Divergent thirty-year trajectories of two co-occurring Mediterranean sea urchin species reveal climatic and trophic drivers

Federico Pinna
1*
Mario Minguito-Frutos
2
Giovanni Romagnoni
3
Martin Marzloff
2
Antonio Calò
4
Teresa Alcoverro
5
Jordi Boada
1,5
Giulia Ceccherelli
6
Antonio Di Franco
7
Elena Desiderà
1
Daniele Grech
8
Ivan Guala
8
Candela Marco-Méndez
5
Paolo Guidetti
1
Gabriella La Manna
6
Skye Brown
9
Arianna Pansini
6
Luigi Piazzi
10
Alessandra Puccini
6
Matteo Sinerchia
11
Laura Tamburello
12
Bernat Hereu
9
Simone Farina
1
1
Department of Integrative Marine Ecology (EMI), Genoa Marine Centre, Stazione Zoologica Anton Dohrn, Genoa Marine Centre, Villa del Principe, Piazza del Principe 4, Genova, GE - 16126, Italy
2
DYNECO- Coastal Environment Dynamics department, IFREMER Centre de Bretagne, Pointe du diable CS 10070, Plouzané, Finistère (29) - 29280, France
3
Department of Biology, University of Padova, via U. Bassi 58/b, Padova, PD - 35121, Italy
4
Department of Earth and Marine Sciences, (DiSTeM), University of Palermo, Via Archirafi 20-22, Palermo, PA - 90123, Italy
5
, Centre d’Estudis Avançats de Blanes (CEAB-CSIC), Carrer Accés Cala Sant Francesc, 14, Blanes, GI - 17300, Spain
6
Department of Chemical Physical Mathematical and Natural Science, University of Sassari, Via Vienna 2, Sassari, SS - 07100, Italy
7
Department of Integrative Marine Ecology (EMI), Sicily Marine Centre, Stazione Zoologica Anton Dohrn, Lungomare Cristoforo Colombo, Palermo, PA - 90149, Italy
8
, Fondazione IMC - International Marine Centre, Via Domenico Millelire, Torre Grande, OR - 09170, Italy
9
Department de Biologia Evolutiva, Ecologia i Ciències Ambientals, Facultat de Biologia, Institut de Recerca de la Biodiversitat (IRBIO), Universitat de Barcelona, Diagonal, 643, Barcelona, B - 08028, Spain
10
, Centro Interuniversitario di Biologia Marina e Ecologia Applicata "G. Bacci", viale  N. Sauro 4, Livorno, LI - 57128, Italy
11
Institute for the Study of Anthropic Impacts and Sustainability in the Marine Environment (CNR-IAS), National Research Council, Via De Marini, 6, Torre Grande, OR - 16149, Italy
12
Department of Integrative Marine Ecology, Sicily Marine Centre, Stazione Zoologica Anton Dohrn, Lungomare Cristoforo Colombo, Palermo, PA - 90149, Italy

Species population trajectories mostly arise from the combined influence of anthropogenic disturbance, biotic interactions and abiotic factors. However, assessing the relative contribution of these drivers remains challenging, as long-term ecological datasets, essential for robust inference, are scarce. We examined the population dynamics of the co-occurring sea urchins Paracentrotus lividus and Arbacia lixula using time series spanning up to 33 years from two Western Mediterranean Marine Protected Areas (MPAs): Medes (Spain) and Tavolara Punta Coda Cavallo (Italy). We quantified long-term population trends, assessed the influence of climatic, hydrodynamic and trophic drivers, and identified abrupt shifts in population trajectories. Generalised additive (mixed) models were combined with structural breakpoint analyses i) to investigate both contemporaneous and lagged effects of marine heatwaves (MHWs), storm-driven wave exposure and predatory fish biomass, and ii) to identify abrupt shifts in population trajectories. Our time series analysis showed that while P. lividus has declined consistently across the two MPAs, regardless of protection status, A. lixula has remained fairly stable at Medes and underwent only a moderate decline at Tavolara Punta Coda Cavallo. Lagged cumulative MHWs intensity, emerged as the strongest predictor of P. lividus population decline. Storm-driven wave impact provided an additional source of mortality at highly exposed sites. Breakpoint analyses identified abrupt and persistent reductions in P. lividus density at Medes, followed by limited evidence of population recovery. By contrast, A. lixula exhibited weak and inconsistent responses to MHWs and no detectable response to storm impact, likely reflecting its greater thermal tolerance and morphological adaptations to hydrodynamic stress. These different trajectories are progressively altering rocky-reef sea urchin assemblage composition. Our results highlight the role of extreme climatic events as key drivers of Mediterranean sea urchin dynamics, with potential consequences for herbivory, trophic regulation, rocky-reef community structure and ecosystem functioning as extreme events become increasingly frequent.

Reti trofiche, funzionamento degli ecosistemi ed ecologia di comunità, Ecosistemi, biodiversità e cambiamento climatico
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