and Johnson et may also be harder to colonize due to biotic barriers al. (2008) reported that small reservoirs and dams such as increased algal growth, competition, and also can facilitate the spread of invasive species into predation. Limitations on potential settlement seemingly isolated habitats. Similarly, perhaps substrates can result in the use of any available unique ecosystems, such as stromatolite pools, surfaces, including roots or other decomposing plant which provide suitable settlement surfaces, serve as material, which is not ideal as the worms are bound stepping stones for the spread of a variety of to be dislodged. Dislodging may also happen when organisms along the coast, including invasive species.

264 Invasive polychaete in marine stromatolites

Acknowledgements Davies BR, Stuart V, de Villiers M (1989) The filtration activity of a serpulid polychaete population Ficopomatus enigmaticus This work was supported by the South African Research Chairs (Fauvel) and its effects on water quality in a coastal marina. Initiative of the Department of Science and Technology (DST) and Estuarine Coastal and Shelf Science 29: 613–620, http://dx.doi.org/ National Research Foundation (NRF) of South Africa. Any opinion, 10.1016/0272-7714(89)90014-0 finding, and conclusion or recommendation expressed in this Day JH (1951) The polychaete fauna of South Africa. Part I. The document is that of the authors and the NRF does not accept any intertidal and estuarine Polychaeta of Natal and Mozambique. liability in this regard. The authors wish to thank the South African Annals of the Natal Museum 12: 1–67 Weather Service for providing climate data, Windguru for their swell Day JH (1981) Estuarine ecology with particular reference to and wave predictions, and the South African Environmental southern Africa. AA Balkema Publishers, Netherlands, 441 pp Observation Network (SAEON) for providing hourly underwater Dittmann S, Rolston A, Benger SN, Kupriyanova EK (2009) Habitat temperature data for the inshore environment. We are also grateful to requirements, distribution and colonisation of the tubeworm the anonymous reviewers and to Ryan Reisinger and Chris Oosthuizen Ficopomatus enigmaticus in the Lower Lakes and Coorong. for their constructive input which strengthened the paper. Report for the South Australian Murray-Darling Basin Natural Resources Management Board, Adelaide, 99 pp Forbes M, Vogwill R, Onton K (2010) A characterisation of the References coastal tufa deposits of south–west Western Australia. Airoldi L, Turon X, Perkol-Finkel S, Rius M (2015) Corridors for Sedimentary Geology 232: 52–65, http://dx.doi.org/10.1016/j.sedgeo. aliens but not for natives: effects of marine urban sprawl at a 2010.09.009 regional scale. Diversity and Distributions 21: 755–768, Fornos JJ, Forteza V, Martinez-Taberner A (1997) Modern poly- http://dx.doi.org/10.1111/ddi.12301 chaete reefs in Western Mediterranean lagoons: Ficopomatus Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA+ for enigmaticus (Fauvel) in the Albufera of Menorca, Balearic PRIMER: Guide to software and statistical methods. PRIMER- Islands. Palaeogeography, Palaeoclimatology, Palaeoecology E, Plymouth, UK 128: 175–186, http://dx.doi.org/10.1016/S0031-0182(96)00045-4 Apte S, Holland B, Godwin LS, Gardner JA (2000) Jumping Ship: a Gaines SD, Bertness MD (1992) Dispersal of juveniles and variable stepping stone event mediating transfer of a non-indigenous recruitment in sessile marine species. Nature 360: 579–580, species via a potentially unsuitable environment. Biological http://dx.doi.org/10.1038/360579a0 Invasions 2: 75–79, http://dx.doi.org/10.1023/A:1010024818644 Gallardo B, Clavero M, Sánchez MI, Vilà M (2016) Global eco- Bax N, Williamson A, Aguero M, Gonzalez E, Geeves W (2003) logical impacts of invasive speices in aquatic ecosystems. Global Marine invasive alien species: a threat to global biodiversity. Change Biology 22: 151–163, http://dx.doi.org/10.1111/gcb.13004 Emerging Issues in Oceans, Coasts, and Islands 27: 313–323, Glasby T, Connell S, Holloway M, Hewitt C (2007) Nonindigenous http://dx.doi.org/10.1016/s0308-597x(03)00041-1 biota on artificial structures: could habitat creation facilitate Bellard C, Leroy B, Thuiller W, Rysman J-F, Courchamp F (2016) biological invasions? Marine Biology 151: 887–895, Major drivers of invasion risks throughout the world. Ecosphere http://dx.doi.org/10.1007/s00227-006-0552-5 7: e01241, http://dx.doi.org/10.1002/ecs2.1241 Grotzinger JP, Knoll AH (1999) Stromatolites in precambrian Bianchi CN, Morri C (2001) The battle is not to the strong: serpulid carbonates: evolutionary mileposts or environmental dipsticks? reefs in the lagoon of Orbetello (Tuscany, Italy). Estuarine Annual Review of Earth and Planetary Sciences 27: 313–358, http://dx.doi.org/10.1146/annurev.earth.27.1.313 Coastal and Shelf Science 53: 215–220, http://dx.doi.org/10.1006/ ecss.2001.0793 Hannah L, Flint L, Syphard AD, Moritz MA, Buckley LB, Bianchi CN, Morri C (1996) Ficopomatus “Reefs” in the Po River McCullough IM (2014) Fine-grain modeling of species' Delta (Northern Adriatic): their constructional dynamics, response to climate change: holdouts, stepping-stones, and biology, and influences on the brackish-water biota. Marine microrefugia. Trends in Ecology and Evolution 29: 390–397, http://dx.doi.org/10.1016/j.tree.2014.04.006 Ecology 17: 51–66, http://dx.doi.org/10.1111/j.1439-0485.1996.tb00489.x Havel JE, Lee CE, Zanden MJV (2005) Do reservoirs facilitate Blackburn TM, Lockwood JL, Cassey P (2015) The influence of invasions into landscapes? BioScience 55: 518–525, numbers on invasion success. Molecular Ecology 24: 1942– http://dx.doi.org/10.1641/0006-3568(2005)055[0518:DRFIIL]2.0.CO;2 1953, http://dx.doi.org/10.1111/mec.13075 Johnson PTJ, Olden JD, Zanden MJV (2008) Dam invaders: Bosak T, Knoll AH, Petroff AP (2013) The meaning of stromatolites. impoundments facilitate biological invasions into freshwaters. Annual Review of Earth and Planetary Sciences 41: 21–44, Frontiers in Ecology and the Environment 6: 357–363, http://dx.doi.org/10.1146/annurev-earth-042711-105327 http://dx.doi.org/10.1890/070156 Bruschetti M, Luppi T, Fanjul E, Rosenthal A, Iribarne O (2008) Kupriyanova EK, Nishi E, ten Hove HA, Rzhavsky AV (2001) Life- Grazing effect of the invasive reef-forming polychaete history patterns in serpulimorph polychaetes: ecological and Ficopomatus enigmaticus (Fauvel) on phytoplankton biomass in evolutionary perspectives. Oceangraphy and Marine Biology: a SW Atlantic coastal lagoon. Journal of Experimental Marine an Annual Review 39: 1–101 Biology and Ecology 354: 212–219, http://dx.doi.org/10.1016/ Lau JA, Schultheis EH (2015) When two invasion hypotheses are j.jembe.2007.11.009 better than one. New Phytologist 205: 958–960, http://dx.doi.org/ Burnham KP, Anderson DR (2002) Model selection and multimodel 10.1111/nph.13260 inference: a practical information-theoretical approach, 2nd ed. Legendre P, Anderson MJ (1999) Distance-based redundancy Springer-Verlag, New York analysis: testing multi-species responses in multi-factorial Burridge CP, Hurt AC, Farrington LW, Coutin PC, Austin CM ecological experiments. Ecological Monographs 69: 1–24, (2004) Stepping stone gene flow in an estuarine-dwelling sparid http://dx.doi.org/10.1890/0012-9615(1999)069[0001:DBRATM]2.0.CO;2 from south-east Australia. Journal of Fish Biology 64: 805–819, McArdle BH, Anderson MJ (2001) Fitting multivariate models to http://dx.doi.org/10.1111/j.1095-8649.2004.0347.x community data: a comment on distance-based redundancy Cooper JAG, Smith AM, Arnscheidt J (2013) Contemporary analysis. Ecology 82: 290–297, http://dx.doi.org/10.1890/00129658(20 stromatolite formation in high intertidal rock pools, Giant's 01)082[0290:FMMTCD]2.0.CO;2 Causeway, Northern Ireland: preliminary observations. In: McQuaid KA, Griffiths CL (2014) Alien reef-building polychaete Conley DC, Masselink G, Russell PE, O'Hare TJ (eds), drives long-term changes in invertebrate biomass and diversity Proceedings 12th International Coastal Symposium (Plymouth, in a small, urban estuary. Estuarine Coastal and Shelf Science England), pp 1675–1680, http://dx.doi.org/10.2112/si65-283.1 138: 101–106, http://dx.doi.org/10.1016/j.ecss.2013.12.016

265 N.A.F. Miranda et al.

Mead A, Carlton JT, Griffiths CL, Rius M (2011a) The introduced Heidelberg, Germany, pp 29–74, http://dx.doi.org/10.1007/978-3-642- and cryptogenic marine and estuarine species of South Africa. 10415-2_3 Journal of Natural History 45: 2463–2524, http://dx.doi.org/10.1080/ Ruiz GM, Carlton JT, Grosholz ED, Hines AH (1997) Global 00222933.2011.595836 invasions of marine and estuarine habitats by non-indigenous Mead A, Carlton J, Griffiths C, Rius M (2011b) Revealing the scale species: Mechanisms, extent, and consequences. American of marine bioinvasions in developing regions: a South African Zoologist 37: 621–632, http://dx.doi.org/10.1093/icb/37.6.621 re-assessment. Biological Invasions 13: 1991–2008, http://dx.doi.org/ Saura S, Bodin Ö, Fortin M-J (2013) Stepping stones are crucial for 10.1007/s10530-011-0016-9 species' long-distance dispersal and range expansion through Mesel ID, Kerckhof F, Norro A, Rumes B, Degraer S (2015) habitat networks. Journal of Applied Ecology 51: 171–182, Succession and seasonal dynamics of the epifauna community http://dx.doi.org/10.1111/1365-2664.12179 on offshore wind farm foundations and their role as stepping Schwindt E, Iribarne OO (2000) Settlement sites, survival and effects stones for non-indigenous species. Hydrobiologia 756: 37–50, on benthos of an introduced reef-building polychaete in a SW http://dx.doi.org/10.1007/s10750-014-2157-1 Atlantic coastal lagoon. Bulletin of Marine Science 67: 73–82 Norkko A, Bonsdorff E (1996) Population responses of coastal Schwindt E, Bortolus A, Iribarne OO (2001) Invasion of a reef- zoobenthos to stress induced by drifting algal mats. Marine builder polychaete: direct and indirect impacts on the native Ecology Progress Series 140: 141–151, http://dx.doi.org/10.3354/ benthic community structure. Biological Invasions 3: 137–149, meps140141 http://dx.doi.org/10.1023/A:1014571916818 O'Sullivan D, Benton TG, Cameron TC (2014) Inter‐patch Schwindt E, De Francesco CG, Iribarne OO (2004a) Individual and movement in an experimental system: the effects of life history reef growth of the invasive reef-building polychaete Fico- and the environment. Oikos 123: 623–629, http://dx.doi.org/10.1111/ pomatus enigmaticus in a south-western Atlantic coastal lagoon. j.1600-0706.2013.01150.x Journal of the Marine Biological Association of the United Obenat SM, Pezzani SE (1994) Life cycle and population structure Kingdom 84: 987–993, http://dx.doi.org/10.1017/S0025315404010288h of the polychaete Ficopomatus enigmaticus (Serpulidae) in Mar Schwindt E, Iribarne OO, Isla FI (2004b) Physical effects of an Chiquita coastal lagoon, Argentina. Estuaries 17: 263–270, invading reef-building polychaete on an Argentinean estuarine http://dx.doi.org/10.2307/1352574 Penk MR, Jeschke JM, Minchin D, Donohue I (2016) Warming can environment. Estuarine Coastal and Shelf Science 59: 109–120, enhance invasion success through assymetries in energetic http://dx.doi.org/10.1016/j.ecss.2003.06.004 Smith AM, Uken R, Thackeray Z (2005) Cape Morgan peritidal performance. Journal of Animal Ecology 85: 419–426, http://dx.doi.org/10.1111/1365-2656.12480 stromatolites: the origin of lamination. South African Journal of Perissinotto R, Bornman TG, Steyn P-P, Miranda NAF, Dorrington Science 101: 107–108 RA, Matcher GF, Strydom N, Peer N (2014) Tufa stromatolite Smith AM, Andrews JE, Uken R, Thackeray Z, Perissinotto R, ecosystems on the South African south coast. South African Leuci R, Marca-Bell A (2011) Rock pool tufa stromatolites on a Journal of Science 110: 89–96, http://dx.doi.org/10.1590/sajs.2014/ modern South African wave-cut platform: partial analogues for 20140011 Archaean stromatolites? Terra Nova 23: 375–381, http://dx.doi.org/ Pernet B, Barton M, Fitzhugh K, Harris LH, Lizárraga D, Ohl R, 10.1111/j.1365-3121.2011.01022.x Whitcraft CR (2016) Establishment of the reef-forming Tebble N (1953) A source of danger to harbour structures— tubeworm Ficopomatus enigmaticus (Fauvel, 1923) (Annelida: encrustation by a tubed marine worm. Journal of the Institution Serpulidae) in southern California. BioInvasions Records 5: 1–7, of Municipal Engineers 80: 259–265 http://dx.doi.org/10.3391/bir.2016.5.1.03 ten Hove HA, Weerdenburg JCA (1978) A generic revision of the Plisko D, Griffiths C (2011) Segmented worms. In: Picker M, brackish-water serpulid Ficopomatus Southern 1921 Griffiths C (eds) Alien and invasive animals: a South-African (Polychaeta: Serpulinae), including Mercierella Fauvel 1923, perspective. Struik Nature, Cape Town, South Africa, pp 174–180 Sphaeropomatus Treadwell 1934, Mercierellopsis Rioja 1945 and Neopomatus Pillai 1960. Biological Bulletin 154: 96–120, Reid RP, Visscher PT, Decho AW, Stolz JF, Bebout BM, Dupraz C, http://dx.doi.org/10.2307/1540777 Macintyre IG, Paerl HW, Pinckney JL, Prufert-Bebout L, Steppe Thorp CH (1994) Population variation in Ficopomatus enigmaticus TF, DesMarais DJ (2000) The role of microbes in accretion, (Fauvel) (Polychaeta, Serpulidae) in a brackish water millpond lamination and early lithification of modern marine at Emsworth, West Sussex, U.K. Mémoires du Muséum stromatolites. Nature 406: 989–992, http://dx.doi.org/10.1038/35023158 National d'Histoire Naturelle 162: 585–591 Reynolds TV, Matthee CA, Von Der Heyden S (2014) The influence Tulbure MG, Kininmonth S, Broich M (2014) Spatiotemporal of Pleistocene climatic changes and ocean currents on the dynamics of surface water networks across a global biodiversity phylogeography of the southern African barnacle, Tetraclita hotspot—implications for conservation. Environmental Research serrata (Thoracica; Cirripedia). PLoS One 9: e102115, Letters 9: e114012, http://dx.doi.org/10.1088/1748-9326/9/11/114012 http://dx.doi.org/10.1371/journal.pone.0102115 Wasson K, Zabin CJ, Bedinger L, Diaz MC, Pearse JS (2001) Riding R (2011) The nature of stromatolites: 3,500 million years of Biological invasions of estuaries without international shipping: history and a century of research. In: Reitner J, Quéric N-V, Arp G the importance of intraregional transport. Biological Conse- (eds) Advances in Stromatolite Geobiology. Springer, Berlin rvation 102: 143–153, http://dx.doi.org/10.1016/S0006-3207(01)00098-2

Supplementary material The following supplementary material is available for this article: Table S1. Mean values of abiotic data collected during 2014 from four stromatolite pools invaded by F. enigmaticus and four uninvaded pools.

This material is available as part of online article from: http://www.aquaticinvasions.net/2016/Supplements/AI_2016_Miranda_etal_Supplement.xls

266