Spatio-temporal patterns in coastal zoobenthos under environmental stress Federica Nasi University of Trieste Supervised by Co-supervised by Dr. Paola Del Negro Dr. Rocco Auriemma Sezione di Oceanografia, Sezione di Oceanografia, Istituto Nazionale di Istituto Nazionale di Oceanografiae e di Geofisica Oceanografia e di Geofisica Sperimentale (OGS) Sperimentale (OGS) Italy Italy Professor Erik Bonsdorff Environmental andMarine Biology, Faculty of Science and Engineering Åbo Akademy University Finland Dr. Tamara Cibic Sezione di Oceanografia, Istituto Nazionale di Oceanografia e di Geofisica Sperimentale (OGS) Italy Reviewed by Dr. Christos Arvanitidis Institute of Marine Biology, Biotechnology and Aquaculture Hellenic Center for Marine Research Greece Dr. Roberto Simonini Dipartimento di Scienze della Vita University of Modena and Reggio-Emilia Modena ABSTRACT The human exploitations of coastal marine systems have led to rapid degradation of the soft-sediment benthic ecosystems, variation of food supplies for the benthic assemblages, and loss of habitats and consequent reductions in species diversity. Sediments, in particular, act as a sink for organic matter and contaminants. Since benthic populations are directly exposed to dissolved contaminants, they constitute one of the most effective tools for assessing the state of environmental health of any given sedimentary habitat. Disturbances from natural or human influences result in shaping and structuring of the ecosystems to a degree that often exceeds what nature can cope with and hence threatens ecosystem resilience and thus also the functions (goods and services) the ecosystems provide. Among the soft-sediment benthic communities, macrozoobenthos drives important ecosystem processes in marine coastal sediments such as nutrient cycling, sediment reworking, bio-irrigation, organic matter decomposition, and secondary production (i.e. acts as a trophic link). Environmental disturbances threaten macrofaunal communities in terms of biodiversity, functional expressions, and trophic structure, modifying their stability and ecosystem resilience. The main aim of this doctoral research was to investigate the structural and functional variations of coastal marine macrofaunal communities subjected to diversified types of impact, from natural phenomena to anthropogenic pressures. For this reason, to study the natural fluctuations of the ecosystem, I chose a Marine Protected Area where the anthropogenic pressure is low. To investigate how the macrozoobenthos is affected by different stressors and contaminants, I selected three diversely impacted areas: the Po River delta, the harbour of Trieste and the Mar Piccolo of Taranto. The benthic infaunal community was analysed along a temporal scale at a relatively undisturbed station located in the buffer zone of the Miramare-MPA (Gulf of Trieste). The aim of the study was to assess the temporal variability of the community structure (biodiversity, feeding- and reproductive traits) related to food sources and environmental variations. The community displayed an intermediate level of stability from high diversity and unvarying feeding habits, to high turnover of diversity, and large variations in reproductive frequencies. The capability of the community to maintain its structure (number of individuals, species diversity and feeding strategies), despite the physical disturbance events, illustrates the resistance to natural stress exhibited by these macrofaunal invertebrates. The coastal area nearby the Po River delta is characterized by a high amount of organic matter loads, derived from the terrigenous river outflow. The aim of the study was to analyse the proportions of various primary producers contributing to the plume of suspended organic matter and the extent to which subsidies from rivers may influence the macrobenthic community structure and biomass. An increase in biomass close to the tributary of the principal river was registered, as well as changes in the trophic composition and variation in food sources determined from the isotopic signal along the river gradient. Further, the study highlighted a close link between grain-size and macrofaunal structure and trophic pathways in a variable and highly hydrodynamic system such as this deltaic area. The Port of Trieste represents an area with a diffuse sediment contamination deriving from several productive activities: shipbuilding, iron and steel plant, petroleum industry, and port activities. The aim of this study was to detect variation (deviation) in the structure of the macrofaunal community, such as number of individuals, biodiversity and trophic functional groups, as a response to anthropogenic impacts. The species composition varied among stations: species that are more tolerant to stress were observed in high numbers in vicinity of contaminated sites (e.g. the bivalve Corbula gibba and the polychaete Lumbrineris latreilli), highlighting a clear separation among stations along the studied gradients. Overall, despite the presence of stress-tolerant species, the environmental contamination within the harbour seems not too severe to affect the macrofaunal feeding structure. As an example of an area severely contaminated by heavy metals and synthetic organic compounds, the Mar Piccolo of Taranto was chosen. The macrofaunal community was investigated and a marked influence of contamination on the abundance and biodiversity was observed. The presence of stress-resistant species and highly reduced abundance of some sensitive organisms were registered, indicating poor conditions for the benthic ecological status in the Mar Piccolo. To assess the influence of contamination on trophic pathways, stable isotope analysis was conducted on macrofaunal communities. These results showed that chemical contamination affected the trophic structure in the absence of intermediate consumers that link basal organic matter sources to higher predators. The high biomass of predators compared to that of deposit feeders resulted in a simplification of the food web that compromises the energy transfer efficiency. The functional features of polychaetes associated with levels of contaminated sediments were analysed and compared in the harbour of Trieste and in the Mar Piccolo of Taranto, using biological trait analysis. Functional diversity and trait richness displayed fairly constant values despite varying taxa richness, highlighting the presence of functional redundancy among polychaetes. Functional identity illustrated the relationships and adaptation to contaminated sediments. In fact, high motility of the species seems to be an essential trait for living in highly contaminated sediments. This could be linked to the ability to avoid hotspots of contaminants through active movements, thus, influencing sediment reworking and especially the diffusion of contaminants towards the water column. These findings confirmed that soft-sediment macrofaunal communities responded differently to natural and, more subtly, to anthropogenic stress in the different environments. These results would not have been obtained without applying the novel approach used in this work, i.e. using stable isotopes (trophic links) and functional trait analysis. Integrative approaches that consider the whole environmental features in relation to structural and functional macrofaunal patterns provide useful tools for understanding, monitoring and assessing the ecosystem functioning in coastal environments subjected to multiple stressors. RIASSUNTO Nel corso degli ultimi cinquanta anni, il molteplice e sempre più esteso utilizzo delle coste ha portato in alcuni casi ad una rapida degradazione degli ecosistemi bentonici, inducendo una frammentazione degli habitat costieri, alterando l’approvvigionamento di cibo delle comunità bentoniche con una conseguente riduzione della biodiversità specifica. I sedimenti, in particolare, costituiscono un deposito della sostanza organica ed in alcuni casi anche di agenti contaminati derivanti dalle attività antropiche che determinano l’esposizione di numerosi invertebrati bentonici a tali fattori di stress. Poiché gli organismi bentonici sono sessili o a ridotta mobilità risultano direttamente e costantemente esposti ai sedimenti contaminanti. Il loro studio perciò, costituisce uno degli strumenti più efficaci per la valutazione dello stato di salute di un ecosistema marino. Disturbi di origine naturale o antropica provocano un’alterazione del funzionamento dell’ecosistema e quindi una conseguente riduzione delle funzioni (beni e servizi) che tali ecosistemi forniscono all’uomo. Tra le comunità bentoniche costiere di fondo mobile, il macrozoobenthos è coinvolto nei principali processi ecologici come il ciclo dei nutrienti, la mobilitazione dei sedimenti, la bio-irrigazione, la decomposizione della materia organica e la produzione secondaria. Alterazioni ambientali minacciano le comunità macrofaunali in termini di biodiversità, di cambiamenti nella struttura trofica e in generale nell’espressione dei tratti funzionali modificandone la stabilità, e conseguentemente la resistenza e resilienza. L’obiettivo principale del presente progetto di dottorato è stato quello di valutare le variazioni strutturali e funzionali delle comunità macrofaunali costiere soggette a diverse tipologie d’impatto, dai fenomeni naturali alle pressioni antropiche. Per questo motivo, per valutare le fluttuazioni naturali dell'ecosistema, ho scelto una Riserva Marina Naturale (MPA), dove la pressione antropica è relativamente bassa.