Contrasting effects of giant kelp on dynamics of surfperch populations

Summary The effect of giant kelp, Macrocystis pyrifera, on the population dynamics of two temperate reef fishes, striped surfperch (Embiotoca lateralis) and black surfperch (E. jacksoni), was examined. Based on an understanding of how particular reef resources influence abundances of the surfperch and of the effect of giant kelp on those resources, we anticipated that Macrocystis would adversely affect populations of striped surfperch but would enhance those of black surfperch. The natural establishment of giant kelp at sites at Santa Cruz Island, California, resulted in the predicted dynamical responses of surfperch. Abundances of striped surfperch declined rapidly when and where dense forests of giant kelp appeared, but showed little change where Macrocystis was continuously absent over the 8 y period of study. Abundances of adult black surperch, which increased following the appearance of giant kelp, were lagged by >1 y because the dynamical response involved enhanced local recruitment. No change in abundance of black surfperch populations was evident at areas without giant kelp.The mechanism by which giant kelp altered the dynamics of the surfperch involved modification of the assemblage of understory algae used by surfperch as foraging microhabitat. Foliose algae (including Gelidium robustum) were much reduced and turf was greatly enhanced following the appearance of Macrocystis; these two benthic substrata are the favored foraging microhabitat for striped surfperch and black surfperch respectively. Populations of both surfperch species tracked temporal changes in the local availability of their favored foraging microhabitat. Thus, while neither species used Macrocystis directly, temporal and spatial variation in giant kelp indirectly influenced the dynamics of these fishes by altering their foraging base. These results indicate that the dynamics of striped surfperch and black surfperch were governed to a large degree by density-dependent consumer-resource interactions. The present work underscores the predictive value that arises from a knowledge of the mechanisms by which processes operate.     

Climate‐driven substitution of habitat‐forming species leads to reduced biodiversity within a temperate marine community

Aim

In marine ecosystems, habitat‐forming species (HFS) such as reef‐building corals and canopy‐forming macroalgae alter local environmental conditions and can promote biodiversity by providing biogenic living space for a vast array of associated organisms. We examined community‐level impacts of observed climate‐driven shifts in the relative abundances of two superficially similar HFS, the warm‐water kelp Laminaria ochroleuca and the cool‐water kelp Laminaria hyperborea.

Location

Western English Channel, north‐east Atlantic

Methods

We compared algal and invertebrate assemblages associated with kelp stipes and holdfasts, across multiple sites and sampling events. Significant differences were recorded in the structure of assemblages between the host kelp species at each site and event.

Results

Assemblages associated with stipes of the cool‐water HFS were, on average, >12 times more diverse and supported >3600 times more biomass compared with the warm‐water HFS. Holdfast assemblages also differed significantly between species, although to a lesser extent than those associated with stipes. Overall, assemblages associated with the warm‐water HFS were markedly impoverished and comprised far fewer rare or unique taxa.

Main conclusions

While previous research has shown how climate‐driven loss of HFS can cause biodiversity loss, our study demonstrates that climate‐driven substitutions of HFS can also lead to impoverished assemblages. The indirect effects of climate change remain poorly resolved, but shifts in the distributions and abundances of HFS may invoke widespread ecological change, especially in marine ecosystems where facilitative interactions are particularly strong.     

Seasonal variation in epifaunal communities associated with giant kelp (Macrocystis pyrifera) at an upwelling‐dominated site

Kelp forests are highly productive and species‐rich benthic ecosystems in temperate regions that provide biogenic habitat for numerous associated species. Diverse epifaunal communities inhabit kelp sporophytes and are subject to variations in the physical environment and to changes experienced by the kelp habitat itself. We assessed seasonal variations in epifaunal invertebrate communities inhabiting giant kelps, Macrocystis pyrifera, and their effects on this seaweed. Six seasonal samplings were conducted over a year at an upwelling‐dominated site in northern‐central Chile where physical conditions are known to fluctuate temporally. More than 30 taxa were identified, among which peracarid crustaceans stood out in both diversity and abundance. Species richness and abundance differed among sporophyte sections (holdfast and fronds) and throughout the year. The frond community was dominated by two grazers (the amphipod Peramphithoe femorata and the isopod Amphoroidea typa), while suspension feeders, grazers, and omnivores (the amphipod Aora typica, the isopod Limnoria quadripunctata, and polychaetes) dominated the holdfasts. Abundances of the dominant species fluctuated throughout the year but patterns of variation differed among species. The most abundant grazer (P. femorata) had highest densities in summer, while the less abundant grazer (A. typa) reached its peak densities in winter. Interestingly, the area of kelp damaged by grazers was highest in autumn and early winter, suggesting that grazing impacts accumulate during periods of low kelp growth, which can thus be considered as ‘vestiges of herbivory past.’ Among the factors determining the observed seasonal patterns, strong variability of environmental conditions, reproductive cycles of associated fauna, and predation by fishes vary in importance. Our results suggest that during spring and early summer, bottom‐up processes shape the community structure of organisms inhabiting large perennial seaweeds, whereas during late summer and autumn, top‐down processes are more important.     

Ecological effects of harvesting Lessonia (Laminariales,Phaeophyta) in central Chile

Lessonia nigrescens and L. trabeculata are economically important canopy-forming kelps in Chile. Experimental harvesting of stipes above the first dichotomy reduces stipe movement and inter-stipe friction, allowing the development of a heavy epiphytic load and increased grazing. Complete stipe removal leads to holdfast death as neither species is able to simultaneously regenerate all stipes. The invertebrate fauna inside the holdfast does not respond to upper canopy changes, but mortality does occur in partial or complete plant removals. Kelp removal also affects inter-plant distances, results in increased access of grazers to the outside and inside of kelp holdfasts, reduces recruitment of other algal species, and modifies the morphology of L. trabeculata such that the plants become more susceptible to removal by water movement.     

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.     

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.     

PHENOTYPIC PLASTICITY RECONCILES INCONGRUOUS MOLECULAR AND MORPHOLOGICAL TAXONOMIES: THE GIANT KELP,MACROCYSTIS (LAMINARIALES,PHAEOPHYCEAE), IS A MONOSPECIFIC GENUS1

The giant kelp genus Macrocystis C. Agardh (Laminariales, Phaeophyceae) is one of the world’s most ecologically and economically important seaweed taxa, yet its taxonomy remains uncertain. Although the genus currently contains four accepted species based on variable holdfast and blade morphology [M. pyrifera (L.) C. Agardh, M. integrifolia Bory, M. angustifolia Bory, and M. laevis C. H. Hay], numerous recent studies on Macrocystis interfertility, genetic relatedness, and morphological plasticity all suggest that the genus is monospecific. We reviewed this evidence and present an explanation for the extreme phenotypic plasticity that results in morphological variability within Macrocystis, driven by the effects of environmental factors on early development of macroscopic sporophytes. We propose that the genus be collapsed back to a single species, with nomenclatural priority given to M. pyrifera.     

Food preference,food quality and diets of three herbivorous gastropods (Trochidae: Tegula) in a temperate kelp forest habitat

Summary The relationship between food preference and food quality (i.e. a food's contribution to growth and reproductive development) was examined in the laboratory for 3 species of herbivorous kelp forest gastropods (Tegula). The preference hierarchies of the 3 Tegula for 6 common algal species are the same: giant kelp (Macrocystis) is the most preferred food and brown algae are consumed at higher rates than red algae. Despite their strong preference for Macrocystis, the 3 species had significantly greater growth and/or reproductive development on a mixed-algae diet than on either brown or red algae alone. Laboratory preferences of the snails did not correspond closely with caloric content, estimated availability or quality of the algal species used in this study. However, the 3 Tegula are subject to strong benthic predation and Macrocystis provides an important spatial refuge in nature. The potential role of non-nutritional factors such as predator avoidance on the formation of food preferences is discussed.     

Macroalgal farming in the sea: water motion and nitrate uptake

A better understanding of water motion effects on nutrient uptake by marine crop plants should make it possible to farm the sea more effectively. Farms in China, Japan and the Philippines now grow plants on slack lines or nets that move with passing waves and currents. Nutrient uptake rates are increased onLaminaria farms in China by adding nitrogen-containing fertilizer. In contrast, forests of the giant kelp,Macrocystis grow in California at low nutrient levels without fertilization. The giant kelp, compared as a structure with the slack Chinese farms, has float-supported, spring-like stipes that stretch and recoil as waves pass. This motion seems likely to enhance flow over the thallus surface. In thus study we modified flow around kelp blades in a water tunnel in the laboratory by changing orifice plates, and flow around Chinese-style long-line farms in the sea by tightening them under various sea conditions. Our measurements suggest that if marine farms were designed and operated to increase water movement over the plants being grown, their rates of nutrient uptake, and growth would increase.This paper was presented at the Symposium on Applied Phycology at the Fourth International Phycological Congress, Duke University.     

SPORE SUPPLY AND HABITAT AVAILABILITY AS SOURCES OF RECRUITMENT LIMITATION IN THE GIANT KELP MACROCYSTIS PYRIFERA (PHAEOPHYCEAE)1

The causes of spatial variation in the recruitment of benthic marine algae are frequently misunderstood because of difficulties in distinguishing among the many factors that influence the supply and establishment of microscopic propagules. We used the recently constructed San Clemente Artificial Reef (SCAR) experiment to examine the roles of dispersal distance, size of spore source, and habitat availability as sources of variation in the recruitment of the giant kelp Macrocystis pyrifera (L.) C. Ag., a species whose recruitment has often been considered to be dispersal limited. Sparse colonization on SCAR by adult Macrocystis occurred within 6 months after reef construction via drifters (i.e. individuals from neighboring kelp beds that became dislodged and set adrift). The abundance of drifters on SCAR declined exponentially with distance from the nearest source population (San Mateo), suggesting that San Mateo was the likely source of drifters. Dense recruitment of small Macrocystis sporophytes was observed within 8 months of reef construction. The density of recruits on SCAR showed an initial increase with distance from San Mateo before declining exponentially. Nonetheless, substantial recruitment was observed at the most distant locations on SCAR located 3.5 km from San Mateo. In contrast to drifters, the density of recruits was positively correlated to the bottom cover of artificial reef substrate. Importantly, no correlation was found between the local density or fecundity of drifters and the local density of kelp recruits suggesting that recruitment on SCAR resulted from widespread spore dispersal rather than from the local dispersal of spores from drifters.     

Behavioral ecology of young-of-the-year kelp rockfish, Sebastes atrovirens Jordan and Gilbert (Pisces: Scorpaenidae)

Young-of-the-year (YOY) kelp rockfish, Sebastes atrovirens, recruit initially to the canopy of the giant kelp, Macrocystis pyrifera (L.), along the coast of central California. During the summer of 1991, I observed major fluctuations in YOY kelp rockfish abundance in the canopy before the onset of a vertical migration downward to the Macrocystis holdfasts. Within the Macrocystis canopy, YOY kelp rockfish make a series of microhabitat shifts preparatory to their downward migration, forming smaller and more closely held aggregations. Experimental manipulations of Macrocystis architecture indicate that YOY kelp rockfish densities are reduced in areas with only small Macrocystis (few stipes) compared to unmanipulated areas with a range of Macrocystis sizes. Unusually large Macrocystis, created by binding multiple kelps together, did not compensate for a preponderance of small Macrocystis in the surrounding areas. In unmanipulated habitat, YOY kelp rockfish densities were correlated with the size of the Macrocystis (number of stipes). Habitat selection in the canopy and holdfasts appears to be behavioral and is closely tied to the architecture of the alga. The onset of the downward migration appears to be triggered by a combination of ontogenetic and environmental cues.     

Cultivation of Macrocystis integrifolia (Laminariales,Phaeophyta) in southeastern Alaskan waters

The artificial culture of Macrocystis integrifolia in southeastern Alaskan waters has been initiated as a first step in a project to augment the existing herring roe-on-kelp fishery in the state. The growing of Macrocystis in Prince William Sound has the potential of considerably enhancing this fishery by eliminating the costly importation of this kelp from southeast Alaska. In an ongoing feasibility study, Macrocystis has been cultured under laboratory conditions through the embryonic sporophyte stage and outplanted in waters near Sitka, Alaska (57° N). Growth of the outplanted kelps has been monitored as a function of the time and depth of the outplanting. Preliminary results suggest that light is limiting for growth in winter and that the optimal depth for outplanting will vary with the season.     

Looking into the black box: simulating the role of self‐fertilization and mortality in the genetic structure of Macrocystis pyrifera

Patterns of spatial genetic structure (SGS), typically estimated by genotyping adults, integrate migration over multiple generations and measure the effective gene flow of populations. SGS results can be compared with direct ecological studies of dispersal or mating system to gain additional insights. When mismatches occur, simulations can be used to illuminate the causes of these mismatches. Here, we report a SGS and simulation‐based study of self‐fertilization in Macrocystis pyrifera, the giant kelp. We found that SGS is weaker than expected in M. pyrifera and used computer simulations to identify selfing and early mortality rates for which the individual heterozygosity distribution fits that of the observed data. Only one (of three) population showed both elevated kinship in the smallest distance class and a significant negative slope between kinship and geographical distance. All simulations had poor fit to the observed data unless mortality due to inbreeding depression was imposed. This mortality could only be imposed for selfing, as these were the only simulations to show an excess of homozygous individuals relative to the observed data. Thus, the expected data consistently achieved nonsignificant differences from the observed data only under models of selfing with mortality, with best fits between 32% and 42% selfing. Inbreeding depression ranged from 0.70 to 0.73. The results suggest that density‐dependent mortality of early life stages is a significant force in structuring Macrocystis populations, with few highly homozygous individuals surviving. The success of these results should help to validate simulation approaches even in data‐poor systems, as a means to estimate otherwise difficult‐to‐measure life cycle parameters.     

PRESENCE OF SPOROPHYLLS IN FLOATING KELP RAFTS OF MACROCYSTIS SPP. (PHAEOPHYCEAE) ALONG THE CHILEAN PACIFIC COAST1

Some species of macroalgae continue to live for extended periods of time after detachment and may even maintain reproductive structures, yet very little is known about this process. Here, we describe the presence of sporophylls (with sporogenous tissues) on floating kelp rafts of Macrocystis spp. along the coast of Chile. Surveys were conducted at nine sites (18–50° S) during austral summer 2002, and floating kelp rafts were seen and collected at seven of these nine sites (between 22 and 50° S). Fifteen (26.8%) of the 56 samples had sporophylls, indicating maintenance of sporophylls after detachment. Some of the kelp sporophytes with reproductive blades showed signs of having been afloat for long periods (indicated by the large size of attached stalked barnacles). Additionally, experiments showed that floating kelps released viable zoospores. To understand the reproductive dynamics of floating kelps, we compared these results with information from attached populations of Macrocystis spp. at nearby coastal sites. In general, attached kelp had higher proportions of sporophylls than floating rafts, suggesting that detachment may negatively affect reproductive status. Nevertheless, floating kelps remained functionally reproductive, suggesting that zoospores may be dispersed via floating rafts. Published reports on other macroalgae indicate that some species (Lessoniaceae, Fucaceae, and Sargassaceae) are fertile and probably release zoospores or zygotes while floating or drifting in ocean currents. Because dispersal distances achieved by spores of most macroalgae are relatively short, release of spores from floating algae may be an alternative mechanism of long‐distance dispersal.     

THE RECLASSIFICATION OF LESSONIA LAMINARIOIDES (LAMINARIALES,PHAEOPHYCEAE): PSEUDOLESSONIA GEN. NOV.1

A new genus, Pseudolessonia, is proposed for the kelp Lessonia laminarioides Postels et Ruprecht (Laminariales, Phaeophyceae), which occurs on the northwest side of the Sea of Okhotsk, in the northwest Pacific Ocean. Pseudolessonia is monotypic and differs from Lessonia in its short primary stipes and its corrugated, unilaterally arranged blades with entire margins. This species is transferred on the basis of morphology and plastid gene sequence comparisons. We determined psaA and rbcL gene sequences from 17 taxa of Pseudolessonia, Lessonia, and putative relatives. Analyses of individual and combined data sets resulted in congruent trees showing a clear separation of Pseudolessonia laminarioides from Lessonia, but suggesting its sister relationships with the clade of Nereocystis, Macrocystis, Pelagophycus, and Postelsia in the North Pacific Ocean. On the other hand, Lessonia species from the South Pacific Ocean formed a strongly supported clade. The results indicate that the basal splitting of the blade, which has been considered a diagnostic character for the family Lessoniaceae, is a result of convergent evolution.     

Seasonal changes of pCO2 over a subantarctic Macrocystis kelp bed

The partial pressure of carbon dioxide (pCO₂), calculated from pH and total alkalinity measurements, was monitored together with chlorophyll a and bacterioplankton biomass in shallow coastal water located inside and outside a giant kelp bed (Macrocystis pyrifera) situated in the Kerguelen Archipelago, Southern Ocean. In spite of large changes over a short time-scale, pCO₂ variations over the year are large and exhibit a seasonal pattern in which the different stages of the annual biological turnover are well marked. The overall pattern of pCO₂ variations is related to biological activity (development of both photosynthesis and respiration) during almost the whole year. However, physical and thermodynamical constraints exert a strong influence on pCO₂ at meso time-scale (10 days) and/or when biological activity is weak. Macrocystis acts to maintain pCO₂ below saturation almost the whole year and large undersaturations (pCO₂ as low as 20 μatm) were observed within the kelp bed. Furthermore, primary production of Macrocystis covers a period of 8 ∼ 9 months a year from winter to late summer and the kelp bed seems to favour the spring phytoplanktonic bloom. The buffer factor β indicates that, outside the kelp bed, inorganic carbon dynamics are mainly influenced by air-sea exchange and photosynthesis without calcification. Inside the kelp bed, β suggests calcification by the epiphytic community. Accepted: 1 April 2000     

Mathematical model ofLaminaria production near a British Columbian salmon sea cage farm

The technical and economical feasibility of farmingLaminaria saccharina for a food base product near a salmon sea cage farm was evaluated. Suitability of kelp for nutrient removal was also analyzed. A computer model of a conceptualized system was developed in order to make the assessments. Kelp growth was modelled as a linear function of temperature and background dissolved inorganic nitrogen concentration, and it was partially experimentally validated. Based on model simulations, aLaminaria farm containing 10,60 m ropes on each end of a salmon sea cage farm is fertilized by the salmon farm and yields annually 1600 kg of dried kelp. The payback period for the initial investment of $61 × 10³ is 6 years after which an annual net profit of 20 × 10³ Canadian dollars ($16.68 × 10³ US) can be achieved. The net present worth of the kelp farm was positive for a rate of return up to 25%. Kelp production on multiple salmon farms or at a higher kelp density could increase the overall revenue.The kelp farm does not appreciably affect background nutrient or oxygen levels. With a few modifications in the model,Nereocystis andMacrocystis farming can be substituted and evaluated for feasibility and nutrient removal efficiency.     

Family‐level variation in early life‐cycle traits of kelp

Temperate kelp forests (Laminarians) are threatened by temperature stress due to ocean warming and photoinhibition due to increased light associated with canopy loss. However, the potential for evolutionary adaptation in kelp to rapid climate change is not well known. This study examined family‐level variation in physiological and photosynthetic traits in the early life‐cycle stages of the ecologically important Australasian kelp Ecklonia radiata and the response of E. radiata families to different temperature and light environments using a family × environment design. There was strong family‐level variation in traits relating to morphology (surface area measures, branch length, branch count) and photosynthetic performance (F_v/F_m) in both haploid (gametophyte) and diploid (sporophyte) stages of the life‐cycle. Additionally, the presence of family × environment interactions showed that offspring from different families respond differently to temperature and light in the branch length of male gametophytes and oogonia surface area of female gametophytes. Negative responses to high temperatures were stronger for females vs. males. Our findings suggest E. radiata may be able to respond adaptively to climate change but studies partitioning the narrow vs. broad sense components of heritable variation are needed to establish the evolutionary potential of E. radiata to adapt under climate change.     

Telomeric localization of the Arabidopsis‐type heptamer repeat, (TTTAGGG)n,at the chromosome ends in Saccharina japonica (Phaeophyta)

Telomeres generally consist of short repeats of minisatellite DNA sequences and are useful in chromosome identification and karyotype analysis. To date, telomeres have not been characterized in the economically important brown seaweed Saccharina japonica, thus its full cytogenetic research and genetic breeding potential has not been realized. Herein, the tentative sequence of telomeres in S. japonica was identified by PCR amplification with primers designed based on the Arabidopsis‐type telomere sequence (TTTAGGG)_n, which was chosen out of three possible telomeric repeat DNA sequences typically present in plants and algae. After PCR optimization and cloning, sequence analysis of the amplified products from S. japonica genomic DNA showed that they were composed of repeat units, (TTTAGGG)_n, in which the repeat number ranged from 15 to 63 (n = 46). This type of repeat sequence was verified by a Southern blot assay with the Arabidopsis‐type telomere sequence as a probe. The digestion of S. japonica genomic DNA with the exonuclease Bal31 illustrated that the target sequence corresponding to the Arabidopsis‐type telomere sequence was susceptible to Bal31 digestion, suggesting that the repeat sequence was likely located at the outermost ends of the kelp chromosomes. Fluorescence in situ hybridizations with the aforementioned probe provided the initial cytogenetic evidence that the hybridization signals were principally localized at both ends of S. japonica chromosomes. This study indicates that the telomeric repeat of the kelp chromosomes is (TTTAGGG)_n which differs from the previously reported (TTAGGG)_n sequence in Ectocarpus siliculosus through genome sequencing, thereby suggesting distinct telomeres in brown seaweeds.