Marine Environmental Research 131 (2017) 243e257

Contents lists available at ScienceDirect

Marine Environmental Research

journal homepage: www.elsevier.com/locate/marenvrev

A review of three decades of research on the invasive kelp Undaria pinnatifida in Australasia: An assessment of its success, impacts and status as one of the world's worst invaders

* Paul M. South a, b, , Oliver Floerl a, Barrie M. Forrest a, Mads S. Thomsen c, d a Cawthron Institute, 98 Halifax Street East, Nelson 7010, New Zealand b Institute of Marine Science, University of Auckland, Private bag 92019, Auckland, New Zealand c Marine Ecology Research Group, School of Biological Sciences, University of Canterbury, Private Bag 4800, Christchurch, New Zealand d UWA Oceans Institute & School of Biological Sciences, University of Western Australia, Crawley, WA 6009, Australia article info abstract

Article history: Marine invasive macroalgae can have severe local-scale impacts on ecological communities. The kelp Received 18 July 2017 Undaria pinnatifida is one of the most successful marine invasive species worldwide, and is widely Received in revised form regarded as one of the worst. Here, we review research on Undaria in Australasia, where the kelp is 10 September 2017 established throughout much of New Zealand and south-eastern Australia. The presence of Undaria for at Accepted 16 September 2017 least three decades in these locations makes Australasia one of the longest-invaded bioregions globally, Available online 20 September 2017 and a valuable case study for considering Undaria's invasion success and associated impacts. In Aus- tralasia, Undaria has primarily invaded open spaces, turf communities, and gaps in native canopies Keywords: Invasive macroalgae within a relatively narrow elevation band on rocky shores. Despite its high biomass, Undaria has rela- NIS tively few direct impacts on native species, and can increase community-wide attributes such as primary Kelp productivity and the provision of biogenic habitat. Therefore, Australasian Undaria research provides an Canopy-forming species example of a decoupling between the success and impact of an invasive species. Undaria will most likely Invasion pathways continue to spread along thousands of kilometres of rocky coastline in temperate Australasia, due to its Population control tolerance to large variations in temperature, ability to exploit disturbances to local communities, and the Eradication continued transfer among regions via vessel movements and aquaculture activities. However, the spread Biodiversity of Undaria remains difficult to manage as eradication is challenging and seldom successful. Therefore, Undaria pinnatifida understanding potential invasion pathways, maintaining native canopy-forming species that limit Non-indigenous Undaria success, and effectively managing anthropogenic vectors of Undaria spread, should be key management priorities. © 2017 Elsevier Ltd. All rights reserved.

Contents

1. Introduction ...... 244 2. Establishment and spread of Undaria in Australasia ...... 244 2.1. Discovery and vectors of initial introduction ...... 244 2.2. Ongoing human-mediated spread ...... 244 2.3. Rate and mechanisms of natural dispersal and spread ...... 246 3. Factors affecting the invasion success of Undaria ...... 247 3.1. Life-cycle characteristics ...... 247 3.2. Population biology ...... 247 3.3. Response to physical variables in the recipient environment ...... 247 3.4. Biological interactions and physical disturbances ...... 250 4. Impact of Undaria on structure and function of recipient assemblages ...... 251

* Corresponding author. Cawthron Institute, 98 Halifax Street East, Nelson 7010, New Zealand. E-mail address: [email protected] (P.M. South). https://doi.org/10.1016/j.marenvres.2017.09.015 0141-1136/© 2017 Elsevier Ltd. All rights reserved. 244 P.M. South et al. / Marine Environmental Research 131 (2017) 243e257

4.1. Taxa-specific impacts ...... 251 4.2. Impacts on native communities ...... 252 4.3. Impacts on primary production and biochemical cycles ...... 252 4.4. Impact on secondary production and cross-system subsidies ...... 252 5. Eradication and sustained control of established populations ...... 253 6. Conclusions ...... 254 Acknowledgements ...... 254 Supplementary data ...... 254 References ...... 254

1. Introduction (Hayden et al., 2009). Therefore, research in Australasia provides unique insight into Undaria's role as an invasive species, and an Biological invasions are a significant threat to native biodiversity opportunity to critically evaluate its reputation as being among the and the ecological services it provides. The rate of biological in- world's worst invaders. vasions has increased throughout the world and many high profile More specifically, we collate, summarise and review peer- invaders have been implicated in structural and functional changes reviewed research on Undaria in New Zealand and Australia, in recipient ecosystems (Crooks, 2002; Thomsen et al., 2009; Maggi drawing on literature from other invaded regions where doing so et al., 2015). In recent years, many species of introduced macroalgae leads to greater insight. We highlight factors that drive Undaria's have become conspicuous components of coastal ecosystems, invasion success, the types of impacts it causes, its future invasion where they can have a wide range of impacts on local communities, potential, and associated research gaps. We also consider man- ecosystem function and ecosystem services (Thomsen et al., 2016b). agement successes and failures of Undaria. In total, our review in- One of the most successful and purportedly problematic macro- cludes 50 published journal articles and 6 unpublished post- algal invaders is the laminarian kelp, Undaria pinnatifida (Harvey) graduate theses specifictoUndaria in Australasia, focusing on Suringar (hereafter Undaria). Undaria hasbeenincludedasoneof content that was electronically available following searches on nine marine species in a list of the world's 100 worst invasive species Google Scholar, SCOPUS and Web of Science (S 1). The review is not (Lowe et al., 2000), and in Europe was rated as one of the top 10 exhaustive in terms of the grey literature on Undaria, and does not worst invasive species (Gallardo, 2014) and the third most hazardous necessarily include published research in which Undaria was not of 113 macroalgal introductions (Nyberg and Wallentinus, 2005). the sole focus. Undaria is native to Russia and Asia, with large populations in China, Japan and North Korea, and is extensively cultivated to 2. Establishment and spread of Undaria in Australasia provide a highly prized food resource (e.g., Chaoyuan and Jianxin, 1997; Morita et al., 2003; Skriptsova et al., 2004; Na et al., 2016). 2.1. Discovery and vectors of initial introduction As a result of its commercial importance, Undaria has been widely studied, with aspects of its early life history, genetics and chemical Undaria was first discovered in Australasia in Wellington, New composition receiving particular attention (Lee et al., 2004; Zealand, in 1987, and in Tasmania, Australia, in 1988 (Figs. 1 and 2). Prabhasankar et al., 2009; Wang et al., 2009). However, Undaria However, the arrival time in each location was likely several years has also become one of the most widely distributed invasive marine earlier, given the extensive populations documented in the first macroalgae worldwide, having established in extensive areas in the reports of its occurrence (Hay and Luckens, 1987; Sanderson, 1990). NE Atlantic, SW Atlantic, NE Pacific, SE Pacific, SW Pacific and the For example, the Tasmanian population already extended over Mediterranean and North Seas. 10 km of coastline (Sanderson, 1990), while, in Wellington Harbour, In the light of the continuing spread of Undaria into native thousands of sporophytes were recorded over 7e8km(Hay and communities, and its increasing encroachment onto port and Luckens, 1987). International shipping and fishing vessels are aquaculture facilities (Dellatorre et al., 2014; Heiser et al., 2014; considered to be the likely vectors of initial introduction; for James et al., 2014; Minchin and Nunn, 2014; Pereyra et al., 2015; example, mature sporophytes were found on recently-arrived Atalah et al., 2016b), it is useful to assess the scientific findings ocean-going vessels in the early stages of the invasion in New with respect to the kelp's invasiveness, impacts and management. Zealand (Hay, 1990). However, there have been multiple subse- Here, we focus on Australasia (Australia and New Zealand), where quent introductions to Australasia (Stuart et al., 1999; Wotton et al., Undaria was observed for the first time three decades ago, making 2004; Uwai et al., 2006). In the southern South Island of New this part of the world one of Undaria's longest-invaded bioregions Zealand (e.g., Lyttelton, Timaru and Oamaru Harbours), genetic globally (Fig. 1). Australasia is also the most studied bioregion with variation among populations suggests that, before 2005, there had respect to Undaria's dispersal (Forrest et al., 2000; Sliwa et al., been at least eight different introductions from source populations 2006; Russell et al., 2008; James and Shears, 2016a), population in continental Asia and northern Japan (Uwai et al., 2006). Inter- biology (Schaffelke et al., 2005; Primo et al., 2010; Schiel and estingly, genetic analyses appear to confirm initial hypotheses on Thompson, 2012; James and Shears, 2016b), ecological in- the origins of Undaria into different regions of New Zealand that teractions (Forrest and Taylor, 2002; Valentine and Johnson, 2004; were based on morphological comparisons (Hay and Villouta, 1993; 2005; Thompson and Schiel, 2012), and management (Hewitt et al., Campbell and Burridge, 1998). In Australia, invaded sites showed 2005; Forrest and Hopkins, 2013), reflecting concerns regarding the little haplotype variation, indicating a lower number of successful impacts of this species on the area's unique and diverse native introductions (Voisin et al., 2005; Uwai et al., 2006). marine biota (Battershill et al., 1998). Additionally, the high con- nectivity of coastal areas by anthropogenic activities (e.g., vessel 2.2. Ongoing human-mediated spread movements) within Australia and New Zealand means there is potential for Undaria to invade vast areas of coast in the future Anthropogenic vectors, including commercial shipping, fishing P.M. South et al. / Marine Environmental Research 131 (2017) 243e257 245

Fig. 1. Map showing invaded locations in Australasia and their time of invasion in 5 year bins. A ¼ Australasian overview, B & C ¼ invaded regions in New Zealand and Australia, respectively. The dashed line in A indicates the estimated maximum thermal range in Australasia (Sanderson, 1990; James et al., 2015); note that massive tracts of Australia remain un-invaded, and the entire mainland of NZ is within the this range. Distribution data were obtained from Sanderson (1990), Forrest and Blakemore (2006), James et al. (2014, 2015), James and Shears (2016a), and Atlas of Living Australia (2017). and recreational vessels, and the transfer of aquaculture stock and vectors have facilitated the spread of Undaria far beyond that equipment, are strongly implicated in the spread of Undaria among achievable by natural dispersal mechanisms (Hay and Luckens, regions in Australasia (Hay, 1990; Sanderson, 1990; Floerl et al., 1987; Forrest et al., 2000; Sliwa et al., 2006; Uwai et al., 2006). 2004; Forrest, 2016). The occurrence of Undaria in ports, harbours The occurrence of Undaria on a variety of vessels, including a tug, a and aquaculture regions, and genetic data that show close re- ferry and fishing boats, was documented early in the invasion lationships among distant sites, indicate that anthropogenic timeline (Hay, 1990). Regional dispersal by vessel movements 246 P.M. South et al. / Marine Environmental Research 131 (2017) 243e257

Fig. 2. Undaria pinnatifida in natural and artificial habitats. In A, an extensive population of Undaria occupies the low zone in Moeraki, New Zealand. B, the common grazer Lunella smaragda grazes on senescent Undaria in late summer. C, a mature sporophyte of Undaria attached to mussel aquaculture ropes in Marlborough, New Zealand. D, juvenile Undaria attached to the hull of boat. Photograph credits: Paul South (A), Mads Thomsen (B) Barrie Forrest (C), Cawthron Institute (D). appears to have been particularly important in the upper South 2.3. Rate and mechanisms of natural dispersal and spread Island and the North Island of New Zealand, where only one haplotype was found prior to 2005 in all of six invaded sites that The rate of local-scale spread of Undaria from founding pop- were sampled (Uwai et al., 2006). In addition, this same haplotype ulations in Australasia has been highly variable among regions. In was present in Port Phillip Bay, indicating that inter-regional Timaru, New Zealand, Undaria achieved only a 1-km expansion transfer was taking place up to ten years after the discovery of onto the open coast despite a prolific 20-year tenure within the Undaria in Australasia (Campbell and Burridge, 1998). harbour (Hay and Villouta, 1993; Russell et al., 2008). In that loca- Undaria continues to spread to new regions both in Australasia tion, the range of Undaria was likely constrained by unconsolidated and worldwide (Dellatorre et al., 2014; James et al., 2014; Minchin gravel substrata that dominate the coastline, preventing colonisa- and Nunn, 2014; Ministry for Primary Industries, 2017). As hubs of tion (Russell et al., 2008). Once Undaria has invaded open coastal vessel activity (e.g., ports, marinas) and aquaculture have become systems with suitable hard substrata, its spread can become more increasingly colonised by Undaria, so has the kelp's association with rapid. For example, the rate of spread from two harbours (Otago human transport vectors. For example, during monitoring conducted and Moeraki) in southern New Zealand was 1- and 2-km per year, in several southern New Zealand ports in 1998e2001, Undaria was respectively (Russell et al., 2008). The most dramatic spread from a encountered on 31e50% of commercial and recreational vessels, founding population has been in Tasmania where Undaria (Forrest and Hopkins, 2013). Consequently, Undaria is being trans- increased its range by around ten kilometres per year along the ported into remote and often pristine coastal regions to which it eastern coast, to occupy 320 km of coastline in 2002 (Shepherd, would be unable to spread via natural dispersal. For example, in 2010 2013). However, it is difficult to calculate rates of secondary Undaria was detected in the vicinity of an isolated vessel mooring in spread with certainty, as it is not possible to distinguish whether New Zealand's Fiordland region, a remote area of high biodiversity new areas are colonised through natural dispersal alone (drift of value. An ongoing effort to eradicate the population was recently set- reproductive sporophytes or microscopic propagules; see below), back by the discovery of Undaria at a second mooring area a few or whether rates of spread have been enhanced by anthropogenic kilometres away from the initial incursion (Fiordland Marine vectors (Forrest et al., 2000; Sherman et al., 2016). Guardians, 2017). These Australasian examples clearly highlight The mechanisms underlying the spread of Undaria in natural that understanding the pathways of anthropogenic vectors is of environments likely include interactions among local hydrody- primary importance when assessing the likely spread of Undaria,and namic conditions, propagule pressure, substratum type, and indeed any invasive macroalga. To this end, studies of genetic vari- structure of the local assemblages (Forrest et al., 2000; Sliwa et al., ation (e.g., Voisin et al., 2005; Uwai et al., 2006) offer valuable insight 2006; Russell et al., 2008; Schiel and Thompson, 2012; James and into patterns of spread over more traditional morphological com- Shears, 2016a). Dispersal from asexual reproduction of the sporo- parisons, due to the high morphological plasticity of Undaria (Stuart phytes is estimated to be small (1e100 m), and depends on mor- et al., 1999; Sherman et al., 2016). tality of the spores, current velocity and direction, dilution of spores in the water column, and availability of settlement substrata (Forrest et al., 2000; Schiel and Thompson, 2012). Local-scale spread can be increased by one to two orders of magnitude by P.M. South et al. / Marine Environmental Research 131 (2017) 243e257 247 the drift of unattached sporophytes, or by sporophytes attached to 2012). In Wellington, a narrow band of reproductive adults was unstable substrata such as cobbles that are transported by wave- found on artificial substrata in February and March (late summer, action and water currents (Schaffelke et al., 2005; Sliwa et al., 1991) when the majority of the previous cohort had senesced (Hay 2006). Such variation in modes of dispersal allows Undaria to and Villouta, 1993). Similarly in the North Island, Undaria sporo- make episodic range expansions across a range of spatial scales phytes with reproductive structures were found throughout the (Sliwa et al., 2006; Forrest et al., 2009). The resulting founding year on mussel farms in the Hauraki Gulf, but individuals were in populations may occur in intertidal pools (Russell et al., 2008)or very low abundance in late summer (mean ~ 0.5 m 2)(James and result from a step-wise or episodic progression in the shallow Shears, 2016a). It is likely that the shift of Undaria in New Zea- subtidal (Forrest et al., 2000; Schiel and Thompson, 2012). Given land from a strictly annual species to one whose inter-annual co- that Undaria is negatively buoyant, the success of subtidal drift is horts overlap is due to the smaller, more favourable temperature likely to vary among sites due to variations in water depth, currents, range in New Zealand compared to its native range (Hay and nearshore topography and habitat availability. In southern New Villouta, 1993; James and Shears, 2016b). Zealand for example, Undaria can dominate the algal assemblage on In addition to the occurrence of overlapping inter-annual pop- rocky shores in certain locations, yet comprise only 9e20% of ulations, Undaria has been reported to produce biannual cohorts of stranded wrack on adjacent sandy beaches (Jimenez et al., 2015a). recruits in parts of New Zealand (Schiel and Thompson, 2012). In Hence, it is likely to be the case that some of the detached Undaria is Moeraki, pulses of recruits were observed in autumn and spring, transported offshore, although this possibility has not been tested with the spring recruitment occurring during senescence of the in Australasia and remains a significant research gap (Table 1, also autumn cohort (Schiel and Thompson, 2012). In such situations, it is see section 4.4). likely that the loss of conspecific canopy associated with Undaria senescence increases light availability and facilitates recruitment 3. Factors affecting the invasion success of Undaria from gametophytes or juvenile sporophytes in the understorey (Thompson and Schiel, 2012). In northern New Zealand, however, 3.1. Life-cycle characteristics populations of Undaria on artificial habitats (marina jetties) have one annual cohort during a constricted growth period that more Biological traits such as a high reproductive output, fast growth, closely resembles the annual life-cycle of Undaria in its native range early and rapid maturation, and ability to delay development for (James and Shears, 2016b). extended periods in unfavourable conditions, have allowed Undaria The distinction between populations that have either a high, to become a highly successful invader in Australasia (Campbell, low, or fluctuating year-round cover is critical, because high year- 1999; Schaffelke et al., 2005; Dean and Hurd, 2007; Schiel and round cover is likely to have a greater impact on the structure Thompson, 2012). Undaria has an annual, heteromorphic life- and function of the recipient assemblage than populations with cycle characterised by alternating macroscopic sporophytes intermittent periods of high and low cover. Indeed, it has been (longevity ¼ 5e7 months) and microscopic gametophytes and hypothesised that the lack of a persistent dense perennial cover is sporelings (Saito, 1975). The development of the meiospore to responsible for the relatively weak direct impact of Undaria on dioecious gametophytes, zygotes and embryonic sporophytes (c. recipient communities in some locations (Thompson and Schiel, 1 mm in length) can take three weeks, but all stages can delay or 2012; South et al., 2016; South and Thomsen, 2016). Multiple co- exhibit reduced development when resources are limited horts might enhance the invasion success of Undaria as they can (Thompson, 2004; Morelissen et al., 2013). Indeed, initial pulses of increase temporal propagule pressure in invaded sites (Schiel and autumn recruitment are typically derived from microscopic spo- Thompson, 2012). It is also likely that the occurrence of two co- relings or gametophytes that have survived over summer (c. 5 e 7- horts annually contributes to over-lapping inter-annual pop- months) (Thompson, 2004; Schiel and Thompson, 2012; ulations and a more sustained macroscopic presence of Undaria in Morelissen et al., 2013). It is unknown exactly how long the invaded habitats. Further work at a greater number of invaded lo- different microscopic life-stages can persist, although recruitment cations is needed to more broadly understand the persistence and from such stages has been observed to take place for up to 2.5-years population biology of Undaria in Australia and New Zealand. It is (Hewitt et al., 2005). The capacity to delay development, coupled crucial that such studies report not only abundances of Undaria, but with a massive reproductive output (1.2 million spores per cm2 of also include relevant population metrics such as cover, biomass and tissue and up to 700 million per individual), gives Undaria signifi- sporophyte size (Table 1). cant potential to persist microscopically in invaded locations (Schiel and Thompson, 2012). Under favourable conditions, Undaria 3.3. Response to physical variables in the recipient environment can grow at 15 mm per day, allowing it to occupy space quickly, and become reproductive within one to three months after recruitment Undaria is able to tolerate wide variations in physical factors (Schaffelke et al., 2005; Primo et al., 2010; Schiel and Thompson, such as substratum conditions, water temperature, and wave 2012). climate (Hay, 1990; Russell et al., 2008; James et al., 2014, Fig. 3). A key factor in the initial success of an Undaria invasion is likely to be 3.2. Population biology its ability to settle and develop to reproductive maturity on almost any hard substratum in the marine environment. For example, Undaria is an annual species in its native range, with a distinct Undaria has been found attached to natural cobbles, bedrock, snail hiatus when its macroscopic form is absent (Morita et al., 2003). In shells (including abalone), coralline algae, canopy forming algae New Zealand, Undaria can have a modified phenology, being found and seagrass blades; as well as artificial surfaces including plastic at some sites year-round (Hay and Villouta, 1993; Schiel and buoys, metal boat hulls (and associated marine coatings), concrete Thompson, 2012; James et al., 2015), although in many of these wharf pilings, steel cable, wooden pontoons, mooring ropes, and sites it still exhibits an annually occurring period of low abundance commercial mussel crops (Hay, 1990; Brown and Lamare, 1994; and cover (Thompson and Schiel, 2012; James and Shears, 2016a). Campbell and Burridge, 1998; Wotton et al., 2004; Forrest and For example, year-round populations were found at Moeraki where Blakemore, 2006; Sliwa et al., 2006; Thompson and Schiel, 2012). the remnants of old individuals from the previous year overlapped Ports, harbours, marinas and aquaculture sites offer extensive with new recruits in the following year (Schiel and Thompson, artificial substrata, including shallow floating structures (e.g. 248 P.M. South et al. / Marine Environmental Research 131 (2017) 243e257

Table 1 Knowledge gaps pertaining to the invasion of Undaria in Australasia.

Topic Question Rationale Possible methods

Dispersal Does Undaria continue to be introduced to Gauging whether the transfer of Undaria from natal Genetic analyses of haplotype variation. already invaded areas via human vectors? realms and among already invaded regions continues remains a considerable research gap that has implications for population resilience (due to increased genetic diversity), the potential for Undaria to expand its range, and the likely efficacy of eradication programmes Dispersal What are the relative importance of natural and Natural dispersal mechanisms (e.g., drifting Modelling of relative dispersal among natural and human mechanisms of dispersal in episodic sporophytes) are often considered to be more human mechanisms of spread. Vessel movement range expansions? important than human mediated spread (e.g., thalli and fouling surveys. Detailed benthic surveys attached to boat hulls) in open coast situations. within and across years. However, this has never been shown to be the case Dispersal/ What is the fate of sunken Undaria biomass and Undaria is negatively buoyant and sunken drifting Subtidal surveys in the vicinity of Undaria beds. trophic how does it affect trophic subsidies and patterns plants could be an important dispersal mode. Stable isotope studies. Hydrological modelling of effects of dispersal? Furthermore sunken Undaria biomass could potential pathways. subsidise benthic detritivore communities, especially since this has been observed on intertidal beaches where Undaria biomass was relatively low Distribution What is the abundance of Undaria at increasing The abundance of Undaria at depths greater than 6 Structured surveys of Undaria cover and density water depth? (NZ) or 12 (Australia) metres has not been reported and recipient assemblages across depth gradients. and is critical if the impact of this species is to be understood Distribution What factors determine the vertical distribution The distribution of Undaria appears to be depth- Correlative studies of Undaria and abiotic variables of Undaria in the subtidal? Is this due to light limited such as light availability, turbidity, nutrients and limitation, negative interactions with native native assemblages. Experiments to manipulate species (e.g., grazing and competition) or other light availability, nutrients and grazer density in factors? recipient habitats. Distribution What factors determine the vertical distribution Undaria does not generally occur above low water Transplant experiments, grazer exclusion of Undaria in the intertidal? Is this due to neap in Australasia experiments. desiccation, negative interactions with native species or other factors? Competition Do early life-stages of Undaria and native species Competition among early life stages of native algae Factorial laboratory experiments, out-plants of compete for resources such as nutrients, space and Undaria has not been studied in any detail Undaria and native gametophytes, sporelings and and light? recruits at manipulated, crossed densities. Phenology What are the percent cover, density, biomass, Year-round populations have been reported in Surveys to quantify cover, biomass, density and demography, and reproductive phenology of some studies, however, ecologically relevant demographic variables such as age, size and year round populations of Undaria in natural metrics (in particular, cover and biomass) that reproductive status and output. assemblages? might mediate impacts, are infrequently recorded. A full understanding of the temporal presence of Undaria remains evasive Phenology Does recruitment occur from newly released The occurrence of two cohorts annually is an Assessments of reproductive outputs, viability, and spores, or from extant gametophytes or ecologically important demographic change that fitness and longevity of meiospores, gametophytes demography sporelings (from the previous cohort) in areas could be due to favourable environments for early and sporelings among cohorts. that have two cohorts annually? life stages (e.g. increased longevity of sporelings) or adults (i.e., a second reproductive adult cohort per year) Impact How does the ecological impact of Undaria vary The impacts of Undaria have only been tested in a Undaria removal or addition experiments. among habitats (e.g., mussel beds, Macrocystis few habitats Correlation studies. pyrifera forests, Ecklonia radiata stands)? Impact Are impacts of Undaria density dependent? No study has used more than 2 levels (±)ofUndaria Factorial experiments with multiple managed density/cover and tested for linearity of effects densities of Undaria. Impact Does Undaria have sub-lethal, cryptic or delayed The responses of relatively few variables (e.g., Manipulative experiments quantifying a wider impacts on the recipient environment? cover, density, productivity) have been studied for range of response variables. Undaria. However, Undaria could impact less easily (or frequently) measured variables such as the reproductive out-put, growth and sub-lethal physiological responses of native species Impact What are the socio-economic impacts of Undaria Undaria is a high value seaweed that is now Socio-economic impact analysis. in Australasia? harvested or actively cultured in some areas of Australasia. By contrast, scientific research, and control and eradication are costly activities. There are likely to be many economic costs and benefits associated with the advent of Undaria Impact/trophic How does Undaria affect food-web structure? Native species consume Undaria differentially Modelling of food-web networks. effects therefore this could modify food-web structure Impact/trophic How does primary production and epifaunal Undaria can displace native species, but their Targeted surveys, epifaunal sampling and effects assemblages of Undaria compare to the species it ecology is often poorly understood - to gauge the assessments of primary productivity. has been shown to displace (e.g., Colpomenia effects of Undaria relevant contrasts must be made sinuosa)? Spread, How does Undaria colonise and impact new Undaria is purported to have negative impacts on Establish baseline surveys in areas that have the mechanisms areas? important taxa in the recipient community (e.g., potential to be invaded. Use Before After Control of invasion other canopy-forming algae), but this has not been Impact (BACI) analysis or manipulative and impact shown, potentially due to a lack of base line data experiments to assess impacts. and the difficulty in studying the invasion process as it occurs P.M. South et al. / Marine Environmental Research 131 (2017) 243e257 249 marina pontoons, marine farms) on which Undaria can be prolific Fig. 1). Furthermore, future water temperature and pH scenarios (James and Shears, 2016a). Reasons for Undaria's success on such anticipated in New Zealand are unlikely to affect population structures are likely to include the absence of benthic grazers and viability and ongoing spread, as Undaria meiospore and gameto- other large canopy-forming algal species that might otherwise limit phyte development and germination are not expected to be invasion success (e.g., Atalah et al., 2016b), and a light environment, adversely affected (Leal et al., 2016, 2017). at least on floating structures, that is not influenced by depth- There are many aspects of the ecology of Undaria that remain related tidal changes (Fig. 3, see section 3.4 for detail). Thus, little-studied or unclear (Table 1). For example, from limited Undaria has thrived in artificial coastal habitats within which it can studies, Undaria appears to be highly competitive for nutrients, spread largely unimpeded (Hay, 1990). In Wellington Harbour for especially in its juvenile period during winter when nitrate is example, Undaria spread among coastal infrastructure over 4 km in available in relatively high concentrations (Campbell, 1999; Dean 1-year (Hay, 1990). In port and harbour locations, invasive species and Hurd, 2007). Similarly, Undaria gametophytes, zygotes and such as Undaria can make use of the extensive hard substrata as sporelings benefit from elevated nutrients, although this can “stepping stones” to further their spread and population develop- depend on irradiance levels (Morelissen et al., 2013). The ment (Floerl et al., 2009; Bulleri and Chapman, 2010). These stable geographical limits resulting from light availability, and salinity, and extensive populations can serve as sources of propagules for wave-exposure, and their interactions with depth, are uncertain, introductions into distant sites (i.e., by human-mediated spread), partly due to contradictions among results from laboratory studies and conceivably can put intense propagule pressure on adjacent and the reported distribution of Undaria. native communities (Ruiz et al., 2009; Simkanin et al., 2012; Forrest Undaria has a lower saturated light requirement and compen- and Hopkins, 2013). sation points, and greater photosynthetic efficiency than several The tolerance of Undaria to wide variations in temperature is native Australasian laminarian and fucoid algae (Campbell et al., one of the attributes that has allowed it to become a successful 1999; Tait et al., 2015). However, the native species can be domi- invader, and makes it likely that Undaria will continue to expand its nant to depths of 15 and > 40 m in New Zealand (Schiel, 1990) and range throughout uninvaded temperate zones in Australasia (James Australia (Sanderson, 1997), respectively. In New Zealand, for et al., 2015). Indeed, based on its maximum and minimum thermal example, the abundance of Undaria below six metres depth has not limits (13.5e29.5 C and 0.1e15.5 C, respectively) across latitudes been quantified, despite anecdotal observations about its occur- in its native range (Sanderson, 1990; James et al., 2015), Undaria has rence in deeper waters (Hay and Luckens, 1987; Dean and Hurd, the potential to colonise much of the southern Australian coastline 2007). The limited evidence about Undaria distribution along from Cape Leeuwin in the south-west to Woolongong in the south- depth gradients, suggests that Undaria peaks in abundance just east of Australia, and the entire mainland of New Zealand as well as below the intertidal zone (to 4 m) and thereafter declines with Stewart Island, the Chatham Islands (both already invaded) and the depth (Brown and Lamare, 1994; Russell et al., 2008; Richards et al., southern sub-Antarctic islands (Snares Island is already invaded, 2011). Similarly, most Australasian studies have focused on

Fig. 3. Overview of local environmental conditions that control invasion success of Undaria pinnatifida. Blue ¼ facilitation, Red ¼ inhibition. Interactions between the local con- ditions (e.g., resources, facilitators and enemies) are important. For example, Undaria might not be successful <4 m depth because of combined effects of light limitation and dominance of large perennial canopy formers. Citations from experimental (italics) and correlative (underlined) studies are given. Image credits: Integration and Application Network, University of Maryland Centre for Environmental Science (ian.umces.edu/imagelibrary/). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.) 250 P.M. South et al. / Marine Environmental Research 131 (2017) 243e257 populations of Undaria in shallow water (0e6m,Edgar et al., 2004; disturbances and grazing pressure on Undaria abundance Hewitt et al., 2005; Jimenez, 2015) with the exception of two (Thompson, 2004; Valentine and Johnson, 2005, Fig. 3). In southern studies done on Tasmanian reefs (7e12 m, Valentine and Johnson, New Zealand, recruitment of Undaria was similar among plots 2003; Valentine and Johnson, 2005) and in which the cover of where grazers had been excluded with cages and open controls, Undaria was low relative to other studies from shallower water despite the fact that a common grazer (Lunella smaragda) reduced (Jimenez et al., 2015a; South et al., 2016). If Undaria does have sporeling abundances in laboratory experiments (Thompson, reduced abundance at depth this could be explained by light lim- 2004). By contrast, Undaria was the only canopy-forming macro- itation during its early life history. For example, gametophyte alga to inhabit sea urchin (Heliocidaris erythrogramma) barrens in development is stunted at low levels of irradiance (below c. 10 mmol Tasmania regardless of whether the sea urchins were excluded or quanta m 2 s 1), although gametophytes and embryonic sporo- not, suggesting indirect facilitation from urchins on Undaria phytes can grow vegetatively in such low light environments until abundance by inhibition of native competitive canopy forming conditions favour photosynthetic growth (Morelissen et al., 2013). species (Valentine and Johnson, 2005). The advent of Undaria on Overall, the reasons for the apparent reduced abundance of Undaria urchin barrens has also been noted in north-eastern New Zealand at depth are unclear (Table 1). As well as reduced physiological (James and Shears, 2016a). performance in low light conditions, other limiting factors could By contrast with the limited knowledge of grazer effects, the include competition with native canopy-formers, increased grazing role of physical disturbance in facilitating invasion of native as- pressure, less substratum availability and increased stress from semblages by Undaria has received considerable attention in Aus- sedimentation (Valentine and Johnson, 2005; Thompson and tralasia. Studies have typically shown high recruitment into areas Schiel, 2012; Geange et al., 2014). where native canopy-formers have been removed by single pulse At the upper extent of Undaria's vertical distribution, intertidal disturbances (Valentine & Johnson 2003, 2004, 2005; Thompson populations do not typically occur higher on the shore than the low and Schiel, 2012; Carnell and Keough, 2014; South and Thomsen, water neap tide mark (Forrest and Taylor, 2002; South et al., 2016), 2016). This outcome is likely a response to increased light and meaning Undaria does not inhabit the neap tide to mid-shore zone decreased physical abrasion by fronds in the absence of the native that is often occupied by native algal species such as Hormosira canopy-formers (Valentine and Johnson, 2003; 2004; Thompson banksii and Cystophora torulosa (Lilley and Schiel, 2006). We expect and Schiel, 2012; Morelissen et al., 2013). Positive effects of can- that desiccation likely constrains the neap tide upper limit of opy loss on Undaria recruitment were shown to be consistent Undaria, although are not aware of any studies that have experi- across clearings of different sizes (0.01, 0.0625, 0.25 m-2) and mentally investigated this or alternative mechanisms, such as regardless of whether the canopy is inter- or intraspecific competition with intertidal algae or grazing by invertebrates (Thompson and Schiel, 2012). However, Undaria does not appear to (Table 1). Overall, a vertical distribution in which Undaria typically be able to maintain its cover, and in one study was replaced by the occurs in a narrow band from neap low tide to 4 m subtidal, mirrors initial canopy-former over five months to a year (Thompson and that in its native range (Morita et al., 2003). Schiel, 2012), and in another study by mixed communities in Patterns in the geographic distribution of Undaria suggest that it which Undaria became a subordinate species over 1- to 2-years is limited by excessive wave action and low salinity. For example, (Valentine and Johnson, 2003). Thus, it appears that Undaria is Undaria has not been reported from the exposed west coast of New competitively inferior to many native canopy-forming species over Zealand, where significant wave heights between seven and eight longer-term stable conditions (Valentine and Johnson, 2003; Schiel metres are not uncommon (National Institute of Water and and Thompson, 2012). A consistent result emerging from these Atmosphere, 2017). However, Undaria has invaded wave exposed experiments is that the presence of a dense bed of intact native regions of south eastern (Russell et al., 2008) and north eastern canopy-forming algae greatly reduces the local-scale invasion (James and Shears, 2016a) New Zealand. Such a discontinuity success of Undaria. Furthermore, the ability of dense stands of among east and west coasts could reflect greater and more native canopy-forming macroalgae to resist invasion by Undaria consistent significant wave height on the west coast, or variations appears to be consistent among geographic regions, and variations in anthropogenic or biological factors. For example, north-eastern in the identity of native species (Raffo et al., 2009; De Leij et al., populations of Undaria in exposed locations appear to be associ- 2017). ated with urchin barrens (James and Shears, 2016b). It is unknown The majority of experimental studies that have tested for the whether Undaria has the ability to establish on exposed coasts in effects of disturbance on Undaria recruitment have focused on deeper subtidal habitats that are less affected by wave energy, and disturbance to stands of native canopy-forming algae, and have where other factors such as low-light conditions are not limiting. simulated disturbances by removing the canopy in order to mimic Furthermore, optimal hydrodynamic conditions for Undaria have events such as storms, grazing or die-back. However, habitats on not been assessed and remain a considerable research gap (Table 1). temperate reefs commonly vary from those dominated by canopy- With respect to salinity, Undaria has not been reported from forming macroalgae, to low-lying assemblages that are charac- estuarine locations in Australasia, contrasting its distribution in the terised by coralline algae (Dayton et al., 1984) or invertebrates such UK (Fletcher and Farrell, 1998). The absence of Undaria from estu- as mussels (Menge et al., 2007). Low-lying assemblages dominated arine locations is surprising given the ability of zoospores to by coralline algae are readily invaded by Undaria, and experimental germinate in salinities as low as 8 SA (Bite, 2001), and because adult disturbance to these assemblages does not increase Undaria tissues remain photosynthetically viable down to 6 SA (Bollen et al., recruitment (Schiel and Thompson, 2012; Thompson and Schiel, 2016). However, the distribution of Undaria in low salinity envi- 2012; Morelissen et al., 2016). For example, the removal of entire ronments is possibly limited by differences in tolerance among low-lying assemblages of predominantly coralline turf and other different life stages of Undaria (Peteiro and Sanchez, 2012), small algae had no effect on the number of Undaria recruits smothering by sediment (Geange et al., 2014), or factors discussed compared to intact control plots, indicating that Undaria does not above such as light-limitation (Morelissen et al., 2013). require disturbance to invade low-lying intertidal assemblages (Morelissen et al., 2016). Indeed, Undaria appears to be facilitated 3.4. Biological interactions and physical disturbances by geniculate coralline algae, likely due to a reduction of desiccation stress and grazing pressure (Thompson, 2004; Thompson and Surprisingly, little is known about the role of biological Schiel, 2012). By contrast, coralline turfs can inhibit the P.M. South et al. / Marine Environmental Research 131 (2017) 243e257 251 recruitment of native canopy-forming algae that do not attach to Johnson, 2003; Edgar et al., 2004; Thompson and Schiel, 2012; the turf or the sediment within its matrix (Schiel et al., 2006; South and Thomsen, 2016). Furthermore, invader-removal studies Bellgrove et al., 2010; Alestra et al., 2014), and which could other- suggest that Undaria does not reduce the abundance of canopy- wise outcompete Undaria (Valentine and Johnson, 2003). There- forming seaweeds (Valentine and Johnson, 2005; South et al., fore, coralline turfs can facilitate invasion by Undaria through direct 2016; South and Thomsen, 2016). For example, native canopy for- and indirect pathways (Thompson, 2004; Thompson and Schiel, mers did not colonise plots that were kept free of Undaria for over 2012). Furthermore, disturbance to stands of native canopy- 2-years in southern New Zealand, and native recruits were similar forming algae can facilitate coralline and other turf-forming algae among plots with and without Undaria following experimental that can in turn prevent re-colonisation by the native species, removals of the native canopy (South et al., 2016; South and providing a mechanistic explanation for the continued presence of Thomsen, 2016). The results from experimental studies are sup- Undaria in some locations (Valentine and Johnson, 2005). ported by BACI analyses done across four sites over three years in Importantly, areas lacking high cover of native canopy-forming Lyttelton Harbour, New Zealand that suggested Undaria did not macroalgae can maintain dense populations of Undaria, with negatively affect local assemblages, rather it became most abun- mature Undaria sporophytes providing a supply of propagules to dant under conditions that simultaneously favoured native mac- canopy understoreys that allow the invader to exploit canopy loss roalgae (Forrest and Taylor, 2002). However, in Victoria, Australia, (Schiel and Thompson, 2012). Given the wide variety of substrata Undaria reduced the size of re-colonising Ecklonia radiata recruits, and assemblages to which Undaria can recruit, a key niche seems to but only when simultaneously exposed to elevated nutrient levels, be any space lacking large native perennial canopy-formers. Given suggesting that Undaria might be capable of causing long-term the patchy nature of many coastal assemblages it is likely that there changes to invaded assemblages (Carnell and Keough, 2014). Still, are many vacant niches in space and time that can be filled by this the impact of Undaria on recruitment of native perennial canopy invader, which is an important consideration for managers under- forming species in Australasia appears to be weaker than that of taking site-specific risk analysis of the invasion threat (Russell et al., other large invasive algae such as Codium fragile ssp. tomentosoides 2008; Schiel and Thompson, 2012). Indeed, the ability of Undaria to (Levin et al., 2002; Scheibling and Gagnon, 2006) and Sargassum fill vacant space has become prescient on the Kaikoura coast of New muticum (Ambrose and Nelson, 1982; Stæhr et al., 2000; Britton- Zealand, where a 7.8 magnitude earthquake caused massive uplift Simmons, 2004). (1e6 m over 100 km) of reefs on November 14, 2016. This uplift There is, however, increasing evidence that Undaria can inhibit resulted in the almost complete die-off of dense forests of intertidal smaller seasonal or opportunistic native species (Valentine and and subtidal algae in which Undaria had only occurred in small, Johnson, 2005; South et al., 2016; South and Thomsen, 2016). For isolated, populations (South and Thomsen, unpubl. data and pers. example, invading Undaria reduced the cover of the seasonal alga obs). It is highly possible that Undaria will benefit from losses of Colpomenia sinuosa (Phaeophyceae, Ectocarpales) compared to native canopy-formers, expanding its range to become an abundant experimental plots where Undaria had been removed (South and species on the Kaikoura coast. Furthermore, it is also possible to Thomsen, 2016). Similarly, filamentous algae were inhibited by envision accelerated invasion success along much of the uninvaded Undaria on subtidal urchin barrens in Tasmania, suggesting that coastline of Australasia, in the event that native canopies shift to Undaria can be a ‘passenger-turned driver’ of change (Valentine and turf-dominated assemblages due to stressors such as moving ur- Johnson, 2005; Bulleri et al., 2010). In addition, established stands chin fronts (Ling et al., 2009), heatwaves (Wernberg et al., 2013), of Undaria occasionally displaced the seasonal alga Lophothamnion ocean warming (Connell and Russell, 2010) and acidification hirtum (Rhodophyceae, Ceramiales) during a 2.5-year Undaria (Connell et al., 2013), urbanisation (Benedetti-Cecchi et al., 2001; removal experiment (South et al., 2016). Gorman and Connell, 2009), and eutrophication (Airoldi, 1998; Taken in concert, these results highlight that negative impacts Bellgrove et al., 2010). only occurred when Undaria cover was greatest (i.e., in spring e early summer), and did not persist within and between years 4. Impact of Undaria on structure and function of recipient (Valentine and Johnson, 2005; South et al., 2016). Therefore, the assemblages direct effects of Undaria are space, time and taxon-specific, and might be of greater importance when the recipient assemblage is 4.1. Taxa-specific impacts dominated by small taxa with temporally variable distributions that match that of Undaria. Still, we caution against strong in- The most important questions regarding the impact of invasive ferences about the impact of Undaria, as direct effects have only species are whether they simply follow ecological change or exploit been tested with manipulative experiments in five published vacant niches (‘passenger’), are a direct cause of ecological change studies worldwide (Casas et al., 2004; Valentine and Johnson, 2005; (‘driver’), or whether this role changes over time (‘passenger- Irigoyen et al., 2011a; South et al., 2016; South and Thomsen, 2016), turned-driver’)(Didham et al., 2005; MacDougall and Turkington, and the context dependency of its impact remains poorly under- 2005; Bulleri et al., 2010; Bauer, 2012). In Australasia, the impacts stood (Thomsen et al., 2011). Furthermore, these five removal ex- of Undaria on native species have been determined via experiments periments are potentially biased because the removals necessarily that have either removed native canopy-forming algae (Valentine took place at an already invaded site, which may already have been and Johnson, 2003; Edgar et al., 2004; Thompson and Schiel, affected by the invader (or another independent factor, e.g., 2012; Carnell and Keough, 2014), the invader itself (Valentine and elevated nutrients) prior to the experiment (Didham et al., 2005; Johnson, 2005; Morelissen, 2012; South et al., 2016), natives and Bulleri et al., 2010). Similarly, small-scale removal experiments do the invader (South and Thomsen, 2016), or have used mensurative not account for possible functional impacts (e.g., due to detrital Before-After Control-Impact (BACI) experimental designs (Forrest production) from the Undaria adjacent to cleared plots. Accord- and Taylor, 2002) to infer its effects. ingly, removing the invader could, in contrast to the true initial Studies that have experimentally tested the competitive ability invasion effects, have little measurable effect (Bulleri et al., 2010). It of Undaria to invade intact stands of native canopy-formers indicate is therefore necessary that future research takes steps to incorpo- that it does not ‘drive’ change, because un-manipulated canopies rate factors that decouple the causes and effects of Undaria invasion were generally not invaded and canopy-formers were able to (e.g., Bulleri et al., 2010; Mulas and Bertocci, 2016; South and recolonise areas despite the presence of Undaria (Valentine and Thomsen, 2016). 252 P.M. South et al. / Marine Environmental Research 131 (2017) 243e257

4.2. Impacts on native communities the displaced or replaced species. An alternative view of Undaria recruitment following canopy loss is that it buffers losses of pri- Reported impacts of Undaria on community metrics such as mary production until the native canopy can recolonise the species richness, evenness, or diversity have generally been neutral, disturbed habitat (e.g., Thompson and Schiel, 2012). regardless of the trophic level studied. For example, no impact on the richness, diversity or community structure of large mobile in- 4.4. Impact on secondary production and cross-system subsidies vertebrates (>5 mm) was detected over 2.5-years at Moeraki, New Zealand (South et al., 2016). Direct negative effects of Undaria on Canopy-forming macroalgae provide biogenic habitat for many algal assemblages appear to be few and tend to reflect reductions in organisms and can have cascading effects on epiphytic algae, ephemeral algae (see earlier discussion in this section), rather than epifauna and secondary production (Bulleri et al., 2006; Gribben widespread structural change (South et al., 2016; South and and Wright, 2006; Schmidt and Scheibling, 2007; Thomsen, Thomsen, 2016). However, effects on algae may also be facilita- 2010). Invasive macroalgae are often novel in structure, palat- tive; an increased richness of small native macroalgae in the low ability, and function, and lack co-evolutionary interactions with intertidal of Lyttelton Harbour was associated with increased native organisms. However, Undaria is morphologically simple Undaria cover or abundance, possibly because the Undaria canopy compared to many Australasian canopy-forming macroalgae and provided shelter from desiccation, or alternatively because Undaria can support fewer epifaunal organisms (Jimenez, 2015), a pattern and the small native taxa had similar habitat requirements (Forrest that is similar in other parts of the world (Arnold et al., 2015). The and Taylor, 2002). abundance and diversity of epiphytes on Undaria has not been studied, to our knowledge, in Australasia. In Spain, epiphytes on 4.3. Impacts on primary production and biochemical cycles Undaria represent small filamentous species such as those within the orders Ectocarpales and Ceramiales (Peteiro and Freire, 2013) The establishment of large populations of Undaria can sub- and contrast with the many larger epiphytic species observed on stantially increase net primary production and the capture of nu- native macroalgae in Australasia (Thomsen, unpubl. data). Thus, trients on invaded reefs during its macroscopic period (Dean and due to a combination of rapid growth, ephemeral life strategy, Hurd, 2007; Tait et al., 2015; South et al., 2016). For example, simple blade-like morphology and ‘smooth’ surface, Undaria pro- Undaria doubled net primary production and contributed an vides a poor habitat for both sessile and mobile epibiota. The im- additional 140.5 and 2.66 g m 2 of Carbon and Nitrogen (dry plications of fewer epibiota on Undaria compared to native weights), respectively, to a low-lying assemblage in southern New macroalgae could represent a net loss of diversity, if Undaria dis- Zealand (South et al., 2016). Undaria thalli erode from the apices of places native species, or a net gain if it either increases biogenic the laminae (from 0.24 ± 0.07 to 0.79 ± 0.2 cm d -1) until only habitat in invaded low-lying assemblages (Irigoyen et al., 2011a), or sporophylls and holdfasts remain at the end of their life (Dean and temporarily fills an open gap following disturbances (Thompson Hurd, 2007). Therefore, nutrients stored in the entire thallus are and Schiel, 2012). slowly redistributed into the water column and likely modify local To date, there is little evidence to support that Undaria displaces biochemical cycles and food webs, especially when Undaria occurs native canopy-forming species (Forrest and Taylor, 2002; Valentine in high abundance (Dean and Hurd, 2007; South et al., 2016). and Johnson, 2005; South et al., 2016; South and Thomsen, 2016). Undaria is atypical compared to native canopy-forming algae in Rather, it seems likely that Undaria has a facilitative effect on Australasia due to its annual life history, fast growth and the timing invertebrate abundances, through the provision of additional re- of its development during the cooler parts of the year (Campbell sources, that could have cascading implications for local food-web et al., 1999; Dean and Hurd, 2007; Schiel and Thompson, 2012). structures (Schmidt and Scheibling, 2006). Some native taxa such Photosynthetic rates are greatest in winter and spring during as abalone (Haliotis iris), amphipods (Aora typica) and turbonid growth, and lower in summer during senescence, with the alga snails (Cookia sulcata and Lunella smaragda) consume Undaria having mean photosynthetic maxima over these two periods of readily (Thompson, 2004; Jimenez et al., 2015b, Fig. 2), although the 1 1 1 1 38.14 mg O2 g dw h and 15.90 mg O2 g dw h , respectively common epifaunal isopod Badedotea elongata rejected it as a food (Campbell et al., 1999). Maximum values of oxygen production of source in feeding trials (Jimenez et al., 2015b). On the other hand, Undaria can be ten times greater than that of other laminarians little is known about the epifaunal communities associated with such as Macrocystis pyrifera (Campbell et al., 1999). However, this algal species that are displaced by Undaria (e.g. filamentous algae difference is less pronounced on an areal basis due to Undaria's and Lophothamnion hirtum, Valentine and Johnson, 2005, South relatively small size compared to native laminarians (Dean and et al., 2016; respectively). Therefore, the impact of Undaria on Hurd, 2007), and is less pronounced temporally due to its food-webs is likely to be complex, with many areas of uncertainties absence from the shoreline for part of the year in many locations that warrant further investigation (Table 1). (Tait et al., 2015). By contrast, modelled annual net primary pro- The export of kelp detritus can be an important trophic subsidy duction is relatively similar between Undaria and smaller fucoid across ecosystems (Wernberg et al., 2006; Vanderklift and algae that are common habitat-forming species in Australia and Wernberg, 2008; Krumhansl and Scheibling, 2012b). Invasive New Zealand, despite the perennial life history of the native species macroalgae can modify such subsidies and, consequently, local (Edgar et al., 2004; Valentine and Johnson, 2004; Schiel, 2006; Tait assemblages of detritivores (Krumhansl and Scheibling, 2012a) and et al., 2015). Whether Undaria (or other invasive macroalgae) rep- possibly filter-feeders. As noted in Section 2.3, it is possible that resents a gain or a loss of system-wide primary production de- much of the negatively buoyant Undaria biomass detached from pends, in part, on whether the invader is a driver or passenger of heavily-infested shores in southern New Zealand is exported to ecological change. If Undaria is a passenger, then impacts are likely deeper waters offshore. Indeed, sunken Undaria biomass can to be additive or substitutive, following its recruitment into un- reduce subtidal reef complexity by filling cracks and crevices suf- disturbed (e.g., Morelissen et al., 2016; South et al., 2016), or ficiently enough to reduce habitat for reef fish in Argentina disturbed (e.g., Edgar et al., 2004; Valentine and Johnson, 2004; (Irigoyen et al., 2011b). However, the detritivore communities Thompson and Schiel, 2012) assemblages, respectively. However, associated with subtidal detritus from Undaria have not been if Undaria is a driver of change (or a passenger-turned-driver), then studied in Australasia or elsewhere (Table 1). Where Undaria does differences in net primary production will depend on the identity of get washed ashore it can provide a considerable trophic subsidy P.M. South et al. / Marine Environmental Research 131 (2017) 243e257 253

(Jimenez et al., 2017). For example, the talitrid amphipod Bel- are directed to this goal, largely reflects the challenges presented by lorchestia quoyana consumes Undaria at similar rates to other algae the kelp's life-history characteristics (Hewitt et al., 2005; Forrest that are commonly stranded on sandy beaches (Jimenez et al., et al., 2009; Forrest and Hopkins, 2013). The rapid growth of 2017). It therefore seems likely that Undaria represents a signifi- Undaria, whereby sporophytes can reach maturity within less than cant addition to coastal food-webs. However, more research is 2-months after recruitment, means that manual removal needs to warranted to determine the extent and scale of trophic provision- be regular (typically monthly). This situation, combined with the ing associated with this invader (Table 1). apparent persistence of Undaria's benthic gametophyte life-stage Overall, the impacts of Undaria are not well understood due to a (Hewitt et al., 2005), means that managed zones that are clear of deficit of studies, but it seems likely that its advent has modified visible Undaria need to be rechecked monthly for at least 3-years patterns of biogenic habitat provision and trophic subsidies locally after the last sporophyte has been detected. However, detection and across ecosystems, despite its seeming inability to displace can be difficult, especially in the presence of native canopy-forming many native taxa. However, it should be noted that research has algae whose juvenile life-stages are superficially similar in colour focused on a relatively small number of response variables, and morphology to Undaria. The failure to detect even a single whereas impacts might be restricted to less easily quantified re- sporophyte, which subsequently matures, can lead to the re- sponses. These include reproductive capacity (Lyons and establishment of the population and undermine years of previous Scheibling, 2007), growth (Carnell and Keough, 2014) and sub- effort. To overcome such barriers, the more recent and ongoing lethal stress (Terlizzi et al., 2011), all of which could compromise attempt to eradicate Undaria from Fiordland involved the trans- the resilience of coastal ecological communities and therefore plant of ~30,000e35,000 sea urchins (Evechinus chloroticus) into warrant further research (Table 1). the primary control zone. This approach artificially created urchin barrens, which were expected to not only eliminate Undaria, but by 5. Eradication and sustained control of established removing the native macroalgal cover, also made it easier for divers populations to detect new Undaria recruits (Atalah et al., 2013). Perhaps the most significant impediment to successful eradi- A number of Undaria eradication or sustained population con- cation arises due to Undaria's multiple dispersal strategies. trol attempts have been undertaken in Australasia, which have Although spore dispersal is limited (see section 2.3), dispersal- varied in both their effort and efficacy. Generally the experiences to modes such as sporophyte drift can lead to episodic leaps in date support the need to manage pathways of Undaria spread as a Undaria distribution across scales of kilometres. Due to Undaria's first priority, on the basis that management post-establishment is strong association with human transport vectors, this situation can difficult, expensive and seldom successful. In fact, successful be compounded in localities having a complex network of eradications of marine invasive species generally required a sus- anthropogenic vector activity (Floerl et al., 2009), particularly tained and intensive effort, and it often appears to be atypical cir- where vessels move into remote coastal areas outside main vessel cumstances that make eradication tractable (Willan et al., 2000; hubs. These different mechanisms and scales of dispersal make it Wotton et al., 2004; Hopkins et al., 2011). In the case of Undaria, difficult to define surveillance boundaries for ongoing population this situation was exemplified by the successful hot water treat- delimitation. In fact, the ultimate reason for failure of the ment of the infected hull of a fishing vessel that sank at Chatham 1997e2004 management programme was that, despite monthly Island (Fig.1); a remote locality 700 km to the east of mainland New removals from the primary management area, a well-established Zealand (Wotton et al., 2004). This eradication effort was successful Undaria population was detected in the wider managed region, in because: (a) the vessel was already known to have Undaria on the a vessel hub that was checked only infrequently (Forrest and hull (Stuart, 2004), hence the response was rapid; (b) the criteria Hopkins, 2013). (temperature and exposure time) for effective Undaria heat treat- Similarly, at the time of writing, the future of the Fiordland ment were known; (c) the area was isolated and surrounded by eradication programme is in doubt, following the detection of sand, with the vessel hull representing a discrete and ‘treatable’ another infested site (a vessel mooring and surrounding seabed) a surface compared with more complex natural and artificial marine few kilometres from the primary control zone. Hence, in both of habitats; and (d) the risk of imminent reinvasion was low, with the these examples, eradication success appears to have been nearest stable established Undaria populations on mainland New compromised by anthropogenic vectors, most likely vessels. This Zealand. situation highlights the fundamental importance of effectively By contrast, other attempts to eradicate Undaria from port and managing these risk pathways, in order to support the manage- harbours having a range of natural seabed and artificial habitats ment of established Undaria populations (Fiordland Marine have all failed. The most comprehensive and sustained pro- Guardians, 2017). Partly in response to the recent incursions of grammes to date have been the ongoing effort in the Fiordland Undaria into Fiordland, vessel operators are now required to obtain region of south-western New Zealand (also see Section 2.2) and a a “Clean Vessel Pass” before going to that region, as part of a Marine regional scale programme undertaken in the far south of New Regional Pathway Management Plan developed by the regional Zealand during 1997e2004 (Forrest and Hopkins, 2013). Although authority (Environment Southland, 2017). the latter programme failed to eradicate Undaria, it did demon- While regular antifouling remains one of the best strategies for strate that through sustained and intensive control, employing a reducing Undaria and other biofouling on vessels (Piola et al., range of measures (e.g., physical removal, chemical treatments), 2009a; Floerl et al., 2016), the need for a more comprehensive Undaria populations could be contained, and the infestation of toolbox has seen considerable research effort on tools to reduce or vessels in managed areas could be reduced to near-zero (Hunt et al., eliminate Undaria and other risk species that are associated with 2009; Forrest and Hopkins, 2013). It also developed initial proof of anthropogenic transport vectors. It is beyond our present scope to concept for a range of marine pest control methods that are now detail these, but examples include: encapsulation-based steri- routinely implemented operationally, at least in New Zealand lisation methods for vessel hulls (Coutts and Forrest, 2007; Atalah (Coutts and Forrest, 2007; Piola et al., 2009b; Hopkins et al., 2010, et al., 2016a), which are needed on the basis that antifouling is 2016; Piola and Hopkins, 2012; Atalah et al., 2016a; Hopkins not completely effective; chemical or heat treatments for internal et al., 2016). recesses and pipework on vessels (Piola and Hopkins, 2012); and The failure to eradicate Undaria, even when significant resources treatments for aquaculture equipment and seed-stock (Forrest and 254 P.M. South et al. / Marine Environmental Research 131 (2017) 243e257

Blakemore, 2006; Forrest et al., 2007). However, despite some ex- faceted management (e.g., targeted population control in key vec- amples of operational application of these tools for vessels and tor hubs, strict regulations on vessel and gear biofouling, and im- aquaculture pathways, risks from Undaria and other pests associ- mediate, intensive eradication responses when incursions are ated with anthropogenic vectors on domestic pathways remain discovered) might reduce the risk of Undaria establishing in pris- poorly managed in Australasia. Nonetheless, both Australia and tine or high value sites. Even more ambitious would be the effective New Zealand are at the global forefront in terms of implementing management of anthropogenic stressors with the potential to cause border standards to reduce the risk of incursions of new invasive declines in canopy-forming species across broad geographic scales, species from international source regions. making native communities more susceptible to invasion.

6. Conclusions Acknowledgements

Undaria is often considered to be one of the world's worst The authors greatly acknowledge their respective funding invasive species. It is a species that, due to its large and conspicuous agencies: PS, BF and OF were funded by Cawthron Institute. MT was sporophyte stage, can have a dramatic appearance at high popu- funded by the Marsden Fund of the Royal Society of New Zealand lation densities in heavily invaded locations. However, the Aus- (UOC1302). Javier Atalah kindly made Fig. 1. We thank two anon- tralasian situation shows that, while Undaria can be highly ymous reviewers whose suggestions greatly improved this work. successful at invading a wide range of coastal assemblages, evi- dence for direct adverse impacts is scant. This situation contrasts Appendix A. Supplementary data certain other invasive macroalgae that can have dramatic ecological effects (Ambrose and Nelson, 1982; Stæhr et al., 2000; Scheibling Supplementary data related to this article can be found at and Gagnon, 2006; Bulleri et al., 2010), even when they are in https://doi.org/10.1016/j.marenvres.2017.09.015. relatively low abundance (Bulleri et al., 2017). Such a decoupling of invasion success and impact suggests that perhaps Undaria does not merit the world's worst invader status that has been attributed References to it, and which has become propagated through the scientific Airoldi, L., 1998. Roles of disturbance, sediment stress, and substratum retention on literature in the absence of research documenting actual ecological spatial dominance in algal turf. Ecology 79, 2759e2770. effects. Despite this situation, there remain many knowledge gaps Alestra, T., Tait, L.W., Schiel, D.R., 2014. Effects of algal turfs and sediment accu- concerning the invasion ecology of Undaria, but many of these are mulation on replenishment and primary productivity of fucoid assemblages. Mar. Ecol. Prog. Ser. 511, 59e70. likely to be highly complex and related to its additive effects on Ambrose, R.F., Nelson, B.V., 1982. Inhibition of giant kelp recruitment by an intro- system-wide attributes, such as provision of biogenic habitat, net duced brown alga. Bot. Mar. 25, 265e267. primary production, nutrient cycling and cross-system subsidies Arnold, M., Teagle, H., Brown, M.P., Smale, D.A., 2015. The structure of biogenic habitat and epibiotic assemblages associated with the global invasive kelp (Dean and Hurd, 2007; Jimenez, 2015; Tait et al., 2015; Thomsen Undaria pinnatifida in comparison to native macroalgae. Biol. Invasions 1e16. et al. 2016a; South et al., 2016; Jimenez et al., 2017). Atalah, J., Hopkins, G.A., Forrest, B.M., 2013. Augmentative biocontrol in natural Insights from the Australasian scientific research on the mech- marine habitats: persistence, spread and non-target effects of the sea urchin Evechinus chloroticus. Plos ONE 8. anisms underlying the spread of Undaria, its invasion biology and Atalah, J., Brook, R., Cahill, P.M., Fletcher, L.A., Hopkins, G., 2016a. It's a wrap: impacts are highly applicable to research and management in other encapsulation as a management tool for marine biofouling. Biofouling 32, regions where this species has become invasive. Furthermore, 277e286. Atalah, J., Fletcher, L.M., Hopkins, G.A., Heasman, K., Woods, C.M.C., Forrest, B.M., synthesis of research on Undaria from Australasia and other regions 2016b. Preliminary assessment of biofouling on offshore mussel farms. J. World of the world suggest some emerging generalities. In particular, Aquac. Soc. 47, 376e386. these include the significant human-mediated spread of Undaria Atlas of Living Australia (2017) https://www.ala.org.au/1 March 2017. (Fletcher and Manfredi, 1995; Pereyra et al., 2015), its proliferation Battershill, C., Miller, K., Cole, R., 1998. The Understorey of Marine Invasions. Sea- food New Zealand, pp. 31e33. on artificial coastal structures (Curiel et al., 2002; Minchin and Bauer, J., 2012. Invasive species: “back-seat drivers” of ecosystem change? Biol. Nunn, 2014), the eventual and sometimes dramatic population Invasions 14, 1295e1304. fi expansions into native communities (Casas and Piriz, 1996; Fletcher Bellgrove, A., McKenzie, P.F., McKenzie, J.L., S ligoj, B.J., 2010. Restoration of the habitat-forming fucoid alga Hormosira banksii at effluent-affected sites: and Farrell, 1998; Heiser et al., 2014; Pereyra et al., 2014), and the competitive exclusion by coralline turfs. Mar. Ecol. Prog. Ser. 419, 47e56. inability to compete with native canopy-forming macroalgae Benedetti-Cecchi, L., Pannacciulli, F., Bulleri, F., Moschella, P., Airoldi, L., Relini, G., (Valentine and Johnson, 2003; Raffo et al., 2009; De Leij et al., 2017). Cinelli, F., 2001. Predicting the consequences of anthropogenic disturbance: large-scale effects of loss of canopy algae on rocky shores. Mar. Ecol. Prog. Ser. In addition, many unique insights have arisen from Undaria 214, 137e150. research in Australasia, most notably concerning facilitation by Bite, J., 2001. The Ecology and Demography of the Introduced Macroalga Undaria native taxa such as coralline algae and sea urchins, and the efficacy pinnatifida (Harvey) Suringar in Port Phillip Bay. Victoria University, Victoria, Australia. MSc thesis. and applicability of control and eradication programmes. By Bollen, M., Pilditch, C.A., Battershill, C.N., Bischof, K., 2016. Salinity and temperature contrast, there are some important aspects of the Undaria invasion tolerance of the invasive alga Undaria pinnatifida and native New Zealand kelps: in Australasia that have received little attention; these include implications for competition. Mar. Biol. 163, 1e14. Britton-Simmons, K.H., 2004. Direct and indirect effects of the introduced alga potential socio-economic factors such as costs that might occur due Sargassum muticum on benthic, subtidal communities of Washington State, to eradication programmes, and benefits that might arise from USA. Mar. Ecol. Prog. Ser. 277, 61e78. exploiting Undaria's commercial value (Table 1). Brown, M.T., Lamare, M.D., 1994. L’algue Japonaise Undaria pinnatifida (Harvey) In the 30 years since Undaria was first recorded in Australasia, it Suringar within Timaru harbour, New Zealand. Jpn. J. Phyc 42. Bulleri, F., Airoldi, L., Branca, G., Abbiati, M., 2006. Positive effects of the introduced has spread to occupy vast tracts of coastline. Still, there remain green alga, Codium fragile ssp. tomentosoides, on recruitment and survival of expansive uninvaded rocky coastal habitats within the possible mussels. Mar. Biol. 148, 1213e1220. range of Undaria, a situation that is mirrored in other parts of the Bulleri, F., Balata, D., Bertocci, I., Tamburello, L., Benedetti-Cecchi, L., 2010. The seaweed Caulerpa racemosa on Mediterranean rocky reefs: from passenger to world where this alga is invasive (Sanderson, 1990; James et al., driver of ecological change. Ecology 91, 2205e2212. 2015). For reasons described herein, it can be expected that Unda- Bulleri, F., Chapman, M.G., 2010. The introduction of coastal infrastructure as a ria will continue to expand its range, and it is highly unlikely that driver of change in marine environments. J. Appl. Ecol. 47, 26e35. Bulleri, F., Benedetti-Cecchi, L., Ceccherelli, G., Tamburello, L., 2017. A few is enough: eradication or population control based on existing tools will have a low cover of a non-native seaweed reduces the resilience of Mediterranean any widespread effectiveness. Perhaps at best, intensive multi- macroalgal stands to disturbances of varying extent. Biol. Invasions 19, 1e15. P.M. South et al. / Marine Environmental Research 131 (2017) 243e257 255

Campbell, S., Bite, J., Burridge, T., 1999. Seasonal patterns in the photosynthetic habitat and socio-economic factors. Ethol. Ecol. Evol. 26, 130e151. capacity, tissue pigment and nutrient content of different developmental stages Geange, S.W., Powell, A., Clemens-Seely, K., Cardenas, C.A., 2014. Sediment load and of Undaria pinnatifida (Phaeophyta: Laminariales) in Port Phillip Bay, South- timing of sedimentation affect spore establishment in Macrocystis pyrifera and Eastern Australia. Bot. Mar. 42, 231e242. Undaria pinnatifida. Mar. Biol. 161, 1583e1592. Campbell, S.J., Burridge, T.R., 1998. Occurrence of Undaria pinnatifida (Phaeophyta : Gorman, D., Connell, S.D., 2009. Recovering subtidal forests in human-dominated Laminariales) in Port Phillip Bay, Victoria, Australia. Mar. Freshw. Res. 49, landscapes. J. Appl. Ecol. 46, 1258e1265. 379e381. Gribben, P.E., Wright, J.T., 2006. Invasive seaweed enhances recruitment of a native Campbell, S.J., 1999. Uptake of ammonium by four species of macroalgae in Port bivalve: roles of refuge from predation and the habitat choice of recruits. Mar. Phillip Bay, Victoria, Australia. Mar. Freshw. Res. 50, 515e522. Ecol. Prog. Ser. 318, 177e185. Carnell, P., Keough, M., 2014. Spatially variable synergistic effects of disturbance and Hay, C.H., Luckens, P.A., 1987. The asian kelp Undaria Pinnatifida (Phaeophyta, additional nutrients on kelp recruitment and recovery. Oecologia 175, 409e416. Laminariales) found in a New Zealand harbour. N. Z. J. Bot. 25, 329e332. Casas, G., Scrosati, R., Piriz, M.L., 2004. The invasive kelp Undaria pinnatifida Hay, C.H., 1990. The dispersal of sporophytes of Undaria pinnatifida by coastal (Phaeophyceae, Laminariales) reduces native seaweed diversity in Nuevo Gulf shipping in New Zealand, and implications for further dispersal of Undaria in (Patagonia, Argentina). Biol. Invasions 6, 411e416. France. Br. Phycol. J. 25, 301e313. Casas, G.N., Piriz, M.L., 1996. Surveys of Undaria pinnatifida (Laminariales, Phaeo- Hay, C.H., Villouta, E., 1993. Seasonality of the adventive asian kelp Undaria Pin- phyta) in Golfo Nuevo, Argentina. Hydrobiologia 327, 213e215. natifida in New Zealand. Bot. Mar. 36, 461e476. Chaoyuan, W., Jianxin, M., 1997. Translocation of assimilates in Undaria and its Hayden, B., Unwin, M., Roulston, H., Peacock, L., Floerl, O., Kospartov, M., cultivation in China. Hydrobiologia 352, 287e293. Seaward, K., 2009. Evaluation of Vessel Movements from the 24 ports and Connell, S.D., Russell, B.D., 2010. The direct effects of increasing CO2 and temper- Marinas Surveyed through the port Baseline Survey programmes, ZBS2000e04 ature on non-calcifying organisms: increasing the potential for phase shifts in and ZBS2005-19 (ZBS2005-13). Ministry of Primary Industries, Wellington. kelp forests. Proc. R. Soc. Lond. B Biol. Sci. rspb20092069. Heiser, S., Hall-Spencer, J.M., Hiscock, K., 2014. Assessing the extent of establish- Connell, S.D., Kroeker, K.J., Fabricius, K.E., Kline, D.I., Russell, B.D., 2013. The other ment of Undaria pinnatifida in Plymouth Sound Special area of conservation, UK. ocean acidification problem: CO2 as a resource among competitors for Mar. Biodivers. Rec. 7. ecosystem dominance. Philosophical Trans. R. Soc. Lond. B Biol. Sci. 368, Hewitt, C.L., Campbell, M.L., McEnnulty, F., Moore, K.M., Murfet, N.B., Robertson, B., 20120442. Schaffelke, B., 2005. Efficacy of physical removal of a marine pest: the intro- Coutts, A.D.M., Forrest, B.M., 2007. Development and application of tools for duced kelp Undaria pinnatifida in a Tasmanian marine reserve. Biol. Invasions 7, incursion response: lessons learned from the management of the fouling pest 251e263. Didemnum vexillum. J. Exp. Mar. Biol. Ecol. 342, 154e162. Hopkins, G.A., Forrest, B.M., Coutts, A.D.M., 2010. The effectiveness of rotating brush Crooks, J.A., 2002. Characterizing ecosystem-level consequences of biological in- devices for management of vessel hull fouling. Biofouling J. Bioadhesion Biofilm vasions: the role of ecosystem engineers. Oikos 97, 153e166. Res. 26, 555e566. Curiel, D., Guidetti, P., Bellemo, G., Scattolin, M., Marzocchi, M., 2002. The intro- Hopkins, G.A., Forrest, B.M., Jiang, W., Gardner, J.P.A., 2011. Successful eradication of duced alga Undaria pinnatifida (Laminariales, Alariaceae) in the lagoon of a non-indigenous marine bivalve from a subtidal soft-sediment environment. Venice. Hydrobiologia 477, 209e219. J. Appl. Ecol. 48, 424e431. Dayton, P.K., Currie, V., Gerrodette, T., Keller, B.D., Rosenthal, R., Tresca, D.V., 1984. Hopkins, G.A., Prince, M., Cahill, P.L., Fletcher, L.M., Atalah, J., 2016. Desiccation as a Patch dynamics and stability of some California kelp communities. Ecol. Mon- mitigation tool to manage biofouling risks: trials on temperate taxa to elucidate ogr. 54, 253e289. factors influencing mortality rates. Biofouling 32, 1e11. De Leij, R., Epstein, G., Brown, M.P., Smale, D.A., 2017. The influence of native Hunt, L., Chadderton, L., Stuart, M., Cooper, S., Carruthers, M., 2009. Results of an macroalgal canopies on the distribution and abundance of the non-native kelp Attempt to Control and Eradicate Undaria pinnatifida in Southland, New Zea- Undaria pinnatifida in natural reef habitats. Mar. Biol. 164, 156. land, April 1997-November 2004. Invercargill, New Zealand, 48pp. Dean, P.R., Hurd, C.L., 2007. Seasonal growth, erosion rates, and nitrogen and Irigoyen, A., Trobbiani, G., Sgarlatta, M., Raffo, M., 2011a. Effects of the alien alga photosynthetic ecophysiology of Undaria pinnatifida (Heterokontophyta) in Undaria pinnatifida (Phaeophyceae, Laminariales) on the diversity and abun- southern New Zealand. J. Phycol. 43, 1138e1148. dance of benthic macrofauna in Golfo Nuevo (Patagonia, Argentina): potential Dellatorre, F.G., Amoroso, R., Saravia, J., Orensanz, J., 2014. Rapid expansion and implications for local food webs. Biol. Invasions 13, 1521e1532. potential range of the invasive kelp Undaria pinnatifida in the Southwest Irigoyen, A.J., Eyras, C., Parma, A.M., 2011b. Alien alga Undaria pinnatifida causes Atlantic. Aquat. Invasions 9, 467e478. habitat loss for rocky reef fishes in north Patagonia. Biol. Invasions 13, 17e24. Didham, R.K., Tylianakis, J.M., Hutchison, M.A., Ewers, R.M., Gemmell, N.J., 2005. Are James, K., Middleton, I., Middleton, C., Shears, N., 2014. Discovery of Undaria pin- invasive species the drivers of ecological change? Trends Ecol. Evol. 20, natifida (Harvey) Suringar, 1873 in Northern New Zealand Indicates Increased 470e474. Invasion Threat in Subtropical Regions. Edgar, G.J., Barrett, N.S., Morton, A.J., Samson, C.R., 2004. Effects of algal canopy James, K., Kibele, J., Shears, N.T., 2015. Using satellite-derived sea surface temper- clearance on plant, fish and macroinvertebrate communities on eastern Tas- ature to predict the potential global range and phenology of the invasive kelp manian reefs. J. Exp. Mar. Biol. Ecol. 312, 67e87. Undaria pinnatifida. Biol. Invasions 1e16. Environment Southland (2017) http://www.es.govt.nz 31/05/2017. James, K., Shears, N.T., 2016a. Proliferation of the invasive kelp Undaria pinnatifida at Fiordland Marine Guardians (2017) http://www.fmg.org.nz 31/05/2017. aquaculture sites promotes spread to coastal reefs. Mar. Biol. 163, 1e12. Fletcher, R.L., Manfredi, C., 1995. The occurrence of Undaria pinnatifida (Phaeohy- James, K., Shears, N.T., 2016b. Population ecology of the invasive kelp Undaria ceae, Laminariales) on the south coast of England. Bot. Mar. 38, 355e358. pinnatifida towards the upper extreme of its temperature range. Mar. Biol. 163, Fletcher, R.L., Farrell, P., 1998. Introduced brown algae in the North East Atlantic, 225. with particular respect to Undaria pinnatifida (Harvey) suringar. Helgolander€ Jimenez, R.S., 2015. The Ecology of the Invasive Kelp Undaria pinnatifida: Func- Meeresunters. 52, 259e275. tioning at an Ecosystem Level. PhD thesis. University of Otago. Floerl, O., Pool, T.K., Inglis, G.J., 2004. Positive interactions between nonindigenous Jimenez, R.S., Hepburn, C.D., Hyndes, G.A., McLeod, R.J., Hurd, C.L., 2015a. Contri- species facilitate transport by human vectors. Ecol. Appl. 14, 1724e1736. butions of an annual invasive kelp to native algal assemblages: algal resource Floerl, O., Inglis, G.J., Dey, K., Smith, A., 2009. The importance of transport hubs in allocation and seasonal connectivity across ecotones. Phycologia 54, 530e544. stepping-stone invasions. J. Appl. Ecol. 46, 37e45. Jimenez, R.S., Hepburn, C.D., Hyndes, G.A., McLeod, R.J., Taylor, R.B., Hurd, C.L., Floerl, O., Inglis, G.J., Diettrich, J., 2016. Incorporating human behaviour into the 2015b. Do native subtidal grazers eat the invasive kelp Undaria pinnatifida? Mar. riskerelease relationship for invasion vectors: why targeting only the worst Biol. 162, 0. offenders can fail to reduce spread. J. Appl. Ecol. 53, 742e750. Jimenez, R.S., Hepburn, C.D., Hyndes, G.A., McLeod, R.J., Taylor, R.B., Hurd, C.L., 2017. Forrest, B., Taylor, M., 2002. Assessing invasion impact: survey design consider- Importance of the invasive macroalga Undaria pinnatifida as trophic subsidy for ations and implications for management of an invasive marine plant. Biol. In- a beach consumer. Mar. Biol. 164, 113. vasions 4, 375e386. Krumhansl, K.A., Scheibling, R.E., 2012a. Detrital subsidy from subtidal kelp beds is Forrest, B.M., Brown, S.N., Taylor, M.D., Hurd, C.L., Hay, C.H., 2000. The role of natural altered by the invasive green alga Codium fragile. Mar. Ecol. Prog. Ser. 456, dispersal mechanisms in the spread of Undaria pinnatifida (Laminariales, 73e85. Phaeophyceae). Phycologia 39, 547e553. Krumhansl, K.A., Scheibling, R.E., 2012b. Production and fate of kelp detritus. Mar. Forrest, B.M., Blakemore, K.A., 2006. Evaluation of treatments to reduce the spread Ecol. Prog. Ser. 467, 281e302. of a marine plant pest with aquaculture transfers. Aquaculture 257, 333e345. Leal, P.P., Hurd, C.L., Fernandez, P.A., Roleda, M.Y., 2016. Meiospore development of Forrest, B.M., Hopkins, G.A., Dodgshun, T.J., Gardner, J.P.A., 2007. Efficacy of acetic the kelps Macrocystis pyrifera and Undaria pinnatifida under ocean acidification acid treatments in the management of marine biofouling. Aquaculture 262, and ocean warming: independent effects are more important than their 319e332. interaction. Mar. Biol. 164, 7. Forrest, B.M., Gardner, J., Taylor, M.D., 2009. Internal borders for managing invasive Leal, P.P., Hurd, C.L., Fernandez, P.A., Roleda, M.Y., 2017. Ocean acidification and kelp marine species. J. Appl. Ecol. 46, 46e54. development: reduced pH has no negative effects on meiospore germination Forrest, B.M., Hopkins, G.A., 2013. Population control to mitigate the spread of and gametophyte development of Macrocystis pyrifera and Undaria pinnatifida. marine pests: insights from management of the Asian kelp Undaria pinnatifida J. Phycology 53 (3), 557e566. and colonial ascidian Didemnum vexillum. Manag. Biol. Invasions 4, 317e326. Lee, J.-B., Hayashi, K., Hashimoto, M., Nakano, T., Hayashi, T., 2004. Novel antiviral Forrest, B.M., 2016. Regional Recreational Vessel Hull Fouling Survey and Boater fucoidan from sporophyll of Undaria pinnatifida (Mekabu). Chem. Pharm. Bull. Questionnaire. Top of the South Marine Biosecurity Partnership. Technical 52, 1091e1094. Report 2016/01. 27 pp. Levin, P.S., Coyer, J.A., Petrik, R., Good, T.P., 2002. Community-wide effects of Gallardo, B., 2014. Europe's top 10 invasive species: relative importance of climatic, nonindigenous species on temperate rocky reefs. Ecology 83, 3182e3193. 256 P.M. South et al. / Marine Environmental Research 131 (2017) 243e257

Lilley, S.A., Schiel, D.R., 2006. Community effects following the deletion of a habitat- Springer-Verlag, Berlin Heidelberg, pp. 321e332. forming alga from rocky marine shores. Oecologia 148, 672e681. Russell, L.K., Hepburn, C.D., Hurd, C.L., Stuart, M.D., 2008. The expanding range of Ling, S.D., Johnson, C.R., Frusher, S.D., Ridgway, K.R., 2009. Overfishing reduces Undaria pinnatifida in southern New Zealand: distribution, dispersal mecha- resilience of kelp beds to climate-driven catastrophic phase shift. Proc. Natl. nisms and the invasion of wave-exposed environments. Biol. Invasions 10, Acad. Sci. 106, 22341e22345. 103e115. Lowe, S., Browne, M., Boudjelas, S., De Poorter, M., 2000. 100 of the World's Worst Saito, Y., 1975. Practical significance of algae in Japan. Undaria. In: Tohida, J., Invasive Alien Species: A Selection from the Global Invasive Species Database, Hirose, H. (Eds.), Advance of Phycology in Japan. VEB Gustav Fischer Verlag, vol. 12. Invasive Species Specialist Group Auckland, New Zealand. Jena, pp. 304e320. Lyons, D.A., Scheibling, R.E., 2007. Differences in somatic and gonadic growth of sea Sanderson, J., 1990. A preliminary survey of the distribution of the introduced urchins (Stronglyocentrotus droebachiensis) fed kelp (Laminaria longicruris)or macroalga, Undaria pinnatifida (Harvey) Suringer on the east coast of Tasmania, the invasive alga Codium fragile ssp. tomentosoides are related to energy Australia. Bot. Mar. 33, 153e158. acquisition. Mar. Biol. 152, 285e295. Sanderson, J.C., 1997. Subtidal Macroalgal Assemblages in Temperate Australian MacDougall, A.S., Turkington, R., 2005. Are invasive species the drivers or passen- Coastal Waters: State of the Environment Technical Paper Series (Estuaries and gers of change in degraded ecosystems? Ecology 86, 42e55. the Sea). Department of the Environment, Canberra, 129 pp. Maggi, E., Benedetti-Cecchi, L., Castelli, A., Chatzinikolaou, E., others, 2015. Schaffelke, B., Campbell, M.L., Hewitt, C.L., 2005. Reproductive phenology of the Ecological impacts of invading seaweeds: a meta-analysis of their effects at introduced kelp Undaria pinnatifida (Phaeophyceae, Laminariales) in Tasmania, different trophic levels. Divers. Distributions 21, 1e12. Australia. Phycologia 44, 84e94. Menge, B.A., Daley, B.A., Sanford, E., Dahlhoff, E.P., Lubchenco, J., 2007. Mussel Scheibling, R.E., Gagnon, P., 2006. Competitive interactions between the invasive zonation in New Zealand: An integrative eco-physiological approach. Mar. Ecol. green alga Codium fragile ssp. tomentosoides and native canopy-forming sea- Prog. Ser. 345, 129e140. weeds in Nova Scotia (Canada). Mar. Ecol. Prog. Ser. 325, 1e14. Minchin, D., Nunn, J., 2014. The invasive brown alga Undaria pinnatifida (Harvey) Schiel, D.R., 1990. Macroalgal assemblages in New Zealand: structure, interactions Suringar, 1873 (Laminariales: Alariaceae), spreads northwards in Europe. Bio- and demography. Hydrobiologia 192, 59e76. Invasions Rec. 3, 57e63. Schiel, D.R., 2006. Rivets or bolts? When single species count in the function of Ministry for Primary Industries (2017) http://www.biosecurity.govt.nz/pests/ temperate rocky reef communities. J. Exp. Mar. Biol. Ecol. 338, 233e252. undaria 22/2/2017. Schiel, D.R., Wood, S.A., Dunmore, R.A., Taylor, D.I., 2006. Sediment on rocky Morelissen, B., 2012. Ecological Effects of Undaria pinnatifida (Harvey) Suringar and intertidal reefs: Effects on early post-settlement stages of habitat-forming Nutrient-enrichment on Intertidal Assemblages in the Wellington Region of seaweeds. J. Exp. Mar. Biol. Ecol. 331, 158e172. New Zealand. Victoria University of Wellington. Schiel, D.R., Thompson, G.A., 2012. Demography and population biology of the Morelissen, B., Dudley, B.D., Geange, S.W., Phillips, N.E., 2013. Gametophyte repro- invasive kelp Undaria pinnatifida on shallow reefs in southern New Zealand. duction and development of Undaria pinnatifida under varied nutrient and J. Exp. Mar. Biol. Ecol. 434e435, 25e33. irradiance conditions. J. Exp. Mar. Biol. Ecol. 448, 197e206. Schmidt, A.L., Scheibling, R.E., 2006. A comparison of epifauna and epiphytes on Morelissen, B., Dudley, B., Phillips, N., 2016. Recruitment of the invasive kelp native kelps (Laminaria species) and an invasive alga (Codium fragile ssp. Undaria pinnatifida does not always benefit from disturbance to native algal tomentosoides) in Nova Scotia, Canada. Bot. Mar. 49, 315e330. communities in low-intertidal habitats. Mar. Biol. 163, 241. Schmidt, A.L., Scheibling, R.E., 2007. Effects of native and invasive macroalgal can- Morita, T., Kurashima, A., Maegawa, M., 2003. Temperature requirements for the opies on composition and abundance of mobile benthic macrofauna and turf- growth and maturation of the gametophytes of Undaria pinnatifida and forming algae. J. Exp. Mar. Biol. Ecol. 341, 110e130. U. undarioides (Laminariales, Phaeophyceae). Phycol. Res. 51, 154e160. Shepherd, S., 2013. Ecology of Australian Temperate Reefs: the Unique South. CSIRO Mulas, M., Bertocci, I., 2016. Devil's tongue weed (Grateloupia turuturu Yamada) in publishing. northern Portugal: Passenger or driver of change in native biodiversity? Mar. Sherman, C., Lotterhos, K., Richardson, M., Tepolt, C., Rollins, L., Palumbi, S., Environ. Res. 118, 1e9. Miller, A., 2016. What are we missing about marine invasions? Filling in the Na, Y.J., Jeon, D.V., Han, S.J., Maranguy, C.A.O., others, 2016. Crossed effects of light gaps with evolutionary genomics. Mar. Biol. 163, 198. and temperature on the growth and maturation of gametophytes in Costaria Simkanin, C., Davidson, I.C., Dower, J.F., Jamieson, G., Therriault, T.W., 2012. costata and Undaria pinnatifida. Korean J. Fish. Aquatic Sci. 49, 190e197. Anthropogenic structures and the infiltration of natural benthos by invasive National Institute of Water and Atmosphere (2017) https://www.niwa.co.nz/ ascidians. Mar. Ecol. 33, 499e512. natural-hazards/hazards/waves 31/05/2017. Skriptsova, A., Khomenko, V., Isakov, V., 2004. Seasonal changes in growth rate, Nyberg, C.D., Wallentinus, I., 2005. Can species traits be used to predict marine morphology and alginate content in Undaria pinnatifida at the northern limit in macroalgal introductions? Biol. Invasions 7, 265e279. the Sea of Japan (Russia). J. Appl. Phycol. 16, 17. Pereyra, P.J., Arias, M., Gonzalez, R., Narvarte, M., 2014. Moving forward: the Japa- Sliwa, C., Johnson, C.R., Hewitt, C.L., 2006. Mesoscale dispersal of the introduced nese kelp Undaria pinnatifida (Harvey) Suringar, 1873 expands in northern kelp Undaria pinnatifida attached to unstable substrata. Bot. Mar. 49, 396e405. Patagonia, Argentina. BioInvasions Rec. 3, 65e70. South, P.M., Lilley, S.A., Tait, L.W., Alestra, T., Hickford, M.J., Thomsen, M.S., Pereyra, P.J., Narvarte, M., Tatian, M., Gonzalez, R., 2015. The simultaneous intro- Schiel, D.R., 2016. Transient effects of an invasive kelp on the community duction of the tunicate Styela clava (Herdman, 1881) and the macroalga Undaria structure and primary productivity of an intertidal assemblage. Mar. Freshw. pinnatifida (Harvey) Suringar, 1873, in northern Patagonia. BioInvasions Rec. 4, Res. 67, 103e112. 179e184. South, P.M., Thomsen, M.S., 2016. The ecological role of invading Undaria pinnati- Peteiro, C., Sanchez, N., 2012. Comparing salinity tolerance in early stages of the fida: an experimental test of the driverepassenger models. Mar. Biol. 163, 1e12. sporophytes of a non-indigenous kelp (Undaria pinnatifida) and a native kelp Stæhr, P.A., Pedersen, M.F., Thomsen, M.S., Wernberg, T., Krause-Jensen, D., 2000. (Saccharina latissima). Russ. J. Mar. Biol. 38, 197e200. Invasion of Sargassum muticum in Limfjorden (Denmark) and its possible Peteiro, C., Freire, O., 2013. Epiphytism on blades of the edible kelps Undaria pin- impact on the indigenous macroalgal community. Mar. Ecol. Prog. Ser. 207, natifida and Saccharina latissima farmed under different abiotic conditions. 79e88. J. World Aquac. Soc. 44, 706e715. Stuart, M.D., Hurd, C.L., Brown, M.T., 1999. Effects of seasonal growth rate on Piola, R.F., Dafforn, K.A., Johnston, E.L., 2009a. The influence of antifouling practices morphological variation of Undaria pinnatifida (Alariaceae, Phaeophyceae). In: on marine invasions. Biofouling 25, 633e644. Kain, J.M., Brown, M.T., Lahaye, M. (Eds.), Sixteenth International Seaweed Piola, R.F., Denny, C.M., Forrest, B.M., Taylor, M.D., 2009b. Marine biosecurity: Symposium: Proceedings of the Sixteenth International Seaweed Symposium management options and response tools. In: Williams, P.A., Clout, M.N. (Eds.), Held in Cebu City, Philippines, 12e17 April 1998. Springer, Netherlands, Dor- Invasive Species Management: a Handbook of Principles and Techniques. Ox- drecht, pp. 191e199. ford University Press, United Kingdom, pp. 205e231. Stuart, M.D., 2004. Review of Research on Undaria pinnatifida in New Zealand and Piola, R.F., Hopkins, G.A., 2012. Thermal treatment as a method to control transfers its potential Impacts on the Eastern Coast of the South Island. DOC Science of invasive biofouling species via vessel sea chests. Mar. Pollut. Bull. 64, Internal Series 166. Department of Conservation, Wellington, 40pp. 1620e1630. Tait, L.W., South, P.M., Lilley, S.A., Thomsen, M.S., Schiel, D.R., 2015. Assemblage and Prabhasankar, P., Ganesan, P., Bhaskar, N., Hirose, A., others, 2009. Edible Japanese understory carbon production of native and invasive canopy-forming macro- seaweed, wakame (Undaria pinnatifida) as an ingredient in pasta: chemical, algae. J. Exp. Mar. Biol. Ecol. 469, 10e17. functional and structural evaluation. Food Chem. 115, 501e508. Terlizzi, A., Felline, S., Lionetto, M.G., Caricato, R., Perfetti, V., Cutignano, A., Mollo, E., Primo, C., Hewitt, C.L., Campbell, M.L., 2010. Reproductive phenology of the intro- 2011. Detrimental physiological effects of the invasive alga Caulerpa racemosa duced kelp Undaria pinnatifida (Phaeophyceae, Laminariales) in Port Phillip Bay on the Mediterranean white seabream Diplodus sargus. Aquat. Biol. 12, 109e117. (Victoria, Australia). Biol. Invasions 12, 3081e3092. Thompson, G.A., 2004. Mechanisms of Invasion and persistence of the Intertidal Raffo, M.P., Eyras, M.C., Iribarne, O.O., 2009. The invasion of Undaria pinnatifida to a Kelp Undaria pinnatifida (Harvey) Suringar within Intertidal Areas of Southern Macrocystis pyrifera kelp in Patagonia (Argentina, south-west Atlantic). J. Mar. New Zealand. PhD thesis. University of Canterbury. Biol. Assoc. U. K. 89, 1571e1580. Thompson, G.A., Schiel, D.R., 2012. Resistance and facilitation by native algal Richards, D.K., Hurd, C.L., Pritchard, D.W., Wing, S.R., Hepburn, C.D., 2011. Photo- communities in the invasion success of Undaria pinnatifida. Mar. Ecol. Prog. Ser. synthetic response of monospecific macroalgal stands to density. Aquat. Biol. 13, 468, 95e105. 41e49. Thomsen, M.S., Wernberg, T., Tuya, F., Silliman, B.R., 2009. Evidence for impacts of Ruiz, G.M., Freestone, A.L., Fofonoff, P.W., Simkanin, C., 2009. Habitat distribution non-indigenous macroalgae; a meta-analysis of experiemental field studies. and heterogeneity in marine invasion dynamics: the importance of hard sub- J. Phycol. 45, 812e819. strate and artificial structure. In: Rilov, G., Crooks, J.A. (Eds.), Biological Invasions Thomsen, M.S., 2010. Experimental evidence for positive effects of invasive seaweed in Marine Ecosystems: Ecological, Management, and Geographic Perspectives. on native invertebrates via habitat-formation in a seagrass bed. Aquat. P.M. South et al. / Marine Environmental Research 131 (2017) 243e257 257

Invasions 5, 341e346. Valentine, J.P., Johnson, C.R., 2005. Persistence of the exotic kelp Undaria pinnatifida Thomsen, M.S., Wernberg, T., Olden, J.D., Griffin, J.N., Silliman, B.R., 2011. does not depend on sea urchin grazing. Mar. Ecol. Prog. Ser. 285, 43e55. A framework to study the context-dependent impacts of marine invasions. Vanderklift, M.A., Wernberg, T., 2008. Detached kelps from distant sources are a J. Exp. Mar. Biol. Ecol. 400, 322e327. food subsidy for sea urchins. Oecologia 157, 327e335. Thomsen, M.S., Wernberg, T., South, P.M., Schiel, D.R., 2016a. To include or not to Voisin, M., Engel, C.R., Viard, F., 2005. Differential shuffling of native genetic di- include (the invader in community analyses)? That is the question. Biol. In- versity across introduced regions in a brown alga: aquaculture vs. maritime vasions 18, 1515e1512. traffic effects. Proc. Natl. Acad. Sci. U. S. A. 102, 5432e5437. Thomsen, M.S., Wernberg, T., South, P.M., Schiel, D.R., 2016b. Non-native seaweeds Wang, C., Shi, S.-S., Hong, Q.-M., Wang, S.-C., Wang, Z.-T., Hu, Z.-B., 2009. Isolation, drive changes in marine coastal communities around the world. In: Hu, Z.-M., purification and structural Analysis of Polymannuronic Acid from Undaria Fraser, Ceridwen (Eds.), Seaweed Phylogeography: Adaptation and Evolution of pinnatifida [J]. Chem. J. Chin. Univ. 11, 017. Seaweeds under Environmental Change. Springer, Netherlands, Dordrecht, Wernberg, T., Vanderklift, M., How, J., Lavery, P., 2006. Export of detached macro- pp. 147e185. algae from reefs to adjacent seagrass beds. Oecologia 147, 692e701. Uwai, S., Nelson, W., Neill, K., Wang, W.D., others, 2006. Genetic diversity in Undaria Wernberg, T., Smale, D.A., Tuya, F., Thomsen, M.S., others, 2013. An extreme climatic pinnatifida (Laminariales, Phaeophyceae) deduced from mitochondria genes e event alters marine ecosystem structure in a global biodiversity hotspot. Nat. origins and succession of introduced populations. Phycologia 45, 687e695. Clim. Change 3, 78e82. Valentine, J.P., Johnson, C.R., 2003. Establishment of the introduced kelp Undaria Willan, R.C., Russell, B.C., Murfet, N.B., Moore, K.L., others, 2000. Outbreak of pinnatifida in Tasmania depends on disturbance to native algal assemblages. Mytilopsis sallei (Recluz, 1849)(Bivalvia: Dreissenidae) in Australia. Molluscan J. Exp. Mar. Biol. Ecol. 295, 63e90. Res. 20, 25e30. Valentine, J.P., Johnson, C.R., 2004. Establishment of the introduced kelp Undaria Wotton, D.M., O'Brien, C., Stuart, M.D., Fergus, D.J., 2004. Eradication success down pinnatifida following dieback of the native macroalga Phyllospora comosa in under: heat treatment of a sunken trawler to kill the invasive seaweed Undaria Tasmania, Australia. Mar. Freshw. Res. 55, 223e230. pinnatifida. Mar. Pollut. Bull. 49, 844e849.