Patterns of abundance and assemblage structure of epifauna inhabiting two morphologically different kelp holdfasts

The mobile fauna associated with two sympatric kelp species with different holdfast morphology (Saccorhiza polyschides and Laminaria hyperborea) was compared to test for differences in the assemblage structure of holdfast-associated mobile epifauna. A total of 24,140 epifaunal individuals were counted from 30 holdfasts of each kelp species. Overall epifaunal abundances exceeded faunal abundances previously reported from holdfasts of other kelps. Three taxonomic groups, Amphipoda, Mollusca, and Polychaeta, accounted for ca. 85% of all individuals. Total abundances increased with the amount of habitat available, quantified either as the volume or the area provided by the holdfasts. The multivariate structure of the epifaunal assemblage did not differ between holdfasts of the two kelp species. However, epifaunal assemblages responded differentially to the habitat attributes provided by each type of kelp holdfast: multivariate variation in the assemblage structure of epifauna was mostly explained by holdfast area and volume for L. hyperborea, and by the surface-to-volume ratio for S. polyschides holdfasts. Therefore, the physical attributes of biogenic habitats, here kelp holdfasts that better predict patterns in the assemblage structure of associated fauna can differ according to their different physical morphology, even though the overall assemblage structure of associated fauna was similar.     

Evaluating stress in rocky shore and shallow reef habitats using the macrofauna of kelp holdfasts

Kelp often dominates hard rocky substrata in the coastal watersof temperate, boreal and subantarctic regions of the world's oceans. The habitat providedby kelp holdfasts supports high species richness and high abundance of a range of invertebratetaxa. Studies conducted on the effects of stress on these communities have indicated that theyare sensitive to stressors and that the response is often predictable. With the growing body ofliterature on natural variation in holdfast community structure, studies of the impacts of stressare becoming more readily interpretable making the macrofauna of this habitat a potentiallyimportant tool for evaluating anthropogenic effects on hard substrata in coastal environments. Limitations of the use of holdfast fauna in studies of stress include the fact that brownseaweeds may disappear from polluted areas of reef, and where they persist, holdfaststructure may be altered directly by the stressor. An additional problem is that manipulative,experimental studies are difficult. Artificial holdfasts may provide a means by which thedemonstrated sensitivity of the holdfast community can be combined with a manipulative approach to testspecific hypotheses related to effects of stress in shallow coastal environments.     

Phenology of annual kelp Eckloniopsis (Phaeophyceae,Laminariales) forest on a Diadema barren in Uchiura Bay,Central Pacific Coast of Honshu,Japan

On the southern coast of Uchiura Bay, central Pacific, Japan, Diadema barrens have expanded since the 1980s but Eckloniopsis radicosa (annual kelp endemic to Japan) has remained in deeper waters (>10 m in depth). Phenology of the kelp was studied on isolated boulders from December 2011 for a year. Young sporophytes appeared in December and rapid growth from April brought the maximum blade length (83.3?±?13.9 cm) and width (56.8?±?12.7 cm) and standing crop (7.4 kg m^?2) in May and June, respectively. Sorus formation began in June and spore release occurred from July to September. Blade length decreased from August and disappeared in November though holdfast remained. The unique holdfast-like spiny ball was found to provide habitats for mobile animals; its forests have an important role to maintain the biodiversity on barrens. During the period, water temperature was between 14.6 and 27.8 °C, salinity was stable around 34–35?‰, and nutrients were never depleted. Tolerance to large and frequent fluctuation of water temperature (7 °C in a day), rapid growth in winter to spring, and occurrence on limited boulders in soft substrata may be the reasons for the success in the maintenance of its forest in Diadema barrens.     

Giant kelp vegetative propagation: Adventitious holdfast elements rejuvenate senescent individuals of the Macrocystis pyrifera “integrifolia” ecomorph

Recent findings on holdfast development in the giant kelp highlighted its key importance for Macrocystis vegetative propagation. We report here for the first time the development of adventitious holdfasts from Macrocystis stipes. Swellings emerge spontaneously from different areas of the stipes, especially in senescent or creeping individuals. After being manually fastened to solid substrata, these swellings elongated into haptera, which became strongly attached after 1 month. Within 4 months, new thalli increased in size and vitality, and developed reproductive fronds. Our results suggest the usage of these structures for auxiliary attachment techniques. These could act as a backup, when primary holdfasts are weak, and thus improve the survival rate of the giant kelp in natural beds.     

Are kelp holdfasts islands on the ocean floor? – indication for temporarily closed aggregations of peracarid crustaceans

During the colonisation process of islands, newly immigrating species often arrive as single individuals. Islands that have received single colonisers may subsequently harbour large populations of a species, while other islands may completely lack this species. Exchange between islands is limited, thereby strongly affecting evolutionary processes. While this concept is widely used in the context of oceanic islands or habitat patches on the mainland, it is rarely used to explain and examine the distribution patterns of marine invertebrates. Benthic marine organisms inhabiting patches with island-like features may also be restricted in their movements between patches. Once established in a patch, it may be more favourable to remain there rather than moving to another patch. Juveniles of species with direct development may recruit to the island patch of their parents. Herein, we examined the peracarid fauna in patches that have island-like features, i.e. kelp holdfasts. The number of peracarid species within an individual holdfast increased with its size. Similarly, the number of individuals per holdfast increased with holdfast size. However, several peracarid species showed a strongly aggregated distribution pattern, being highly abundant in some holdfasts and almost completely absent in others. Our results suggest that these aggregations of conspecifics may be a consequence of the peracarid reproductive biology: fully developed juveniles emerge from the female's marsupium and recruit to the immediate vicinity of their mother, showing little or no tendency to emigrate towards other patches. At present, while it is not known how long peracarid aggregations within kelp holdfasts persist, our data suggest that some juveniles may remain with the natal holdfast and possibly reproduce therein. It is concluded that, during certain time periods, reproduction rates of peracarids in a holdfast may exceed their migration rates between holdfasts.     

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 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.     

Spatial and temporal variability of the benthic assemblages associated to the holdfasts of the kelp <Emphasis Type="Italic">Macrocystis pyrifera</Emphasis> in the Straits of Magellan,Chile

Macrocystis pyrifera (L.) C. Agardh is a characteristic macroalga in the Magellan region covering almost 30% of the shallow coastal waters. The focus of this study was to analyse the spatial and seasonal patterns in macrofauna communities associated to the holdfasts of Macrocystis pyrifera at two study sites in the Straits of Magellan, South Chile. In total, 114 species from 10 major taxa were isolated from the holdfasts. MDS clearly separated the holdfast fauna collected in different seasons, with autumn and winter collections being richer in terms of species richness and abundance as compared to the spring and summer situation. MDS also clearly separated the holdfast associated faunas of the two study sites, Bahía Laredo and Fuerte Bulnes. The community structure and species composition of the associated macro-invertebrates and vertebrates appeared rather heterogeneous, probably due to the extremely heterogeneous environmental conditions along the entire coastline of the Subantarctic Magellan region.     

Nonlinear multivariate models of successional change in community structure using the von Bertalanffy curve

von Bertalanffy curves were used to describe the nonlinear relationship between assemblages inhabiting holdfasts of the kelp Ecklonia radiata and the volume of the holdfast. This was done using nonlinear canonical analyses of principal coordinates (NCAP). The volume of the holdfast is a proxy for the age of the plant and, thus, the canonical axis is a proxy for succession in the marine invertebrate community inhabiting the holdfast. Analyses were done at several different taxonomic resolutions on the basis of various dissimilarity measures. Assemblages in relatively large holdfasts demonstrated ongoing variation in community structure with increasing volume when the dissimilarity used was independent of sample size. Smaller holdfasts had proportionately greater abundances of ophiuroids and encrusting organisms (bryozoans, sponges, ascidians), while larger holdfasts were characterised by proportionately greater abundances of crustaceans, polychaetes and molluscs. Such linear and nonlinear multivariate models may be applied to analyse system-level responses to the growth of many habitat-forming organisms, such as sponges, coral reefs, coralline algal turf or forest canopies.     

Consistency and variation in kelp holdfast assemblages: Spatial patterns of biodiversity for the major phyla at different taxonomic resolutions

The focus of this study was to measure natural spatial variability in the biodiversity of fauna inhabiting kelp holdfasts in northeastern New Zealand at several spatial scales: from meters up to hundreds of kilometers. We wished to test the hypothesis that multivariate variation and biodiversity would vary significantly at different spatial scales in different ways for the major phyla in the holdfast community (Arthropoda, Annelida, Mollusca and Bryozoa). Biodiversity was considered in terms of richness, total abundance, structural composition (as measured by the Bray-Curtis dissimilarity measure) and taxonomic breadth for each major phylum and for the assemblage as a whole. We also examined the effect of taxonomic resolution on multivariate patterns. Species richness and total abundance increased with increases in holdfast volume. Multivariate variation was greatest at the smallest spatial scale for all phyla, but different phyla showed different patterns of multivariate variation at different spatial scales. Variations among locations at the largest spatial scale were primarily due to differences in the composition and richness of bryozoans and molluscs. Location effects became less and less distinct with decreases in taxonomic resolution. There were very few significant differences in richness or abundance for holdfasts of a given volume, taxonomic breadth did not vary significantly across locations, nor did the proportional abundances of phyla. These consistencies across large spatial scales in the absence of environmental impacts and results from other studies suggest that holdfast communities in New Zealand systems would provide a useful model assemblage against which future impacts may be detected as changes in proportions of component phyla. In addition, high variability detected at small and large scales at the species level, especially for bryozoans and molluscs, suggest that these communities may also provide unique opportunities for studying and understanding sources and functions of marine biodiversity.     

Short-term dispersal of kelp fauna to cleared (kelp-harvested) areas

The kelp Laminaria hyperborea forms large forests and houses a numerous and diverse fauna, especially in the kelp holdfast and stipe epiphytes. Kelp harvesting creates cleared areas and fragmentizes the kelp forest. We investigated the dispersal ability of kelp fauna to cleared, harvested areas by studying their colonization pattern to artificial substrata (kelp mimics) exposed for a short (3 days) and longer time period (35 days) at different sites within the kelp forest (one site) and at a cleared area (two sites). Most of the kelp fauna (111 species) showed a rapid dispersal and colonized the artificial substrata within the cleared area. The similarity of the faunal community in the mimics with the natural kelp holdfast community increased with the length of the exposure period. During the experiments, 87% of the mobile species in the kelp plants were found in the kelp mimics, indicating good dispersal for slow-moving animals like gastropods, polychaetes and tube-building crustaceans. Relating the frequency of the different faunal groups in the untrawled kelp forest to their frequency in the kelp mimics, showed gastropods, amphipods and decapods to have relatively high dispersal rates, whereas isopods, bivalves, polychaetes and tanaids showed a lower dispersal rate than expected. Amphipods dispersed as juveniles and adults. No significant differences were found between the faunal composition and number of species in the mimics placed inside the kelp forest and in the cleared area. Remaining holdfasts and pebbles were identified as refuges/alternative habitats in the harvested area, and may together with the nearest kelp vegetation, serve as sources for colonization to new substrata. The high dispersal ability of most of the kelp fauna provides maintenance of the faunal composition of disturbed habitats and ensures colonization of recovering algal habitats regardless of reproduction strategy.     

Diurnal, horizontal and vertical dispersal of kelp-associated fauna

The kelp Laminaria hyperborea is host for a rich fauna of mobile invertebrates. Dispersal patterns of these animals may be crucial for their availability to visual predators like fish, which are known to search for food in these productive habitats. Diurnal, horizontal and vertical dispersal within and out of the kelp forest were studied by analysing colonization of artificial substrata placed among kelps. The species composition of the fauna was different on three parts of the kelp: lamina, stipes (with epiphytes) and holdfast. The artificial substrata were colonized mainly by species associated with kelp. More species and individuals colonized the artificial substrata at night than during the day. The most abundant faunal groups on the kelps and the artificial substrata were amphipods and gastropods. Both groups dispersed at a significantly higher rate at night than during the day. Rapid horizontal dispersal out of the kelp forest was found. The artificial substrata were also colonized quickly by kelp fauna at all vertical levels inside and above the kelp forest. However, species associated with the kelp holdfast tended to disperse close to the bottom, while stipe-associated fauna moved through all parts of the kelp forest and even above the canopy layer. A high dispersal rate appears common amongst the mobile species living on kelp and seems to be advantageous, despite the risks involved in emigrating from the habitat and being exposed to predators. Higher activity at night may reduce availability to predators.     

莱州湾大型砂壳纤毛虫群落季节变化

为揭示莱州湾砂壳纤毛虫群落季节变化规律, 在莱州湾设置8个站位, 于2011年5-11月及2012年3-4月进行了9个航次的调查, 用浅海III型浮游生物网由底至表垂直拖网采集砂壳纤毛虫。结果表明, 莱州湾3-11月砂壳纤毛虫物种丰富度的变化范围为5-19, 周年变化呈现一峰两谷的趋势。丰度的范围为0-318 ind./L, 丰度较大(> 50 ind./L)的种类有运动类铃虫(Codonellopsis mobilis)和清兰拟铃虫(Tintinnopsis chinglanensis)。各月平均丰度随时间的变化趋势为双峰型, 最大值出现在7月(63 ind./L), 次峰值出现在5月(48 ind./L), 最小值出现在3月(2 ind./L)。黏着壳种类在3-11月均有出现, 透明壳种类仅在温度较高(> 15°C)的6-9月出现。各月的优势种数目为1种(5月)到8种(8月), 其中运动类铃虫在所有月中都是优势种, 对砂壳纤毛虫丰度周年的变化规律产生较大影响。使用各月所有种类的平均丰度对各月砂壳纤毛虫群落进行聚类分析, 得到两个群落(相似度30%): 群落I(7-9月)和群落II(3-6月、10-11月), 说明砂壳纤毛虫群落发生了明显的季节变化。砂壳纤毛虫的物种丰富度、丰度与环境因子(温度、盐度)均没有明显的相关性。     

Utilization of holdfast fragments for vegetative propagation of Macrocystis integrifolia in Atacama, Northern Chile

We attempted to propagate Macrocystis integrifolia (giant kelp) by fragmentation and regeneration of holdfasts, which consist of creeping stolons with lateral haptera. Stolons from a natural kelp population in Bahia Chasco (Atacama, North Chile) were cut into fragments, each containing one or more lateral stipe and frond initials. Fragments were attached to longlines with elastic bands. We used two additional types of inoculants as controls: (1) natural recruits from the local parent population and (2) laboratory-cultured young sporophytes. Length, reproductive phenology, and mortality were determined monthly. Our results confirmed the feasibility of M. integrifolia propagation by reattachment of stolon fragments, and we obtained up to eight new individuals from one parent holdfast. Individuals from holdfast regeneration formed sporangial sori 3 months earlier than control specimens from recruits and laboratory culture, while all three types gave similar values for mortality. Holdfast morphology of regenerates differed strongly depending on their origin: stolon fragments continued growth and developed new haptera except in the cut surfaces, natural recruits formed typical M. integrifolia holdfast morphs, and sporophytes originating from laboratory culture produced minor stolons with many haptera. Implications of our results on ecology, repopulation, and aquaculture are discussed.     

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.     

Diverse invertebrate fauna using dry sediment as a refuge in semi-arid and temperate Australian rivers

Dormant aquatic invertebrates can remain viable in riverbed sediment during dry phases, forming a source for recolonisation during wet periods. Regional differences in capacity for invertebrates to survive drying in this way are poorly understood, but may indicate regional differences in vulnerability to altered flow regimes. We compared diversity of invertebrates in dry sediment from intermittent rivers in temperate and semi-arid Australia after 4–8 weeks of drying. We predicted adaptations of semi-arid biota to severe and unpredictable drying would make dry sediment a more significant recolonisation source, with higher relative diversity when compared with temperate rivers. Emerging aquatic invertebrate assemblages were compared to those sampled in nearby pools, as a common drying refuge. Relative taxa richness in rehydrated sediments was higher in the semi-arid region (83 ± 16% of pool taxa) than the temperate (47 ± 6% of pool taxa), despite lower overall richness (24 taxa in semi-arid, 32 taxa in temperate). Semi-arid rivers had greater potential for dry riverbeds to act as a source for recolonisation, given high relative diversity and abundance in dry sediment, combined with the frequent absence of alternative refuges. However, dry riverbeds in both regions provided a significant short-term refuge for aquatic invertebrates.     

Multivariate dispersion as a measure of beta diversity

Beta diversity can be defined as the variability in species composition among sampling units for a given area. We propose that it can be measured as the average dissimilarity from individual observation units to their group centroid in multivariate space, using an appropriate dissimilarity measure. Differences in beta diversity among different areas or groups of samples can be tested using this approach. The choice of transformation and dissimilarity measure has important consequences for interpreting results. For kelp holdfast assemblages from New Zealand, variation in species composition was greater in smaller holdfasts, while variation in relative abundances was greater in larger holdasts. Variation in community structure of Norwegian continental shelf macrobenthic fauna increased with increases in environmental heterogeneity, regardless of the measure used. We propose a new dissimilarity measure which allows the relative weight placed on changes in composition vs. abundance to be specified explicitly.     

Benthic macro- and meso-invertebrates of a sandy riverbed in a mountain stream, central Japan

Quantitative samples of benthic invertebrates were collected from a sandy riverbed of a mountainous stream (Kozu site of Takami-gawa stream, Nara Prefecture), central Japan by core samplers in five sampling occasions through the years 2008–2009. A total of 120 taxa were identified, representing 55 families and 97 genera. Insects formed about 92% of the total recorded taxa and 88% of individuals’ abundance. A total of 111 taxa of aquatic insects, belonging to 49 families and 92 genera, were identified and represented by ten orders. Oligochaeta and Acari were dominant non-insect invertebrates. Diptera was the most diverse insect group, followed by Trichoptera and Ephemeroptera. Dominant taxa were mesoinvertebrates, younger stages of macroinvertebrates, both of which predominantly inhabit the interstitial zone of a sandy riverbed. Both taxon richness and invertebrate abundance were higher in February 2009 and lower in April and August 2008. A few major invertebrate taxa demonstrated distinct seasonal trends; i.e. Nymphomyia alba, Rheosmittia, and Corynoneura were abundant in February 2009. Newly hatched larvae of Larcasia akagiae were abundant in May 2008. This study also demonstrated the effectiveness of core samplers to collect small-sized benthic fauna that inhabit the interstitial or hyporheic zone of the sandy riverbed.     

Ediacaran macroalgal holdfasts and their evolution: a case study from China

A macroalgal holdfast (root-like structure) anchored or grown into sediments is a key trait of metaphytes and eukaryotic algae. Various patterns and taphonomic variants of congeneric holdfasts are preserved on the bedding planes of black shales of the Ediacaran Wenghui biota in South China. The macroalgal holdfast, which commonly consists of a rhizome, rhizoid and pith (perhaps mechanical tissue), can be morphologically classified into ten types within four groups of rhizomes: bare rhizome holdfasts (Grypania, Tongrenphyton and Sectoralga-type holdfasts), canopy rhizome holdfasts (Gemmaphyton, Gesinella, Discusphyton and Baculiphyca-type holdfasts), pithy rhizome holdfasts (Zhongbaodaophyton and pithy-cone-type holdfasts) and differentiated rhizome holdfasts (Wenghuiphyton-type holdfasts). Analysis of the Precambrian macroalgal record indicates that rhizomes played a more important role in the evolution of macroalgal holdfast than rhizoids. The following evolutionary stages of development of macroalgal holdfasts are proposed: (1) growth of the basal thallus into sediments (Grypania-type holdfast); (2) development of a primitive (indistinct) rhizome from the base of a stipe or thallus (Tongrenphyton-type and Sectoralga-type holdfasts); (3) growth of a distinct rhizome with rhizoid (Gemmaphyton-type, Gesinella-type and Discusphyton-type holdfasts); (4) development of a pith in the stipe (Baculiphyca-type holdfast); (5) pith extension into the rhizome (Zhongbaodaophyton-type and pithy-cone-type holdfasts); and (6) rhizome differentiation and development of a complex holdfast system (Wenghuiphyton-type holdfast).