(Or Shifting) Baseline Syndrome

Protected Areas in the Mediterranean Sharing expertise for effective conservation Malta, 11-14 September 2017

EVALUATING THE STATUS OF THREE ICONIC MEDITERRANEAN MARINE HABITATS: SEAGRASS MEADOWS, CAVES AND ROCKY REEFS. A SCHOLARLY ODYSSEY BETWEEN THE SLIDING BASELINE SYNDROME AND THE NEED FOR REFERENCE CONDITIONS

Carlo Nike BIANCHI & Carla MORRI

DiSTAV, University of Genoa, Italy ECOSYSTEM STATUS ASSESSMENT

• Expert judgement • Biotic indices • Comparison with a reference condition ECOSYSTEM STATUS ASSESSMENT

• Expert judgement • Biotic indices • Comparison with a reference condition

THE SLIDING BASELINE SYNDROME (SBS) IN ENVIRONMENTAL CONSERVATION THE SLIDING (OR SHIFTING) BASELINE SYNDROME

– Significant changes to a system are measured against previous reference points (baselines), which themselves may represent significant changes from the original state of the system. – Loss of perception of change occurs when each generation redefines what is "natural". ―– Shift over time in the expectation of what a healthy ecosystem baseline looks like. A conceptual metaphor for a shifting baseline is the price of coffee. A cup of coffee may have only cost a $0.05 in the 1950s, but in the 1980s the cost shifted to $1.00 (ignoring inflation). The current (21st century) coffee prices are based on the 1980s model, rather than the 1950s model. The point of reference moved. the European Marine Strategy Framework Directive (MSFD, 2008/56/EC)

Reference conditions

Pristine areas Historical data Modelling the European Marine Strategy Framework Directive (MSFD, 2008/56/EC) No “pristine areas” left! “Unnatural oceans” (Jackson & Sala, 2001) “Research on intact marine ecosystems: a lost era” (Stachowitsch, 2003)

Paul J. Crutzen (2010) The 'Anthropocene': a new geologic epoch dominated by human activities “Good environmental status” cannot be defined exclusively as “pristine environmental status”, but rather status when impacts of all uses were sustainable. [... meaning?] the European Marine Strategy Framework Directive (MSFD, 2008/56/EC)

Reference conditions

Pristine areas Historical data Modelling the European Marine Strategy Framework Directive (MSFD, 2008/56/EC)

Reference conditions

Pristine areas Historical data Modelling

Protected areas the European Marine Strategy Framework Directive (MSFD, 2008/56/EC)

Reference conditions

Protected areas Historical data Modelling Selected examples of the three approaches in three Mediterranean Sea iconic habitats: seagrass meadows, caves, and rocky reefs Protected areas 1 Historical data 1 Modelling 1 Zone: Gulf of Tigullio Habitat: rocky reefs Depth: 5-8 m

Position of sampling sites and of the main human-induced pressures in the study area.

Parravicini V., Micheli F., Montefalcone M., Morri C., Villa E., Castellano M., Povero P., Bianchi C.N., 2013. Conserving biodiversity in a human-dominated world: degradation of marine sessile communities within a protected area with conflicting human uses. Public Library of Science One, 8 (10): e75767. Protected areas 1 Historical data 1 Modelling 1 Zone: Gulf of Tigullio Habitat: rocky reefs Depth: 5-8 m

red = MPA sites

Parravicini V., Micheli F., Montefalcone M., Morri C., Villa E., Castellano M., Povero P., Bianchi C.N., 2013. Conserving biodiversity in a human-dominated world: degradation of marine sessile communities within a protected area with conflicting human uses. Public Library of Science One, 8 (10): e75767. Protected areas 2 Historical data 1 Modelling 1 Zone: NW Mediterranean Habitat: coralligenous reefs Depth: 30-35 m

Location of the study site at Mesco Reef (MR) for the temporal dataset and the 15 sites for the spatial dataset: Portofino (PO), Montecristo Island (MO), Pianosa Island (PI), Tavolara Island (TA), Capo Carbonara (CC), Vada Shoals (VA), Elba Island (EL), Argentario (AR), Giglio Island (GI), Costa Paradiso (CP), Meloria Shoals (ME), Livorno (LI), Piombino (PB), Civitavecchia (CI) and Santa Marinella (SM).

Montefalcone M., Morri C., Bianchi C.N., Bavestrello G., Piazzi L., 2017. The two facets of species sensitivity: stress and disturbance on coralligenous assemblages in space and time. Marine Pollution Bulletin, 117: 229-238. Protected areas 2 Historical data 1 Modelling 1 Zone: NW Mediterranean Habitat: coralligenous reefs Depth: 30-35 m

Mean quality (± s.e.) of the coralligenous assemblages expressed as ecological quality ratio of the integrated sensitivity level of coralligenous assemblages (ISLA) index in three different conditions: P = protected LU = little urbanised HU = highly urbanised Good quality (0.6 ≤ ISLA < 0.8) is shown in light grey, moderate quality (0.4 ≤ ISLA < 0.6) in dark grey. The dotted line represents the threshold value (ISLA = 0.6) for changing from good quality to moderate quality. Results of one-way PERMANOVA analyses are reported: * = p < 0.05.

Montefalcone M., Morri C., Bianchi C.N., Bavestrello G., Piazzi L., 2017. The two facets of species sensitivity: stress and disturbance on coralligenous assemblages in space and time. Marine Pollution Bulletin, 117: 229-238. Protected areas 3 Historical data 1 Modelling 1 Zone: Liguria Habitat: seagrass meadows Depth: ~ 10 m

MO: Mortola; OS: Ospedaletti; GA: Gallinara; BE: Bergeggi; CA: Cogoleto - Arenzano; FO: Genoa - Foce, ST: Sturla; QA: Quarto; QI: Quinto; NE: Nervi; PO: Portofino; PS: Prelo - San Michele di Pagana; MA: Manara; FR: Framura; MM: Monterosso al Mare. Montefalcone M., Albertelli G., Morri C., Parravicini V., Bianchi C.N., 2009. Legal protection is not enough: Posidonia oceanica meadows in marine protected areas are not healthier than those in unprotected areas of the northwest Mediterranean Sea. Marine Pollution Bulletin, 58: 515-519. Protected areas 3 Historical data 1 Modelling 1 Zone: Liguria Habitat: seagrass meadows Depth: ~ 10 m

Mean values (± se) of the Conservation Index (CI) in 15 Posidonia oceanica meadows: Mortola (MO), Ospedaletti (OS), Gallinara (GA), Bergeggi (BE), Cogoleto - Arenzano (CA), Genoa - Foce (FO), Sturla (ST), Quarto (QA), Quinto (QI), Nervi (NE), Portofino (PO), Prelo - San Michele di Pagana (PS), Manara (MA), Framura (FR), Monterosso al Mare (MM)

Montefalcone M., Albertelli G., Morri C., Parravicini V., Bianchi C.N., 2009. Legal protection is not enough: Posidonia oceanica meadows in marine protected areas are not healthier than those in unprotected areas of the northwest Mediterranean Sea. Marine Pollution Bulletin, 58: 515-519. Protected areas 4 Historical data 1 Modelling 1

Marine Protected Areas

• too young • too small • not sufficiently enforced (“paper parks”) • designed to manage fisheries, not ecosystems Protected areas 3 Historical data 1 Modelling 1 Zone: SE Aegean Sea Habitat: various Depth: 1 to 10 m

The Island of Kos with study sites: B, Agios Fokas; G, Kako Skali; K, Kardamena; N, Agios Nikolaos; P, Psalidi; S, Marmari; T, Piso Thermi; Y, Cape Louros. The anchor symbol indicates harbour and marinas, the drumstick coastal wastewater treatment plants. Inset: the Aegean Sea between Greece (GR) and Turkey (TR), with the Island of Kos framed.

Bianchi C.N., Corsini-Foka M., Morri C., Zenetos A, 2014. Thirty years after: dramatic change in the coastal marine ecosystems of Kos Island (Greece), 1981-2013. Mediterranean Marine Science, 15 (3): 482-497. Protected areas 3 Historical data 1 Modelling 1 CHANGE IN STRESS REGIME Zone: SE Aegean Sea Habitat: various Depth: 1 to 10 m

Sea water temperature

Change in sea surface temperature (SST) in the coastal waters of Kos. A - Trend of yearly means from 1975 to 2012. B - Monthly means for 1981 and 2013.

Human pressures

Change in human pressure intensity at Kos. A - Resident population. B - Receptive capacity for tourists (the number of rooms rent by privates is probably underestimated). C - Number of overnights (in hotels). D - Passenger arrivals by flight and by ship. E - Arrivals of dry cargo ships and tankers to Kos port. F - Total gross tonnage of fishing vessels.

Biological invasions

Number of alien marine species per decade (bars) and overall trend for the last century (line) in the Dodecanese area (to which Kos belongs).

Bianchi C.N., Corsini-Foka M., Morri C., Zenetos A, 2014. Thirty years after: dramatic change in the coastal marine ecosystems of Kos Island (Greece), 1981-2013. Mediterranean Marine Science, 15 (3): 482-497. Protected areas 3 Historical data 1 Modelling 1 CHANGE IN BIOLOGICAL COMMUNITIES Zone: SE Aegean Sea Habitat: various Depth: 1 to 10 m

Correspondence Analysis ordination model on the plane formed by the first two axes extracted. 1st axis (horizontal) explains 14.2 % of the total variance, 2nd axis (vertical) 12.1 %. Site-points are BIOTIC represented by capital letters, followed by the relevant year of survey. Sites are HOMOGENISATION grouped by year of survey, and time trajectories of individual sites are also indicated.

Bianchi C.N., Corsini-Foka M., Morri C., Zenetos A, 2014. Thirty years after: dramatic change in the coastal marine ecosystems of Kos Island (Greece), 1981-2013. Mediterranean Marine Science, 15 (3): 482-497. Protected areas 3 Historical data 1 Modelling 1 CHANGE IN BIOLOGICAL COMMUNITIES Zone: SE Aegean Sea Cystoseira Habitat: various crinita

Cystoseira Depth: 1 to 10 m Dasycladus corniculata vermicularis Sargassum vulgare Cystoseira From algal reefs to sponge reefs foeniculacea Liagora viscida Padina Schematic profile of a reef slope down to pavonica about 7 m depth at site N, to illustrate change between 1981 and 2013.

Sarcotragus foetidus

Chondrosia reniformis

Crambe crambe

Bianchi C.N., Corsini-Foka M., Morri C., Zenetos A, 2014. Thirty years after: dramatic change in the coastal marine ecosystems of Kos Island (Greece), 1981-2013. Mediterranean Marine Science, 15 (3): 482-497. Protected areas 3 Historical data 1 Modelling 1 CHANGE IN BIOLOGICAL COMMUNITIES Zone: SE Aegean Sea Habitat: various Depth: 1 to 10 m

From algal reefs to sponge reefs

Shift from algal dominance to sponge dominance, both in terms of substrate cover (left panel) and species richness (right panel), on A massive specimen of Ircinia retidermata on Kos reefs between 1981 and 2013. shallow rocks at Kos in 2013

Bianchi C.N., Morri C., Pronzato R., 2014. The other side of rarity: recent habitat expansion and increased abundance of the horny sponge Ircinia retidermata (Demospongiae: Dictyoceratida) in the southeast Aegean. Italian Journal of Zoology, 81 (4): 564-570. Protected areas 3 Historical data 1 Modelling 1 CHANGE IN BIOLOGICAL COMMUNITIES Zone: SE Aegean Sea Habitat: various Depth: 1 to 10 m

From algal reefs to sponge reefs

Structural change on rocky reefs. A - Forest of Cystoseira spp in 1981 at site N. B - Sarcotragus foetidus and other sponges on a substratum deprived of algal cover in 2013 at site N. C - School of Siganus luridus overgrazing algal turf on otherwise barren rock in 2013.

Bianchi C.N., Corsini-Foka M., Morri C., Zenetos A, 2014. Thirty years after: dramatic change in the coastal marine ecosystems of Kos Island (Greece), 1981-2013. Mediterranean Marine Science, 15 (3): 482-497. Protected areas 3 Historical data 2 Modelling 1 the diver and the scientist ... Zone: Portofino Promontory Duilio Marcante (1914-1985) and Enrico Tortonese (1911-1987) Habitat: rocky reefs Depth: 0 to 40 m

D. Marcante

E. Tortonese Gatti G., Bianchi C.N., Montefalcone M., Venturini S., Diviacco G., Morri C., 2017. Observational information on a temperate reef community helps understanding the marine climate and ecosystem shift of the 1980–90s. Marine Pollution Bulletin, 114 (1): 528–538. Protected areas 3 Historical data 2 Modelling 1 Changes in climate and human pressure Zone: Portofino Promontory regimes in the region of Portofino, 1956–2013. Habitat: rocky reefs Depth: 0 to 40 m

Left panel: yearly averages of sea surface temperature (SST, from NOAA satellite data) and of air temperature (from the Meteorological Observatory of the University of Genoa). Smoothed thick lines depict the 11-year moving averages. Right panel: receptive capacity for tourists (number of beds), resident population (inhabitants) and commercial activity (firms) in the district of Portofino Promontory. Shadow encompasses the years since the establishment of the Marine Protected Area.

Gatti G., Bianchi C.N., Montefalcone M., Venturini S., Diviacco G., Morri C., 2017. Observational information on a temperate reef community helps understanding the marine climate and ecosystem shift of the 1980–90s. Marine Pollution Bulletin, 114 (1): 528–538. Protected areas 3 Historical data 2 Modelling 1 Zone: Portofino Promontory Habitat: rocky reefs Depth: 0 to 40 m

Winners and losers in Portofino reefs. From upper left to lower right: four species that disappeared or got rarer in recent years: Sargassum vulgare in 1980, Cystoseira sp. in 1979, Dictyopteris polypodioides in 1991, Alcyonium coralloides (on Paramuricea clavata) in 1987; and five species that newly appeared or got commoner: Caulerpa cylindracea in 2011, Axinella verrucosa in 2000, Eunicella verrucosa in 2001, Salmacina dysteri in 2012, Frondipora verrucosa in 2012.

Change through time in mean (± se) richness and abundance of the seven species groups (Roman numerals). Period 1 = 1950–70s; 2 = 1980–90s; 3 = 2000–10s.

Change through time in depth range preference (mean ± se) of the seven species groups (Roman numerals). Depth range a = 0–10 m; b = 11–20 m; c = 21–30 m; d = 31–40 m. Period Species groups (Roman numerals) 1 = 1950–70s; 2 = 1980–90s; 3 = 2000–10s. resulted from cluster analysis. Gatti G., Bianchi C.N., Montefalcone M., Venturini S., Diviacco G., Morri C., 2017. Observational information on a temperate reef community helps understanding the marine climate and ecosystem shift of the 1980–90s. Marine Pollution Bulletin, 114 (1): 528–538. Protected areas 3 Historical data 2 Modelling 1 Zone: Portofino Promontory Habitat: rocky reefs Depth: 0 to 40 m

Ordination model on the plane formed by the first two axes extracted by Correspondence Analysis. 1st axis is horizontal, 2nd vertical; the cross depicts the centre of the axes. Observation points are represented by alphanumeric codes, where numbers indicate the time periods (1 = 1950–70s, 2 = 1980–90s, 3 = 2000–10s), capital letters the zones (A, BE, BW, C), and lower-case letters the depth ranges (a = 0–10 m, b = 11–20 m, c = 21–30 m, d = 31–40 m); species are identified by codes in italics. Observation-point BIOTIC centroids are used to highlight the time- HOMOGENISATION trajectories of the zones.

LESSONS TO BE LEARNT # 1

“No matter the age, the science matters” Elsevier, ScienceDirect Newsletter: Valuing older research

“It is essential to turn anecdotal accounts into robust scientific evidence” Martin Goodall, Cornwall Wildlife Trust Protected areas 3 Historical data 3 Modelling 1 Zone: Mesco Shoal Geographical setting of the study area in the Ligurian Sea (a) and three-dimensional reconstruction of the Mesco Shoal based on Habitat: coralligenous reef multibeam data (b). Depth: 17 to 44 m

Number of papers (each quadrat is one document) per decade on the epibenthic assemblages of Mesco Reef, according to the year of publication. Grey quadrats represent descriptive ‘natural history’ reports (including species lists and/or environmental information), black quadrats represent studies based on quantitative (cover) data.

Gatti G., Bianchi C.N., Parravicini V., Rovere A., Peirano A., Montefalcone M., Massa F., Morri C., 2015. Ecological change, sliding baselines and the importance of historical data: lessons from combining observational and quantitative data on a temperate reef over 70 years. PLoS ONE, 10 (2): e0118581. Protected areas 3 Historical data 3 Modelling 1 Change with time in the occurrence of a number of selected species Zone: Mesco Shoal mentioned in both qualitative and quantitative studies on the epibenthic assemblages of Mesco Reef. Continuous lines indicate Habitat: coralligenous reef the presumed persistence of a species, with thicker lines Depth: 17 to 44 m representing an increase in abundance or frequency and thinner lines a decrease, as perceived by the different authors.

most perceived changes reported between 1985 and 1996

Bathymetric map of Mesco Point rocky outcrops based on Zone: Mesco Shoal multibeam data, with study sites (capital letters). Habitat: coralligenous reef Depth: 17 to 44 m

Gianni Roghi (1927-1967)

Gatti G., Bianchi C.N., Parravicini V., Rovere A., Peirano A., Montefalcone M., Massa F., Morri C., 2015. Ecological change, sliding baselines and the importance of historical data: lessons from combining observational and quantitative data on a temperate reef over 70 years. PLoS ONE, 10 (2): e0118581. Protected areas 3 Historical data 3 Modelling 1 Zone: Mesco Shoal Roghi’s photostations studied by Lucia Rossi, their physical features and the sites to which they have been assigned for the purposes of the Habitat: coralligenous reef present work. For the localisation of the sites see bathymetric map. Depth: 17 to 44 m

Guidetti P., Parravicini V., Morri C., Bianchi C.N., 2014. Against nature? Why ecologists should not diverge from natural history. Vie et milieu - Life and environment, 64 (1): 1-8. Protected areas 3 Historical data 3 Modelling 1 Photographic sampling : a, b) shooting photographs using a rigid spacer Zone: Mesco Shoal and a frame marked in centimetres; c) an example of a photography illustrating a sessile assemblage dominated by Paramuricea clavata . Habitat: coralligenous reef Depth: 17 to 44 m

Selected examples of species whose cover (mean + se) has decreased from 1961 to 2008 (the losers), increased from 1961 to 2008 (the winners), or exhibited major change in the 1990s (the commuters).

Ordination plot on the first three axes (Roman numerals) from Correspondence Analysis of the cover data of the epibenthic assemblages of Mesco Reef, from 1961 to 2008. The upper left panel depicts the plot of all species points (crosses) and photoquadrat points (dots) to show the overall geometry of the ordination model. Details for each site are illustrated separately for the sake of clarity in the subsequent five panels, clockwise: trajectory and species of the assemblage at site B; ditto, site C; ditto, site D; ditto, site F; ditto, site I; ditto, site P; ditto, site S. Codes refer to the name of the species. Gatti G., Bianchi C.N., Parravicini V., Rovere A., Peirano A., Montefalcone M., Massa F., Morri C., 2015. Ecological change, sliding baselines and the importance of historical data: lessons from combining observational and quantitative data on a temperate reef over 70 years. PLoS ONE, 10 (2): e0118581. Protected areas 3 Historical data 3 Modelling 1 Zone: Mesco Shoal Kite diagrams of the change in cover over time of Habitat: coralligenous reef four categories of species: winners, losers, commuters, constants. Depth: 17 to 44 m

COMPOSITIONAL CHANGE

BIOTIC HOMOGENISATION

Pie diagrams of the average cover of the most important species for the periods 1961-1990 and 1996-2008, all sites confounded. Only the species with mean cover higher than 5% are considered, the remaining are grouped within “others”.

Gatti G., Bianchi C.N., Parravicini V., Rovere A., Peirano A., Montefalcone M., Massa F., Morri C., 2015. Ecological change, sliding baselines and the importance of historical data: lessons from combining observational and quantitative data on a temperate reef over 70 years. PLoS ONE, 10 (2): e0118581. Protected areas 3 Historical data 3 Modelling 1 The shift experienced by the epibenthic assemblages of Mesco Reef Zone: Mesco Shoal was probably induced by a combination of seawater warming and local human pressures, the latter mainly resulting in increased water Habitat: coralligenous reef turbidity; in turn, cumulative stress may have favoured the Depth: 17 to 44 m establishment of alien species.

Womersleyella setacea

Caulerpa cylindracea

Plan view map of the Bergeggi marine cave, with indication of the four Zone: Bergeggi sectors investigated (C: chambers; G: gulley; H: hall; L: lakes) and Habitat: marine cave position of the sampling stations in each sector (1 and 2). Depth: 0 to 7 m

Axonometric representation of the submarine cave of Bergeggi, viewed from the sea, to show morpholo- gical complexity.

Parravicini V., Guidetti P., Morri C., Montefalcone M., Donato M., Bianchi C.N., 2010. Consequences of sea water temperature anomalies on a Mediterranean submarine cave ecosystem. Estuarine, Coastal and Shelf Science, 86 (2): 276–282. Protected areas 3 Historical data 4 Modelling 1 Zone: Bergeggi Habitat: marine cave Depth: 0 to 7 m

Upper panels: progress of extension works of Vado Ligure harbour between 1986 and 2013; aerial imagery from Google Earth ®. Lower panels: photos of Cape Vado taken from Bergeggi cave in 1986 and in 2013; arrows indicate an old building (left) and the Vado’s lighthouse (right) to serve as reference points. Change in the pressure regime in the Bergeggi area, 1985 to 2013.

de Falco G., Canessa M. , Montefalcone M., Nepote E., Bavestrello G., Morri C., Bianchi C.N., in press. Multiple stressors, habitat heterogeneity and trajectory of change in a marine cave ecosystem over 27 years. Protected areas 3 Historical data 4 Modelling 1 Zone: Bergeggi Habitat: marine cave Depth: 0 to 7 m

Contour map of the scores obtained by the 1st axis of the PCO analysis on growth forms dataset for the two years investigated. BIOTIC PCO1 explained 63.7% of the total variation. HOMOGENISATION

nMDS ordination plots of station centroids in 1986 and 2004 obtained from growth forms datasets. C: chambers; G: gulley; H: hall; L: lakes. Parravicini V., Guidetti P., Morri C., Montefalcone M., Donato M., Bianchi C.N., 2010. Consequences of sea water temperature anomalies on a Mediterranean submarine cave ecosystem. Estuarine, Coastal and Shelf Science, 86 (2): 276–282. Protected areas 3 Historical data 5 Modelling 1 Zone: Ventimiglia Habitat: marine caves Depth: 0 to 4 m

Progress of the extension works for the Ventimiglia tourist harbour in 2010 (a), 2011 (b), 2012 (c), and 2013 (d). Aerial imagery from Google Earth ®. Locations of the two underwater caves and the main directions followed by littoral drift and Roja river flow are indicated.. Geographic location of the study area with the relative annual wave climate (data from Corsini et al., 2006, modified). HS0 is the mean annual significant offshore wave height (m) recorded by the La Spezia buoy (43°55′41.99″N; 09°49′36.01″E) (a); topography of the Grotta Grande (b) and of the Grotta Piccola (c), redrawn from “Catasto delle Grotte della Liguria DSL/SSI” and with the position of the sampling stations (GG-a to GG-f in the Grotta Grande, GP-a to GP-c in the Grotta Piccola).

Nepote E., Bianchi C.N., Morri C., Ferrari M., Montefalcone M., 2017. Impact of a harbour construction on the benthic community of two shallow marine caves. Marine Pollution Bulletin, 114 (1): 35-45. Protected areas 3 Historical data 5 Modelling 1 Zone: Ventimiglia Habitat: marine caves Depth: 0 to 4 m

Representative photographic samples from Grotta Grande (left) and Grotta Piccola (right) in 2010, 2011 and 2015.

Ecological distance, expressed as mean Euclidean distance (ED) (±se), of the stations GG-a,GG-b, GG-c,GG-d, GG-e, GG-f in the Grotta Grande and GP-a, GP-b and GP-c in the Grotta Piccola.

LESSONS TO BE LEARNT # 2

Regime shift: A large-scale, long-lasting, and normally sudden change in the nature, intensity, and/or frequency of one or more of the factors governing the dynamics of the ecosystem (from Latin regere, to rule, and Old English sciftan, to arrange).

Phase shift: A sharp transition along a process of change in species diversity and abundance, community composition, and/or trophic organization that leaves the ecosystem in a different structural state (from Greek phasis, appearance, and Old English sciftan, to arrange).

Montefalcone M., Parravicini V., Bianchi C.N., 2011. Quantification of coastal ecosystem resilience. In: Treatise on estuarine and coastal science (E. Wolanski & D. S. McLusky, Eds). Elsevier, Waltham: Academic Press, Vol. 10 (Ecohydrology and Restoration): 49–70. Protected areas 3 Historical data 2 Modelling 1

Phase shifts in marine ecosystems

Gallinara Island: a) geographical situation in the Ligurian Sea; b) Digital Elevation Model with main toponyms; c) bathymetric map with survey sites (capital letters)

Bianchi C.N., Cocito S., Diviacco G., Dondi N., Fratangeli F., Montefalcone M., Parravicini V., Rovere A., Sgorbini S., Vacchi M., Morri C., 2017. The park never born: results of a quarter of century of inaction on the seafloor integrity of a proposed but never established Marine Protected Area. Aquatic Conservation: Marine and Freshwater Ecosystems, submitted. Protected areas 3 Historical data 6 Modelling 1 Zone: Gallinara Island Habitat: rocky reefs Depth: 0 to 43 m

Aerial orthophotograph of Gallinara Island on 8 June 2014.

Species accumulation curves (with 95% confidence envelopes) in three years of study, with different sampling effort (number of dives).

1991: sponge reefs 2016: dumping area?

Bianchi C.N., Cocito S., Diviacco G., Dondi N., Fratangeli F., Montefalcone M., Parravicini V., Rovere A., Sgorbini S., Vacchi M., Morri C., in prep. The park never born: results of a quarter of century of inaction on the seafloor integrity of a proposed but never established Marine Protected Area. Protected areas 3 Historical data 6 Modelling 1 Zone: Gallinara Island Habitat: rocky reefs Depth: 0 to 43 m 2016

1991 shallow BIOTIC

HOMOGENISATION Ordination plot on the first two axes from 1991 Correspondence Analysis of epibenthic deep species abundance data of Gallinara Island, from 1991 to 2016. Station points are identified by year/site/depth, species by three-letter codes in italics.

Bianchi C.N., Cocito S., Diviacco G., Dondi N., Fratangeli F., Montefalcone M., Parravicini V., Rovere A., Sgorbini S., Vacchi M., Morri C., 2017. The park never born: results of a quarter of century of inaction on the seafloor integrity of a proposed but never established Marine Protected Area. Aquatic Conservation: Marine and Freshwater Ecosystems, submitted. Protected areas 3 Historical data 7 Modelling 1 Zone: Western Liguria Habitat: seagrass meadows Depth: 2 to 30 m

Location of Western Liguria and delimitation of each sub-area where historical cartographies of Posidonia oceanica meadows were available. VM: Ventimiglia; SR: Sanremo; SS: Santo Stefano al Mare; PM: Porto Maurizio; DM: Diano Marina; LA: Laigueglia; GA: Isola Gallinara; AL: Albenga – Loano; PL: Pietra Ligure; NS: Noli – Spotorno; BE: Isola di Bergeggi; VA: Vado Ligure; SV: Savona; AC: Albissola Marina – Celle Ligure; AR: Arenzano; VE: Genova Vesima

Montefalcone M., Rovere A., Parravicini V., Albertelli G., Morri C., Bianchi C.N., 2013. Evaluating change in seagrass meadows: a time- framed comparison of side-scan sonar maps. Aquatic Botany, 104: 204–212.

Protected areas 3 Historical data 7 Modelling 1 Zone: Western Liguria Habitat: seagrass meadows Depth: 2 to 30 m

Extent in hectares (ha) of the three habitat types in each sub- area of the three cartographies (1990,1991, 2006).

Protected areas 3 Historical data 7 Modelling 1

A fictitious example to show how concordance analysis has been carried out. Let Map 1 and Map 2 depict the same habitat X (e.g., seagrass meadows). Let the two maps be georeferenced and rendered at the same nominal scale. They can then be overlaid to each other and algebraically summed. This procedure allows measuring the extent of the habitat in common to both maps, and concordance can therefore be computed.

Protected areas 3 Historical data 7 Modelling 1 Zone: Western Liguria

Habitat: seagrass meadows Depth: 2 to 30 m

Examples of concordance and discordance Examples of concordance and discordance maps maps for the Posidonia oceanica meadow for the Posidonia oceanica meadow in the sub- areain the of Isolasub- areaGallinara of Isola (GA) .Gallinara (GA).

Protected areas 3 Historical data 7 Modelling 1 Zone: Western Liguria Habitat: seagrass meadows Depth: 2 to 30 m

The largest negative discordances were observed between the maps of 1990 and those of 1991, leading to estimate that in a single year the Posidonia oceanica meadows lost a surface of about 800 ha (i.e. about 25%), which is hardly credible in absence of any large- scale environmental catastrophe. The large discrepancies between the maps of 1990 and 1991 are likely due to human errors, depending on the difficulty of interpreting sonograms where the habitat type showed a limited extent and a complex shape.

Protected areas 3 Historical data 7 Modelling 1 Zone: Western Liguria Habitat: seagrass meadows Depth: 2 to 30 m

Protected areas 4 Historical data 1 Modelling 1

Historical data

• heterogeneous data quality • change in technology with time • different sampling designs • difference between observers Protected areas 3 Historical data 3 Modelling 1 Protected areas 3 Historical data 3 Modelling 1 Zone: Prelo (Liguria) Habitat: seagrass meadows Depth: 0 to 18 m

The jetty built in Prelo cove at the beginning of the 20th century for pleasure crafts. Lasagne R., Montefalcone M., Albertelli G., Corrode N., Ferrari M., Morri C., Bianchi C.N., 2011. Much damage for little advantage: field studies and morphodynamic modelling highlighted the environmental impact of an apparently small coastal mismanagement. Estuarine, Coastal and Shelf Science, 94: 255-262. Protected areas 3 Historical data 3 Modelling 1 a) The shadow zone originated by the southern headland in Prelo Zone: Prelo (Liguria) cove; b) Simulation of the transitional circulation with weak backwash flows occurring in the whole embayed cove before the Habitat: seagrass meadows jetty construction; c) Present situation of Prelo with a transitional Depth: 0 to 18 m circulation in the southern artificial sub-cove and a cellular circulation with occurrence of rip-currents in the northern artificial sub-coves.

Lasagne R., Montefalcone M., Albertelli G., Corrode N., Ferrari M., Morri C., Bianchi C.N., 2011. Much damage for little advantage: field studies and morphodynamic modelling highlighted the environmental impact of an apparently small coastal mismanagement. Estuarine, Coastal and Shelf Science, 94: 255-262. Protected areas 3 Historical data 3 Modelling 1 Zone: Prelo (Liguria) Habitat: seagrass meadows Depth: 0 to 18 m b) Map of the sedimentological features of Prelo cove (A = very coarse sand; B = coarse and medium sand; C = fine and very fine sand)

a) Map of the Posidonia oceanica meadow c) Map of the morphology sediment transport vectors

Lasagne R., Montefalcone M., Albertelli G., Corrode N., Ferrari M., Morri C., Bianchi C.N., 2011. Much damage for little advantage: field studies and morphodynamic modelling highlighted the environmental impact of an apparently small coastal mismanagement. Estuarine, Coastal and Shelf Science, 94: 255-262. Protected areas 3 Historical data 3 Modelling 2 Zone: Liguria Habitat: seagrass meadows Depth: 2 to 7 m Breaking limit Closure depth

Vacchi M., Montefalcone M., Bianchi C. N., Morri C., Ferrari M., 2010. The influence of coastal dynamics on the upper limit of the Posidonia oceanica meadow. Marine Ecology, 31 (4): 546-554. Protected areas 3 Historical data 3 Modelling 2 Zone: Liguria Habitat: seagrass meadows Depth: 2 to 7 m Breaking limit 1 Closure depth

Vacchi M., Montefalcone M., Bianchi C. N., Morri C., Ferrari M., 2010. The influence of coastal dynamics on the upper limit of the Posidonia oceanica meadow. Marine Ecology, 31 (4): 546-554. Protected areas 3 Historical data 3 Modelling 2 Zone: Liguria Study areas along the Ligurian coastline Habitat: seagrass meadows Depth: 2 to 7 m

Black dots = 10 Posidonia oceanica meadows investigated White dots = 4 meadows where the predictive model was tested (T).

Vacchi M., Montefalcone M., Schiaffino C.F., Parravicini V., Bianchi C.N. , Morri C., Ferrari M., 2014. Towards a predictive model to assess the natural position of the Posidonia oceanica seagrass meadows upper limit. Marine Pollution Bulletin, 83: 458-466. Protected areas 3 Historical data 3 Modelling 2 Zone: Liguria Habitat: seagrass meadows Depth: 2 to 7 m

Morphodynamic domains R = reflective I = intermediate D = dissipative

Mean values (± se) of the distance of the meadow upper limit in the three morphodynamic domains. ** P <0.01, * P <0.05.

Vacchi M., Montefalcone M., Bianchi C.N., Morri C., Ferrari M., 2010. The influence of coastal dynamics on the upper limit of the Posidonia oceanica meadow. Marine Ecology, 31 (4): 546-554. Protected areas 3 Historical data 3 Modelling 2 Zone: Liguria Habitat: seagrass meadows Depth: 2 to 7 m

Polynomial model between the linear distance

κobs and the morphodynamic domain (expressed by the surf scaling index ε). CV–R2 is the cross-validated R2 value estimated by the 10-fold procedure. Grey dotted lines represent the fits of the individual ten folds used for cross-validation.

Results of the predictive model in the 4 test areas. White squares Zone: Liguria indicate the breaking depth position, whereas dashed lines define the Habitat: seagrass meadows two boundaries (κmin and κmax) of the predicted reference condition zone (pale grey). The white-striped portion of the seafloor represents Depth: 2 to 7 m the quantitative assessment of the upper limit regression in the areas affected by high human pressures.

Montefalcone M., Misson G., Vacchi,M. Archetti R., Bianchi C.N., Pergent G., Ardizzone G., Criscoli A., Astruch P., Fernàndez- Torquemada Y., Luzzo F., Ferrari M., in prep. A geospatial approach to predict the reference condition of the Posidonia oceanica meadow upper limit. Protected areas 3 Historical data 3 Modelling 3 Zone: Liguria Habitat: seagrass meadows Depth: 21 to 35 m

Location of the 26 coastal areas investigated along the Ligurian coastline, with the relative annual wave climate.

H0 is the significant offshore wave height (m) recorded by the La Spezia buoy (4355041.9900 N; 0949036.0100 E).

Vacchi M., Montefalcone M., Bianchi C.N., Morri C., Ferrari M., 2012. Hydrodynamic constraints to the seaward development of Posidonia oceanica meadows. Estuarine, Coastal and Shelf Science, 97: 58-65.

Protected areas 3 Historical data 3 Modelling 3 Zone: Mean depth ( sd) of Liguria the meadow lower Habitat: seagrass meadows limits according to wave exposure. Most Depth: 21 to 35 m intense waves from SW, least intense waves from S and SE. The explicative case of the Portofino ** = very significant headland: depth of the lower limits of the difference (p < 0.001). Posidonia oceanica meadows.

Protected areas 3 Historical data 3 Modelling 3

A schematic representation of the hydrodynamic constrains to the Zone: Liguria Posidonia oceanica meadow development. L0 is the annual Habitat: seagrass meadows offshore wave length. MLLW is the mean lower low water and MHHW is the mean higher high water. Depth: 21 to 35 m

Protected areas 3 Historical data 3 Modelling 3 Zone: Liguria Habitat: seagrass meadows Depth: 21 to 35 m Depth of the lower limit of Posidonia oceanica meadows. -1.07 Light (Duarte, 1991): Zc = 1.297 · K where Zc is the meadow lower limit (in meters) and K is the coefficient of light attenuation underwater.

Water movement (Vacchi et al., 2012): Zc = 0.32· L0 + 5.62 where Zc is the depth of meadow lower limit (in meters), and L0 is the offshore wave length (in meters), computed as a climatological mean. The shallower of the two resulting values is the likely baseline for the depth of the meadow lower limit in “natural” condition.

Protected areas 3 Historical data 3 Modelling 4 Zone: Liguria Spatial extent of Posidonia oceanica meadows between two Habitat: seagrass meadows hydrodynamic boundaries (the wave break limit and the annual storm wave base), as expected to occur under natural conditions. Depth: 2 to 35 m

Vacchi M., Montefalcone M., Parravicini V., Rovere A., Vassallo P., Ferrari M., Morri C., Bianchi C.N., 2014. Spatial models to support the management of coastal marine ecosystems: a short review of best practices in Liguria, Italy. Mediterranean Marine Science, 15 (1): 189-197. Protected areas 3 Historical data 3 Modelling 4 Zone: Liguria Habitat: seagrass meadows Depth: 2 to 35 m

Examples of the application of the predictive models in Liguria. Extents of Posidonia oceanica and Cymodocea nodosa meadows are taken from Diviacco and Coppo (2009). On maps are represented kmin and kmax, which encompass the seafloor region where the predicted upper limit is located, and the two predicted lower limits controlled by water movement and by light, respectively.

Burgos E., Montefalcone M., Ferrari M., Paoli C., Vassallo P., Morri C., Bianchi C.N., 2017. Ecosystem functions and economic wealth: trajectories of change in seagrass meadows. Journal of Cleaner Production, JCLEPRO-D-17-02796 Protected areas 4 Historical data 1 Modelling 1

Modelling

• conceptual difficulties • identification of the descriptor • idiosyncrasy of ecological assemblages Protected areas 4 Historical data + Modelling 1 Zone: Bergeggi Habitat: seagrass meadows Depth: ~ 7 m

Paoli C., Morten A., Bianchi C.N., Morri C., Fabiano M., Vassallo P., 2016. Capturing ecological complexity: OCI, a novel combination of ecological indices as applied to benthic marine habitats. Ecological Indicators, 66: 86-102. Protected areas 4 Historical data + Modelling 1 Posidonia oceanica meadow of Bergeggi Zone: Bergeggi Change in the position of the upper limit Habitat: seagrass meadows Depth: ~ 7 m

κmin

κmax upper limit distance (m) distance limit upper

Survey records

Oprandi A., Montefalcone M., Ferrari M., Morri C., Bianchi C.N. , 2014. Spreading of the alien green alga Caulerpa racemosa and phase shift within the Posidonia oceanica seagrass meadow of Bergeggi. Biologia Marina Mediterranea, 21 (1): 75-78. Protected areas 4 Historical data + Modelling 1 Posidonia oceanica meadow of Bergeggi Zone: Bergeggi Change in the position of the upper limit Habitat: seagrass meadows Depth: ~ 7 m

Morphodynamic modelling

κmin

κmax upper limit distance (m) distance limit upper

Survey records

Morphodynamic modelling

κmin

κmax upper limit distance (m) distance limit upper

Last decades trend Survey records

Morphodynamic modelling

κmin

κmax upper limit distance (m) distance limit upper

MPA Last decades trend Survey records

Oprandi A., Montefalcone M., Ferrari M., Morri C., Bianchi C.N. , 2014. Spreading of the alien green alga Caulerpa racemosa and phase shift within the Posidonia oceanica seagrass meadow of Bergeggi. Biologia Marina Mediterranea, 21 (1): 75-78. Protected areas 4 Historical data + Modelling 2 Zone: Liguria Habitat: seagrass meadows Depth: ~0 to 36 m

Temporal trend of Posidonia oceanica meadow extent in Liguria, combining modelling, estimations, and quantitative cartographic measurements. The second-grade polynomial represents the best fit of the data.

Temporal trend of the value added of tertiary sector in Zone: Liguria Liguria and of the ecosystem services provided by Habitat: seagrass meadows Posidonia oceanica meadows. Depth: ~0 to 36 m

Temporal trend of the seagrass meadow extent (total, Posidonia oceanica and Cymodocea nodosa) in Liguria (a) and of the percentage of beaches, rocky coasts and artificial structures characterizing the Ligurian coastline (b). In panel a, open symbols indicate estimations, solid symbols measurements from maps.

1987 1992

2009

2012

Posidonia oceanica Cymodocea nodosa Caulerpa cylindracea 2004 dead matte sand

LESSONS TO BE LEARNT # 3

Hysteresis: The path dependence of the state of the ecosystem on its previous history, generally in the form of a lagging of the effect when the cause has ceased or diminished in intensity (from Greek husterein, to be behind). Schematic representation of an ecosystem as a river where the water is constantly moving between the edges of the river. The flow of the water along the bed of the river (the basin of attraction) represents the state of the ecosystem in relationship to ecological variables. Affectors erode resilience of ecosystem (dotted lines), thus causing the ecosystem to shift into alterative states. The path in (a) may be predicted knowing change in affectors’ regime; path in (b) envisages the invasion by alien species and has thus elements of stochasticity implying unpredictability.

Historical Current Direction / baseline baseline trend ? ? ? Protected Areas in the Mediterranean Sharing expertise for effective conservation Malta, 11-14 September 2017 Thank you for your attention

This presentation is a synthesis of the ongoing research of the Seascape Ecology team: Carlo Nike Bianchi, Marco Ferrari, Giulia Gatti, Monica Montefalcone, Carla Morri, Alice Oprandi, Chiara Paoli, Valeriano Parravicini, Alessio Rovere, Matteo Vacchi, Paolo Vassallo.