Non-indigenous species and their realized niche in tidepools along the South-East Pacific coast.

Non-indigenous species (NIS) have the potential to colonize and become established in a wide range of coastal habitats. Species with broad environmental tolerances can quickly adapt to local conditions and expand their niches along environmental gradients, and even colonize habitats with extreme abiotic conditions. Here we report and document the distribution of eight marine NIS (four seaweed and four invertebrate species) found in tidepools along a 3000 km latitudinal gradient along the Pacific coast of Chile (18.4°S to 41.9°S). The seaweed NIS Codium fragile, Capreolia implexa, Schottera nicaeensis and Mastocarpus latissimus were mostly distributed towards high latitudes (i.e., more southerly locations), where temperatures in tidepools were low. The invertebrate NIS Anemonia alicemartinae, Ciona robusta, Bugula neritina and Bugulina flabellata were more common towards low latitudes, where high temperatures were registered in the tidepools. Across the intertidal gradient, seaweed NIS were mostly found in pools in the mid and low intertidal zone, while invertebrate NIS occurred mostly in pools from the mid and upper intertidal zones. The realized niche spaces of NIS (based on the Outlying Mean Index, OMI) in the study area were mainly influenced by environmental conditions of temperature and salinity (along the latitudinal and intertidal gradients), while other tidepool characteristics (depth, surface area, exposition, and complexity) only had minor effects. Five of the eight NIS exhibited a realized niche space coinciding with the average tidepool environmental conditions, while marginal niches were occupied by species with affinities for specific temperatures and salinities along the latitudinal and intertidal gradients. Our results indicate that physiological tolerances to environmental factors play a fundamental role in the distribution of seaweed and invertebrate NIS in tidepools along the Chilean coast. This study confirms that tidepools offer suitable conditions for some seaweed and invertebrate NIS, potentially facilitating their invasion into new natural habitats.

Diverse inorganic carbon uptake strategies in Antarctic seaweeds: Revealing species-specific responses and implications for Ocean Acidification.

Seaweeds are important components of coastal benthic ecosystems along the Western Antarctic Peninsula (WAP), providing refuge, food, and habitat for numerous associated species. Despite their crucial role, the WAP is among the regions most affected by global climate change, potentially impacting the ecology and physiology of seaweeds. Elevated atmospheric CO2 concentrations have led to increased dissolved inorganic carbon (Ci) with consequent declines in oceanic pH and alterations in seawater carbonate chemistry, known as Ocean Acidification (OA). Seaweeds possess diverse strategies for Ci uptake, including CO2 concentrating mechanisms (CCMs), which may distinctly respond to changes in Ci concentrations. Conversely, some seaweeds do not operate CCMs (non-CCM species) and rely solely on CO2. Nevertheless, our understanding of the status and functionality of Ci uptake strategies in Antarctic seaweeds remains limited. Here, we investigated the Ci uptake strategies of seaweeds along a depth gradient in the WAP. Carbon isotope signatures (δ13C) and pH drift assays were used as indicators of the presence or absence of CCMs. Our results reveal variability in CCM occurrence among algal phyla and depths ranging from 0 to 20 m. However, this response was species specific. Among red seaweeds, the majority relied solely on CO2 as an exogenous Ci source, with a high percentage of non-CCM species. Green seaweeds exhibited depth-dependent variations in CCM status, with the proportion of non-CCM species increasing at greater depths. Conversely, brown seaweeds exhibited a higher prevalence of CCM species, even in deep waters, indicating the use of CO2 and HCO3-. Our results are similar to those observed in temperate and tropical regions, indicating that the potential impacts of OA on Antarctic seaweeds will be species specific. Additionally, OA may potentially increase the abundance of non-CCM species relative to those with CCMs.

Past climate-driven range shifts structuring intraspecific biodiversity levels of the giant kelp (Macrocystis pyrifera) at global scales.

The paradigm of past climate-driven range shifts structuring the distribution of marine intraspecific biodiversity lacks replication in biological models exposed to comparable limiting conditions in independent regions. This may lead to confounding effects unlinked to climate drivers. We aim to fill in this gap by asking whether the global distribution of intraspecific biodiversity of giant kelp (Macrocystis pyrifera) is explained by past climate changes occurring across the two hemispheres. We compared the species' population genetic diversity and structure inferred with microsatellite markers, with range shifts and long-term refugial regions predicted with species distribution modelling (SDM) from the last glacial maximum (LGM) to the present. The broad antitropical distribution of Macrocystis pyrifera is composed by six significantly differentiated genetic groups, for which current genetic diversity levels match the expectations of past climate changes. Range shifts from the LGM to the present structured low latitude refugial regions where genetic relics with higher and unique diversity were found (particularly in the Channel Islands of California and in Peru), while post-glacial expansions following ~ 40% range contraction explained extensive regions with homogenous reduced diversity. The estimated effect of past climate-driven range shifts was comparable between hemispheres, largely demonstrating that the distribution of intraspecific marine biodiversity can be structured by comparable evolutionary forces across the global ocean. Additionally, the differentiation and endemicity of regional genetic groups, confers high conservation value to these localized intraspecific biodiversity hotspots of giant kelp forests.

Southern Hemisphere coasts are biologically connected by frequent, long-distance rafting events.

Globally, species distributions are shifting in response to environmental change,1 and those that cannot disperse risk extinction.2 Many taxa, including marine species, are showing poleward range shifts as the climate warms.3 In the Southern Hemisphere, however, circumpolar oceanic fronts can present barriers to dispersal.4 Although passive, southward movement of species across this barrier has been considered unlikely,5,6 the recent discovery of buoyant kelp rafts on beaches in Antarctica7,8 demonstrates that such journeys are possible. Rafting is a key process by which diverse taxa-including terrestrial, e.g., Lindo,9 Godinot,10 and Censky et al.,11 and marine, e.g., Carlton et al.12 and Gillespie et al.13 species-can cross oceans.14 Kelp rafts can carry passengers7,15-17 and thus can act as vectors for long-distance dispersal of coastal organisms. The small numbers of kelp rafts previously found in Antarctica7,8 do not, however, shed much light on the frequency of such dispersal events.18 We use a combination of high-resolution phylogenomic analyses (>220,000 SNPs) and oceanographic modeling to show that long-distance biological dispersal events in Southern Ocean are not rare. We document tens of kelp (Durvillaea antarctica) rafting events of thousands of kilometers each, over several decades (1950-2019), with many kelp rafts apparently still reproductively viable. Modeling of dispersal trajectories from genomically inferred source locations shows that distant landmasses are well connected, for example South Georgia and New Zealand, and the Kerguelen Islands and Tasmania. Our findings illustrate the power of genomic approaches to track, and modeling to show frequencies of, long-distance dispersal events.

The Biogeographic Importance of Buoyancy in Macroalgae: A Case Study of the Southern Bull-Kelp Genus Durvillaea (Phaeophyceae), Including Descriptions of Two New Species1.

Long-distance dispersal plays a key role in evolution, facilitating allopatric divergence, range expansions, and species movement in response to environmental change. Even species that seem poorly suited to dispersal can sometimes travel long distances, for example via hitchhiking with other, more intrinsically dispersive species. In marine macroalgae, buoyancy can enable adults-and diverse hitchhikers-to drift long distances, but the evolution and role of this trait are poorly understood. The southern bull-kelp genus Durvillaea includes several non-buoyant and buoyant species, including some that have only recently been recognized. In revising the genus, we not only provide updated identification tools and describe two new species (D. incurvata comb. nov. from Chile and D. fenestrata sp. nov. from the Antipodes Islands), but also carry out biogeographic analyses to determine the evolutionary history of buoyancy in the genus. Although the ancestral state was resolved as non-buoyant, the distribution of species suggests that this trait has been both gained and lost, possibly more than once. We conclude that although buoyancy is a trait that can be useful for dispersal (creating evolutionary pressure for its gain), there is also evolutionary pressure for its loss as it restricts species to narrow environmental ranges (i.e., shallow depths).

Long-term persistence of the floating bull kelp Durvillaea antarctica from the South-East Pacific: Potential contribution to local and transoceanic connectivity.

Current knowledge about the performance of floating seaweeds as dispersal vectors comes mostly from mid latitudes (30°-40°), but phylogeographic studies suggest that long-distance dispersal (LDD) is more common at high latitudes (50°-60°). To test this hypothesis, long-term field experiments with floating southern bull kelp Durvillaea antarctica were conducted along a latitudinal gradient (30°S, 37°S and 54°S) in austral winter and summer. Floating time exceeded 200d in winter at the high latitudes but in summer it dropped to 90d, being still higher than at low latitudes (<45d). Biomass variations were due to loss of buoyant fronds. Reproductive activity diminished during long floating times. Physiological changes included mainly a reduction in photosynthetic (Fv/Fm and pigments) rather than in defence variables (phlorotannins and antioxidant activity). The observed long floating persistence and long-term acclimation responses at 54°S support the hypothesis of LDD by kelp rafts at high latitudes.

Widely distributed red algae often represent hidden introductions, complexes of cryptic species or species with strong phylogeographic structure.

Despite studies suggesting that most seaweeds are poor dispersers, many red algal species are reported to have circumglobal distributions. Such distributions have mostly been based on morphological identifications, but molecular data have revealed a range of issues with morphologically defined species boundaries. Consequently, the real distribution of such reportedly circumglobal species must be questioned. In this study, we analyzed molecular data sets (rbcL gene) of nine species in the Rhodomelaceae for which samples were available from widely spaced geographical locations. Three overall patterns were identified: (i) species showing strong phylogeographic structure (i.e., phylogenetic similarity correlates with geographical provenance), often to the point that populations from different locations could be considered as different species (Lophosiphonia obscura, Ophidocladus simpliciusculus, Polysiphonia villum, and Xiphosiphonia pinnulata); (ii) species with a broad distribution that is explained, in part, by putative human-mediated transport (Symphyocladia dendroidea and Polysiphonia devoniensis); and (iii) non-monophyletic complexes of cryptic species, most with a more restricted distribution than previously thought (Herposiphonia tenella, Symphyocladia dendroidea, and the Xiphosiphonia pennata complex that includes the species Xiphosiphonia pinnulata and Symphyocladia spinifera). This study shows that widely distributed species are the exception in marine red algae, unless they have been spread by humans.

The variable routes of rafting: stranding dynamics of floating bull kelp Durvillaea antarctica (Fucales, Phaeophyceae) on beaches in the SE Pacific.

Dispersal on floating seaweeds depends on availability, viability, and trajectories of the rafts. In the southern hemisphere, the bull kelp Durvillaea antarctica is one of the most common floating seaweeds, but phylogeographic studies had shown low connectivity between populations from continental Chile, which could be due to limitations in local supply and dispersal of floating kelps. To test this hypothesis, the spatiotemporal dynamics of kelp strandings were examined in four biogeographic districts along the Chilean coast (28°-42°S). We determined the biomass and demography of stranded individuals on 33 beaches for three subsequent years (2013, 2014, 2015) to examine whether rafting is restricted to certain districts and seasons (winter or summer). Stranded kelps were found on all beaches. Most kelps had only one stipe (one individual), although we also frequently found coalesced holdfasts with mature males and females, which would facilitate successful rafting dispersal, gamete release, and reproduction upon arrival. High biomasses of stranded kelps occurred in the northern-central (30°S-33°S) and southernmost districts (37°S-42°S), and lower biomasses in the northernmost (28°S-30°S) and southern-central districts (33°S-37°S). The highest percentages and sizes of epibionts (Lepas spp.), indicative of prolonged floating periods, were found on stranded kelps in the northernmost and southernmost districts. Based on these results, we conclude that rafting dispersal can vary regionally, being more common in the northernmost and southernmost districts, depending on intrinsic (seaweed biology) and extrinsic factors (shore morphology and oceanography) that affect local supply of kelps and regional hydrodynamics.

Chloroplast genomes as a tool to resolve red algal phylogenies: a case study in the Nemaliales.

BACKGROUND: Obtaining strongly supported phylogenies that permit confident taxonomic and evolutionary interpretations has been a challenge in algal biology. High-throughput sequencing has improved the capacity to generate data and yields more informative datasets. We sequenced and analysed the chloroplast genomes of 22 species of the order Nemaliales as a case study in the use of phylogenomics as an approach to achieve well-supported phylogenies of red algae. RESULTS: Chloroplast genomes of the order Nemaliales are highly conserved, gene-dense and completely syntenic with very few cases of gene loss. Our ML estimation based on 195 genes recovered a completely supported phylogeny, permitting re-classification of the order at various taxonomic levels. Six families are recognised and the placement of several previously contradictory clades is resolved. Two new sub-orders are described, Galaxaurineae and Nemaliineae, based on the early-branching nature and monophyly of the groups, and presence or absence of a pericarp. Analyses of subsets of the data showed that >90 % bootstrap support can be achieved with datasets as small as 2500 nt and that fast and medium evolving genes perform much better when it comes to resolving phylogenetic relationships. CONCLUSIONS: In this study we show that phylogenomics is an efficient and effective approach to investigate phylogenetic relationships. The six currently circumscribed Nemaliales families are clustered into two evolutionary lineages with strong statistical support based on chloroplast phylogenomic analyses. The conserved nature of red algal chloroplast genomes is a convenient and accessible source of data to resolve their ancient relationships.

The bladed Bangiales (Rhodophyta) of the South Eastern Pacific: Molecular species delimitation reveals extensive diversity.

A molecular taxonomic study of the bladed Bangiales of the South Eastern Pacific (coast of Chile) was undertaken based on sequence data of the mitochondrial COI and chloroplast rbcL for 193 specimens collected from Arica (18°S) in the north to South Patagonia (53°S) in the south. The results revealed for the first time that four genera, Porphyra, Pyropia, Fuscifolium and Wildemania were present in the region. Species delimitation was determined based on a combination of a General Mixed Yule Coalescence model (GMYC) and Automatic Barcode Gap Discovery (ABGD) coupled with detection of monophyly in tree reconstruction. The overall incongruence between the species delimitation methods within each gene was 29%. The GMYC method led to over-splitting groups, whereas the ABGD method had a tendency to lump groups. Taking a conservative approach to the number of putative species, at least 18 were recognized and, with the exception of the recently described Pyropia orbicularis, all were new to the Chilean flora. Porphyra and Pyropia were the most diverse genera with eight 'species' each, whereas only a 'single' species each was found for Fuscifolium and Wildemania. There was also evidence of recently diverging groups: Wildemania sp. was distinct but very closely related to W. amplissima from the Northern Hemisphere and raises questions in relation to such disjunct distributions. Pyropia orbicularis was very closely related to two other species, making species delimitation very difficult but provides evidence of an incipient speciation. The difference between the 'species' discovered and those previously reported for the region is discussed in relation to the difficulty of distinguishing species based on morphological identification.

Variation in patterns of metal accumulation in thallus parts of Lessonia trabeculata (Laminariales; Phaeophyceae): implications for biomonitoring.

Seaweeds are well known to concentrate metals from seawater and have been employed as monitors of metal pollution in coastal waters and estuaries. However, research showing that various intrinsic and extrinsic factors can influence metal accumulation, raises doubts about the basis for using seaweeds in biomonitoring programmes. The thallus of brown seaweeds of the order Laminariales (kelps) is morphologically complex but there is limited information about the variation in metal accumulation between the different parts, which might result in erroneous conclusions being drawn if not accounted for in the biomonitoring protocol. To assess patterns of individual metals in the differentiated parts of the thallus (blade, stipe, holdfast), concentrations of a wide range of essential and non-essential metals (Fe, Cr, Cu, Zn, Mn, Pb, Cd, Ni and Al) were measured in the kelp Lessonia trabeculata. Seaweeds were collected from three sampling stations located at 5, 30 and 60 m from an illegal sewage outfall close to Ventanas, Chile and from a pristine location at Faro Curaumilla. For the majority of metals the highest concentrations in bottom sediment and seaweed samples were found at the site closest to the outfall, with concentrations decreasing with distance from the outfall and at control stations; the exception was Cd, concentrations of which were higher at control stations. The patterns of metal concentrations in different thallus parts were metal specific and independent of sampling station. These results and the available literature suggest that biomonitoring of metals using seaweeds must take account of differences in the accumulation of metals in thallus parts of complex seaweeds.