162 Interactions Between Planktonic Microalgae and Protozoan Grazers

Invasive algal species have the potential to change the structure and ecology of native algal communities. One well‐known invader, the large Japanese kelp Undaria pinnatifida, has recently become established at several locations along the central and southern California coast (Monterey, Santa Barbara, Catalina, and others). Previous to its introduction in the northeastern Pacific, Undaria has become established along the coastlines of several countries, including Australia, New Zealand, Argentina, England, and France. However, the seasonal population dynamics, rate of spread, and impact on local communities at each invasion site varies. Undaria in the Santa Barbara, CA harbor exhibits two distinct recruitment pulses per year (fall, late winter), with nonoverlapping generations of adult individuals. Individuals can grow rapidly and become reproductive a month after appearing as recruits (2–3 cm long), indicating a potential for rapid spread. However, Undaria may be effectively controlled by grazing via natural recruitment of the kelp crab Pugettia producta. However, Undaria invasions in other California invasions have not been controlled by herbivory, and Undaria populations in these areas have the potential to compete with a wide diversity of native California kelp species for habitat space and light.     

CONTRASTING LIFE HISTORIES AND DEMOGRAPHIES OF LAMINARIAN AND FUCOID ALGAE

Introductions of non-native macroalgae and the subsequent displacement of native species are globally becoming more frequent. The algal genera Undaria, Sargassum , Caulerpa and Codium have been identified as being particularly invasive. An overview on the present knowledge on macroalgal introductions in the Australian region is presented and options for management are discussed, mostly using examples from studies on the introduced Japanese kelp, Undaria pinnatifida. Undaria pinnatifida was first detected in Tasmania, Australia in the early 1980's. Since then, its range has expanded despite eradication efforts. Long distance jumps appear to be the major mode of spread of U. pinnatifida in Tasmania. Studies are underway to distinguish the relative importance of spore dispersal, drift of adult plants and anthropogenic factors in spreading this invasive kelp. Although information on the real impacts of U. pinnatifida and other introduced macroalgae is sparse, the development of management and control strategies is of vital importance to prevent further spread and translocation of these "pest" species.     

PHYLOGENETIC AND BIOGEOGRAPHIC AFFINITIES OF THE HALYMENIALES AND RHODYMENIALES (RHODOPHYTA) FROM THE GULF OF MEXICO

A kelp/red algal symbiosis is described from nature based on extensive collections from the San Juan Islands, Washington. Kelp gametophytes were found as endophytes in the cell walls of seventeen species of red algae in three different kelp communities. Host red algae were mostly filamentous (e.g., Pleonosporium vancouverianum ) or polysiphonous (e.g. Polysiphonia paniculata ). The kelp gametophytes completed vegetative and reproductive development in the hosts with gametangia formed at the host surface and with sporophytes up to several mm in height being produced while still attached to the host. To date, none of the kelp gametophytes from nature have been identified to genus or species, although the gametophyte of Nereocystis luetkeana is a potential candidate for the symbiosis. Preliminary observations from Nova Scotia and the Isle of Man have not found the association in the Atlantic Ocean. Laboratory studies in Korea successfully reconstructed the symbiosis in the red alga Aglaothamnion oosumiense using zoospores of Undaria pinnatifida but not Laminaria religiosa. Here we outline the development of the symbiosis and discuss the potential adaptive significance of the kelp/red algal interaction.     

INTRODUCED MACROALGAE IN THE AUSTRALIAN REGION: CURRENT STATE OF KNOWLEDGE

Introductions of non‐native macroalgae and the subsequent displacement of native species are globally becoming more frequent. The algal genera Undaria, Sargassum, Caulerpa and Codium have been identified as being particularly invasive. An overview on the present knowledge on macroalgal introductions in the Australian region is presented and options for management are discussed, mostly using examples from studies on the introduced Japanese kelp, Undaria pinnatifida. Undaria pinnatifida was first detected in Tasmania, Australia in the early 1980's. Since then, its range has expanded despite eradication efforts. Long distance jumps appear to be the major mode of spread of U. pinnatifida in Tasmania. Studies are underway to distinguish the relative importance of spore dispersal, drift of adult plants and anthropogenic factors in spreading this invasive kelp. Although information on the real impacts of U. pinnatifida and other introduced macroalgae is sparse, the development of management and control strategies is of vital importance to prevent further spread and translocation of these “pest” species.     

BIOGEOGRAPHY AND ECOLOGY OF THE KELP/RED ALGAL SYMBIOSIS

A kelp/red algal symbiosis is described from nature based on extensive collections from the San Juan Islands, Washington. Kelp gametophytes were found as endophytes in the cell walls of seventeen species of red algae in three different kelp communities. Host red algae were mostly filamentous (e.g., Pleonosporium vancouverianum) or polysiphonous (e.g. Polysiphonia paniculata). The kelp gametophytes completed vegetative and reproductive development in the hosts with gametangia formed at the host surface and with sporophytes up to several mm in height being produced while still attached to the host. To date, none of the kelp gametophytes from nature have been identified to genus or species, although the gametophyte of Nereocystis luetkeana is a potential candidate for the symbiosis. Preliminary observations from Nova Scotia and the Isle of Man have not found the association in the Atlantic Ocean. Laboratory studies in Korea successfully reconstructed the symbiosis in the red alga Aglaothamnion oosumiense using zoospores of Undaria pinnatifida but not Laminaria religiosa. Here we outline the development of the symbiosis and discuss the potential adaptive significance of the kelp/red algal interaction.     

Effects of Zoospore Aggregation and Substrate Rugosity on Kelp Recruitment Success

Successful kelp recruitment is important for kelp population persistence and associated kelp forest communities. The proximity of settled kelp zoospores is a known requirement for successful kelp recruitment and proximity can be increased as zoospores aggregate. Substrate rugosity can also be an important factor affecting macroalgal settlement and recruitment in wave‐swept areas, and may affect kelp recruitment by aggregating zoospores. In this study, kelp zoospores were cultured at different levels of small‐scale aggregation and kelp recruitment was quantified. Sporophyte production significantly increased as zoospores became more aggregated indicating that processes that aggregate kelp zoospores have the potential to enhance kelp recruitment. A 13‐month field experiment demonstrated differential kelp recruitment onto settlement plates that mimicked surface rugosities of two common rock types within Stillwater Cove, Carmel Bay in central California (Carmelo Formation sandstone and Santa Lucia granodiorite). Significantly more kelp recruited to molds mimicking granodiorite over the yearlong study (granodiorite = 2.7 recruits ± SE 0.50, sandstone = 1.2 recruits ± SE 0.51). There was a significant difference in recruitment between seasons and this variability was due to the fact that spring had the highest average number of kelp recruits per mold. However, the interaction between substrate and season was not significant. This study emphasizes the importance of kelp zoospore aggregation on kelp recruitment and demonstrates that small‐scale rugosity affects kelp recruitment.     

Invasive sweetclover (<Emphasis Type="Italic">Melilotus alba</Emphasis>) impacts native seedling recruitment along floodplains of interior Alaska

Sweetclover (Melilotus alba) is a non-native legume that has formed dense and extensive patches along several rivers in Alaska. Our research objective was to determine if sweetclover impacts recruitment of native seedlings in floodplain habitats. To determine if sweetclover impacted recruitment, we conducted a removal experiment along two rivers in interior Alaska. When compared to areas where sweetclover was removed, areas with sweetclover had approximately 50% greater mortality of native seedlings, 25% less recruiting species, and a significant reduction in the quantity of light available to seedlings on floodplain surfaces. To determine if sweetclover shading was a mechanism that limited seedling recruitment, we grew eight common early-successional floodplain plant species in a greenhouse under a range of lighting conditions that were representative of shading under sweetclover. We observed that species restricted to the earliest seral stages of floodplain succession experienced greater reductions in biomass than species that persist into later stages of floodplain succession. Shading seedlings in a greenhouse did not lead to mortality during the growing season. However, when seedlings were over-wintered, we observed that greater shading during the growing season can result in higher seedling mortality. Our study indicates sweetclover invasions have created a novel shade environment in early seral floodplain plant communities, which has the potential to alter community composition. To preserve biodiversity and structure of plant communities, sweetclover should be actively managed to prevent its spread onto additional glacial rivers in Alaska.     

Marine invasion history and vector analysis of California: a hotspot for western North America

Aim We examine the regional dominance of California as a beachhead for marine biological invasions in western North America and assess the relative contribution of different transfer mechanisms to invasions over time. Location Western North America (California to Alaska, excluding Mexico). Methods We undertook extensive analysis of literature and collections records to characterize the invasion history of non‐native species (invertebrates, microalgae and microorganisms) with established populations in coastal marine (tidal) waters of western North America through 2006. Using these data, we estimated (1) the proportion of first regional records of non‐native species that occurred in California and (2) the relative contribution of transfer mechanisms to California invasions (or vector strength) over time. Results Excluding vascular plants and vertebrates, we identified 290 non‐native marine species with established populations in western North America, and 79% had first regional records from California. Many (40–64%) of the non‐native species in adjacent states and provinces were first reported in California, suggesting northward spread. California also drives the increasing regional rate of detected invasions. Of 257 non‐native species established in California, 59% had first regional records in San Francisco Bay; 57% are known from multiple estuaries, suggesting secondary spread; and a majority were attributed to vessels (ballast water or hull fouling) or oysters, in some combination, but their relative contributions are not clear. For California, more than one vector was possible for 56% of species, and the potential contribution of ballast water, hull fouling and live trade increased over time, unlike other vectors. Main conclusions California, especially San Francisco Bay, plays a pivotal role for marine invasion dynamics for western North America, providing an entry point from which many species spread. This pattern is associated historically with high propagule supply and salinity. Any effective strategies to minimize new invasions throughout this region must (1) focus attention on California and (2) address current uncertainty and future shifts in vector strength.     

Cover

Taxon‐specific measurements of biomass provide reliable estimates of annual net primary production by entire assemblages of macroalgae in giant kelp forests off Santa Barbara, California, USA. Photo by Ron McPeak. [Vol. 49, No. 2, pp. 248–257]     

Impacts of the invasive alga Sargassum muticum on ecosystem functioning and food web structure

Biological invasions have the potential to cause severe alterations to the biodiversity of natural ecosystems. At the same time, variation in the diversity and composition of native communities may have an important influence on the impact of invasions. Here, effects of the invasive Japanese wireweed, Sargassum muticum, were tested across a range of native marine algal assemblages using a combined additive and substitutive design. The invasive alga significantly reduced primary production, an important component of ecosystem functioning, and increased connectance, a key property of the food webs associated with the algal resources. These impacts were mediated by changes in the proportions of intermediate and top species, as well as apparent reductions in faunal species richness and diversity. Some key alterations to faunal species composition (including the arrival of generalist species associated with S. muticum) may have been important in determining these patterns. Overall results suggest that S. muticum not only directly impeded the native algal community, but that these effects extended indirectly to the native fauna and therefore caused major changes throughout the ecosystem.     

Undaria pinnatifida: A case study to highlight challenges in marine invasion ecology and management

Marine invasion ecology and management have progressed significantly over the last 30 years although many knowledge gaps and challenges remain. The kelp Undaria pinnatifida, or “Wakame,” has a global non‐native range and is considered one of the world's “worst” invasive species. Since its first recorded introduction in 1971, numerous studies have been conducted on its ecology, invasive characteristics, and impacts, yet a general consensus on the best approach to its management has not yet been reached. Here, we synthesize current understanding of this highly invasive species and adopt Undaria as a case study to highlight challenges in wider marine invasion ecology and management. Invasive species such as Undaria are likely to continue to spread and become conspicuous, prominent components of coastal marine communities. While in many cases, marine invasive species have detectable deleterious impacts on recipient communities, in many others their influence is often limited and location specific. Although not yet conclusive, Undaria may cause some ecological impact, but it does not appear to drive ecosystem change in most invaded regions. Targeted management actions have also had minimal success. Further research is needed before well‐considered, evidence‐based management decisions can be made. However, if Undaria was to become officially unmanaged in parts of its non‐native range, the presence of a highly productive, habitat former with commercial value and a broad ecological niche, could have significant economic and even environmental benefit. How science and policy reacts to the continued invasion of Undaria may influence how similar marine invasive species are handled in the future.     

Seascape genetics of the stalked kelp Pterygophora californica and comparative population genetics in the Santa Barbara Channel

We conducted a population genetic analysis of the stalked kelp, Pterygophora californica, in the Santa Barbara Channel, California, USA. The results were compared with previous work on the genetic differentiation of giant kelp, Macrocystis pyrifera, in the same region. These two sympatric kelps not only share many life history and dispersal characteristics but also differ in that dislodged P. californica does not produce floating rafts with buoyant fertile sporophytes, commonly observed for M. pyrifera. We used a comparative population genetic approach with these two species to test the hypothesis that the ability to produce floating rafts increases the genetic connectivity among kelp patches in the Santa Barbara Channel. We quantified the association of habitat continuity and oceanographic distance with the genetic differentiation observed in stalked kelp, like previously conducted for giant kelp. We compared both overall (across all patches) and pairwise (between patches) genetic differentiation. We found that oceanographic transit time, habitat continuity, and geographic distance were all associated with genetic connectivity in P. californica, supporting similar previous findings for M. pyrifera. Controlling for differences in heterozygosity between kelp species using Jost's D_EST, we showed that global differentiation and pairwise differentiation were similar among patches between the two kelp species, indicating that they have similar dispersal capabilities despite their differences in rafting ability. These results suggest that rafting sporophytes do not play a significant role in effective dispersal of M. pyrifera at ecologically relevant spatial and temporal scales.     

外来种入侵的过程、机理和预测

生物入侵是指某种生物从原来的分布区域扩展到一个新的（通常也是遥远的）地区,在新的区域里,其后代可以繁殖、扩散并持续维持下去,生物入侵成功的原因,即与入侵者本身的生物学,生态学特征有关,也与群落的脆弱性有关,入侵者可能较本地种的竞争能力强,更适应当地的环境,有的入侵者还可以改变环境,使之对已有利,而不利于本地种。缺乏天敌制约。群落的稳定性低和异常的环境扰动往往导致生物入侵,生物入侵的预测包括哪一种外来种会变成入侵种？哪些生态系统区域会被入侵？影响程度如何？入侵种的扩散态势如何等内容,对有关的理论和模型作了评介。     

Shading by giant kelp canopy can restrict the invasiveness of Undaria pinnatifida (Laminariales,Phaeophyceae)

The spread of non-indigenous and invasive seaweeds has increased worldwide, and their potential effects on native seaweeds have raised concern. Undaria pinnatifida is considered among the most prolific non-indigenous species. This species has expanded rapidly in the Northeast Pacific, overlapping with native communities such as the iconic giant kelp forests (Macrocystis pyrifera). Canopy shading by giant kelp has been argued to be a limiting factor for the presence of U. pinnatifida in the understory, thus its invasiveness capacity. However, its physiological plasticity under light limitation remains unclear. In this work, we compared the physiology and growth of juvenile U. pinnatifida and M. pyrifera sporophytes transplanted to the understory of a giant kelp forest, to juveniles growing outside of the forest. Extreme low light availability compared to that outside (~0.2 and ~4.4 mol photon ⋅ m⁻² ⋅ d⁻¹, respectively) likely caused a “metabolic energy crisis” in U. pinnatifida, thus restricting its photoacclimation plasticity and nitrogen acquisition, ultimately reducing its growth. Despite M. pyrifera juveniles showing photoacclimatory responses (e.g., increases in photosynthetic efficiency and lower compensation irradiance, E_c), their physiological/vegetative status deteriorated similarly to U. pinnatifida, which explains the low recruitment inside the forest. Generally, our results revealed the ecophysiological basis behind the limited growth and survival of juvenile U. pinnatifida sporophytes in the understory.     

Biodiversity influences invasion success of a facultative epiphytic seaweed in a marine forest

The biotic resistance hypothesis predicts that more diverse communities should have greater resistance to invasions than species-poor communities. However for facultative and obligate epiphytic invaders a high native species richness, abundance and community complexity might provide more resources for the invader to thrive to. We conducted surveys across space and time to test for the influence of native algal species abundance and richness on the abundance of the invasive facultative epiphytic filamentous alga Lophocladia lallemandii in a Mediterranean Cystoseira balearica seaweed forest. By removing different functional groups of algae, we also tested whether these relationships were dependent on the complexity and abundance of the native algal community. When invasion was first detected, Lophocladia abundance was positively related to species richness, but the correlation became negative after two years of invasion. Similarly, a negative relationship was also observed across sites. The removal experiment revealed that more complex native communities were more heavily invaded, where also a positive relationship was found between native algal richness and Lophocladia, independently of the native algal abundance. Our observational and experimental data show that, at early stages of invasion, species-rich seaweed forests are not more resistant to invasion than species-poor communities. Higher richness of native algal species may increase resource availability (i.e. substrate) for invader establishment, thus facilitating invasion. After the initial invasion stage, native species richness decreases with time since invasion, suggesting negative impacts of invasive species on native biodiversity.     

Species richness and interacting factors control invasibility of a marine community

Anthropogenic vectors have moved marine species around the world leading to increased invasions and expanded species'' ranges. The biotic resistance hypothesis of Elton (in The ecology of invasions by animals and plants, 1958) predicts that more diverse communities should have greater resistance to invasions, but experiments have been equivocal. We hypothesized that species richness interacts with other factors to determine experimental outcomes. We manipulated species richness, species composition (native and introduced) and availability of bare space in invertebrate assemblages in a marina in Monterey, CA. Increased species richness significantly interacted with both initial cover of native species and of all organisms to collectively decrease recruitment. Although native species decreased recruitment, introduced species had a similar effect, and we concluded that biotic resistance is conferred by total species richness. We suggest that contradictory conclusions in previous studies about the role of diversity in regulating invasions reflect uncontrolled variables in those experiments that modified the effect of species richness. Our results suggest that patches of low diversity and abundance may facilitate invasions, and that such patches, once colonized by non-indigenous species, can resist both native and non-indigenous species recruitment.     

Upper-montane plant invasions in the Hawaiian Islands: Patterns and opportunities

In the Hawaiian Islands, massive volcanoes have created extreme elevation gradients, resulting in environments ranging from nearly tropical to alpine, spread across a distance of only a few dozen kilometers. Although the Hawaiian Islands are widely recognized for opportunities to study lowland tropical forest invasions, less attention has been paid to invasions of Hawaii's upper-montane forest, sub-alpine and alpine environments. This study synthesizes current knowledge of plant naturalization in upper-montane environments of the Hawaiian Islands in order to (1) determine whether patterns of tropical versus temperate species invasion change with elevation, and (2) evaluate whether upper-montane invaders are having significant impacts on native plant communities. A total of 151 naturalized plant species have been recorded at 2000 m or higher. Most species (93%) are herbaceous, and over half (52%) are native to Europe/Eurasia. Twenty-one species (14%) are reported to be disruptive in native plant communities, mainly by forming dense stands that appear to inhibit recruitment of natives, but also by altering vegetation structure or causing changes in ecosystem processes. Fourteen species (9%) were first recorded within the past 30 years, indicating that new invasions of upper-montane habitats are ongoing. At 1200 m elevation, only 38% of naturalized species are temperate in origin, but the proportion of temperate species increases linearly with elevation up to 3000 m (alpine habitat), where all naturalized species are temperate in origin and over 80% are native to Europe/Eurasia. Declining temperature along the elevation gradient probably drives this pattern. The extreme elevation gradients in the Hawaiian Islands provide specific opportunities for comparative studies on the ecology and evolution of temperate invaders while also creating a unique field environment for understanding interactions between temperate and tropical species.     

Climate‐driven increases in storm frequency simplify kelp forest food webs

Climate models predict a dramatic increase in the annual frequency and severity of extreme weather events during the next century. Here we show that increases in the annual frequency of severe storms lead to a decrease in the diversity and complexity of food webs of giant kelp forests, one of the most productive habitats on Earth. We demonstrate this by linking natural variation in storms with measured changes in kelp forest food web structure in the Santa Barbara Channel using structural equation modeling (SEM). We then match predictions from statistical models to results from a multiyear kelp removal experiment designed to simulate frequent large storms. Both SEM models and experiments agree: if large storms remain at their current annual frequency (roughly one major kelp‐removing storm every 3.5 years), periodic storms help maintain the complexity of kelp forest food webs. However, if large storms increase in annual frequency and begin to occur year after year, kelp forest food webs become less diverse and complex as species go locally extinct. The loss of complexity occurs primarily due to decreases in the diversity and complexity of higher trophic levels. Our findings demonstrate that shifts in climate‐driven disturbances that affect foundation species are likely to have impacts that cascade through entire ecosystems.     

Kelp and sea urchin settlement mediated by biotic interactions with benthic coralline algal species

Species interactions can influence key ecological processes that support community assembly and composition. For example, coralline algae encompass extensive diversity and may play a major role in regime shifts from kelp forests to urchin-dominated barrens through their role in inducing invertebrate larval metamorphosis and influencing kelp spore settlement. In a series of laboratory experiments, we tested the hypothesis that different coralline communities facilitate the maintenance of either ecosystem state by either promoting or inhibiting early recruitment of kelps or urchins. Coralline algae significantly increased red urchin metamorphosis compared with a control, while they had varying effects on kelp settlement. Urchin metamorphosis and density of juvenile canopy kelps did not differ significantly across coralline species abundant in both kelp forests and urchin barrens, suggesting that recruitment of urchin and canopy kelps does not depend on specific corallines. Non-calcified fleshy red algal crusts promoted the highest mean urchin metamorphosis percentage and showed some of the lowest canopy kelp settlement. In contrast, settlement of one subcanopy kelp species was reduced on crustose corallines, but elevated on articulated corallines, suggesting that articulated corallines, typically absent in urchin barrens, may need to recover before this subcanopy kelp could return. Coralline species differed in surface bacterial microbiome composition; however, urchin metamorphosis was not significantly different when microbiomes were removed with antibiotics. Our results clarify the role played by coralline algal species in kelp forest community assembly and could have important implications for kelp forest recovery.     

The expanding range of Undaria pinnatifida in southern New Zealand: distribution, dispersal mechanisms and the invasion of wave-exposed environments

Very few studies have addressed how the invasive kelp Undaria pinnatifida (Harvey) Suringar spreads beyond initial founding populations in harbours. Surveys of the harbours and accessible areas of open coast throughout southern New Zealand were conducted to determine how far U. pinnatifida populations had extended since initial incursions. Our findings clearly demonstrate that U. pinnatifida is capable of invading native communities and can establish reproductive populations in locations subjected to significant and consistent wave action. The extent of spread from source populations differs between harbours in which it has established. Dispersal is greatest in harbours with long established populations, those where populations have not been strategically managed, harbours with high water exchange with surrounding coastal waters, and where prevailing currents allow establishment of U. pinnatifida on suitable substrata close to harbour entrances. Dispersal along the open coast is primarily achieved by drifting adult sporophytes that are washed up in the rocky intertidal zone. Founding populations are most often found in the intertidal zone, primarily within rockpools. Subtidal transects and observations indicate that U. pinnatifida is well adapted to invade exposed coastlines and can establish within a broad range of niches in wave-exposed areas including rockpools, the low intertidal, shallow subtidal, Macrocystis pyrifera kelp forests, and in low light areas beyond the vertical extent of large native macroalgae. The current range of U. pinnatifida is much greater than expected and appears to be expanding. Due to its ability to grow in a broad range of environments and to form dense monospecific stands, U. pinnatifida has the potential to strongly modify almost all rocky subtidal and intertidal communities in temperate locations.