Threats to large brown algal forests in temperate seas: the overlooked role of native herbivorous fish

www.nature.com/scientificreports OPEN Received: 9 March 2017 Accepted: 12 June 2017 Published: xx xx xxxx Threats to large brown algal forests in temperate seas: the overlooked role of native herbivorous fish Fabrizio Gianni1,2, Fabrizio Bartolini1, Alexis Pey1, Mathieu Laurent1, Gustavo M. Martins Laura Airoldi4 & Luisa Mangialajo1,2 3 , Canopy-forming algae are declining globally due to multiple disturbances. This decline has recently been on the increase due to the spread of some tropical herbivorous fishes. This new phenomenon has drawn attention to the effects of fish herbivory in temperate areas, which have been assumed to be negligible compared to that of invertebrates, such as sea urchins. In this study, the impact of a Mediterranean native herbivorous fish (Sarpa salpa, salema) was assessed on the canopy-forming seaweed Cystoseira amentacea var. stricta. Cystoseira amentacea forms belts in the infralittoral fringe of wave-exposed shores, which has so far been considered a refuge from fish herbivory. To test the effects of salema feeding on natural C. amentacea belts, an innovative herbivore deterrent device was conceived. Salema had a significant effect on C. amentacea by decreasing algal size, biomass and fertility, by up to 97%. The results suggest that the contribution of salema feeding to the loss of Cystoseira forests in the Mediterranean may have been overlooked. In addition, the analysis of temporal and spatial patterns of salema landings in the Mediterranean Sea suggests that salema abundance may have increased recently. Thus, along with invertebrate herbivory and anthropogenic stressors, fish herbivory may also represent a potential threat to algal forests in temperate areas. Marine forests of large brown seaweeds are unique habitats that support a great variety of organisms in coastal zones worldwide and are comparable to terrestrial forests for the services they provide1, 2. Several species, mostly belonging to the orders Fucales and Laminariales, can dominate both shallow and deep-water marine ecosystems (up to their light compensation limit)3, 4. Algal forests are exposed to multiple disturbances that have caused a decline in their abundance in many coastal areas of the world5, 6. A recent survey highlighted that, although global drivers could affect kelp forests at multiple scales, local stressors and regional variations in the effects of these drivers dominate kelp dynamics7. Species thriving in shallow-water zones are the most strongly affected because they are located in a boundary environment, exposed to impacts of both terrestrial and marine origin. For instance, contaminants8, nutrient enrichment9, sediment loads10, increase in seawater temperature11 and habitat alteration, resulting from coastal urbanisation6, are well-known factors responsible for the loss of large brown seaweeds. Fucoids and kelps can also be highly vulnerable to herbivory12. Outbreaks of sea urchins, due to natural fluctuations, but more often as an indirect effect of overfishing of their predators, are responsible for the depletion of macroalgal communities and the subsequent formation of extensive barren grounds13, 14. This phenomenon has been observed in many coastal areas1 and nowadays sea urchin barren grounds are common in many temperate bioregions. As a consequence, sea urchins are considered as the primary herbivorous consumers of algal canopies in the subtidal zone of temperate areas15. In the intertidal zone, where sea urchins do not usually occur, gastropods and limpets are often considered as the primary herbivores16, 17. Therefore, in both subtidal and intertidal temperate ecosystems, herbivory is generally associated with invertebrates. In contrast, the role of herbivorous fishes in regulating macroalgal vegetation is highly variable. In tropical areas, they play an important role in limiting shifts from coral- to macroalgae-dominated communities18. In 1 Université Côte d’Azur, CNRS, ECOMERS, Nice, 06108, France. 2Sorbonne Universités, UPMC Univ Paris 06, INSU-CNRS, UMR 7093 Laboratoire d’Océanographie de Villefranche (LOV), Villefranche sur mer, 06230, France. 3 Department of Biology, Faculty of Sciences and Technology & Centre for Ecology, Evolution and Environmental Changes/Azorean Biodiversity Group (cE3c), University of the Azores, 9501–801, Ponta Delgada, Portugal. 4 Dipartimento di Scienze Biologiche, Geologiche ed Ambientali BIGEA, University of Bologna, UO CoNISMa, Ravenna, 48123, Italy. Correspondence and requests for materials should be addressed to F.G. (email: ) Scientific Reports | 7: 6012 | DOI:10.1038/s41598-017-06394-7 1 www.nature.com/scientificreports/ Figure 1. Study area. The two sampling sites are located in Villefranche Bay, French Riviera, NW Mediterranean Sea. Maps were made by using Adobe Illustrator software CS6. ® ® temperate zones, fish grazing control is assumed to be lower or negligible in comparison to grazing from invertebrates19–21. The gradient of control from herbivorous fishes to invertebrates at high latitudes is hypothesized to be driven by the decrease in herbivorous fish species diversity and abundance22. However, some evidence suggests that the role of herbivorous fishes in temperate regions may have been underestimated. Verlaque observed that the feeding behaviour of Sarpa salpa (salema), the only native herbivorous fish in the Mediterranean Sea, is particularly selective, contributing to maintaining high algal biodiversity23. Salema are also able to determine the distribution of some Cystoseira species, restricting grazer-sensitive species to spatial refuges, in either very shallow or deep areas, where fish grazing pressure is lower 24. The same observations were reported from central Portugal, where S. salpa is responsible for reducing kelp biomass and restricting the survival of recruits to crevices25. Taylor and Schiel did analogous observations on Odax pullus in New Zealand, which is able to significantly reduce the cover and biomass of the kelp Durvillaea antarctica26. In addition, recent studies have highlighted the impact of tropical herbivorous fishes, by expanding their distribution range into temperate areas, on canopy algae27. The aim of the present study was to quantify the potential impact of Sarpa salpa on large brown algal forests and to provide evidence of a potential increase of salema over the last decades. The herbivory effect of S. salpa was investigated on size, biomass and fertility of Cystoseira amentacea var. stricta (hereafter C. amentacea), a species forming narrow belts in the very shallow infralittoral fringe of the Mediterranean Sea, which is considered a refuge from fish herbivory24, 28. In order to experimentally manipulate fish grazing on C. amentacea, an innovative herbivorous fish deterrent device was used (DeFish – herbivorous Fish Deterrent for the conservation and restoration of algal forests (Gianni et al. in prep.)). The hypotheses of the present study were: i (...truncated)