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.

Short-term stress responses and recovery of giant kelp (Macrocystis pyrifera, Laminariales, Phaeophyceae) juvenile sporophytes to a simulated marine heatwave and nitrate scarcity1.

The frequency of marine heatwaves (MHWs) is increasing due to climate change. Although seaweeds are resilient to environmental changes, an increasing body of evidence shows that rising sea surface temperatures have deleterious effects on temperate kelp species. However, information on the vulnerability of juvenile kelp to these stressors and their population stability is limited. This study summarizes findings on the ability of juvenile sporophytes of Macrocystis pyrifera to survive and recover from simulated MHW conditions (22°C, 5 d) in combination with nitrate limitation (<1 µM) by evaluating photosynthetic capacity, nitrate uptake, tissue composition, bio-optical properties, and oxidative stress of single-blade juvenile sporophytes (<20 cm). Temperature, nitrate availability, and their interaction had significant effects on the physiological status of juvenile sporophytes after the exposure and recovery periods. Overall, as expected, the photosynthetic capacity of juvenile sporophytes decreased with increased temperature and lower nitrate availability. Short-term exposure to simulated MHWs resulted in oxidative damage and reduced growth. The termination of the experimental warming allowed partial recovery to control values, indicating high physiological resilience. However, the interaction of both high temperature and nitrate scarcity induced irreversible damage to their photosynthetic capacity, with an increase in compensation irradiance, highlighting potential limitations in the carbon balance of juvenile sporophytes.

Complex interactions between meteorological parameters and the thermal regime of two tropical, high altitude crater lakes (Nevado de Toluca, Mexico).

Using long-term time series of meteorological and water-column parameters, the dynamics of two lakes separated by about 500 m from each other by a central lava dome, located at 4207 m above sea level in the volcano crater of Nevado de Toluca, Mexico were explored. Because of the strong wind-forcing previously measured on the volcano slope and the proximity of the lakes, wind-mixing was expected, with similar dynamics in both lakes. However, the meteorological parameters in the crater were significantly different than on the slope of the volcano, due to the dome and the high walls of the crater, which weakened wind speeds, modified wind direction, and reduced exposure to solar radiation by almost 20% in the crater compared to on the volcano slope. The rate and depth of thermal penetration into each lake differed by an order of magnitude, related with differential insolation due to crater wall shading, along with differences in transparency, most likely due to differential algal growth and suspended matter. At times, rapid surface cooling occurred during periods of reduced insolation and calm winds, leading to strong vertical convection and the formation of a characteristic step profile in the water column rather than the predicted wind mixing. These results are important for interdisciplinary studies of these and other alpine lakes and, in particular for biophysical coupling in these unique hydrological systems.

Mates Matter: Gametophyte Kinship Recognition and Inbreeding in the Giant Kelp, Macrocystis pyrifera (Laminariales, Phaeophyceae).

Inbreeding, the mating between genetically related individuals, often results in reduced survival and fecundity of offspring, relative to outcrossing. Yet, high inbreeding rates are commonly observed in seaweeds, suggesting compensatory reproductive traits may affect the costs and benefits of the mating system. We experimentally manipulated inbreeding levels in controlled crossing experiments, using gametophytes from 19 populations of Macrocystis pyrifera along its Eastern Pacific coastal distribution (EPC). The objective was to investigate the effects of male-female kinship on female fecundity and fertility, to estimate inbreeding depression in the F1 progeny, and to assess the variability of these effects among different regions and habitats of the EPC. Results revealed that the presence and kinship of males had a significant effect on fecundity and fertility of female gametophytes. Females left alone or in the presence of sibling males express the highest gametophyte size, number, and size of oogonia, suggesting they were able to sense the presence and the identity of their mates before gamete contact. The opposite trend was observed for the production of embryos per female gametes, indicating higher costs of selfing and parthenogenesis than outcrossing on fertility. However, the increased fecundity compensated for the reduced fertility, leading to a stable overall reproductive output. Inbreeding also affected morphological traits of juvenile sporophytes, but not their heatwave tolerance. The male-female kinship effect was stronger in high-latitude populations, suggesting that females from low-latitude marginal populations might have evolved to mate with any male gamete to guarantee reproductive success.

Effects of Heat Waves and Light Deprivation on Giant Kelp Juveniles (Macrocystis pyrifera, Laminariales, Phaeophyceae).

Due to climate change, the incidence of marine heat waves (MHWs) has increased, yet their effects on seaweeds are still not well understood. Adult sporophytes of Macrocystis pyrifera, the species forming the iconic giant kelp forests, can be negatively affected by thermal stress and associated environmental factors (e.g., nutrient depletion, light deprivation); however, little is known about the tolerance/vulnerability of juvenile sporophytes. Simultaneously to MHWs, juveniles can be subjected to light limitation for extended periods of time (days-weeks) due to factors causing turbidity, or even because of shading by understory canopy-forming seaweeds. This study evaluated the effects of a simulated MHW (24°C, 7 d) in combination (or not) with light deprivation, on the photosynthetic capacities, nutrient uptake, and tissue composition, as well as oxidative stress descriptors of M. pyrifera juvenile sporophytes (single blade stage, up to 20 cm length). Maximum quantum yield (Fv /Fm ) decreased in juveniles under light at 24°C, likely reflecting some damage on the photosynthetic apparatus or dynamic photoinhibition; however, no other sign of physiological alteration was found in this treatment (i.e., pigments, nutrient reserves and uptake, oxidative stress). Photosynthetic capacities were maintained or even enhanced in plants under light deprivation, likely supported by photoacclimation (pigments increment); by contrast, nitrate uptake and internal storage of carbohydrates were strongly reduced, regardless of temperature. This study indicated that light limitation can be more detrimental to juvenile survival, and therefore recruitment success of M. pyrifera forests, than episodic thermal stress from MHWs.

The influence of species, density, and diversity of macroalgal aggregations on microphytobenthic settlement.

Intertidal macroalgae can modulate their biophysical environment by ameliorating physical conditions and creating habitats. Exploring how seaweed aggregations made up of different species at different densities modify the local environment may help explain how associated organisms respond to the attenuation of extreme physical conditions. Using Silvetia compressa, Chondracanthus canaliculatus, and Pyropia perforata, we constructed monocultures representing the leathery, corticated and foliose functional forms as well as a mixed tri-culture assemblage including the former three, at four densities. Treatment quadrats were installed in the intertidal where we measured irradiance, temperature, particle retention, and water motion underneath the canopies. Additionally, we examined the abundance and richness of the understory microphytobenthos with settlement slides. We found that the density and species composition of the assemblages modulated the amelioration of extreme physical conditions, with macroalgal aggregations of greater structural complexity due to their form and density showing greater physical factor attenuation. However, increasing the number of species within a patch did not directly result in increased complexity and therefore, did not necessarily cause greater amelioration of the environment. Microphytobenthic composition was also affected by species composition and density, with higher abundances under S. compressa and C. canaliculatus canopies at high and mid densities. These results support the idea that the environmental modifications driven by these macroalgae have a significant effect on the dynamics of the intertidal environment by promoting distinct temporal and spatial patchiness in the microphytobenthos, with potentially significant effects on the overall productivity of these ecosystems.

Cryptic diversity, geographical endemism and allopolyploidy in NE Pacific seaweeds.

BACKGROUND: Molecular markers are revealing a much more diverse and evolutionarily complex picture of marine biodiversity than previously anticipated. Cryptic and/or endemic marine species are continually being found throughout the world oceans, predominantly in inconspicuous tropical groups but also in larger, canopy-forming taxa from well studied temperate regions. Interspecific hybridization has also been found to be prevalent in many marine groups, for instance within dense congeneric assemblages, with introgressive gene-flow being the most common outcome. Here, using a congeneric phylogeographic approach, we investigated two monotypic and geographically complementary sister genera of north-east Pacific intertidal seaweeds (Hesperophycus and Pelvetiopsis), for which preliminary molecular tests revealed unexpected conflicts consistent with unrecognized cryptic diversity and hybridization. RESULTS: The three recovered mtDNA clades did not match a priori species delimitations. H. californicus was congruent, whereas widespread P. limitata encompassed two additional narrow-endemic species from California - P. arborescens (here genetically confirmed) and P. hybrida sp. nov. The congruence between the genotypic clusters and the mtDNA clades was absolute. Fixed heterozygosity was apparent in a high proportion of loci in P. limitata and P. hybrida, with genetic analyses showing that the latter was composed of both H. californicus and P. arborescens genomes. All four inferred species could be distinguished based on their general morphology. CONCLUSIONS: This study confirmed additional diversity and reticulation within NE Pacific Hesperophycus/Pelvetiopsis, including the validity of the much endangered, modern climatic relict P. arborescens, and the identification of a new, stable allopolyploid species (P. hybrida) with clearly discernable ancestry (♀ H. californicus x ♂ P. arborescens), morphology, and geographical distribution. Allopolyploid speciation is otherwise completely unknown in brown seaweeds, and its unique occurrence within this genus (P. limitata possibly representing a second example) remains enigmatic. The taxonomic separation of Hesperophycus and Pelvetiopsis is not supported and the genera should be synonymized; we retain only the latter. The transitional coastline between Point Conception and Monterey Bay represented a diversity hotspot for the genus and the likely sites of extraordinary evolutionary events of allopolyploid speciation at sympatric range contact zones. This study pinpoints how much diversity (and evolutionary processes) potentially remains undiscovered even on a conspicuous seaweed genus from the well-studied Californian intertidal shores let alone in other, less studied marine groups and regions/depths.

Seascape drivers of Macrocystis pyrifera population genetic structure in the northeast Pacific.

At small spatial and temporal scales, genetic differentiation is largely controlled by constraints on gene flow, while genetic diversity across a species' distribution is shaped on longer temporal and spatial scales. We assess the hypothesis that oceanographic transport and other seascape features explain different scales of genetic structure of giant kelp, Macrocystis pyrifera. We followed a hierarchical approach to perform a microsatellite-based analysis of genetic differentiation in Macrocystis across its distribution in the northeast Pacific. We used seascape genetic approaches to identify large-scale biogeographic population clusters and investigate whether they could be explained by oceanographic transport and other environmental drivers. We then modelled population genetic differentiation within clusters as a function of oceanographic transport and other environmental factors. Five geographic clusters were identified: Alaska/Canada, central California, continental Santa Barbara, California Channel Islands and mainland southern California/Baja California peninsula. The strongest break occurred between central and southern California, with mainland Santa Barbara sites forming a transition zone between the two. Breaks between clusters corresponded approximately to previously identified biogeographic breaks, but were not solely explained by oceanographic transport. An isolation-by-environment (IBE) pattern was observed where the northern and southern Channel Islands clustered together, but not with closer mainland sites, despite the greater distance between them. The strongest environmental association with this IBE pattern was observed with light extinction coefficient, which extends suitable habitat to deeper areas. Within clusters, we found support for previous results showing that oceanographic connectivity plays an important role in the population genetic structure of Macrocystis in the Northern hemisphere.

Food webs and fishing affect parasitism of the sea urchin Eucidaris galapagensis in the Galápagos.

In the Galápagos Islands, two eulimid snails parasitize the common pencil sea urchin, Eucidaris galapagensis. Past work in the Galápagos suggests that fishing reduces lobster and fish densities and, due to this relaxation of predation pressure, indirectly increases urchin densities, creating the potential for complex indirect interactions between fishing and parasitic snails. To measure indirect effects of fishing on these parasitic snails, we investigated the spatial relationships among urchins, parasitic snails, commensal crabs, and large urchin predators (hogfish and lobsters). Parasitic snails had higher densities at sites where urchins were abundant, probably due to increased resource availability. Commensal crabs that shelter under urchin spines, particularly the endemic Mithrax nodosus, preyed on the parasitic snails in aquaria, and snails were less abundant at field sites where these crabs were common. In aquaria, hogfish and lobsters readily ate crabs, but crabs were protected from predation under urchin spines, leading to a facultative mutualism between commensal crabs and urchins. In the field, fishing appeared to indirectly increase the abundance of urchins and their commensal crabs by reducing predation pressure from fish and lobsters. Fished sites had fewer snails per urchin, probably due to increased predation from commensal crabs. However, because fished sites also tended to have more urchins, there was no significant net effect of fishing on the number of snails per square meter. These results suggest that fishing can have complex indirect effects on parasites by altering food webs.