James A. Coyer

North Atlantic phylogeography and large-scale population differentiation of the seagrass Zostera marina L.

As the most widespread seagrass in temperate waters of the Northern Hemisphere, Zostera marina provides a unique opportunity to investigate the extent to which the historical legacy of the last glacial maximum (LGM18 000–10 000 years bp) is detectable in modern population genetic structure. We used sequences from the nuclear rDNA–internal transcribed spacer (ITS) and chloroplast matK‐intron, and nine microsatellite loci to survey 49 populations (> 2000 individuals) from throughout the species’ range. Minimal sequence variation between Pacific and Atlantic populations combined with biogeographical groupings derived from the microsatellite data, suggest that the trans‐Arctic connection is currently open. The east Pacific and west Atlantic are more connected than either is to the east Atlantic. Allelic richness was almost two‐fold higher in the Pacific. Populations from putative Atlantic refugia now represent the southern edges of the distribution and are not genetically diverse. Unexpectedly, the highest allelic diversity was observed in the North Sea–Wadden Sea–southwest Baltic region. Except for the Mediterranean and Black Seas, significant isolation‐by‐distance was found from ~150 to 5000 km. A transition from weak to strong isolation‐by‐distance occurred at ~150 km among northern European populations suggesting this scale as the natural limit for dispersal within the metapopulation. Links between historical and contemporary processes are discussed in terms of the projected effects of climate change on coastal marine plants. The identification of a high genetic diversity hotspot in Northern Europe provides a basis for restoration decisions.

Glacial refugia and recolonization pathways in the brown seaweed Fucus serratus

The last glacial maximum (20 000–18 000 years ago) dramatically affected extant distributions of virtually all northern European biota. Locations of refugia and postglacial recolonization pathways were examined in Fucus serratus (Heterokontophyta; Fucaceae) using a highly variable intergenic spacer developed from the complete mitochondrial genome of Fucus vesiculosus. Over 1500 samples from the entire range of F. serratus were analysed using fluorescent single strand conformation polymorphism. A total of 28 mtDNA haplotypes was identified and sequenced. Three refugia were recognized based on high haplotype diversities and the presence of endemic haplotypes: southwest Ireland, the northern Brittany‐Hurd Deep area of the English Channel, and the northwest Iberian Peninsula. The Irish refugium was the source for a recolonization sweep involving a single haplotype via northern Scotland and throughout Scandinavia, whereas recolonization from the Brittany‐Hurd Deep refugium was more limited, probably because of unsuitable soft‐bottom habitat in the Bay of Biscay and along the Belgian and Dutch coasts. The Iberian populations reflect a remnant refugium at the present–day southern boundary of the species range. A generalized skyline plot suggested exponential population expansion beginning in the mid‐Pleistocene with maximal growth during the Eems interglacial 128 000–67 000 years ago, implying that the last glacial maximum mainly shaped population distributions rather than demography.

Community-wide effects of nonindigenous species on temperate rocky reefs

Ecological interactions among invading species are common and may often be important in facilitating invasions. Indeed, the presence of one nonindigenous species can act as an agent of disturbance that facilitates the invasion of a second species. However, most studies of nonindigenous species are anecdotal and do not provide substantive evidence that interactions among nonindigenous species have any community-level effects. Here, using a combination of field experiments and observations we examine interactions among introduced species in New England kelp forests and ask whether these interactions have altered paradigms describing subtidal communities in the Gulf of Maine. The green alga Codium fragile was observed at the Isles of Shoals, Maine, USA, in 1983 and has since replaced the native kelp as the dominant seaweed on leeward shores. Experiments manipulating kelp and Codium reveal that Codium does not directly inhibit growth or survival of kelp. Codium does, however, successfully recruit to gaps in the kelp bed and, once established, inhibits recruitment of kelp. A second nonindigenous species, Membranipora membranacea, grows epiphytically on kelp, and experiments reveal that the presence of Membranipora reduces growth and survival of kelp, resulting in defoliation of kelp plants and gap formation in kelp beds. In the absence of Codium, kelp recolonizes these gaps, but when present, Codium colonizes and prevents kelp recolonization. Manipulations of herbivores demonstrate that herbivory will reinforce Codium dominance. Thus, the demise of New England kelp beds appears to result from one invasive species facilitating the spread of a second nonindigenous species.

Post-ice age recolonization and differentiation of Fucus serratus L. (Phaeophyceae; Fucaceae) populations in Northern Europe

The seaweed Fucus serratus is hypothesized to have evolved in the North Atlantic and present populations are thought to reflect recolonization from a southern refugium since the last glacial maximum 18 000–20 000 years bp. We examined genetic structure across several spatial scales by analysing seven microsatellite loci in populations collected from 21 localities throughout the species’ range. Spatial auto‐correlation analysis of seven microsatellite loci revealed no evidence for spatial clustering of alleles on a scale of 100 m despite limited gamete dispersal in F. serratus of ≈ 2 m from parental individuals. Pairwise θ analysis suggested that the minimal panmictic unit for F. serratus was between 0.5 and 2 km. Isolation by distance was significant along some contiguous coastlines. Population differentiation was strong within the Skagerrak–Kattegat–Baltic Seas (SKB) (global θ= 0.17) despite a short history of ≈ 7500 years. A neighbour‐joining tree based on Reynolds distances computed from the microsatellite data revealed a central assemblage of populations on the Brittany Peninsula surrounded by four well‐supported clusters consisting of the SKB, the North Sea (Ireland, Helgoland), and two populations from the northern Spanish coast. Samples from Iceland and Nova Scotia were most closely aligned with northwest Sweden and Brittany, respectively. When sample sizes were standardized (N = 41), allelic diversity was twofold higher for Brittany populations than for populations to the north and threefold higher than southern populations. The Brittany region may be a refugium or a recolonized area, whereas the Spanish populations most likely reflect present‐day edge populations that have undergone repeated bottlenecks as a consequence of thermally induced cycles of recolonization and extinction.

EVOLUTION OF MACROCYSTIS SPP. (PHAEOPHYCEAE) AS DETERMINED BY ITS1 AND ITS2 SEQUENCES1

Macrocystis (Lessoniaceae) displays an antitropical distribution, occurring in temperate subtidal regions along western North America in the northern hemisphere and throughout the southern hemisphere. We used the noncoding rDNA internal transcribed spacer regions (ITS1 and ITS2) to examine relatedness among (1) Macrocystis and several genera of Laminariales, (2) four species of Macrocystis (M. integrifolia Bory from the northern hemisphere, M. angustifolia Bory and M. laevis Hay from the southern hemisphere, and M. pyrifera[L.] C. Ag. from both hemispheres), and (3) multiple clones of several individuals. Of the taxa included in our phylogenetic analysis, the elk kelp, Pelagophycus porra (Lem.) Setch., was the sister taxon to Macrocystis spp. Macrocystis individuals from the southern hemisphere (representing three species) formed a strongly to moderately supported clade, respectively, when the ITS1 and ITS2 sequences were analyzed separately. No distinction was detected between the two species in the northern hemisphere. Thus, Macrocystis may be a monospecific genus (M. pyrifera). A northern‐hemisphere‐to‐southern‐hemisphere pattern of dispersal was inferred, because northern‐hemisphere individuals were more diverse and displayed paraphyletic clades, whereas southern‐hemisphere individuals were less diverse and formed a monophyletic clade. High intraindividual variation in ITS1 sequences was observed in one individual from Santa Catalina Island (CA), suggesting very recent and rapid mixing of genotypes from areas to the north and Baja California (Mexico) or introgressive hybridization with Pelagophycus.

Population genetics of dwarf eelgrass Zostera noltii throughout its biogeographic range

The marine angiosperm Zostera noltii (dwarf eelgrass), an important facilitator species and food source for invertebrates and waterfowl, predominantly inhabits intertidal habitats along eastern Atlantic shores from Mauritania to southern Norway/Kattegat Sea and throughout the Mediterranean, Black and Azov seas. We used 9 microsatellite loci to characterize population struc- ture at a variety of spatial scales among 33 populations from 11 localities throughout the entire biogeographic range. Isolation by distance analysis suggested a panmictic genetic neighborhood of 100 to 150 km. At the global scale, a neighbor-joining tree based on Reynolds distances revealed strongly-supported groups corresponding to northern Europe, Mauritania and the Black/Azov Sea; separate Mediterranean and Atlantic-Iberian groups were poorly supported. Clones (genets with multiple ramets) were present in most populations but were generally small (ca. <3 m 2 ). Exceptions were found in Mauritania (ca. 29 m in length), the Azov Sea (ca. 40 m in length) and the Black Sea (ca. 50 m in length). Although genetic diversity and allelic richness generally decreased from Mauri- tania to Denmark, the putative post-glacial recolonization route, both were unexpectedly high among populations from the German Wadden Sea.

Climate change impact on seaweed meadow distribution in the North Atlantic rocky intertidal.

The North-Atlantic has warmed faster than all other ocean basins and climate change scenarios predict sea surface temperature isotherms to shift up to 600 km northwards by the end of the 21st century. The pole-ward shift has already begun for many temperate seaweed species that are important intertidal foundation species. We asked the question: Where will climate change have the greatest impact on three foundational, macroalgal species that occur along North-Atlantic shores: Fucus serratus, Fucus vesiculosus, and Ascophyllum nodosum? To predict distributional changes of these key species under three IPCC (Intergovernmental Panel on Climate Change) climate change scenarios (A2, A1B, and B1) over the coming two centuries, we generated Ecological Niche Models with the program MAXENT. Model predictions suggest that these three species will shift northwards as an assemblage or “unit” and that phytogeographic changes will be most pronounced in the southern Arctic and the southern temperate provinces. Our models predict that Arctic shores in Canada, Greenland, and Spitsbergen will become suitable for all three species by 2100. Shores south of 45° North will become unsuitable for at least two of the three focal species on both the Northwest- and Northeast-Atlantic coasts by 2200. If these foundational species are unable to adapt to the rising temperatures, they will lose their centers of genetic diversity and their loss will trigger an unpredictable shift in the North-Atlantic intertidal ecosystem.

Biodiversity mediates top–down control in eelgrass ecosystems: a global comparative‐experimental approach

Nutrient pollution and reduced grazing each can stimulate algal blooms as shown by numerous experiments. But because experiments rarely incorporate natural variation in environmental factors and biodiversity, conditions determining the relative strength of bottom-up and top-down forcing remain unresolved. We factorially added nutrients and reduced grazing at 15 sites across the range of the marine foundation species eelgrass (Zostera marina) to quantify how top-down and bottom-up control interact with natural gradients in biodiversity and environmental forcing. Experiments confirmed modest top-down control of algae, whereas fertilisation had no general effect. Unexpectedly, grazer and algal biomass were better predicted by cross-site variation in grazer and eelgrass diversity than by global environmental gradients. Moreover, these large-scale patterns corresponded strikingly with prior small-scale experiments. Our results link global and local evidence that biodiversity and top-down control strongly influence functioning of threatened seagrass ecosystems, and suggest that biodiversity is comparably important to global change stressors.

Interactions between corals and algae on a temperate zone rocky reef: mediation by sea urchins

Abstract Interactions among sea urchins, algae, and a scleractinian coral were examined in a 10-year study off Anacapa Island, California. Abundances of the solitary cup coral Balanophyllia elegans Verrill and percent cover of algae were inversely correlated. Corals could be killed due to overgrowth by kelp holdfasts, ephemeral filamentous algae, or encrusting coralline algae. Overgrowth by filamentous and coralline algae was enhanced by chronic brushing by larger algal species which caused coral polyps to retract. Short- and long-term observations and manipulative experiments demonstrated that significantly more coral polyps were retracted and coral mortality was increased within the brushing zone of natural and artificial algae than in control areas without algae. Additionally, the extent of polyp retraction varied with algal species and degree of water motion. The adverse effects of algae on corals can be mediated by urchin grazing. High densities of urchins remove algae, thereby reducing coral mortality due to algal overgrowth and allowing corals to increase in abundance.

An Expressed Sequence Tag Analysis of the Intertidal Brown Seaweeds Fucus serratus (L.) and F. vesiculosus (L.) (Heterokontophyta, Phaeophyceae) in Response to Abiotic Stressors

In order to aid gene discovery and uncover genes responding to abiotic stressors in stress-tolerant brown algae of the genus Fucus, expressed sequence tags (ESTs) were studied in two species, Fucus serratus and Fucus vesiculosus. Clustering of over 12,000 ESTs from three libraries for heat shock/recovery and desiccation/rehydration resulted in identification of 2,503, 1,290, and 2,409 unigenes from heat-shocked F. serratus, desiccated F. serratus, and desiccated F. vesiculosus, respectively. Low overall annotation rates (18–31%) were strongly associated with the presence of long 3′ untranslated regions in Fucus transcripts, as shown by analyses of predicted protein-coding sequence in annotated and nonannotated tentative consensus sequences. Posttranslational modification genes were overrepresented in the heat shock/recovery library, including many chaperones, the most abundant of which were a family of small heat shock protein transcripts, Hsp90 and Hsp70 members. Transcripts of LI818-like light-harvesting genes implicated in photoprotection were also expressed during heat shock in high light. The expression of several heat-shock-responsive genes was confirmed by quantitative reverse transcription polymerase chain reaction. However, candidate genes were notably absent from both desiccation/rehydration libraries, while the responses of the two species to desiccation were divergent, perhaps reflecting the species-specific physiological differences in stress tolerance previously established. Desiccation-tolerant F. vesiculosus overexpressed at least 17 ribosomal protein genes and two ubiquitin-ribosomal protein fusion genes, suggesting that ribosome function and/or biogenesis are important during cycles of rapid desiccation and rehydration in the intertidal zone and possibly indicate parallels with other poikilohydric organisms such as desiccation-tolerant bryophytes.