The Invasive Kelp Undaria Pinnatifida (Phaeophyceae, Laminariales) Reduces Native Seaweed Diversity in Nuevo Gulf (Patagonia, Argentina)

The kelp Undaria pinnatifida(Phaeophyceae) is a seaweed native to northeast Asia, but during the last two decades, it has been accidentally or intentionally introduced in several temperate coasts worldwide. In central Patagonia (Argentina), this species was first detected in late 1992, and it is progressively spreading from the point of introduction. Through a manipulative experiment involving Undaria removal in 2001, we found that its presence is associated with a dramatic decrease in species richness and diversity of native seaweeds in Nuevo Gulf. Future prospects are worrisome, as, in addition to the negative impact from a biodiversity viewpoint, native commercial macroalgae and invertebrates might also be affected.     

Genetic analysis of a recently established Undaria pinnatifida (Laminariales: Alariaceae) population in the northern Wadden Sea reveals close proximity between drifting thalli and the attached population

Undaria pinnatifida, a kelp species native to East Asia, has become cosmopolitan and drawn increasing attention due to its worldwide spread in recent decades. Floating fragments of this alga were found washed ashore on Sylt in 2016, the first record of this species in Germany. Thalli attached to local oyster reefs were detected in 2017. The genetic relationship between the floating and attached thalli on Sylt, as well as their relevance to the populations from northern Europe and native regions, was hitherto unknown. Here, 10 microsatellite markers were used to assess relationships between the recently established population on Sylt and five other northern European populations in France (Brittany, West English Channel), the Netherlands and England (Plymouth, West English Channel) plus three natural populations in China. Almost no genetic differentiation was detected between the floating and attached populations on Sylt, but they were genetically distinct from all the other studied northern European populations. The very low genetic diversity revealed in the new founder populations of Sylt suggests that they came from genetically similar parents. The marked reduction in both the number of alleles and heterozygosity in the northern European populations, as compared with the Chinese ones, is typical of founder effects in recently populated regions. Prominent genetic divergence was found between most of the northern European populations except those within Brittany and Sylt. Further studies will focus on identifying the putative source populations that might be found on shellfish farms, in local marinas or the benthic habitats around Sylt Island.     

Temperature requirements for the growth of young sporophytes of Undaria pinnatifida and Undaria undarioides (Laminariales, Phaeophyceae)

The relative growth rate of young sporophytes of Undaria pinnatifida (Harvey) Suringar and Undaria undarioides (Yendo) Okamura was examined in order to understand the difference in distribution of these two species around the coast of Japan. The optimal temperature for growth of both species was similar at 20°C and the upper critical temperature for growth was also similar, at 27°C for U. pinnatifida and 26°C for U. undarioides. Therefore, the optimal and upper critical temperatures for growth of the young sporophytes are not the main factors determining the distribution of each species. Next, the lower critical temperatures for growth were examined. For the young sporophytes of U. pinnatifida, the lower limit was less than 5°C while for those of U. undarioides it was 15°C. Thus, the difference in the lower critical temperature for growth between the two species was approximately 10°C. During the period of young sporophyte growth in the field, the temperature at the mouth of Ise Bay, Japan, where U. pinnatifida occurs, ranges from 12.7°C in December to 13.1°C in April, with a minimum of 7.9°C in February. Our experiments indicate that young sporophytes are able to grow throughout this period. The temperature off Hamajima, Japan, where U. undarioides occurs, ranges from 19.1°C to 14.8°C during the same time period. Again, young sporophytes are able to growth throughout this period, although minimum winter temperatures are only just high enough for growth. These natural temperature ranges during the growth season of the sporophytes agree well with the experimentally determined temperature requirements for growth of each species. Therefore, the difference between the two species in the critical temperature required for growth of the young sporophytes, especially in the low temperature range, is one of the major factors determining the distribution pattern of each species.     

Seasonal growth,erosion rates,and nitrogen and photosynthetic ecophysiology of Undaria pinnatifida (Heterokontophyta) in southern New Zealand1

The goal of this study was to examine growth, erosion rates, and the photosynthetic and nitrogen ecophysiology of the invasive seaweed Undaria pinnatifida (Harv.) Suringar. Sporophytes of U. pinnatifida that appeared in Otago Harbour, southeastern New Zealand, in late autumn (May) 1996 were tagged, and their growth rates followed until the onset of senescence in early summer (November 1996). Blade growth rates were maximal between May and August when they ranged from 0.77 ± 0.05 to 0.93 ± 0.05 cm · d^?1 and declined from September onward. In laboratory experiments, U. pinnatifida took up nitrate and ammonium simultaneously at rates ranging from 21.3 ± 2.1 to 179.3 ± 65.1 μmol · g^?1 dry weight (dwt) · h^?1. When monthly patterns of growth rate, seawater inorganic nitrogen, nitrogen uptake kinetics, soluble tissue nitrate, % tissue carbon (C) and nitrogen (N), and C:N ratio were considered together, there was no evidence that N limited the growth of U. pinnatifida. Furthermore, the photosynthetic parameters P_max, α, E_k, E_c, and R_d derived from P versus E curves indicated that the growth of U. pinnatifida was not light limited, and that the population could potentially grow deeper than its observed location at 4 m depth. Nitrogen and light ecophysiological parameters of U. pinnatifida more closely resemble those of small, ephemeral seaweeds, such as Ulva, than other members of the Laminariales. We suggest that a “plastic” physiology may allow U. pinnatifida sporophytes to match their physiology to a range of environments, which is one reason for its success as an invasive seaweed.     

Surveys of Undaria pinnatifida (Laminariales,Phaeophyta) in Golfo Nuevo,Argentina

In December 1992, some sporophytes of the Asian kelp Undaria pinnatiftda were found growing subtidally at 6 m depth below A. Storni Port, Puerto Madryn, Argentina. During the winter of 1994, the species expanded significantly from its original location. Sporelings appear in early autumn and attain their maximum size (1.65 ± 0.10 m) during winter and early spring, when most of them become fertile. The fronds are lost in summer, with only some holdfasts and sporophylls surviving, and these disappear by the end of summer. The occurrence of U. pinnatida in Golfo Nuevo is reportedly due to an accidental introduction by cargo ships or fishing vessels arriving from Asian ports.     

The introduced alga Undaria pinnatifida (Laminariales,Alariaceae) in the lagoon of Venice

Since its appearance in 1992 in the lagoon of Venice, the brown algae Undaria pinnatifida (kelp) has gradually expanded along the banks of canals both at Chioggia and Venice, becoming the dominant species in the local algal community chiefly from February to July. In Chioggia Island, where another brown seaweed (Sargassum muticum) is present since 1992, the spreading of Undaria reaches a plateau. In Venice Island, instead, the colonisation process is still in progress. During 1999, the kelp has colonised the main canals (e.g. The Grand Canal) and, subsequently, the small inner ones. In order to evaluate the dynamics of substrate re-colonisation by Undaria, two mechanical eradications were carried out during (March) and after the fertile period (July) of the algae. Such experimental manipulations provided evidence of the fast re-colonisation potential of the algae mainly attributable to its efficient reproductive system. Eradication made during the fertile period, in fact, permitted the kelp development during the following year, while re-colonisation has started 2 years later where eradication was performed after the reproductive period. A significant decrease in the surface covered by other species has been observed both in shallow (Ulva rigida, Enteromorpha spp., Antithamnion pectinatum, Chondracanthus acicularis) and deeper areas (Rhodymenia ardissonei) during the period of maximum development of U. pinnatifida. On the basis of the results of this study, the following conclusions can be drawn: (1) the alga U. pinnatifida is continuously expanding in lagoon environments of Venice; (2) in order to limit its spreading, mechanical eradications would be done on a large spatial scale and before the zoospores release; (3) there is suggestive evidence of competition between Undaria and the remaining indigenous algae.     

Regeneration from callus of Undaria pinnatifida (Harvey) Suringar (Laminariales,Phaeophyta)

Calli were formed on the explants of midrib, meristem and immature stipe parts from freshly collected Undaria pinnatifida sporophytes. Each part was sterilized by Betadine and ethanol, and was cut into explants. The explants were incubated on an agar medium at 10 hours light and 14 hours dark photoperiod under a photon flux density of 80 µmol m^–2 s^–1. Callus was formed best on the explants of meristem parts at a temperature of 13 °C on PESI medium. Calli were cut off from the explants and were transferred into a sterile liquid PESI medium in flasks. Callus was dark brown in colour and was composed of well-pigmented cells. The cells were loosely bound and were separated by low power sonication, and were easy to attach to vinylon strings. From the calli formed on the explants of meristem parts, entire fronds were regenerated, but from the calli formed on the explants of midrib parts, only thin layered laminae were regenerated. The calli formed on the explants of immature stipe parts did not exhibit any regeneration at all.     

Microsatellite markers for the intertidal kelp Postelsia palmaeformis (Heterokontophyta; Laminariales)

Postelsia palmaeformis (Ruprecht) is an intertidal brown alga belonging to the ecologically and economically important group of seaweeds commonly referred to as kelp (Order Laminariales). Six polymorphic microsatellite loci were identified for this monotypic genus. The number of alleles ranged from two to five, with observed heterozygosities ranging from 0.00 to 0.704.     

The effect of fertilizer application on farming of the seaweed Undaria pinnatifida (Laminariales, Phaeophyta)

A slow-release ammonium phosphate fertilizer coated with porous plastic was tested on Undaria pinnatifida (Harvey) Suringar as a possible solution to the nutrient deficiency in seawater that causes quality and yield deterioration in seaweed farming. The yield of U. pinnatifida within the fertilized area was 17–40% greater than that of the control area (unfertilized area). In addition, two harvests were possible per season and the quality of harvested U. pinnatifida was also better than that outside the fertilizer diffusion area. The released NH₄-N did not increase the concentration of NH₄-N outside the farming area. Therefore, this fertilizer increased yield and improved quality without causing water pollution.     

Examining the reproductive success of bull kelp (Nereocystis luetkeana,Phaeophyceae, Laminariales) in climate change conditions

Climate change is affecting marine ecosystems in many ways, including raising temperatures and leading to ocean acidification. From 2014 to 2016, an extensive marine heat wave extended along the west coast of North America and had devastating effects on numerous species, including bull kelp (Nereocystis luetkeana). Bull kelp is an important foundation species in coastal ecosystems and can be affected by marine heat waves and ocean acidification; however, the impacts have not been investigated on sensitive early life stages. To determine the effects of changing temperatures and carbonate levels on Northern California's bull kelp populations, we collected sporophylls from mature bull kelp individuals in Point Arena, CA. At the Bodega Marine Laboratory, we released spores from field-collected bull kelp, and cultured microscopic gametophytes in a common garden experiment with a fully factorial design crossing modern conditions (11.63 ± 0.54°C and pH 7.93 ± 0.26) with observed extreme climate conditions (15.56 ± 0.83°C and 7.64 ± 0.32 pH). Our results indicated that both increased temperature and decreased pH influenced growth and egg production of bull kelp microscopic stages. Increased temperature resulted in decreased gametophyte survival and offspring production. In contrast, decreased pH had less of an effect but resulted in increased gametophyte survival and offspring production. Additionally, increased temperature significantly impacted reproductive timing by causing female gametophytes to produce offspring earlier than under ambient temperature conditions. Our findings can inform better predictions of the impacts of climate change on coastal ecosystems and provide key insights into environmental dynamics regulating the bull kelp lifecycle.     

Bathymetric origin shapes the physiological responses of Pterygophora californica (Laminariales,Phaeophyceae) to deep marine heatwaves

Kelp communities are experiencing exacerbated heat-related impacts from more intense, frequent, and deeper marine heatwaves (MHWs), imperiling the long-term survival of kelp forests in the climate change scenario. The occurrence of deep thermal anomalies is of critical importance, as elevated temperatures can impact kelp populations across their entire bathymetric range. This study evaluates the impact of MHWs on mature sporophytes of Pterygophora californica (walking kelp) from the bathymetric extremes (8–10 vs. 25–27 m) of a population situated in Baja California (Mexico). The location is near the southernmost point of the species's broad distribution (from Alaska to Mexico). The study investigated the ecophysiological responses (e.g., photobiology, nitrate uptake, oxidative stress) and growth of adult sporophytes through a two-phase experiment: warming simulating a MHW and a post-MHW phase without warming. Generally, the effects of warming differed depending on the bathymetric origin of the sporophytes. The MHW facilitated essential metabolic functions of deep-water sporophytes, including photosynthesis, and promoted their growth. In contrast, shallow-water sporophytes displayed metabolic stress, reduced growth, and oxidative damage. Upon the cessation of warming, certain responses, such as a decline in nitrate uptake and net productivity, became evident in shallow-water sporophytes, implying a delay in heat-stress response. This indicates that variation in temperatures can result in more prominent effects than warming alone. The greater heat tolerance of sporophytes in deeper waters shows convincing evidence that deep portions of P. californica populations have the potential to serve as refuges from the harmful impacts of MHWs on shallow reefs.     

Streblonema (Ectocarpales,Phaeophyceae) infection in the kelp Laminaria saccharina (Laminariales,Phaeophyceae) in the western Baltic

The brown alga Laminaria saccharina is the dominant subtidal macroalga in Kiel Bay, western Baltic. It is infected by the microscopic brown alga, Streblonema aecidioides. Infected thalli may show symptoms of Streblonema disease, i.e. alterations of blade and stipe, ranging from dark spots to heavy deformations and completely crippled thalli. Samples taken from a single locality all year round show that (i) the host population is infected at a high rate of 87±13% (SD), but that (ii) a considerable proportion of thalli containing Streblonema does not show disease symptoms, and that (iii) juvenile hosts, which mainly appear in autumn, are infected at almost the same rate. Thus the infection seems to occur early in the host's life. Juveniles in nature show fewer symptoms of the disease than adults. Two months after infection, oxygen production and growth in laboratory-raised experimentally infected juvenile hosts was not different from uninfected controls. Experimental thalli showed more severe morphological alterations than uninfected controls only four months after infection. Both field and laboratory observations indicate that a lag phase exists between infection and outbreak of the disease.     

Epi-endophytic symbiosis between Laminariocolax aecidioides (Ectocarpales, Phaeophyceae) and Undaria pinnatifida (Laminariales, Phaeophyceae) growing on Argentinian coasts

The present is the first study on epi-endophytic algae on thalli of Undaria pinnatifida growing along Argentinian coasts. The main goal is to describe the nature and the morphology of this symbiosis. Individuals of Laminariocolax aecidioides were detected in both June and December 2004, growing on U. pinnatifida sporophytes. In nature, the epi-endophyte were macroscopically observed as dark zones that partially covered the hosts’ fronds. L. aecidioides vegetative thalli were irregularly branched uniseriate filaments. The life cycle is described from laboratory cultures started from Patagonian populations. Caryology revealed that the sporophytic diploid phase presented 16 chromosomes whereas the gametophytic haploid phase presented 8 chromosomes. Isolates made from thalli growing in the interior of infected hosts developed into filamentous, branched sporophytes that reproduced by both unispores and plurispores that were produced in unilocular and plurilocular sporangia, respectively. The results of this paper also allowed us to conclude that L. aecidioides uses the thalli of U. pinnatifida as a proper substrate. The penetration of endophitic filaments among the host′s cortical cells produced a lateral compression and, finally, their thalli development generated perforations in the host tissues. The effects of the epi-endophytic infection of L. aecidioides on U. pinnatifida are neither severe nor deleterious.     

Undaria pinnatifida (Laminariales,Phaeophyta) 12 years after its introduction into the Atlantic Ocean

Since its first introduction into the Atlantic for farming purposes in 1983, the brown alga Undaria pinnatifida has been found at several sites along the European coasts. The present study deals with an ecological experiment that was performed at the island of Ushant (Brittany, France) in order to check the ability of Undaria to recruit to a rocky substratum in situ. On the one hand, the authors were unsuccessful in getting Undaria to colonize a previously denuded area of shore, which was subsequently colonized by other native species, a result that may speak for a competition between Undaria and the local kelps. On the other hand, evidence is presented that Undaria pinnatifida has become a member of the Atlantic flora for good. The sporophytes can be found growing from low water mark of neap tide (+1.5 m) down to at least –15 m below lower water mark of spring tide. Its propagation is thought to occur in at least two ways: either step by step from cultivation sites along the coasts, or from the hulls of ships sailing from harbour to harbour. The preference of Undaria for settlement is on artificial structures.     

Dominant (AFLP) and co‐dominant (microsatellite) markers for the kelp Postelsia palmaeformis (Laminariales)

To aid in understanding the structure, dispersal and genetic dynamics of their populations, we developed microsatellite and amplified fragment length polymorphism (AFLP) markers for the sea palm, Postelsia palmaeformis (Laminariales) for samples taken from nine sites in the area of Cape Flattery, Washington State, USA. We identified two AFLP primers that yielded 798 variable fragments and five microsatellite markers with three to seven alleles each. We also report patterns of allelic variation for four previously identified microsatellite markers in this species and several new alleles.     

First Record of Undaria Pinnatifida (Laminariales, Phaeophyta) in Southern Patagonia, Argentina

The Japanese kelp Undaria pinnatifida was found on 7th September 2005 in Ría Deseado (Santa Cruz, Argentina). This invasive algae was registered from the lower intertidal to the upper levels of the subtidal zone. The sporophytes were fixed to slabs, gravel and rocks of variable sizes and were also present as epibionts of tunicates. The sporophytes total length ranged between 3 and 88 cm, with a mean of 28.75 cm in the intertidal and 38.3 cm in the subtidal. The density and biomass increased from the intertidal to the subtidal. The kelp population showed a higher number of small immature individuals in the intertidal than␣subtidal where the organisms were bigger and with more individual biomass. This first record of U. pinnatifida in Southern Patagonia extends its southern distribution limit in Argentina, showing progressive expansion in the southwestern Atlantic. More surveys must be conducted to understand the evolution of U. pinnatifida invasion and its impact on the native benthic community.     

Morphological variability of Undaria pinnatifida (Harvey) Suringar, 1873 (Phaeophyceae, Laminariales) in Peter the Great Bay, Sea of Japan

The morphological variability of the brown alga Undaria pinnatifida was studied in Peter the Great Bay (Sea of Japan). Comparison of the morphology of algae growing at eight sites of the bay that have different water movement revealed three phenotypically different population groups. A discriminant analysis of a set of morphological traits demonstrated that the width of the undivided part of the lamina and the stipe length make the most significant contribution to the discrimination of the detected groups. Analysis of the environmental dependence of morphological traits showed that lamina width and width of undivided part of lamina depend generally on water movement intensity, whereas the stipe length and thallus length are influenced by light intensity and surf degree.     

Effects of temperature and nutrients on microscopic stages of the bull kelp (Nereocystis luetkeana,Phaeophyceae)

Warming ocean temperatures have been linked to kelp forest declines worldwide, and elevated temperatures can act synergistically with other local stressors to exacerbate kelp loss. The bull kelp Nereocystis luetkeana is the primary canopy-forming kelp species in the Salish Sea, where it is declining in areas with elevated summer water temperatures and low nutrient concentrations. To determine the interactive effects of these two stressors on microscopic stages of N. luetkeana, we cultured gametophytes and microscopic sporophytes from seven different Salish Sea populations across seven different temperatures (10–22°C) and two nitrogen concentrations. The thermal tolerance of microscopic gametophytes and sporophytes was similar across populations, and high temperatures were more stressful than low nitrogen levels. Additional nitrogen did not improve gametophyte or sporophyte survival at high temperatures. Gametophyte densities were highest between 10 and 16°C and declined sharply at 18°C, and temperatures of 20 and 22°C were lethal. The window for successful sporophyte production was narrower, peaking at 10–14°C. Across all populations, the warmest temperature at which sporophytes were produced was 16 or 18°C, but sporophyte densities were 78% lower at 16°C and 95% lower at 18°C compared to cooler temperatures. In the field, bottom temperatures revealed that the thermal limits of gametophyte growth (18°C) and sporophyte production (16–18°C) were reached during the summer at multiple sites. Prolonged exposure of bull kelp gametophytes to temperatures of 16°C and above could limit reproduction, and therefore recruitment, of adult kelp sporophytes.