Understanding the sexual recruitment of one of the oldest and largest organisms on Earth, the seagrass Posidonia oceanica

The seagrass Posidonia oceanica is considered one of the oldest and largest living organisms on Earth. Notwithstanding, given the difficulty of monitoring its fruits and seeds in the field, the development of P. oceanica during its sexual recruitment is not completely understood. We studied the stages of development of P. oceanica seeds from their dispersion in the fruit interior to their settlement in sediment through histological, ultrastructural and mesocosm experiments. P. oceanica sexual recruitment can be divided into three main stages that focus on maximising photosynthesis and anchoring the seedlings to the sediment. In the first stage (fruit dispersion), seeds perform photosynthesis while being transported inside the fruit along the sea surface. In the second stage (seed adhesion), seeds develop adhesive microscopic hairs that cover the primary and secondary roots and favour seed adhesion to the substrate. In the last stage (seedling anchorage), roots attach the seedlings to the substrate by orienting them towards the direction of light to maximise photosynthesis. The adaptations observed in P. oceanica are similar to those in other seagrasses with non-dormant seeds and fruits with membranous pericarps, such as Thalassia sp. and Enhalus sp. These common strategies suggest a convergent evolution in such seagrasses in terms of sexual recruitment. Understanding the sexual recruitment of habitat-forming species such as seagrasses is necessary to adequately manage the ecosystems that they inhabit

A review of coastal anthropogenic impacts on mytilid mussel beds: Effects on mussels and their associated assemblages

Mussel beds are an important habitat in many coastal systems, harboring a high diversity of biota. They are threatened by anthropogenic impacts that affect mussels and their associated assemblages. Pollution, harvesting, trampling, dredging and trawling are major threats faced by these communities. Most of the studies on the effects of such impacts on the mussel beds overlook the associated fauna. Since mussels are very resilient, especially to pollution, the associated fauna can provide a better footprint of the impacts’ effects. In this review, we looked into the main remarks regarding the effects of anthropogenic impacts in mussel bed communities. Organic pollution was the best studied impact and the Atlantic region was the best studied zone. Low values of abundance, biomass, diversity, evenness and species richness were reported for all categories of impacts, with some studies describing declines in at least three of these descriptors. Among the associated fauna, some tolerant species benefited from the impacts, particularly organic enrichment, and became more abundant, but sensitive species suffered considerable declines in density, mainly in dredging and trawling impacts. Therefore, fauna associated with mussel beds is a suitable indicator of anthropogenic disturbance

Recent changes on the abundance and distribution of non-indigenous macroalgae along the southwest coast of the Bay of Biscay

Twenty-three rocky shores along approximately 225 km on the southwest coast of the Bay of Biscay were sampled during the springs of 2014 and 2021, to explore changes in the distribution and abundance of four non-indigenous species (NIS) macroalgae (i.e., Asparagopsis armata, Grateloupia turuturu, Sargassum muticum, and Undaria pinnatifida) by using a semi-quantitative scale. Results showed relevant changes in the distribution and abundance of NIS. The kelp U. pinnatifida was recorded in 2021 for the first time on two shores. The distribution of G. turuturu showed an extension in its range of distribution of 200 km to the east. The other two target species S. muticum and A. armata were widely distributed along the whole 225 km of the studied area in 2014 and 2021, with higher abundance in 2021. Therefore, we strongly advise the necessity of future monitoring programs for these four NIS species. These monitoring programs will explore the progress of invasion and resilience of native species.This study was supported by the project ATLANTIDA (ref. NORTE-01-0145-FEDER-000040), supported by the Norte Portugal Regional Operational Program (NORTE 2020), under the PORTUGAL 2020 Partnership Agreement and through the European Regional Development Fund (ERDF). This study was supported by the FCT-Foundation for Science and Technology through national funds within the scope of Contrato-Programa” UIDB/04050/2020 funded by national funds through the FCT I.P and, UIDB/04423/2020, UIDP/04423/2020. L. Guerrero-Meseguer was financed thanks to a grant from the Department of European Funds, University, and Culture of the Government of the Balearic Islands. P. Veiga was hired through the Regulamento do Emprego Científico e Tecnológico-RJEC from the Portuguese Foundation for Science and Technology (FCT) program (CEECIND/03893/2018)

Does Ocean Acidification Benefit Seagrasses in a Mesohaline Environment? A Mesocosm Experiment in the Northern Gulf of Mexico

Ocean acidification is thought to benefit seagrasses because of increased carbon dioxide (CO2) availability for photosynthesis. However, in order to truly assess ecological responses, effects of ocean acidification need to be investigated in a variety of coastal environments. We tested the hypothesis that ocean acidification would benefit seagrasses in the northern Gulf of Mexico, where the seagrasses Halodule wrightii and Ruppia maritima coexist in a fluctuating environment. To evaluate if benefits of ocean acidification could alter seagrass bed composition, cores of H. wrightii and R. maritima were placed alone or in combination into aquaria and maintained in an outdoor mesocosm. Half of the aquaria were exposed to either ambient (mean pH of 8.1 ± 0.04 SD on total scale) or high CO2 (mean pH 7.7 ± 0.05 SD on total scale) conditions. After 54 days of experimental exposure, the δ13C values were significantly lower in seagrass tissue in the high CO2 condition. This integration of a different carbon source (either: preferential use of CO2, gas from cylinder, or both) indicates that plants were not solely relying on stored energy reserves for growth. Yet, after 41 to 54 days, seagrass morphology, biomass, photo-physiology, metabolism, and carbon and nitrogen content in the high CO2 condition did not differ from those at ambient. There was also no indication of differences in traits between the homospecific or heterospecific beds. Findings support two plausible conclusions: (1) these seagrasses rely heavily on bicarbonate use and growth will not be stimulated by near future acidification conditions or (2) the mesohaline environment limited the beneficial impacts of increased CO2 availability

Influence of substrate and burial on the development of Posidonia oceanica: implications for restoration

Posidonia oceanica is one of the few seagrasses that can colonize hard and soft substrates. To test whether substrate could affect root development of the seedlings, with a legacy effect upon transplantation to sand, we germinated seeds on hard (glass slide) versus soft (sand) substrates in microcosms. We found that sand favored root system development, with a compensatory slowing of leaf development, while glass had the opposite effect. After 4 months, we transplanted all seedlings to sand and tested for a legacy effect of initial substrate type. Leaves of seedlings germinated on sand and glass slides reached approximately the same length, but roots from seedlings germinated on glass did not develop fully. Seed burial (0–1.5 cm) did not affect seedling development. These results suggest that the culture of P. oceanica on sand prior to transplantation could enhance seedlings survival in restoration programs.This work was carried out within the research project POSIPLANT (project code: CTM2011-27377), funded by the Ministerio de Ciencia e Innovación from Spain

The effects of natural and anthropogenic drivers on seagrasses

Seagrasses are considered one of the most important organisms in the world, since they form extensive meadows which provide high biodiversity and a wide variety of ecological services. Despite its importance, seagrass meadows are globally declining, especially due to anthropogenic pressures and climate change. The sexual reproduction of the seagrasses is responsible of the genetic variability of the species and therefore, it is the principal way to develop characters to resist future environmental perturbations. However, due to the difficulties of monitoring the dispersion of the fruits and seeds of seagrasses in the field, the sexual reproduction is poorly understood. This limits the effective conservation of the seagrass meadows. In addition, seagrasses have numerous bottlenecks during the sexual recruitment, especially during the development of the seedlings. These bottlenecks affect its rates of colonization and also lead in the uprooting of the transplants in environmental restoration projects. To increase our understanding in these areas, the general aim of this thesis is to shed light on sexual recruitment strategies, and also on the effects of natural and anthropogenic drivers on seagrasses. Different approaches, species and development stages of seagrasses are used to achieve this aim, resulting in five different chapters whose methodology, results and conclusions are exposed below. In the first chapter of the thesis is evaluated the sexual recruitment of the seagrass Posidonia oceanica. To do so, the morphology of fruits and seeds collected in the beaches of the Murcia Region are studied. Subsequently, mesocosm experiments to test the influence of the light and substrata type in the seed development are tested. The results show that the seeds of this seagrass go through three essential stages from its dispersion in the interior of fruits over the sea surface until its settlement in the sediment. In the Chapter 2 are tested the effects of the substrate hardness and seed burial in P. oceanica seedlings. To do so, seeds are cultured in aquaria by using hard and unconsolidated substrata and thus, root and leaf development are compared between treatments. Subsequently, these seedlings are transplanted to sand with three levels of seed burial. The results show that the seedlings which are previously cultured in sand have a greater development than the cultured in hard substrata. In addition, seed burial do not affect the development of P. oceanica. In the Chapter 3 are evaluated the responses of P. oceanica seedlings to the increase of temperatures due to heat waves. The results show that the current and forecasted temperatures expected for the end of the century in the Mediterranean will compromise the colonization capacity of this seagrass. In the Chapter 4 also is evaluated the effects of heat waves in P. oceanica seedlings but in combination of other environmental stressors: seed burial and grazing. The results show that the combination of severe environmental stressors limits the development of P. oceanica seedlings in a more intensive level than when the factors separately occur. In addition, the effects of the heat waves override the effects of both environmental stressors. In the last chapter is studied the effects of ocean acidification in homospecific and heterospecific beds of H. wrightii and R. maritima. The results show that, contrary to expectations, the increase in CO2 availability will not benefit the seagrasses of the estuarine system of the Gulf of Mexico. The information compiled in this thesis about the sexual recruitment and influence of natural and anthropogenic drivers on seagrasses is essential to improve the management and conservation of these important habitat-forming species. Las fanerógamas marinas destacan por ser uno de los ecosistemas más importantes del planeta, ya que forman extensas praderas submarinas con una gran biodiversidad y numerosas funciones ecosistémicas. A pesar de su importancia, las fanerógamas marinas están desapareciendo globalmente, principalmente debido a la presión de las actividades humanas y del cambio climático. La variabilidad genética que proporciona la reproducción sexual permite a estas especies desarrollar caracteres resistentes a futuras perturbaciones ambientales. Sin embargo, el estudio y monitoreo de frutos y semillas de fanerógamas marinas es dificultoso, lo que provoca un escaso conocimiento en esta área. Esto limita la conservación efectiva de las fanerógamas marinas. Además, estas especies cuentan con numerosos cuellos de botella durante el reclutamiento sexual, especialmente durante el crecimiento de las plántulas, lo que conlleva bajas tasas de colonización y también, problemas de anclaje de los trasplantes en programas de restauración ambiental. Con el fin de aumentar nuestro conocimiento en estas áreas, el objetivo principal de esta tesis es incrementar el conocimiento en el reclutamiento sexual y en la influencia de factores naturales y antropogénicos en las fanerógamas marinas. Para ello, se realizaron experimentos con distinto enfoque y en distintas especies y etapas de crecimiento de fanerógamas marinas, resultando en cinco capítulos cuya metodología, resultados y conclusiones se explican a continuación. En el primer capítulo se estudia el reclutamiento sexual de la especie Posidonia oceanica. Para ello, se analiza previamente la morfología de frutos y semillas recolectados en las costas de la Región de Murcia. Posteriormente, se realizan experimentos para comprobar la influencia de la luz y el tipo de sustrato en el desarrollo de la semilla. Los resultados demuestran que las semillas de P. oceanica pasan a través de tres etapas desde su dispersión en el interior de los frutos hasta su asentamiento sobre el fondo marino. En el Capítulo 2, se evalúa los efectos de la consolidación del sustrato y del enterramiento de la semilla en plántulas de P. oceanica. Para ello, las semillas son cultivadas en acuarios con un sustrato duro y otro sustrato no consolidado. Posteriormente, esas mismas plántulas se trasplantan a arena bajo tres niveles diferentes de enterramiento de la semilla. Los resultados muestran que la arena beneficia el crecimiento de las plántulas, sobre todo a nivel del sistema radicular. El enterramiento de la semilla no mostró influencia en el desarrollo. En el Capítulo 3 se estudian las respuestas de las plántulas de P. oceanica al incremento de temperaturas debido a las olas de calor. Los resultados indican que las temperaturas actuales y pronosticadas para finales de este siglo en el Mediterráneo afectará la capacidad de colonización de esta especie. En el Capítulo 4 también se evalúa los efectos de las olas de calor en las plántulas de P. oceanica pero en combinación de otros factores ambientales: enterramiento de semilla y sobrepastoreo. Los resultados muestran que la combinación de varios factores ambientales limitan el desarrollo de las plántulas más intensamente que cuando ambos factores actúan por separado. Además las olas de calor tienen un efecto más negativo en las plántulas que los otros factores ambientales. En el último capítulo, se estudian los efectos de la acidificación oceánica en praderas de H. wrightii y R. maritima. Los resultados indican que, al contrario de lo esperado, el aumento de CO2 en los estuarios no beneficia a las fanerógamas marinas a corto plazo. La información recopilada en esta tesis acerca de la reproducción sexual y efectos de los factores naturales y antropogénicos en fanerógamas marinas es fundamental para mejorar el manejo y la conservación de estos importantes ecosistemas en el futuro

Heat wave intensity can vary the cumulative effects of multiple environmental stressors on Posidonia oceanica seedlings

Climate change is introducing new stressors into already stressed ecosystems. Among these, extreme events such as heat waves play a crucial role in determining the structure of ecosystems. We tested single and combined effects of overgrazing, burial and heat waves on the seedlings of the habitat-forming species Posidonia oceanica. At current heat wave temperatures, overgrazing in isolation had more deleterious effects than seed burial, and effects were synergistic and additive when both factors co-occurred. The combined effect of overgrazing and seed burial with current heat waves could hamper P. oceanica seedling development, with similar or even higher levels than the sole effect of heat waves in the near future (29 °C). The effects of overgrazing and seed burial are expected to be overridden if heat waves temperatures exceed 29 °C. These results suggest that co-occurring environmental stressors, in combination with current heat waves, could compromise the sexual recruitment of this seagrass.This work was carried out as part of Research Project NEREIDAS (Project Code: 2012-ES-92177- S), funded by the European Commission. C.S. was funded by the University of Alicante (Ref. UATALENTO 17-11)

Flowering effort and reproductive phenology of intertidal colonizing Zostera marina

The seagrass Zostera marina can inhabit the intertidal where the variable environmental conditions mean that the seagrass meadows are frequently in a continuous state of colonization, influencing, among others, their phenology and flowering effort. This could be especially notable in the southern limits of the species' distribution, where light exposure and temperature reach extreme values during the warmer seasons. In this study, we evaluate the flowering effort, phenology, photophysiology and vegetative development of recent colonizing Z. marina patches inhabiting the intertidal of a lagoon located near its southern limit of distribution, in the Ria de Aveiro (Portugal). To evaluate the effects of low tide exposure, tidepool and emerged seagrass patches were selected. Results showed short-lived differences in the phenology of the flowering of the patches and in their vegetative development, but in general, the photosynthetic activity, timing of flowering, densities of spathes and flowering shoots were similar in emerged and tidepool patches throughout the entire reproductive period (from June to August). The spathes per flowering shoot and the spathe and flowering shoot densities per unit of area of the colonizing patches were comparable to that obtained in other perennial intertidal meadows of this species and its timing was adjusted to that which occurred in areas of similar latitudes, ending when the temperature exceeded 25 °C. These results imply that intertidal colonizing Z. marina patches can flowering similarly to perennial meadows, regardless of whether or not they are submerged in pools at low tide, which implies a great adaptability of the species to intertidal areas. However, to fully understand the reproductive capacity of Z. marina in the Ria de Aveiro, future studies should determine the capacity of these flowers to form mature seeds, as well as their ability to germinate naturally in the area.This research was developed under Project No. 029818, co-financed by COMPETE 2020, Portugal 2020 and the European Union through the ERDF, and by FCT through national funds and was partially funded by the FCT Strategic Funding UID/Multi/04423/2019. Laura Guerrero-Meseguer was funded by a grant from the Department of European Funds, University and Culture of the Government of the Balearic Islands

Spatio-Temporal Variability of Wrack Along the Northern Portuguese Sandy Beaches

Wrack accumulations are a source of nutrients on sandy beaches and host invertebrate species, increasing local biodiversity. The distribution of these important accumulations varies in space and time depending on the environmental conditions and the composition of species that are in the wrack. Species composition and spatiotemporal variability in wrack accumulations remain poorly understood in some regions. In this study, we evaluated the spatiotemporal variability in wrack biomass and diversity on four sandy beaches in northern Portugal over the course of 1 year. The results revealed that both the diversity and biomass of wrack varied temporally depending on the beach and tidal level where it was collected. Wrack biomass was about 20 to 35 times greater at higher than at the low tide level and was more abundant (87%) and twice as diverse at the two northernmost beaches of the study, probably due to a greater proximity to rocky shores. Large brown temperate and boreal macroalgae species such as fucoids (Fucus spp., Cystoseira spp., and Ascophyllum nodosum) and the kelp Saccorhiza polyschides were the most abundant taxa in the wrack. Fucoids were in the wrack throughout the year, while kelps predominated in the warmer months, generating 8% more biomass than that produced by fucoids throughout the year. However, since large brown macroalgae species are reducing their size and recruitment due to global warming in the north of the Iberian Peninsula, the biomass and diversity of wrack in northern Portugal could be limited in the future, compromising crucial functions of wrack in ecosystems.Open Access funding provided thanks to the CRUE-CSIC agreement with Springer Nature. This research was developed under Project No. 029818, co-financed by COMPETE 2020, Portugal 2020, and the European Union through the ERDF, and by FCT through national funds. This study was partially funded by the FCT Strategic Funding UID/Multi/04423/2019. Laura Guerrero-Meseguer was funded by a grant from the Department of European Funds, University and Culture of the Government of the Balearic Islands, and Puri Veiga was hired through the Regulamento do Emprego Científico e Tecnológico—RJEC from the Portuguese Foundation for Science and Technology (FCT) program (CEECIND/03893/2018).Peer reviewe

Future heat waves due to climate change threaten the survival of Posidonia oceanica seedlings

Extreme weather events are major drivers of ecological change, and their occurrence is likely to increase due to climate change. The transient increases in atmospheric temperatures are leading to a greater occurrence of heat waves, extreme events that can produce a substantial warming of water, especially in enclosed basins such as the Mediterranean Sea. Here, we tested the effects of current and predicted heat waves on the early stages of development of the seagrass Posidonia oceanica. Temperatures above 27 °C limited the growth of the plant by inhibiting its photosynthetic system. It suffered a reduction in leaf growth and faster leaf senescence, and in some cases mortality. This study demonstrates that the greater frequency of heat waves, along with anticipated temperature rises in coming decades, are expected to negatively affect the germination of P. oceanica seedlings.This workwas carried out within the research project NEREIDAS (project code: 2012-ES-92177- S), funded by the European Commission under the Trans-European Transport Network Programme (TEN-T)