Nutrient enrichment stimulates herbivory and alters epibiont assemblages at the edge but not inside subtidal macroalgal forests

AbstractNutrient enrichment is a major threat to subtidal macroalgal forests. Several studies have shown that nutrient inputs can enhance the ability of opportunistic algal species to acquire space freed by disturbance, at the expense of architecturally complex species that form forests. However, competition between canopy- and turf-forming macroalgae is not limited to the aftermath of disturbance. Canopy-forming macroalgae can provide suitable substratum for diverse epibiont assemblages, including both algae (epiphytes) and sessile invertebrates (epizoans). Despite evidence of enhanced epiphyte loading under eutrophic conditions, few experimental studies have assessed how nutrient enrichment influences the structure of epibiont assemblages on canopy-forming macroalgae at the edge versus inside forests. In oligotrophic waters of the NW Mediterranean, we experimentally tested the hypothesis that nutrient-driven proliferation of opportunistic epiphytic algae would affect the performance of the fucoid, Carpodesmia brachycarpa, and reduce the richness and abundance of the epizoan species they support. We predicted negative effects of nutrient enrichment to be greater at the edge than inside forests and on thalli that had recovered in cleared areas than on those within undisturbed canopy stands. Nutrient enrichment did not affect the photosynthetic efficiency and reproductive output of C. brachycarpa. By contrast, it enhanced herbivore consumption and decreased the cover and diversity of epizoans at forest edges, likely by stimulating the foraging activity of Arbacia lixula, the most abundant sea urchin in adjacent encrusting coralline barrens. Fertilization of areas inside forests had no effect on either C. brachycarpa or epibiont assemblages. Finally, nutrient enrichment effects did not vary between cleared and undisturbed areas. Our results show that moderate nutrient enrichment of oligotrophic waters does not necessarily cause the proliferation of epiphytes and, hence, a strengthening of their competitive effects on canopy-forming macroalgae. Nevertheless, enhanced herbivory damage to fertilized thalli at forest edges suggests that fragmentation could reduce the resilience of macroalgal forests and associated epibiont assemblages to nutrient enrichment

Nutrient Loading Fosters Seagrass Productivity under Ocean Acidification

The effects of climate change are likely to be dependent on local settings. Nonetheless, the compounded effects of global and regional stressors remain poorly understood. Here, we used CO2vents to assess how the effects of ocean acidification on the seagrass, Posidonia oceanica, and the associated epiphytic community can be modified by enhanced nutrient loading. P. oceanica at ambient and low pH sites was exposed to three nutrient levels for 16 months. The response of P. oceanica to experimental conditions was assessed by combining analyses of gene expression, plant growth, photosynthetic pigments and epiphyte loading. At low pH, nutrient addition fostered plant growth and the synthesis of photosynthetic pigments. Overexpression of nitrogen transporter genes following nutrient additions at low pH suggests enhanced nutrient uptake by the plant. In addition, enhanced nutrient levels reduced the expression of selected antioxidant genes in plants exposed to low pH and increased epiphyte cover at both ambient and low pH. Our results show that the effects of ocean acidification on P. oceanica depend upon local nutrient concentration. More generally, our findings suggest that taking into account local environmental settings will be crucial to advance our understanding of the effects of global stressors on marine systems

Ecological impacts of invading seaweeds: A meta-analysis of their effects at different trophic levels

Aim Biological invasions are among the main threats to biodiversity. To promote a mechanistic understanding of the ecological impacts of non-native seaweeds, we assessed how effects on resident organisms vary according to their trophic level. Location Global. Methods We performed meta-analytical comparisons of the effects of non-native seaweeds on both individual species and communities. We compared the results of analyses performed on the whole dataset with those obtained from experimental data only and, when possible, between rocky and soft bottoms. Results Meta-analyses of data from 100 papers revealed consistent negative effects of non-native seaweeds across variables describing resident primary producer communities. In contrast, negative effects of seaweeds on consumers emerged only on their biomass and, limited to rocky bottoms, diversity. At the species level, negative effects were consistent across primary producers' response variables, while only the survival of consumers other than herbivores or predators (e.g. deposit/suspension feeders or detritivores) decreased due to invasion. Excluding mensurative data, negative effects of seaweeds persisted only on resident macroalgal communities and consumer species survival, while switched to positive on the diversity of rocky-bottom consumers. However, negative effects emerged for biomass and, in rocky habitats, density of consumers other than herbivores or predators. Main conclusions Our results support the hypothesis that seaweeds' effects on resident biodiversity are generally more negative within the same trophic level than on higher trophic guilds. Finer trophic grouping of resident organisms revealed more complex impacts than previously detected. High heterogeneity in the responses of some consumer guilds suggests that impacts of non-native seaweeds at higher trophic levels may be more invader- and species-specific than competitive effects at the same trophic level. Features of invaded habitats may further increase variability in seaweeds' impacts. More experimental data on consumers' response to invasion are needed to disentangle the effects of non-native seaweeds from those of other environmental stressors

Cross-basin and cross-taxa patterns of marine community tropicalization and deborealization in warming European seas.

Ocean warming and acidification, decreases in dissolved oxygen concentrations, and changes in primary production are causing an unprecedented global redistribution of marine life. The identification of underlying ecological processes underpinning marine species turnover, particularly the prevalence of increases of warm-water species or declines of cold-water species, has been recently debated in the context of ocean warming. Here, we track changes in the mean thermal affinity of marine communities across European seas by calculating the Community Temperature Index for 65 biodiversity time series collected over four decades and containing 1,817 species from different communities (zooplankton, coastal benthos, pelagic and demersal invertebrates and fish). We show that most communities and sites have clearly responded to ongoing ocean warming via abundance increases of warm-water species (tropicalization, 54%) and decreases of cold-water species (deborealization, 18%). Tropicalization dominated Atlantic sites compared to semi-enclosed basins such as the Mediterranean and Baltic Seas, probably due to physical barrier constraints to connectivity and species colonization. Semi-enclosed basins appeared to be particularly vulnerable to ocean warming, experiencing the fastest rates of warming and biodiversity loss through deborealization

Ecological effects of multiple stressors on coastal benthic systems

Coastal ecosystems are simultaneously exposed to a variety of stressors that operate at different spatial and temporal scales. The effects of global climate changes are likely to be dependent on local settings, yet combined effects of global and regional stressors are poorly understood. Predicting the outcome of multiple stressors is further complicated by variations in their temporal regimes. My thesis aims to investigate the cumulative effects of multiple stressors on coastal benthic systems. I focused on three different benthic habitats: the seagrass, Posidonia oceanica, assemblages dominated by the canopy forming algae, Cystoseira spp., and permeable soft sediment hosting a diverse infaunal invertebrate community. In Chapter 2, I used shallow water CO2 vents to assess how the effects of ocean acidification on the seagrass, P. oceanica, and the associated epiphytic community can be modified by enhanced nutrient loading. The compounded effects of global and local stressors were evaluated across different organization levels, from genes to the whole community. The results showed that nutrient enrichment compensated the negative effects of ocean acidification on the seagrass leaf production. The antagonistic interaction of these stressors was likely the result of direct effects on the physiology of the plant and indirect effects due to changes in species interactions (plant-epiphytes). These results show that the effects of global stressors are likely to be context-dependent and may have important implication for management strategies aimed to sustain the functioning of marine ecosystems in face of climate change. In Chapter 3, I investigated the compounded effects of nutrient supply and simulated herbivory on a shallow P. oceanica bed. To assess the temporal variability of disturbances, chronic and pulse nutrient loading were combined with simulated herbivory, treated as a pulse stress. I evaluated traits underpinning tolerance and resistance to herbivory in P. oceanica under different regimes of nutrients loading. The results showed that both chronic and pulse nutrient enrichment can compromise the ability of the seagrass to cope with high herbivory, either directly, by altering plant physiology, or, indirectly, by stimulating consumption. High grazing pressure caused a more severe reduction of plant biomass when combined with chronic than pulse nutrient enrichment. These results suggest that taking into account herbivore pressure in necessary to accurately assess the effects of different temporal regimes of nutrient supply on seagrass meadows. In chapter 4, I used shallow rocky reefs, composed by a mosaic of stands of the canopy-forming macroalga, Cystoseira spp., and barren patches, to experimentally investigate the role of canopy degradation, nutrient enrichment and sea urchin density, in triggering the shift from canopy-dominated to alternative states inside and at the margin of macroalgal forests. High grazing pressure altered the structure of the whole assemblages, possibly leading to the transition from high diverse habitats to low productive barren grounds, in particular at high levels of disturbance (canopy removal). In contrast, under weak control by consumers, moderate or severe events of disturbance on habitat-forming macroalgae did not result in a change of the relative extent of contrasting habitats. Understanding the mechanism that regulate the switches to alternative habitats requires taking into account interactions among species that compose each habitats and the way they are modified by abiotic and biotic stressors. In chapter 5, I experimentally investigated the cumulative effects of ocean acidification and hypoxia on the organic matter cycling in soft sediments, through a short-term mesocosm experiment. I used isotopically labelled macroalgae as a tracer to assess faunal uptake of organic carbon and carbon incorporation into the sediment under different experimental conditions. The results showed that the effects of elevated [CO2] on C-uptake by fauna varied with different oxygen concentration. Under normoxia, elevated [CO2] significantly enhanced faunal uptake of organic carbon, likely due to the higher energetic cost of living associated to high level of CO2. By contrast, following the hypoxia event, there was limited C-uptake by fauna exposed to high CO2, potentially leading to the metabolic depression of invertebrates. The results suggest that the capacity of invertebrates to maintain vital physiological processes could impair under the combined effects of the two stressors. This research helps to better understanding the cumulative nature of human impacts on key structural and functional systems and may have important implications for management strategies aimed to sustain the functioning of marine ecosystems in face to multiple anthropogenic stressors

Il problema delle invasioni biologiche: influenza della latitudine e del disturbo antropico sugli effetti di alghe invasive

Le invasioni biologiche sono un fenomeno diffuso e rappresentano una componente significativa dei cambiamenti ambientali causati dall'uomo. I processi che regolano le invasioni biologiche sono molto dinamici e non dipendono soltanto dal trasporto mediato dalle attività umane, ma anche da fattori fisici, chimici e biologici dell'ambiente in cui si stabiliscono. Nonostante il numero di studi che riporta gli effetti delle specie aliene sia aumentato, uno dei problemi che emerge attualmente è la mancanza di una sintesi quantitativa su come tali impatti varino in base alle caratteriste degli ambienti riceventi ed alle caratteristiche stesse dell'invasore. Inoltre, la mancanza di un adeguato numero di studi sperimentali impedisce di comprendere il ruolo delle specie invasive e le potenziali conseguenze sull'ambiente ricevente. La prima parte di questa tesi consiste nello svolgimento di una meta-analisi con lo scopo di fornire una sintesi quantitativa della variazione degli impatti di macroalghe marine invasive, secondo un gradiente latitudinale. I risultati ottenuti dalla meta-analisi mostrano una tendenza generale ad avere un impatto maggiore delle macroalghe intorno alle latitudini minori del gradiente considerato e tali risultati sono stati messi in relazione con i gradienti latitudinali della ricchezza in specie e della competizione. Tuttavia, il modello di regressione spiega soltanto una piccola parte dell'eterogeneità totale degli impatti delle macroalghe invasive investigate. La seconda parte di questa tesi consiste in un esperimento manipolativo multifattoriale, dove vengono analizzati gli effetti dell'alga invasiva Caulerpa racemosa in siti caratterizzati da differenti condizioni ambientali. L'obiettivo specifico dell'esperimento è quello di testare se i popolamenti nativi, sottoposti ad una differente pressione antropica, siano influenzati diversamente dalla presenza dell'alga invasiva. Al tal proposito, abbiamo manipolato la presenza di C. racemosa e dei polamenti nativi di habitat subtidali poco profondi, lungo un gradiente di urbanizzazione (Urbano, Extraurbano ed Isole). I primi risultati sperimentali indicano che la rimozione di C. racemosa abbia effetti differenti sui popolamenti nativi non disturbati, lungo il gradiente di urbanizzazione. La presenza di C. racemosa può causare una riduzione della variabilità spaziale delle specie, nei popolamenti delle isole, a livelli comparabili a quelli che caratterizzano i popolamenti in aree urbane. In seguito alla rimozione dell'alga invasiva, i popolamenti delle isole mostrano una maggiore variabilità a piccola scala, rispetto a quelli urbani ed extra-urbani. Al contrario, i popolamenti delle aree urbane ed extra-urbane non differiscono tra di loro e la scarsa variabilità spaziale riscontrata è probabilmente il risultato della costante influenza delle attività umane. In questo caso è possibile supporre che la rimozione di C. racemosa abbia effetti limitati sui popolamenti nativi, già degradati

Molecular level responses to chronic versus pulse nutrient loading in the seagrass Posidonia oceanica undergoing herbivore pressure

Seagrasses are key marine foundation species, currently declining due to the compounded action of global and regional anthropogenic stressors. Eutrophication has been associated with seagrass decline, while grazing has been traditionally considered to be a natural disturbance with a relatively low impact on seagrasses. In the recent years, this assumption has been revisited. Here, by means of a 16-month field-experiment, we investigated the molecular mechanisms driving the long-term response of Posidonia oceanica to the combination of nutrient enrichment, either as a chronic (press) or pulse disturbance, and herbivory. Changes in expression levels of 19 target genes involved in key steps of photosynthesis, nutrient assimilation, chlorophyll metabolism, oxidative-stress response and plant defense were evaluated through reverse transcription-quantitative polymerase chain reaction (RT-qPCR). High herbivore pressure affected the molecular response of P. oceanica more dramatically than did enhanced nutrient levels, altering the expression of genes involved in plant tolerance and resistance traits, such as photosynthesis and defense mechanisms. Genes involved in carbon fixation and N assimilation modulated the response of plants to high nutrient levels. Availability of resources seems to modify P. oceanica response to herbivory, where the upregulation of a nitrate transporter gene was accompanied by the decline in the expression of nitrate reductase in the leaves, suggesting a change in plant-nutrient allocation strategy. Finally, press and pulse fertilizations altered nitrate uptake and reduction-related genes in opposite ways, suggesting that taking into account the temporal regime of nutrient loading is important to assess the physiological response of seagrasses to eutrophication

Macro-grazer herbivory regulates seagrass response to pulse and press nutrient loading

Coastal ecosystems are exposed to multiple stressors. Predicting their outcomes is complicated by variations in their temporal regimes. Here, by means of a 16-month experiment, we investigated tolerance and resistance traits of Posidonia oceanica to herbivore damage under different regimes of nutrient loading. Chronic and pulse nutrient supply were combined with simulated fish herbivory, treated as a pulse stressor. At ambient nutrient levels, P. oceanica could cope with severe herbivory, likely through an increase in photosynthetic activity. Elevated nutrient levels, regardless of the temporal regime, negatively affected plant growth and increased leaf nutritional quality. This ultimately resulted in a reduction of plant biomass that was particularly severe under chronic fertilization. Our results suggest that both chronic and pulse nutrient loadings increase plant palatability to macro-grazers. Strategies for seagrass management should not be exclusively applied in areas exposed to chronic fertilization since even short-term nutrient pulses could alter seagrass meadows