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.     

Elevated Temperature Affects Phenotypic Plasticity in the Bull Kelp (Nereocystis luetkeana,Phaeophyceae)

The sensitivity of kelps to elevated temperatures has been linked to recent declines in some kelp populations, with cascading impacts on marine communities. However, it remains unclear how thermal stress affects the ability of kelps to respond to other environmental factors, which could influence their vulnerability to climate change. We investigated the effect of thermal stress on the ability of the bull kelp Nereocystis luetkeana to acclimate to its surrounding hydrodynamic environment through tension-regulated plasticity in blade morphology. We first determined optimal and stressful temperatures for N. luetkeana by measuring growth over nine temperatures from 5°C to 22°C. We then exposed N. luetkeana blades to a factorial combination of temperature (13°C and 20°C) and tension (0.5 N and 2.0 N) simulating different flow conditions, and measured changes in blade length and width after 7 days. The temperature at which N. luetkeana exhibited maximum growth was estimated to be ~11.9°C, though growth was high over a relatively wide temperature range. When thermally stressed, N. luetkeana maintained morphological responses to simulated high flow, but were inhibited from acclimating to low flow, indicated by an inability of blades to widen. Our results suggest that N. luetkeana in sheltered habitats may be particularly vulnerable to climate warming, where an inability to adjust blade morphology to local hydrodynamic conditions could drive declines at sublethal levels of warming. As ecologically important foundation species, declines in sheltered kelp populations could result in major biodiversity loss and disrupt ecosystem function.     

Factors influencing recruitment and appearance of bull kelp,Nereocystis luetkeana (phylum Ochrophyta)

The dynamics of annual species are strongly tied to their capacity for recruitment each year. We examined how competition and propagule availability influence recruitment and appearance and tracked survivorship of an annual species of marine macroalgae, the bull kelp (Nereocystis luetkeana), which serves as major biogenic habitat in the Salish Sea of Washington State. We hypothesized that (i) juvenile N. luetkeana would exhibit a seasonal appearance as a cohort in the spring and (ii) competition for space would be more limiting than propagules (spores) to recruitment at sites adjacent to established N. luetkeana beds. We tagged N. luetkeana recruits in the field to track appearance and survivorship across seasons (spring, summer, fall, and winter), using a two‐factor crossed design to assess effects of competition and propagule availability on appearance of new N. luetkeana sporophytes. Survivorship of N. luetkeana recruits was low and, whereas most new individuals arose in the spring, some appeared in every season. New N. luetkeana recruits also appeared the earliest (median 8 weeks vs. >20 weeks) after experimental “seeding” in the spring as compared to other seasons. Eliminating macroalgal competitors (“clearing”) influenced the appearance of recruits more than enhancement of propagules in the spring. An improved understanding of factors regulating the seasonal appearance of new N. luetkeana sporophytes furthers our understanding of this crucial foundation species' appearance and persistence across seasons, which is increasingly important as global ocean conditions change, and highlights the importance of studying organisms with complex life histories across multiple stages and geographical regions.     

Under pressure: biomechanical limitations of developing pneumatocysts in the bull kelp (Nereocystis luetkeana,Phaeophyceae)

Maintaining buoyancy with gas‐filled floats (pneumatocysts) is essential for some subtidal kelps to achieve an upright stature and compete for light . However, as these kelps grow up through the water column, pneumatocysts are exposed to substantial changes in hydrostatic pressure, which could cause complications as internal gases may expand or contract, potentially causing them to rupture, flood, and lose buoyancy. In this study, we investigate how pneumatocysts of Nereocystis luetkeana resist biomechanical stress and maintain buoyancy as they develop across a hydrostatic gradient. We measured internal pressure, material properties, and pneumatocyst geometry across a range of thallus sizes and collection depths to identify strategies used to resist pressure‐induced mechanical failure. Contrary to expectations, all pneumatocysts had internal pressures less than atmospheric pressure, ensuring that thalli are always exposed to a positive pressure gradient and compressional loads, indicating that they are more likely to buckle than rupture at all depths. Small pneumatocysts collected from depths between 1 and 9 m (inner radius = 0.4–1.0 cm) were demonstrated to have elevated wall stresses under high compressive loads and are at greatest risk of buckling. Although small kelps do not adjust pneumatocyst material properties or geometry to reduce wall stress as they grow, they are ~3.4 times stronger than they need to be to resist hydrostatic buckling. When tested, pneumatocysts buckled around 35 m depth, which agrees with previous measures of lower limits due to light attenuation, suggesting that hydrostatic pressure may also define the lower limit of Nereocystis in the field.     

Morphological plasticity in the kelp Nereocystis luetkeana (Phaeophyceae) is sensitive to the magnitude,direction, and location of mechanical loading

Nereocystis luetkeana is a canopy-forming kelp that exhibits morphological plasticity across hydrodynamic gradients, producing broad, undulate blades in slow flow and narrow, flattened blades in fast flow, enabling thalli to reduce drag while optimizing photosynthesis. While the functional significance of this phenomenon has been well studied, the developmental and physiological mechanisms that facilitate the plasticity remain poorly understood. In this study, we conducted three experiments to characterize how the (1) magnitude, (2) direction, and (3) location of plasticity-inducing mechanical stimuli affect the morphology of Nereocystis blades. We found that applying a gradient of tensile force caused blades to grow progressively longer, narrower, less ruffled, and heavier in a linear fashion, suggesting that Nereocystis is equally well adapted for all conditions within its hydrodynamic niche. We also found that applying tension transversely across blades caused the growth response to rotate 90°, indicating that there is no substantial separation between the sites of stimulus perception and response and suggesting that a long-distance signaling mechanism, such as a hormone, is unlikely to mediate this phenomenon. Meristoderm cells showed morphological changes that paralleled those of their respective blades in this experiment, implying that tissue-level morphology is influenced by cell growth. Finally, we found that plasticity was only induced when tension was applied directly to the growing tissue, reinforcing that long-distance signaling is probably not involved and possibly indicating that the mechanism on display generally requires an intercalary meristem to facilitate mechanoperception.     

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.     

Effects of chelated iron on oogenesis and vegetative growth of kelp gametophytes (Phaeophyceae)

The supply of iron has been reported to affect gametogenesis in the gametophytes of some species of kelps (order Laminariales). Spores of the kelps Alaria marginata Postels & Ruprecht, Dictyoneurum californicum Ruprecht, Egregia menziesii (Turner) Areschoug, Laminaria setchellii Silva, and Macrocystis pyrifera (L.) C. Agardh were cultured in enriched seawater with and without added chelated iron (Fe‐ethylenediaminetetraacetate) to determine the effects of iron on oogenesis. All species showed a decrease in oogenesis without added Fe‐ethylenediaminetetraacetic acid (EDTA). Gametophytes of E. menziesii showed predominant gametogenesis with or without supplied iron, resulting in all cells being converted to gametes so that vegetative growth did not continue. Vegetative gametophytes were obtained in the other species used. Gametophytes of M. pyrifera did not show any oogenesis without added Fe‐EDTA, while those of L. setchellii, A. marginata and D. californicum were intermediate in their response, showing some gametogenesis without added Fe‐EDTA. When Fe‐EDTA supply was delayed by 6, 13 and 20 days with spores of M. pyrifera, the gametophytes produced fewer eggs, with a greater decrease as the delay grew longer. A range of Fe‐EDTA concentrations was investigated using isolated female gametophytes of two strains of M. pyrifera and one of Macrocystis integrifolia Bory. None of these three strains produced gametes without the addition of Fe‐EDTA. Gametophytes of M. integrifolia required the least amount of added Fe‐EDTA to achieve gametogenesis while gametophytes of M. pyrifera required higher amounts, with the two strains showing somewhat different responses. Iron nutrition appears to be an essential factor for gametogenesis in several species of kelps.     

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.     

Culture studies on early development of Lessonia trabeculata (Phaeophyceae,Laminariales): Seasonality and acclimation to light and temperature

Lessonia trabeculata is an important economic and ecological algal resource of Chile. Due to intense use in abalone and alginate industries, severe problems of over‐harvesting are emerging. We compared sporophyte‐initiation and ‐growth in two populations from northern and southern Chile (Bahía Inglesa and Maicolpué) under laboratory conditions. Irradiance and temperature were the most important factors affecting gametophyte development. Meiospores harvested in spring exhibited maximum reproductive and growth potential, while spores released during autumn were moribund, and died within a few days. In both study sites, we found evidence for acclimation: Meiospores collected in summer required higher levels of irradiance and temperature for maximum development than winter spores. Juvenile sporophytes from both localities responded similarly to temperature and/or irradiance. The best conditions for recruitment of sporophytes from both localities were 15°C and white fluorescent light of 40–70 μmol m^?2 s^?1. Although due to its low growth potential L. trabeculata is not a good candidate for mariculture, our results provide the necessary knowledge for laboratory‐based seedling production, which is needed for restoration and repopulation projects in damaged areas.     

Thermal performance curves identify seasonal and site-specific variation in the development of Ecklonia radiata (Phaeophyceae) gametophytes and sporophytes

Rapid ocean warming is affecting kelp forests globally. While the sporophyte life stage has been well studied for many species, the microscopic life stages of laminarian kelps have been understudied, particularly regarding spatial and temporal variations in thermal tolerance and their interaction. We investigated the thermal tolerance of growth, survival, development, and fertilization of Ecklonia radiata gametophytes, derived from zoospores sampled from two sites in Tasmania, Australia, throughout a year, over a temperature gradient (3–30°C). For growth we found a relatively stable thermal optimum at ~20.5°C and stable thermal maxima (25.3–27.7°C). The magnitude of growth was highly variable and depended on season and site, with no consistent spatial pattern for growth and gametophyte size. Survival also had a relatively stable thermal optimum of ~17°C, 3°C below the optimum for growth. Gametophytes grew to single cells between 5 and 25°C, but sporophytes were only observed between 10 and 20°C, indicating reproductive failure outside this range. The results reveal complex effects of source population and season of collection on gametophyte performance in E. radiata, with implications when comparing results from material collected at different localities and times. In Tasmania, gametophytes grow considerably below the estimated thermal maxima and thermal optima that are currently only reached during summer heatwaves, whereas optima for survival (~17°C) are frequently reached and surpassed during heatwaves, which may affect the persistence and recruitment of E. radiata in a warmer climate.     

Seasonal changes in taxon richness and abundance of mobile invertebrates inhabiting holdfast of annual kelp Ecklonia radicosa (Phaeophyceae,Lessoniaceae) at the central Pacific coast of Japan

To investigate seasonal changes in the taxon richness and abundance of mobile invertebrates inhabiting holdfasts of the warm temperate annual kelp Ecklonia radicosa, five holdfasts were collected monthly at the central Pacific coast of Japan from April to November 2014. During the study period, there was little variation in holdfast height and diameter, which ranged from 5.9 to 8.5 cm and from 7.1 to 10.8 cm, respectively. In total 7087 animals were collected from 40 holdfasts (177.2 individuals inds./holdfast, on average). The number of mobile invertebrates gradually increased from May (15 ± 9.9 inds./holdfast) to August (346 ± 152.5 inds./holdfast), with over 300 inds./holdfast until October before rapidly decreasing in November (110 ± 85.6 inds./holdfast). Similarly, taxon richness increased gradually from April (4.3 ± 1.0 taxa/holdfast) to August (11.0 ± 3.7 taxa/holdfast), and decreased in November (8.6 ± 2.3 taxa/holdfast). Interestingly, hundreds of mobile invertebrates inhabited holdfasts of kelp plants that had shed their blade in October and November. Taxon composition from August to October and the number of invertebrates from July to November were comparable to data previously reported for perennial kelps. In this study, the importance of annual Ecklonian species as biogenic habitats was demonstrated for the first time.     

Influence of waves and currents on the growth rate of the kelp Laminaria digitata (Phaeophyceae)

The kelp Laminaria digitata growing in the low intertidal region along energetic coastlines are exposed to a range of hydrodynamic environments. Macroalgae in the intertidal zone can experience both waves and currents independently, but it is unknown how they influence growth rate. Relative growth rate of the meristematic region and the entire blade of L. digitata were measured to assess the influence of wave and current motion from three hydrodynamic environments: low current and low wave (LCLW), high current and low wave (HCLW), and high wave and low current (HWLC). Alongside hydrodynamic data, seawater nutrient concentrations and temperature were also collected and analyzed. Results suggest that differences in L. digitata relative growth rates were not attributed to the seawater nutrient concentrations or temperature, but attributed to the hydrodynamic environments. At the high current condition, kelp growth rate of the meristematic region was enhanced by 45% compared to the high wave condition. When including the entire blade growth rate, an average increase of 25% was observed between the high current and high wave condition. Potentially, the division in growth rate observed between the wave and current motion is related to the frequency and magnitude at which the hydrodynamic forces act. These findings highlight the complexity of the hydrodynamic environment and that forces associated with waves and currents may have a significant role on the productivity of kelp.     

Assessment of photosynthetic performance in the two life history stages of Alaria crassifolia (Laminariales,Phaeophyceae)

Understanding of the physiological responses of kelp to environmental parameters is crucial, especially in the context of environmental change that may have contributed to the decline of kelp forests all over the world. The current study presents the photosynthetic characteristics of the macroscopic sporophyte and microscopic gametophyte stages of the brown alga Alaria crassifolia from Hokkaido, Japan, as determined by examining their photosynthetic responses over a range of temperature and irradiance using dissolved oxygen and chlorophyll fluorescence measurements. Net photosynthetic rates of the sporophyte were consistently higher than those of gametophyte across temperature gradients and irradiance levels. Photosynthesis–irradiance curves at 8°C, 16°C, and 20°C revealed similar initial slopes (α = 0.4–0.9) on the two life history stages, but higher compensation (E _c = 4–7 μmol photons m^?2 s^?1) and saturation irradiances (E _k = 53–103 μmol photons m^?2 s^?1) for the sporophyte than for the gametophyte (E _c = 0–7 μmol photons m^?2 s^?1; E _k = 7–10 μmol photons m^?2 s^?1). Both stages exhibited chronic photoinhibition, as shown by the failure of recovery in their maximum quantum yields (F _v/F _m) following high irradiance stress, with greater possibility of photodamage at low temperature. Gametophytes were less sensitive to low temperatures than sporophytes, given their relatively stable F _v/F _m response. Nevertheless, temperature optima for photosynthesis of both stages coincide with each other at 20–23°C, which correspond to the growth and maturation periods of A. crassifolia in Japan. This species is also likely to suffer from thermal inhibition as both GP rates and F _v/F _m decreased above 24°C.     

The effect of temperature on stigmatic receptivity in sweet cherry (Prunus avium L.)

Plant reproduction is highly vulnerable to environmental conditions such as temperature and, consequently, planet warming may have significant consequences on the reproductive phase with serious implication in agricultural crops. Although pollen tube growth is clearly affected by temperature, little information is available on its effect on the female side and on flower receptivity. In this work, the effect of temperature has been evaluated on stigmatic receptivity of sweet cherry in vivo, in the laboratory, and in planta, in the field. Results herein show that temperature has a clear effect on the duration of stigmatic receptivity. Thus, whereas high temperature reduced stigmatic receptivity, low temperature enlarged it. The stigma lost the capacity to offer support first for pollen penetration, second for pollen germination and, finally, for pollen adhesion. The effect of temperature was more pronounced on pollen germination and penetration than on pollen adhesion. High temperature reduced the germination capacity of the pollen as early as the first day after anthesis, a time when no apparent signs of stigma degeneration are apparent. This clear effect of temperature on stigmatic receptivity and pollen performance may have clear implication in crop performance and in establishing screening criteria of best‐adapted genotypes.     

Effects of irradiance, water temperature and nutrients on the growth of sporelings of the crustose coralline alga Lithophyllum yessoense Foslie (Corallinales, Rhodophyceae)

Lithophyllum yessoense Foslie is a markedly dominant subtidal, crustose coralline alga in south–western Hokkaido, Japan. In this study, the effects of irradiance, water temperature and nutrients (nitrate and phosphate) on the growth of sporelings of the alga were examined. The relative growth rate (RGR) was saturated at 17.6% d^?1 at a high irradiance (240 umol photon m²s^?1). Even at a low irradiance (10.7–49.9 umol photon m^?2s^?1), RGR was 7.1–12.7% d^?1 The survival rate of sporelings was greater than 80% at irradiance above 10.7 μmol photon m^?2s^?1 throughout the culture period. The growth of L. yessoense sporelings was promoted at 15°C and 20°C, but inhibited at 5°C. The half‐saturation constants (Ks) for growth were about 0.5 umol L^?1 and 0.14 umol L^?1 for nitrate and phosphate, respectively. Saturated nitrate and phosphate concentrations for the growth were about 4.0 μmol L^?1 and 0.4 μmol L^?1, respectively, suggesting that L. yessoense is adaptable to a relatively high water temperature, a wide range of irradiance, and low ambient nitrate and phosphate concentrations. The results provide a possible explanation of why L. yessoense is dominant in the environments of south‐western Hokkaido.     

Interactions between temperature and nutrients across levels of ecological organization

Temperature and nutrient availability play key roles in controlling the pathways and rates at which energy and materials move through ecosystems. These factors have also changed dramatically on Earth over the past century as human activities have intensified. Although significant effort has been devoted to understanding the role of temperature and nutrients in isolation, less is known about how these two factors interact to influence ecological processes. Recent advances in ecological stoichiometry and metabolic ecology provide a useful framework for making progress in this area, but conceptual synthesis and review are needed to help catalyze additional research. Here, we examine known and potential interactions between temperature and nutrients from a variety of physiological, community, and ecosystem perspectives. We first review patterns at the level of the individual, focusing on four traits – growth, respiration, body size, and elemental content – that should theoretically govern how temperature and nutrients interact to influence higher levels of biological organization. We next explore the interactive effects of temperature and nutrients on populations, communities, and food webs by synthesizing information related to community size spectra, biomass distributions, and elemental composition. We use metabolic theory to make predictions about how population‐level secondary production should respond to interactions between temperature and resource supply, setting up qualitative predictions about the flows of energy and materials through metazoan food webs. Last, we examine how temperature–nutrient interactions influence processes at the whole‐ecosystem level, focusing on apparent vs. intrinsic activation energies of ecosystem processes, how to represent temperature–nutrient interactions in ecosystem models, and patterns with respect to nutrient uptake and organic matter decomposition. We conclude that a better understanding of interactions between temperature and nutrients will be critical for developing realistic predictions about ecological responses to multiple, simultaneous drivers of global change, including climate warming and elevated nutrient supply.     

Examining the bank of microscopic stages in kelps using culturing and barcoding

This paper describes a method to study the diversity of young kelp sporophytes that are recruited from the bank of microscopic stages. Small samples of rocky substratum (0.5 cm²) were collected from the low intertidal zone, which was dominated by the kelp Laminaria digitata. Samples were cultivated in the laboratory under conditions permitting gametogenesis. Sporophyte recruits in the cultures were isolated and identified at the species level using the barcoding mitochondrial marker rpl31–rns. Sixty per cent of the collected samples had at least one to a maximum of 30 kelp recruits, belonging to five different species (L. digitata, L. hyperborea, L. ochroleuca, Saccharina latissima and Sacchorhiza polyschides). As the examination of freshly collected rocky samples under a stereo microscope did not reveal any kelp sporophytes, the recruitment in these samples after culture probably occurred from the bank of microscopic forms present on the substratum. Despite the dominance of L. digitata in the field, the young sporophytes obtained after culturing were mainly S. polyschides. This study illustrates the suitability of culturing in combination with molecular identification of young sporophytes to address several key aspects of kelp ecology related to the existence of a bank of microscopic stages in the field.     

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.     

Compensatory growth of the kelp Macrocystis integrifolia (Phaeophyceae, Laminariales) against grazing of Peramphithoe femorata (Amphipoda, Ampithoidae) in northern-central Chile

Compensation of tissue loss has been considered an alternative strategy for seaweeds that have no or only minor chemical or structural defense against herbivory. Compensatory responses are facilitated by resource transfer among different tissues and have been suggested for large kelps. Macrocystis integrifolia (Bory) is a common kelp species from northern-central Chile, which is characterized by high growth rates and the absence of lipophilic chemical defenses against herbivore grazing. Herein, we used the giant kelp M. integrifolia to test for compensatory growth in response to grazing by the nest-dwelling amphipod Peramphithoe femorata (Krøyer). Amphipods were allowed to graze inside nests on subapical blades of M. integrifolia sporophytes for 14 days. We measured growth and chemical composition (C, N, laminaran and mannitol) of apical and subapical blades of grazed and ungrazed (control) sporophytes. Our results revealed the capability of M. integrifolia to maintain elongation rates in grazed subapical blades, which were similar to those of subapical blades from ungrazed sporophytes. Apical blades grew slower in grazed than in ungrazed sporophytes indicating a trade-off between apical and subapical blades when herbivores were present. Thus, compensation occurs in blades directly attacked by grazers and is probably mediated by vertical resource allocation within sporophytes to subapical blades, a suggestion supported by the fact that stipe internodes in these regions grew more on grazed sporophytes. In general, our study indicates that M. integrifolia exhibits compensatory growth against the herbivore amphipod P. femorata, and we suggest that this could be an important strategy of large kelp species to tolerate moderate grazing intensities.     

A phylogeographic investigation of the kelp genus Laminaria (Laminariales,Phaeophyceae), with emphasis on the South Atlantic Ocean

The genus Laminaria has a wide distribution range compared with other kelp genera because it is found in both the North and the South Atlantic, on both sides of the North Pacific, as well as in the Mediterranean. Hypotheses behind this biogeographical pattern have been discussed by several authors but have not yet been fully evaluated with time‐calibrated phylogenies. Based on the analysis of four molecular markers (ITS2, rbcL, atp8 and trnWI), our goal was to reassess the Laminaria species diversity in South Africa, assess its relationship with the other species distributed in the South Atlantic and reconstruct the historical biogeography of the genus. Our results confirm the occurrence of a single species, L. pallida, in southern Africa, and its sister relationship with the North Atlantic L. ochroleuca. Both species belonged to a clade containing the other South Atlantic species: L. abyssalis from Brazil, and the Mediterranean L. rodriguezii. Our time‐calibrated phylogenies suggest that Laminaria originated in the northern Pacific around 25 mya, followed by at least two migration events through the Bering Strait after its opening (~5.32 mya). Today, the first is represented by L. solidungula in the Arctic, while the second gave rise to the rest of the Atlantic species. The colonization of the North Atlantic was followed by a gradual colonization southward along the west coast of Europe, into the Mediterranean (~2.07 mya) and two recent, but disconnected, migrations (~1.34 and 0.87 mya) across the equator, giving rise to L. abyssalis in Brazil and L. pallida in southern Africa, respectively.