Generality in multispecies responses to ocean acidification revealed through multiple hypothesis testing

Decades of research have demonstrated that many calcifying species are negatively affected by ocean acidification, a major anthropogenic threat in marine ecosystems. However, even closely related species may exhibit different responses to ocean acidification and less is known about the drivers that shape such variation in different species. Here, we examine the drivers of physiological performance under ocean acidification in a group of five species of turf‐forming coralline algae. Specifically, quantitating the relative weight of evidence for each of ten hypotheses, we show that variation in coralline calcification and photosynthesis was best explained by allometric traits. Across ocean acidification conditions, larger individuals (measured as noncalcified mass) had higher net calcification and photosynthesis rates. Importantly, our approach was able to not only identify the aspect of size that drove the performance of coralline algae, but also determined that responses to ocean acidification were not dependent on species identity, evolutionary relatedness, habitat, shape, or structural composition. In fact, we found that failure to test multiple, alternative hypotheses would underestimate the generality of physiological performances, leading to the conclusion that each species had different baseline performance under ocean acidification. Testing among alternative hypotheses is an essential step toward determining the generalizability of experiments across taxa and identifying common drivers of species responses to global change.     

CLATHROMORPHUM NEREOSTRATUM (CORALLINALES,RHODOPHYTA): THE OLDEST ALGA?1

The longevity of organisms is intrinsically interesting and can provide useful information on their population structure and dynamics and the dynamics of associated communities. With the exception of perennial Laminariales that have rings in the stipe, the life spans of most perennial macroalgae are unknown or based on anecdotal observations. Using morphological analyses combined with the location and time of the rise in ¹⁴C from atmospheric nuclear testing within the thallus, we determined that the growth rate of a specimen of Clathromorphum nereostratum Lebednik from Adak Island was 0.30 mm·yr^?1, the 3⁰ bands within the thallus were annual, and the specimen sampled was 61–75 years old. Living crusts of this species from the same geographic region are reported to be up to 20 cm thick. Assuming our growth rate is typical, C. nereostratum can be approximately 700 years old, the oldest known living alga. This longevity and consistent banding within the thallus suggest that smaller scale sampling and additional chemical analyses of this alga could provide a detailed long‐term record of environmental variation at high latitudes in the North Pacific.     

Revision of Corallinaceae (Corallinales,Rhodophyta): recognizing Dawsoniolithon gen. nov., Parvicellularium gen. nov. and Chamberlainoideae subfam. nov. containing Chamberlainium gen. nov. and Pneophyllum

A multi‐gene (SSU, LSU, psbA, and COI) molecular phylogeny of the family Corallinaceae (excluding the subfamilies Lithophylloideae and Corallinoideae) showed a paraphyletic grouping of six monophyletic clades. Pneophyllum and Spongites were reassessed and recircumscribed using DNA sequence data integrated with morpho‐anatomical comparisons of type material and recently collected specimens. We propose Chamberlainoideae subfam. nov., including the type genus Chamberlainium gen. nov., with C. tumidum comb. nov. as the generitype, and Pneophyllum. Chamberlainium is established to include several taxa previously ascribed to Spongites, the generitype of which currently resides in Neogoniolithoideae. Additionally we propose two new genera, Dawsoniolithon gen. nov. (Metagoniolithoideae), with D. conicum comb. nov. as the generitype and Parvicellularium gen. nov. (subfamily incertae sedis), with P. leonardi sp. nov. as the generitype. Chamberlainoideae has no diagnostic morpho‐anatomical features that enable one to assign specimens to it without DNA sequence data, and it is the first subfamily to possess both Type 1 (Chamberlainium) and Type 2 (Pneophyllum) tetra/bisporangial conceptacle roof development. Two characters distinguish Chamberlainium from Spongites: tetra/biasporangial conceptacle chamber diameter (<300 μm in Chamberlainium vs. >300 μm in Spongites) and tetra/bisporangial conceptacle roof thickness (<8 cells in Chamberlainium vs. >8 cells in Spongites). Two characters also distinguish Pneophyllum from Dawsoniolithon: tetra/bisporangial conceptacle roof thickness (<8 cells in Pneophyllum vs. >8 cells in Dawsoniolithon) and thallus construction (dimerous in Pneophyllum vs. monomerous in Dawsoniolithon).     

Aragonite infill in overgrown conceptacles of coralline Lithothamnion spp. (Hapalidiaceae,Hapalidiales, Rhodophyta): new insights in biomineralization and phylomineralogy

New empirical and quantitative data in the study of calcium carbonate biomineralization and an expanded coralline psbA framework for phylomineralogy are provided for crustose coralline red algae. Scanning electron microscopy (SEM) and energy dispersive spectrometry (SEM‐EDS) pinpointed the exact location of calcium carbonate crystals within overgrown reproductive conceptacles in rhodolith‐forming Lithothamnion species from the Gulf of Mexico and Pacific Panama. SEM‐EDS and X‐ray diffraction (XRD) analysis confirmed the elemental composition of these calcium carbonate crystals to be aragonite. After spore release, reproductive conceptacles apparently became overgrown by new vegetative growth, a strategy that may aid in sealing the empty conceptacle chamber, hence influencing the chemistry of the microenvironment and in turn promoting aragonite crystal growth. The possible relevance of various types of calcium carbonate polymorphs present in the complex internal structure and skeleton of crustose corallines is discussed. This is the first study to link SEM, SEM‐EDS, XRD, Microtomography and X‐ray microscopy data of aragonite infill in coralline algae with phylomineralogy. The study contributes to the growing body of literature characterizing and speculating about how the relative abundances of carbonate biominerals in corallines may vary in response to changes in atmospheric pCO₂, ocean acidification, and global warming.     

Crusticorallina gen. nov., a nongeniculate genus in the subfamily Corallinoideae (Corallinales,Rhodophyta)

Molecular phylogenetic analyses of 18S rDNA (SSU) gene sequences confirm the placement of Crusticorallina gen. nov. in Corallinoideae, the first nongeniculate genus in an otherwise geniculate subfamily. Crusticorallina is distinguished from all other coralline genera by the following suite of morpho‐anatomical characters: (i) sunken, uniporate gametangial and bi/tetrasporangial conceptacles, (ii) cells linked by cell fusions, not secondary pit connections, (iii) an epithallus of 1 or 2 cell layers, (iv) a hypothallus that occupies 50% or more of the total thallus thickness, (v) elongate meristematic cells, and (vi) trichocytes absent. Four species are recognized based on rbcL, psbA and COI‐5P sequences, C. painei sp. nov., the generitype, C. adhaerens sp. nov., C. nootkana sp. nov. and C. muricata comb. nov., previously known as Pseudolithophyllum muricatum. Type material of Lithophyllum muricatum, basionym of C. muricata, in TRH comprises at least two taxa, and therefore we accept the previously designated lectotype specimen in UC that we sequenced to confirm its identity. Crusticorallina species are very difficult to distinguish using morpho‐anatomical and/or habitat characters, although at specific sites, some species may be distinguished by a combination of morpho‐anatomy, habitat and biogeography. The Northeast Pacific now boasts six coralline endemic genera, far more than any other region of the world.     

Genetic and morphological variation in an ecosystem engineer,Lithophyllum byssoides (Corallinales,Rhodophyta)

Lithophyllum byssoides is a common coralline alga in the intertidal zone of Mediterranean coasts, where it produces biogenic concretions housing a high algal and invertebrate biodiversity. This species is an ecosystem engineer and is considered a target for conservation efforts, but designing effective conservation strategies currently is impossible due to lack of information about its population structure. The morphological and molecular variation of L. byssoides was investigated using morphoanatomy and DNA sequences (psbA and cox2,3) obtained from populations at 15 localities on the Italian and Croatian coasts. Lithophyllum byssoides exhibited a high number of haplotypes (31 psbA haplotypes and 24 cox2,3 haplotypes) in the central Mediterranean. The psbA and cox2,3 phylogenies were congruent and showed seven lineages. For most of these clades, the distribution was limited to one or a few localities, but one of them (clade 7) was widespread across the central Mediterranean, spanning the main biogeographic boundaries recognized in this area. The central Mediterranean populations formed a lineage separate from Atlantic samples; psbA pair‐wise divergences suggested that recognition of Atlantic and Mediterranean L. byssoides as different species may be appropriate. The central Mediterranean haplotype patterns of L. byssoides were interpreted as resulting from past climatic events in the hydrogeological history of the Mediterranean Sea. The high haplotype diversity and the restricted spatial distribution of the seven lineages suggest that individual populations should be managed as independent units.     

Does colonization contribute to spatial patterns of common invertebrates in coralline algal turf?

Abstract The potential of colonization to contribute to the spatial patterns of six common invertebrates in coralline algal turf was investigated on a rocky shore near Sydney, Australia. The species, which included two amphipods (Elasmopus warra, Hyale spp.), a small bivalve (Lasaea australis), a fly larva (Limonia marina), and two microgastropods (Amphithalamus incidata and Eatoniella atropurpurea), had a range of dispersal modes (larval dispersal, crawling, swimming, rafting, and passive transport). Field sampling between May 1997 and November 1999 demonstrated that the amphipods were more abundant in low‐shore areas, the fly larvae and bivalves were more abundant in mid‐shore areas, and the abundances of gastropods did not vary with tidal height. Furthermore, abundances of all species varied among patches separated by tens of metres at one time or another. To test whether rates of colonization could contribute to established patterns of abundance, habitat mimics were deployed for 2‐week periods. The supply of new individuals matched long‐term patterns of abundance at different tidal heights for E. warra and L. marina. Colonization rates also differed among patches separated by tens of metres for three of the six species. Overall, there was little evidence to suggest that common species in coralline turf are limited by colonization on local scales, regardless of their major mode of dispersal. However, the potential for colonization to determine patterns of abundance varied from species to species.     

Responses of crustose corallines to epiphyte and canopy cover

Although a dense cover of epiphytes is generally considered to be harmful for some coralline algae (Corallinaceae, Rhodophyta), crustose corallines in the littoral zone seem to be preserved from bleaching when covered by canopy plants and epiphytes during summer. This study aimed to test the responses of coralline crusts to epiphytes and canopy algae and their interaction with grazing limpets. Growth rates and color changes were followed in two crust species in areas with or without canopy algae in the Isle of Man, British Isles. Limpets were excluded, to allow epiphytes to grow upon crusts. Responses were measured both on pieces of crusts upon acrylic plates and on crusts growing naturally on the shore. Fucus canopy and epiphytic Enteromorpha significantly influenced the crusts' growth, depending on season. Epiphytes reduced the light levels beneath by up to 78%, more than the canopy algae (62%). Crusts exposed outside the canopy bleached in summer, but gradually restored their color once they were covered by epiphytes. The fast-growing Phymatolithon lenormandii (Aresch.) Adey recovered its coloration more quickly than the slow-growing P. purpureum (P. et H. Crouan) Woelkerling et Irvine. However, neither crust species could restore its color when epiphytes were reduced by grazing limpets, Patella vulgata L. Bleaching did not kill the crusts, but seemed to interfere with crusts' growth. Restoration of pigmentation was quantified for the first time on bleached coralline crusts. Epiphyte and canopy algae were experimentally shown to be beneficial, probably by providing shade and also protecting crusts from desiccation.     

Morphology of the crustose coralline alga Pseudolithophyllum muricatum (Corallinales,Rhodophyta) responds to 30 years of ocean acidification in the Northeast Pacific

As the process of ocean acidification alters seawater carbon chemistry, physiological processes such as skeletal accretion are expected to become more difficult for calcifying organisms. The crustose coralline red algae (Corallinales, Rhodophyta) form an important guild of calcifying primary producers in the temperate Northeast Pacific. The morphology of important ecological traits, namely, skeletal density and thallus thickness near the growing edge, was evaluated in Pseudolithophyllum muricatum (Foslie) Steneck & R.T. Paine, the competitively dominant alga within this guild. P. muricatum shows a morphological response to increased ocean acidification in the temperate Northeast Pacific. Comparing historical (1981–1997) and modern (2012) samples from the field, crust thickness near the growing edge was approximately half as thick in modern samples compared with historical samples, while crust calcite density showed no significant change between the two sample groups. Morphological changes at the growing edge have important consequences for mediating competitive interactions within this guild of algae, and may affect the role of crustose coralline algal beds as hosts to infaunal communities and facilitators of recruitment in many invertebrate and macroalgal species.