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EDITORIAL BOARD José M.N. Azevedo, Faculty of Science and Technology, University of the Azores, Ponta Delgada, Azores; Paulo A.V. Borges, Azorean Biodiversity Group, University of the Azores, Angra do Heroísmo, Azores; João M.A. Gonçalves, Faculty of Science and Technology, University of the Azores, Horta, Azores; Louise Allcock, National University of Ireland, Galway, Ireland; Joël Bried, Cabinet vétérinaire, Biarritz, France; João Canning Clode, MARE - Marine and Environmental Sciences Centre, ARDITI, ; Martin A. Collins, British Antarctic Survey, Cambridge, UK; Charles H.J.M. Fransen, Naturalis Biodiversity Center, Leiden, Netherlands, Suzanne Fredericq, Louisiana University at Lafayette, Louisiana, USA; Tony Pitcher, University of British Colombia Fisheries Center, Vancouver, Canada; Hanno Schaefer, Munich Technical University, Munich, Germany.

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Arquipelago - Life and Marine Sciences ISSN: 0873-4704

Bryophytes of Azorean parks and gardens (I): “Reserva Florestal de Recreio do Pinhal da Paz” - São Miguel Island

CLARA POLAINO-MARTIN, ROSALINA GABRIEL, PAULO A.V. BORGES, RICARDO CRUZ

AND ISABEL S. ALBERGARIA

Polaino-Martin, C.P., R. Gabriel, P.A.V. Borges, R. Cruz and I.S. Albergaria 2020. Bryophytes of Azorean parks and gardens (I): “Reserva Florestal de Recreio do Pinhal da Paz” - São Miguel Island. Arquipelago. Life and Marine Sciences 37: 1 – 20. https://doi.org/10.25752/arq.23643

Historic urban parks and gardens are increasingly being considered as interesting refuges for a great number of , including some rare taxa, otherwise almost absent from urban areas, such as many bryophytes and other biota that are not their main focus. After a bibliographic work, the "Reserva Florestal de Recreio do Pinhal da Paz" (RFR-PP), in São Miguel Island (Azores), stood out as one of the least studied areas of the region, without any bryophyte’ references. Thus, the aim of this study was to identify the most striking bryophyte species present along the main visitation track of RFR-PP, in order to increase its biodiversity knowledge. Bryophytes growing on rocks, soil or tree bark were collected ad- hoc, in 17 sites, ca. 100 m apart from each other. In total, 43 species were identified: 23 mosses, 19 liverworts, and one hornwort, encompassing five classes, 15 orders and 27 families. Seven species are endemic from Europe and three from . No invasive bryophytes were found in the surveyed area. These results update the distribution data of São Miguel Island, show that Azorean parks and gardens contribute to the community dynamics of bryophytes at lower elevation and add a new layer of interest to the visitors of RFR-PP.

Key words: Parks & Gardens, Mosses, Liverworts, Hornworts, Macaronesian endemic species, Azores.

Clara P. Martin1 (e-mail: [email protected]), R. Gabriel1, P.A.V. Borges1, R. Cruz2 and I.S. Albergaria2. 1cE3c/ABG – Centre for Ecology, Evolution and Environmental Changes / Azorean Biodiversity Group and University of the Azores, FCAA - Faculty of Agriculture and Environment, Rua Capitão João d’Ávila, sn. 9700-042 Angra do Heroísmo, Portugal. 2CHAM – Centro de Humanidades e Universidade dos Açores, FCSH - Faculty of Social Sciences and Humanities, Rua da Mãe de Deus, 9500-321 Ponta Delgada, Portugal.

INTRODUCTION serve as nodes on a network of natural populations for species occurring in several land- The Urban gardens and recreational parks are uses (Cardoso et al. 2009; Roberts et al. 2007; well known for their contribution to ecosystem Goddard et al. 2009; Mexia et al. 2018). Besides, services. These areas protect the soil against parks and gardens are especially important for erosion, increase water infiltration, mitigate the their cultural and recreational services urban heat island effect, improve air quality – (Sasidharan et al. 2005; Voigt et al. 2014). absorbing carbon from the atmosphere, act In the Azores, urban gardens and parks ashabitat for endemic and native species, and constitute an important heritage due both to their

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biological, geological and hydrological interest, mostly included in the natural parks of the and to their historical, biogeographical and Azores. Presently near 500 taxa of bryophytes are landscape importance (Albergaria 2005; Castel- known from the Azores (Gabriel et al. 2010; Branco & Albergaria 2017). Since the XV Gabriel et al. 2011), including 53 considered of century, Azorean native ecosystems have suffered conservation concern in Europe (Hodgetts et al. major land-use alterations and degradation, with 2019). Bryophyte species perform important large areas of native vegetation, especially native ecosystem services, being engaged in water forests, claimed for urban settlements, agriculture retention, minerals recycling, and organic matter and forestry (Gaspar et al. 2008; Borges et al. decomposition, while protecting and occupying 2019). Parks and gardens, especially those different substrates, many as pioneer species (e.g. occurring at lower elevations, may constitute Porley & Hodgetts 2005). alternative habitats for different biota. Nevertheless, there is still a general lack of Azorean parks and gardens, including a high information about the bryophyte communities number and cover of tree species and particular present in recreational parks and gardens, which ecological conditions, may thus serve as refuge may be potential refuges of native biodiversity. for different taxa, as occurs in different regions Since the first publication in 1937 (Silveira 1937), and countries (Aleffi 2015, 2017). Similarly to which refer to the collections of Pierre and many other parks and gardens, the vast Valentine Allorge and Hermann Persson, other majority of ornamental vascular plant species information followed (e.g. Allorge & Allorge, used in Macaronesia are exotic, introduced 1950, 1952; Hübschmann 1974; Sérgio 1991; originally from different archipelagos and Claro 2008), but publications have been few and continents (e.g. Quintal 2007). More recently, far apart, with no systematic collection of indigenous (native and endemic) species are specimens. In fact, among the vast bryological being used in Azorean gardens, such as the literature of the Azorean Islands (cf. Gabriel et al. “Faial Botanic Garden” or the recent extension 2011), only 25 works mention these habitats for of “Duque da Terceira Garden”, likewise what three islands (São Miguel, Terceira and São is observed in other parts of Europe (e.g. Zerbe Jorge). et al. 2003). Notwithstanding the high number The Recreation Forest Reserve "Pinhal da Paz" of exotic species that constitute the core of (RFR-PP) (Ponta Delgada county, São Miguel most Azorean parks and gardens (e.g. Bogas Island) is a good example of the lack of 2003; Albergaria 2005), and their role as knowledge regarding bryophytes. Although it has sources of invasive species (e.g. Silva et al. been studied in terms of economic value (Pacheco 2008; Gabriel 2019), native species do occur in 2012), and the biodiversity of vascular plants these areas – namely lichens, bryophytes, (Tavares 2016), the richness of other taxonomic invertebrates (e.g. Pérez Santa-Rita et al. 2018) groups had never been considered. and birds, all contributing to the ecosystem The aims of this paper are: i) to start a functioning. systematic documentation through taxonomic Among these particular groups, bryophytes are identification of the bryophytes present in the probably the most striking in area of occupation Recreation Forest Reserve "Pinhal da Paz", and to and one of the richest in number of native species, analyse their main biogeographic affinities, life contributing to the unique landscape of Azorean strategies, and life and growth forms; ii) to start a gardens. In fact, the particular climatic and series of publications aiming to document the geographic conditions of these islands, promote bryological diversity of historic and recreational the presence and conservation of a considerable parks and gardens in the Azores. This diversity of bryophyte species and communities. characterization is of value as bryophytes are In 1995, the European Committee for the important components of these systems, which Conservation of Bryophytes identified in this are under threat due to the effects of climate archipelago six, out of 60, European Areas of change, increasing urbanization and general Special Interest for Bryophytes (ECCB 1995), biodiversity loss.

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MATERIALS AND METHODS Recreio” by the Regional Legislative Decree no. 15/2000 of June 21. It is located in the Study area municipality of Fajã de Cima, in Ponta Delgada The Recreational Forest Reserve “Pinhal da Paz” council (São Miguel Island, Azores, Portugal) (RFR-PP) is a public forest park classified as a (37º 47 '10 .126 '' N; -25º 38 '24.129'' W), recreational reserve “Reserva Florestal de between 240 m and 330 m a.s.l. (Figures 1 and 2).

Fig. 1. Azores archipelago in the North Atlantic .

Fig. 2. Location of the Recreational Forest Reserve “Pinhal da Paz” in São Miguel Island (Azores).

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Formerly a private property, this 49 ha Recreation year, mostly during the summer months (Pacheco Forest Reserve was acquired by the Regional 2012). Government of the Azores in 1982. Before The average temperature of the Recreation opening to the public, the Forest Services of Forest Reserve is mild, ranging from 14º C Ponta Delgada proceeded to several works of (minimum) to 25º C (maximum) throughout the maintenance and cleaning of roads, management year, but air humidity is high (80% of the forested area and general landscaping, thus approximately), and the average precipitation per creating a central lawn, a playground for children year is of 1930 mm, with an evapotranspiration of and a snack area (Figure 3). The number of 580 mm (DROTRH & SRA 2001). visitors of “Pinhal da Paz” exceeds 100 000 per The vascular plants of RFR-PP includes plenty of

Fig. 3. View of the central lawn in RFR-PP (Photo by PB). exotic species, planted mainly with ornamental brevifolia, Picconia azorica and Erica azorica purposes. Among them there are shrubs such as may be observed among the dominant exotic hydrangeas (Hydrangea macrophylla), azaleas species (Tavares 2016). (Rhododendron indicum), camellias (Camellia japonica), different palm species (e.g. Field work Washingtonia robusta, Archontophoenix The sampling of bryophytes at the Recreational cunninghamiana), and other trees as eucalyptus Forest Reserve of “Pinhal da Paz” took place on (Eucalyptus robusta), acacias (Acacia the 2nd June 2018. The authors RG, PAVB and melanoxylon), pines (Pinus pinea, P. pinaster), RC collected 17 samples of ca. 10 cm x 5 cm, ca. and cedars (Cryptomeria japonica, Cupressus 100 m apart from each other, along one of the sempervirens, Chamaecyparis lawsoniana) most common paths for those visiting the Park (Tavares 2016). A few Azorean or Macaronesian (cf. Figure 4). endemic species such as Morella faya, Juniperus The substrates sampled were mostly rock and

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Fig. 3. Map of “Reserva Florestal de Recreio do Pinhal da Paz”, São Miguel Island (Azores). The park has an area of 49 ha and lies from 240 – 330 m a.s.l.. Red dots represent the 17 sampling points. soil, but also the bark of trees and shrubs such as CP and RG using identification guides and Persea indica, Acacia melanoxylon and Erica floras, namely Paton (1999), Schumacker & azorica were studied (cf. Table 1). The samples Váňa (2005) and Casas et al. (2009) for were kept in paper bags and dried at room hornworts and liverworts and Casas et al. temperature, in a dark atmosphere, at the Ecology (2006), Homem & Gabriel (2008) and Smith Laboratory of the Faculty of Agrarian and (2004) for mosses. The nomenclature followed Environmental Sciences, University of the Azores Hodgetts (2015) for mosses and Söderström et (FCAA-UAz, Angra do Heroísmo, Terceira al. (2016) for liverworts. Island). The specimens are kept at the Cryptogamic Collection of the Herbarium of the University Laboratory work of Azores (AZU, FCAA-UAz). All samples were identified to the species level by

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Table 1. Short description of the collection points along the trail in RPP (June 2018).

Substrate Inclination Distance Altitude Coordinates (º) from soil (m) (cm) PP-01 Soil – border of the path 10º 0 261 37.786869, -25.639527 PP-02 Rock on soil 40º 10 262 37.787406, -25.639128 PP-03 Soil – border of the path 10º 0 266 37.787499, -25.638589 PP-04 Soil – slope of the path 75º 0 268 37.787649, -25.637973 PP-05 Soil – slope of the path 75º 0 266 37.787607, -25.638499 PP-06 Dicot stump 50º 20 266 37.787738, -25.637643 PP-07 Soil – border of the path 10º 0 272 37.788784, -25.636595 PP-08 Persea indica - bark 90º 100 274 37.788546, -25.636784 PP-09 Soil – border of the path 10º 0 274 37.789113, -25.636566 PP-10 Acacia melanoxylon – bark 90º 100 278 37.789546, -25.636653 PP-11 Pittosporum undulatum – 90º 20 281 37.789956, -25.635952 dead trunk PP-12a Erica azorica – bark 90º 40 279 37.790070, -25.635550 PP-12b Rock on soil 70º 10 279 37.790070, -25.635550 PP-13 Soil – slope of the path 75º 0 281 37.790093, -25.635816 PP-14 Soil – border of the path 10º 0 292 37.790162, -25.634399 PP-15 Soil – border of the path 10º 0 305 37.788472, -25.630667 PP-16 Rock wall 90º 60 305 37.788472, -25.630667 PP-17 Dicot stump 50º 20 305 37.788366, -25.630507

Analysis The chorological data and the life strategies, Henriques et al. 2017). The IUCN category was growth and life forms follows the BRYOTRAIT- assigned based on the recent European Red List AZO database (Henriques et al. 2017), a (Hodgetts et al., 2019). comprehensive trait dataset for the Azorean To evaluate the completeness of the collection, bryoflora. The BRYOLAT-AZO summarizes we calculated the projected number of species information coming from different sources: using the first-order Jackknife species richness namely, geographic information regarding biomes estimator, which calculates the relationship and Eastern limit categories were attributed based between the number of species and the number of on the work of Hill & Preston (1998); life species found in one sample (SDR-IV, 2019). strategies were used as proposed by During (1979), and life forms by Bates (1998). An ecological analysis was performed using the RESULTS Ellenberg indicator values for moisture, light and soil reaction to the substrate. These ecological Floristics and diversity indicator values have been assigned to bryophytes The investigated area presented a total number of by Düll (1992), and later updated and validated 43 bryophyte species (cf. Table 2; Annex 1), by some authors (Dierßen 2002; Hill et al. 2007; including 23 mosses (Division Bryophyta), 19

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Bryophytes of Azorean parks and gardens (I) liverworts (Division Marchantiophyta), and a Considering the first-order Jackknife estimator, single species of hornwort (Division the number of identified species is not complete, Anthocerothophyta) (Plate 1), exhibiting a high and there is a projected value of 65 species for the ratio of liverworts + hornworts / mosses (0,87). area, with a rate of completeness of 66,5%. Table 2. and number of bryophyte records (N) collected at the Recreational Forest Reserve “Pinhal da Paz” in June 2018. Division Class Order Family Species N Bryophyta Bryopsida Bartramiales Bartramiaceae Philonotis rigida 1 Bryales Bryaceae Anomobryum julaceum 1 Ptychostomum capillare 1 Dicranales Ditrichaceae Ceratodon purpureus 1 Fissidentaceae Fissidens asplenoides 3 Fissidens taxifolius 3 Leucobryaceae Campylopus pilifer 2 Rhabdoweisiaceae Dicranoweisia crispula 1 Grimmiales Ptychomitriaceae Ptychomitrium nigrescens 1 Hookeriales Leucomiaceae Tetrastichium virens 4 Hypnales Amblystegiaceae Amblystegium confervoides 1 Amblystegium serpens 1 Brachytheciaceae Brachythecium velutinum 1 Kindbergia praelonga 6 Hypnaceae Andoa berthelotiana 8 Hypnum jutlandicum 2 Hypnum uncinulatum 1 Sematophyllaceae Sematophyllum 3 substrumulosum Orthotrichales Orthotrichaceae Zygodon rupestris 1 Pottiales Pottiaceae Tortella nitida 1 Trichostomum 3 brachydontium Polytrichopsida Polytrichales Polytrichaceae Atrichum angustatum 1 Polytrichum juniperinum 1 Marchantiophyta Marchantiopsida Lunulariales Lunulariaceae Lunularia cruciata 3 Marchantiales Aytoniaceae Reboulia hemisphaerica 1 Jungermanniopsida Jungermanniales Calypogeiaceae Calypogeia fissa 2 Geocalycaceae Saccogyna viticulosa 2 Lophocoleaceae Lophocolea bidentata 7 Lophocolea fragans 2

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Division Class Order Family Species N Lophocolea heterophylla 2 Metzgeriales Metzgeriaceae Metzgeria furcata 1 Aneuraceae Riccardia multifidia 2 Porellales Frullaniaceae Frullania acicularis 2 Frullania azorica 1 Frullania microphylla 1 Lejeuneaceae Harpalejeunea molleri 4 Lejeunea lamacerina 9 Cololejeunea azorica 1 Drepanolejeunea 1 hamatifolia Porellaceae Porella canariensis 1 Radulaceae Radula aquilegia 1 Radula wichurae 4 Anthocerotophyta Anthocerotopsida Anthocerotales Anthocerotaceae Anthoceros caucasicus 1

Mosses are represented by two classes, nine Four species were collected more than five orders and 14 families, while, liverworts are times, two pleurocarpous mosses (Andoa represented by two classes, five orders and 11 berthelotiana [Plate 1c,d]; Kindbergia praelonga) families. About one third of the moss species and two leafy liverworts (Lejeunea lamacerina; belong to the Hypnales (8 spp.; 34,8%), including Lophocolea bidentata). three species from the Family Hypnaceae. More It is quite striking that three of the five species than half of the liverwort species belong to the of the Frullania referred to the Azores Porellales (10 spp.; 52,6%), including four archipelago may be found in this area, including species belonging to Lejeuneaceae (Table 2). the recently described F. acicularis (Figure 5).

Fig. 4. The leafy liverwort Frullania acicularis recently described for the Azores; a) ventral view of a shoot, with lobules sac-shaped, underleaves not decurrent and rhizoids at the base of an underleaf (magnification 10 x 10);b) apex of the lobe, with the long needle like leaf apices characteristic of the species (magnification 10 x 40) (Photos by RG). 8

Bryophytes of Azorean parks and gardens (I)

Biogeography Boreo-arctic Montane, Wide boreal, Boreal- The taxa found in RFR-PP belong to seven of the Montante, Temperate, Southern-temperate and nine biomes described by Hill & Preston (1998): Mediterranean-Atlantic (Figure 6).

Fig. 5. Distribution of bryophytes from “Reserva Florestal de Recreio Pinhal da Paz” according to their geographic affinities. (a, Anthocerotophyta; h, Marchantiophyta; m, Bryophyta).

Most of the bryophytes present in this However, none of the Azorean endemic recreational park have their main distribution area bryophyte species was found in the area at this in temperate and southern-temperate biomes. time. Among the southern-temperate bryophytes, there A few moss species whose distribution are species with a relatively restricted geographic centre is on Northern biomes are also distribution, including the hornwort Anthoceros represented in RFR-PP, namely the wide-boreal caucasicus, three leafy liverworts (Frullania species Ceratodon purpureus and Polytrichum azorica, F. microphylla, Porella canariensis), an juniperinum (Plate 1a). acrocarpous moss (Ptychomitrium nigrescens) Considering the Eastern limit of distribution and two pleurocarpous mosses (Hypnum in Eurasia, which corresponds quite closely uncinulatum, Sematophyllum substrumulosum). with a scale of continentality, it is clear that the Besides, three Macaronesian endemic species are large majority of liverworts and most mosses present in the area: one liverwort (Radula have oceanic distributions (including wichurae) and two pleurocarpous mosses (Andoa hyperoceanic, oceanic and suboceanic) (Figure berthelotiana and Tetrastichium virens). 7).

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Fig. 6. Distribution of bryophytes from “Reserva Florestal de Recreio Pinhal da Paz” according to their Eastern limit of occurrence in Eurasia. (a, Anthocerotophyta; h, Marchantiophyta; m, Bryophyta).

Notwithstanding, almost a quarter of the with regard to light (Figure 8c), it is observed that represented species in RFR-PP have circumpolar sciophytic species (EV: 1-5) predominate in the distributions, namely the liverwort Reboulia Park, reaching 62,8% of the total flora, followed hemisphaerica and the epiphytic moss Zygodon by the photo-sciophytic (EV: 6-7; 25,6%) species. rupestris. Photophytic species (EV: 8-9; 11,6%) include four mosses (e.g. Tortella nitida, Trichostomum Ecology brachydontium) and the single hornwort found in Bryophytes of RFR-PP comprise species of four the RFR-PP at this time. major life-forms (Figure 8a) – turfs, cushions, Regarding water availability (Figure 8d), mats and wefts. All liverworts form mats (Plate unsurprisingly in the Azores, about half of the 1e), which is the second largest category for bryophytes are hygrophytic (Figure 8d) (EV: 7-9; mosses. The pleurocarpous moss Kindbergia 25,6%) and meso-hygrophytic (EV: 6; 25,6%), praelonga is the only specie collected in the area while xerophytic species (EV: 1-3; 7,0%) are a that forms wefts. minority (e.g. Campylopus pilifer). With respect to life strategy (Figure 8b), more About two thirds of the species (69,8%) occur than half of the species include plants with long in acidic soils/substrates and although half of the potential life spans and with low reproduction moss species are from basic soils/substrates (EV: effort (long-lived shuttle, perennial stayer and 6-9), only three liverworts are characteristic such stress-tolerant perennials), especially among the basic substrate, including the common thallose liverworts (73,7%) (e.g. Lejeunea lamacerina and species Reboulia hemisphaerica, and Lunularia Radula wichurae (Plate 1f). Eight mosses species cruciata (Figure 8e). exhibit a colonist strategy, frequent in the Three environmental parameters, productivity acrocarpous species (e.g. Anomobryum julaceum, values (related to nitrogen requirement) (Figure Ceratodon purpureus, Zygodon rupestris). 8f), salt and heavy-metal tolerance (Figures 8g, Considering the Ellenberg indicator values (EV) 8h), show that these species occupy mostly

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Fig. 8. Information on ecological variables regarding the 43 bryophyte species (one hornwort [a], 19 liverworts [h] and 23 mosses [m] found in RFR-PP during June, 2018. From left to right and top to bottom it is possible to check the spectrum for Life form, Life Strategy, and the Ellenberg indicator values for Light, Moisture, Reaction, Productivity and Salt and Heavy-metal tolerance. Further details in text.

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oligotrophic, not-polluted’ sites. In fact, seven berthelotiana, Kindbergia praelonga), but also liverworts and six moss species are only able to because bryophytes cover relatively large areas, grow on sites where the nitrogen concentration is on tree trunks and shrubs but also on soil and low, while species indicating rich, fertile places rocks. (with high nitrogen concentration values) (e.g. The analysis of the ecological indicator Lunularia cruciata) are quite scarce in the Park. values reveals a community of bryophytes Furthermore, only a few species collected in mainly sciophytic, hygrophytic, acidophytic, RFR-PP are able to tolerate saline or heavy- adapted to low nitrogen concentration and metal conditions; one of the most striking intolerant to salt and heavy-metals. These examples is the acrocarpous moss characteristics are to be expected from low Trichostomum brachydontium, often found in intervention areas and constitute a baseline coastal areas. upon which further environmental change will be assessed by comparing these results with Conservation concern species those coming from future studies in the area. Most of the bryophyte species found in RFR-PP The presence of exotic species and anthropic (n=34; 79,1%) are included in the Least Concern habitats that dominate the area is expected to IUCN category (Hodgetts et al., 2019). However, alter habitat conditions and is likely to reduce this park can be considered a refuge for three biodiversity (Gabriel 2019). In fact, the number Vulnerable mosses (Andoa berthelotiana, of bryophyte species found in this environment Atrichum angustatum and Philonotis rigida) and is relatively low when compared with other, one liverwort (Cololejeunea azorica), as well as more natural ecosystems, such as native forests for three Near Threatened species (the liverworts at similar elevation (e.g. Sjögren 1978; Gabriel Frullania acicularis, Radula wichurae and the & Bates 2005), but further samplings should be moss Tetrastichium virens). made in order to elevate the completeness level of the sampling (66,5%). Notwithstanding, the richness of species, particularly liverworts (19 DISCUSSION AND CONCLUSION species), is still remarkable and similar to those found in larger areas, such as Castel Gandolfo Parks and gardens are generally considered safe (Vatican State), from where 15 liverwort areas for many bryophytes (e.g. Glime 2007) but species were recently recorded (Aleffi 2017). these habitats have not been extensively studied. Considering that island ecosystems are The Azores archipelago, well-known for its high particularly sensitive to environmental impacts, diversity of bryophyte species, is exemplary: no such as climate change (Patiño et al., 2016), the previous systematic collection of bryophytes had introduction of exotic species (Silva et al. been made before the start of the project “Green 2008), and increasing urbanization and Gardens Azores” in 2015, while vascular plant associated fragmentation of ecosystems species were at least enumerated for most of (Borges et al. 2019), recreational parks and them. gardens may indeed play a decisive role to In particular, no bryophyte species had ever preserve bryophytes in the Azores, reinforcing been reported from the Recreational Forest the importance of urban greenery as refuge for Reserve “Pinhal da Paz”, and with this study it native species. The present study is a first was possible to identify a large number of taxa. contribution to the knowledge of the bryoflora The gathered information represents the first data of Azorean parks and gardens and to promote concerning the bryophyte biodiversity of the the conservation of the natural heritage for the Azorean parks and gardens, representing a new future generations. The presence of bryophytes centre of interest for all those visiting RFR-PP. In in RFR-PP offers the opportunity to enrich the fact, bryophytes are easily spotted by visitors visitor’s knowledge of the undervalued world along the main track, not only because they of bryophytes, and increase their appreciation include relatively large species (e.g. Andoa of the Azorean ecosystems.

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ACKNOWLEDGMENTS Cardoso, P., S.C. Aranda, J.M. Lobo, F. Dinis, C. Gaspar and P.A.V. Borges 2009. A spatial scale The authors would like to thank the following assessment of habitat effects on communities of an oceanic island. Acta Oecologica financing institutions and programs: the 35: 590–597. Operational Program Azores 2020, financed in Casas, C., M. Brugués, R.M. Cros & C. Sérgio 2006. 85% by FEDER and 15% by Azorean Public Handbook of mosses of the Iberian Peninsula and funds, through the project GreenGA - Green the Balearic Islands. Institut d’Estudis Catalans, Gardens (ACORES-01-0145-FEDER-000070) for Barcelona. 349 pp. missions and through the project Casas, C., M. Brugués, R.M. Cros, C. Sérgio & M. AZORESBIOPORTAL – PORBIOTA Infante 2009. Handbook of liverworts and (ACORES-01-0145-FEDER-000072), for hornworts of the Iberian Peninsula and the laboratory equipment; the first author, CP was Balearic Islands. Institut d’Estudis Catalans, Barcelona. 177 pp. partially funded by the program Eurodisseia – Castel-Branco, C. and I.S. Albergaria 2017. The Açores (project 961/2018). We would also like to Azores Lake Gardens as touristic asset: using the thank the cooperation of “Direção Regional dos visual preferences method. Methaodos. Revista de Recursos Florestais”, during the visit to the Ciencias Sociales 5 (1): 182-193. “Reserva Florestal de Recreio do Pinhal da Paz”. Claro, G.D. 2008. Briófitos da Ilha de S. Jorge: Conservação e caracterização biogeográfica. MSc in Conservation Biology. Faculty of Sciences, REFERENCES University of Lisbon, Lisboa. 77 pp. DROTRH and SRA 2001. Plano Regional da Água – Albergaria, I.S. 2005. Parques e jardins dos Açores/ Relatório Técnico. Direcção Regional do Azores Parks and Gardens. Lisboa, Argumentum. Ordenamento do Território e dos Recursos 239 pp. Hídricos / Secretaria Regional do Ambiente, Ponta Aleffi, M. 2015. The bryophyte flora of the Vatican Delgada. Available from: City State. Cryptogamie, Bryologie, 36(2):155-170. https://www.azores.gov.pt/Gra/srrn-drotrh/conteudos Aleffi, M. 2017. Contribution to the knowledge of the livres/PRA.htm (cited 16 September 2019) Bryophyte Flora of the Vatican City State: The Dierßen, K. 2002. Distribution, ecological amplitude Pontifical Villas of Castel Gandolfo (Rome, Italy). and phytosociological-characterization of European Flora Mediterranea 27 :137-150. bryophytes. Nova Hedwigia: 74(3-4). Allorge, P. and H. Persson 1938. Contribution à la flore Düll, R. 1992. Indicator values of mosses and hepaticologique des îles Açores. Annales liverworts. Pp. 175–214 in: H. Ellenberg, H.E. Bryologici 11: 6-14. Weber, R. Düll, V. Wirth, W. Werner and D. Allorge, V. and S. Jovet-Ast 1950. Aphanolejeunea Paulißen (Eds). Zeigerwerte von Pflanzen in teotonii nov.sp., hépatique des Açores. Révue Mitteleuropa [Indicator values of plants in Central Bryologique et Lichénologique 19: 19-24. Europe]. Erich Goltze, Göttingen. 258pp. Allorge, P. and V. Allorge 1952. Mousses recoltées par During, H.J. 1979. Life strategies of bryophytes: a P. et V. Allorge aux îles Açores en 1937. Révue preliminary review. Lindbergia 5: 2–18. Bryologique et Lichénologique 21: 50-95. ECCB 1995. Red Data Book of European Bryophytes. Bates, J.W. 1998. Is' life-form'a useful concept in European Committee for the Conservation of bryophyte ecology? Oikos : 223-237. Bryophytes, Trondheim, Norway. 291 pp. Bogas, T.C.S. 2003. Os jardins como expressão da Gabriel, R. and J.W. Bates 2005. Bryophyte organização do mundo rural na transoceanidade community composition and habitat specificity in dos Açores (Angra do Heroísmo). BSc Report of the natural forests of Terceira, Azores. Plant Agricultural Sciences. University of the Azores, Ecology, 177: 125-144. Angra do Heroísmo. 170 pp. Gabriel, R., E. Sjögren, R. Schumacker, C. Sérgio, Borges, P.A.V., A.M.C. Santos, R.B. Elias and R. S.C. Aranda, D. Claro, N. Homem and B. Martins Gabriel 2019. The Azores Archipelago: 2010. List of bryophytes (Anthocerotophyta, Biodiversity erosion and conservation Marchantiophyta, Bryophyta). Pp. 99-115 in: biogeography. Pp. 1-18 in: E. Scott et al. (Eds). P.A.V. Borges, Ä. Costa, R. Cunha, R. Gabriel, Encyclopaedia of the World’s Biomes - Earth V. Gonçalves, A.F. Martins, I. Melo, M. Parente, Systems and Environmental Sciences. Elsevier, P. Raposeiro, P. Rodrigues, R.S. Santos, L. Silva, Amsterdam, Netherlands. P. Vieira and V. Vieira (Eds). A list of the

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terrestrial and marine biota from the Azores. 2018). Princípia Editora, Lda., Cascais. Madeira, M., J. Pinheiro, J. Madruga and F. Monteiro Gabriel, R., N. Homem, A. Couto, S. C. Aranda and 2007. Soils of volcanic systems in Portugal. Pp. 69- P.A.V. Borges 2011. Azorean Bryophytes: a 81: in O. Arnalds, F. Bartoli, P. Buurman, H. preliminary review of rarity patterns. Açoreana, Oskarsson, G. Stoops and E. Garcia-Rodeja (Eds). Supl. 7: 149-206. Soils of Volcanic Regions in Europe. Springer. 351 Gabriel, R. 2019. Não há rosas sem espinhos: O papel pp. dos jardins na disseminação de espécies exóticas e Mexia, T., J. Vieira, A. Príncipe, A. Anjos, P. Silva, N. invasoras - 13 plantas prioritárias para controlo ou Lopes, C. Freitas, M. Santos-Reis, O. Correia, C. erradicação nos Açores. Pp. 53-65 in: I.S. Branquinho and P. Pinho 2018. Ecosystem Albergaria (Ed.) Catálogo da Exposição "Plantas e services: urban parks under a magnifying glass. Jardins: A paixão pela horticultura ornamental na Environmental Research 160: 469-478. ilha de São Miguel". CHAM & Biblioteca Pública Pacheco, J.L.O. 2012. Valor económico da Reserva e Arquivo Regional de Ponta Delgada, Ponta Florestal de Recreio do Pinhal da Paz. Aplicação Delgada. do método de avaliação contingencial. MSc in Gaspar, C., P.A.V. Borges and K.J. Gaston 2008. Nature Conservation and Management, University Diversity and distribution of in natural of the Azores, Ponta Delgada. 82 pp. forests of the Azores archipelago. Arquipelago. Paton, J.A. 1999. The liverwort flora of the British Life and Marine Sciences 25: 1–30. Isles. Harley Books, Essex. 626pp. Glime, J. M. 2007. Economic and ethnic uses of Patiño, J., R.G.Mateo, F. Zanatta, A. Marquet, S.C. bryophytes. Flora of North America, 27: 14-41. Aranda, P.A.V. Borges, G. Dirkse, R. Gabriel, M. Goddard M.A., A.J. Dougill and T.G. Benton 2009. Gonzalez-Mancebo, A. Guisan, J. Muñoz, M. Sim- Scaling up from gardens: biodiversity conservation Sim, and A.Vanderpoorten 2016. Climate threat on in urban environments. Trends in Ecology and the Macaronesian endemic bryophyte flora. Evolution 25: 90-98. Scientific Reports 6: 29156, 1-12 Henriques, D.S.G., Ah-Peng C. and R. Gabriel 2017. Pérez Santa-Rita, J.V., A. Ros-Prieto, V. Vieira, O. Structure and applications of BRYOTRAIT-AZO, Karsholt, R. Gabriel, and P.A.V. Borges 2018. a trait database for Azorean bryophytes. New records of moths (Insecta, Lepidoptera) from Cryptogamie Bryologie, 38(2): 137-152. urban gardens on with new data on Hill, M.O. and C.D. Preston 1998. The geographical recently introduced species to the Azores. relationships of British and Irish bryophytes. Arquipelago. Life and Marine Sciences 35: 47-65. Journal of Bryology 20: 127–226. Porley, R. and N. Hodgetts 2005. Mosses and Hill, M.O., C.D. Preston, S.D.S. Bosanquet and D.B. Liverworts. Harper Collins, London. 495 pp. Roy 2007. BRYOATT: attributes of British and Quintal, R 2007. Quintas, Parques e Jardins do Irish mosses, liverworts and hornworts. Centre for Funchal. Estudo Fitogeográfico. Esfera do Caos, Ecology and Hydrology and Countryside Council Lisboa. 702 pp. for Wales, Norwich. 88 pp. Roberts, D. G., D.J. Ayre and R.J. Whelan 2007. Urban Hodgetts, N. G. and N. Lockhart 2015. Checklist and plants as genetic reservoirs or threats to the country status of European bryophytes - towards a integrity of bushland plant populations. new Red List for Europe, (report) National Parks Conservation Biology 21(3): 842-852. and Wildlife Service, Irish wildlife manuals. 125 Sasidharan, V., F. Willits and G. Godbey 2005. pp. Cultural differences in urban recreation patterns: Hodgetts, N.G., M. Calix, E. Englefield, N. Fettes, M. An examination of park usage and activity García Criado, L. Patin, et al. 2019. European Red participation across six population subgroups. List of Mosses, Hornworts and Liverworts. IUCN, Managing Leisure 10(1):19-38. Brussels, Belgium. 88 pp. Schumacker, R. and J. Váňa 2005. Identification keys Homem, N. and R. Gabriel 2008. Briófitos raros dos to the liverworts and hornworts of Europe and Açores / Azorean rare bryophytes. Princípia Macaronesia (2nd edition). Sorus, Poznań. 208 pp. Editora, Lda. Estoril. 96 pp. SDR-IV 2019. SDR-IV Species Diversity and Hübschmann, A. von. 1974. Bryologische Studien auf Richness. Pisces Conservation, Ltd. Available der Azoreninsel São Miguel. Revista da Faculdade from: http://www.pisces-conservation.com (cited de Ciências de Lisboa, Série 2C, 17: 627-702. 04 October 2019). IUCN 2018. The IUCN Red List of Threatened Sérgio, C. 1991. Notulae Brioflorae Macaronesicae II. Species. Version 2018-1. Available from: 1 - Sphaerocarpus texanus Aust. nova hepática http://www.iucnredlist.org. (cited 11 November para a flora da Macaronésia. Portugaliae Acta

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Biologica, Série B, 15: 419. liverworts. PhytoKeys 59:1-828 Silva, L., L.E. Ojeda and J.L.L. Rodriguez 2008. Flora Tavares, A.M. 2016. Biodiversidade da Reserva e Fauna Terrestre Invasora na Macaronésia. TOP Florestal de Recreio do Pinhal da Paz. MSc in 100 nos Açores, Madeira e Canárias. ARENA, Plant Biodiversity and Biotechnology, University Ponta Delgada. 546 pp. of the Azores, Ponta Delgada. 109 pp. Silveira, T. 1937. Flora briológica. Espécies novas para Voigt, A., N. Kabisch, D. Wurster, D. Haase and J. os Açores. Açoreana 1: 240-247. Breuste 2014. Structural diversity: a multi- Sjögren, E. 1978. Bryophyte vegetation in the Azores dimensional approach to assess recreational Islands. Memórias da Sociedade Broteriana 26: 1– services in urban parks. Ambio 43(4): 480-491. 273. Zerbe, S., U, Maurer, S. Schmitz, and H. Sukopp 2003. Smith, A. J. E. 2004. The moss flora of Britain and Biodiversity in Berlin and its potential for nature Ireland. (2nd edition). Cambridge University Press, conservation. Landscape and urban planning, Cambridge. 1012 pp. 62(3): 139-148. Söderström, L., A. Hagborg, M. von Konrat, S. Bartholomew-Began, D. Bell, L. Briscoe, and E. D. Submitted 13 Nov 2019. Accepted 9 Jan 2020. Cooper 2016. World checklist of hornworts and Published online 18 Feb 2020.

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Annex 1. Catalogue of bryophytes identified in the Recreational Forest Reserve “Pinhal da Paz” (São Miguel Island, Azores). Below it is presented a list of all species collected in the Recreational Forest Reserve “Pinhal da Paz” (São Miguel Island, Azores) in June 2018, alphabetically organized by Division (Anthocerotophyta, Marchantiophyta and Bryophyta). The code of the sampling point and a brief description of the taxa, mostly based in Casas et al. (2006, 2009) and Schumacker & Vana (2005) are also included.

DIVISION ANTHOCEROTOPHYTA the lobe, ending in a very acute tip. Tip - Hornworts gradually narrowed into a long acumen, which ends in a unicellular row of 4-5 cells. Underleaves not decurrent. Anthoceros caucasicus Steph. (PP-15) Thallose species, prostrate, with globose Nostoc Frullania azorica Sim-Sim et al. (PP-10) (cyanobacteria) colonies; thalli cells with one Small leafy liverwort, generally reddish or dark chloroplast per cell, rhizoids unicellular, smooth; brown. Leaves imbricate, bilobed, conduplicate; spores with a wide smooth band along the trilete ventral lobules as long as wide, helmet-shaped; mark. underleaves with acute lobes and lateral margins with 1-2 acute teeth. DIVISION MARCHANTIOPHYTA - Liverworts Frullania microphylla (Gottsche) Pearson (PP- 8) Calypogeia fissa (L.) Raddi (PP-9, PP-14, PP- Small leafy liverwort, generally reddish. Leaves 16) imbricate, bilobed, conduplicate; ventral lobules Leafy liverworts, with prostrate stem, abundant longer than wide, sac-shaped. Leaf cells with rhizoids, leaves longer than wide, widest one walls uniformly thickened, without trigones. third from the base, usually with lobe apex Ocelli in two rows on the dorsal lobe (especially bidentate or more or less acute and underleaves on robust shoots) and sometimes also dispersed. wider than long, divided, with one lateral tooth or protuberance at one or both sides. Harpalejeunea molleri (Steph.) Grolle (PP-8, PP-10, PP-12, PP-13) Cololejeunea azorica V.Allorge et Jovet-Ast Minute leafy liverwort, generally yellowish or (PP-8) greenish yellow; mid-leaf cells without oil- Minute leafy liverwort, withprostrate stem, bodies or trigones; underleaf lobes rounded, 4-6 oblong leaves, ventral lobule abut half the length cells wide at base; commonly found growing as and 80% width of the dorsal lobe, bearing a bryo-epiphyte on other bryophytes. central tooth. Without underleaves. Lejeunea lamacerina (Steph.) Schiffn. (PP-4, Drepanolejeunea hamatifolia Hook.) Schiffn. PP-7, PP-9, PP-12, PP-13, PP-14, PP-15, PP-16, (PP-8) PP-17) Minute leafy liverwort, pale green to yellowish Very small leafy liverwort, usually light green; green, dorsal lobe convex at base, abruptly leaves bilobed, incubus, conduplicate and wide narrowed in an often reflexed, acute or acuminate underleaves. Free part of the lobes at a 120-160° apex, with 1-2-celled teeth at the end; underleaves angle to the keel. Terrestrial and epiphytic. bilobed, with acuminate, diverging lobes. Lophocolea bidentata (L.) Dumort. (PP-6, PP- Frullania acicularis (J.-P.Frahm) Hentschel & 7, PP-9, PP-13, PP-14, PP-15, PP-17) von Konrat (PP-6, PP-7) Small to medium-size leafy liverwort, pale green Small leafy liverwort, with leaves imbricate with to yellowish green. Leaves alternate, spreading, apex incurved for about one third of the length of longitudinally inserted, succubus, bilobed; upper

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Bryophytes of Azorean parks and gardens (I) lobes bilobed, with acuminate lobes; leaf large (25- small hyaline cells, more or less collapsed or 50 μm). Terrestrial and epiphytic. partly broken; this feature may also be seen in the lobules. Lophocolea fragrans (Moris et De Not.) Gottsche, Lindenb. et Nees (PP-16, PP-17) Small leafy, aromatic liverwort. Leafs mostly 3- Reboulia hemisphaerica (L.) Raddi s.l. (PP-13) lobed, especially at the apex, mostly with dentate Thallose liverwort 1-3 cm long, light to dark margin. green colour with reddish spots and margins; margins sinuose, undulate, unistratose. Air pores, Lophocolea heterophylla (Schrad.) Dumort. on the dorsal side, with 4-5 concentric rings of (PP-5, PP-11) cells, and radial walls thickened. Small leafy, liverwort. Leaves with different shape along the stem, upper leaves simple with Riccardia multifida (L.) Gray (PP-9, PP-14) rounded or retuse apex, while lower leaves may Small thallose liverwort with fragile, dark green be bilobed to one third, with lobes acute or thalli, with branches parallel-sided up to their acuminate. apex; ultimate lobes with unistratose, 2-5 cells wide translucent margins. Lunularia cruciata (L.) Dumort ex. Lindb. (PP- 7, PP-14, PP-15) Saccogyna viticulosa (L.) Dumort. (PP-7, PP- Thallose liverwort, glossy green on dorsal side; 14) with thalli furcate with sinuous margins and Medium-sized leafy liverwort, prostrate; Leaves dorsal epidermis reticulate with striking lunate succubus, obliquely inserted, with a rounded gemma receptacles on the dorsal surface. apex; well-developed triangular underleaves, bilobed or toothed. Metzgeria furcata (L.) Corda (PP-10) Small thallose prostrate liverwort, light green, translucent. Thalli plane with marginal hairs, where present, single, straight; midrib on the DIVISION BRYOPHYTA - Mosses ventral face not, or hardly, hairy. Amblystegium confervoides (Brid.) Schimp. Porella canariensis (F. Weber) Bryhn (PP-12) (PP-12) Medium-sized leafy liverwort, generally Small sized pleurocarpous moss, with brownish, usually without a metallic sheen. Lobes procumbent, irregularly branched stem. Leaves bilobed, conduplicate, incubus; Median cells of with entire margin and nerve lacking; plants dorsal lobe relatively small (18-25 μm) with saxicolous, growing mostly on calcareous rocks. uniformly thickened walls; large underleaves, paucispinose. Amblystegium serpens (Hedw.) Schimp. (PP-9) Small and slender pleurocarpous moss, with Radula aquilegia (Hook. F. et Taylor) Gottsche procumbent, irregularly branched stem. Leaves et al. (PP-7) ovate lanceolate, up to 1 mm length; margin Small leafy liverwort, olive green colour. Leaves finely denticulate. bilobed, concave, cell walls thickened with distinct trigones; lobules approximately Andoa berthelotiana (Mont.) Ochyra (PP-4, PP- rectangular; keel region inflated and often 5, PP-7, PP-9, PP-14, PP-15, PP-16, PP-17) strongly arched. Medium-sized to large pleurocarpous moss. Concave, densely imbricated leaves with Radula wichurae Steph. (PP-6, PP-7, PP-8, PP- denticulate acuminate apex. 10) Small leafy liverwort, olive green colour. Lobes Anomobryum julaceum (P. Gaerth., B. Mey. et bilobed; mature leaves bordered with 1-3 rows of Scherb.) Schimp. (PP-1)

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Small acrocarpous moss, up to 1,5 cm tall, glossy and acute or broadly acute apex. The nerve is light green. Shoots julaceous, filiform, with stout and usually excurrent. appressed leaves, ovate or oblong-lanceolate, with median vermicular cells. Hypnum jutlandicum Holmen et E. Warncke (PP-5, PP-7) Atrichum angustatum (Brid.) Bruch et Schimp. Medium-sized, pale green, pleurocarpous moss. (PP-5) Leaves from straight to falciform, ovate or Medium-sized acrocarpous moss, usually dark oblong-lanceolate, loosely imbricate; alar cells green. Stiff, narrow leaves, with 4-7 lamellae over more or less homogeneous and rectangular. the central nerve, 6-9 cells high. Hypnum uncinulatum Jur. (PP-6) Brachytheciastrum velutinum (Hedw.) Ignatov Medium-sized, pale green to brownish et Huttunen (PP-12) pleurocarpous mosses. Leaves falciform, Small pleurocarpous moss, slender, light to dark gradually narrowed to acuminate apex (triangular green. Stem leaves narrowing until a fine dentate shape) and margin denticulate. Alar cells irregular acumen and rectangular alar cells. Leaf margin and heterogeneous. slightly recurved, more or less dentate. Kindbergia praelonga (Hedw.) Ochyra (PP-5, Campylopus pilifer Brid. (PP-1) PP-9, PP-13, PP-14, PP-15, PP-17) Medium-sized acrocarpous moss with very rigid Medium-sized to large pleurocarpous moss, dark stems and strongly imbricate leaves. Basal cells green or greenish brown. Stem and branch leaves narrow, rectangular, hyaline, extending up with different leaves shapes: narrowly decurrent margins in a V-shape; nerve with dorsal lamellae and widely ovate or cordate-triangular at the (2-)3-4 cells high and numerous stereid groups. stem, and ovate or lanceolate at the branches.

Ceratodon purpureus (Hedw.) Brid. subsp. Philonotis rigida Brid. (PP-13) purpureus Small acrocarpous moss, with radiculose erect Small acrocarpous moss, forming green or stems. Densely imbricate leaves; leaf margin reddish turfs to 2 cm high. Leaves erect-patent plane with simple teeth; nerve mamillose at back. with apex slightly denticulate; leaf margin recurved; stout nerve, percurrent or excurrent. Polytrichum juniperinum Hedw. (PP-2) Large acrocarpous moss, up to 8 cm tall, dark Dicranoweisia crispula (Hedw.) Lindb. ex green. Stem not tomentose or with sparce brown Milde (PP-16) tomentum. Long leaves, spreading when dry, Medium-sized acrocarpous moss, up to 3 cm tall. excurrent in short or long arista; nerve with Plants crisped when dry. Leaves with unistratose filaments on ventral side; apical cells of lamellae margin and apex. Median cells of the leaves small pyriform in cross-section, smooth. (6-8 μm wide). Ptychomitrium nigrescens (Kunze) Wijk et Fissidens asplenioides Hedw. (PP-9, PP-15, PP- Marg. (PP-12) 16) Small acrocarpous moss, up to 1 cm tall, blackish Small to medium-sized acrocarpous moss. Leaves to green along the stem. Leaves patent, crisped with three blades, oblong-lingulate; apices often when dry, linear-lanceolate with acute apex. strongly inrolled towards the substrate when dry; crenulate-serrulate margins towards the apex. Ptychostomum capillare (Hedw.) Holyoak & N. Pedersen (PP-13) Fissidens taxifolius Hedw. (PP-7, PP-13, PP-14) Small acrocarpous moss. Leaves ovate, oblong or Small acrocarpous moss, yellowish to dark green. spathulate, abruptly tapering in more or less long Leaves with three blades, long, oblong-lanceolate point; nerve excurrent or ending below aped,

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Bryophytes of Azorean parks and gardens (I) margin formed by longer cells along the whole Tortella nitida (Lindb.) Broth. (PP-13) leaf. Red to brown rhizoidal gemmae, when Small acrocarpous moss, up to 1 cm tall. present. Lanceolate leaves, with very fragile lamina; basal cells smooth, hyaline, ascending up margin; leaf Sematophyllum substrumulosum (Hampe) margin incurved, and nerve conspicuous, Britton (PP-4, PP-8, PP-9) excurrent and glossy back. Slender pleurocarpous moss. Leaves narrowly lanceolate with long, filiform apex, without nerve Trichostomum brachydontium Bruch (PP-5, PP- and large alar group, with 4-6 inflated cells. 7, PP-9) Small acrocarpous moss, up to 2 cm long. Long leaves, erect-patent, with margin plane, entire; Tetrastichium virens (Cardot) S. P. Churchill nerve excurrent in stout apiculus. (PP-14, PP-15, PP-16, PP-17) Medium-sized pleurocarpous moss, irregularly Zygodon rupestris Schimp. ex Lorentz (PP-10) branched, with complanated stem leaves. Leaves Small acrocarpous moss up to 3 cm tall. Leaves lanceolate to ovate-lanceolate, margin entire to contorted or flexuose when dry, with unistratose slightly denticulate near the apex, and small lamina in the upper part and median leaves cells median cells (10-16 μm wide). with 3-6 low papillae per cell. Gemma 20-30 μm wide, without longitudinal walls.

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Plate 1. a) Polytrichum juniperinum; b) Fissidens asplenioides; c) and d) Andoa berthelotiana; e) and f) Radula wichurae; 1g) Reboulia hemisphaerica; 1h) Anthoceros caucasicus.

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Arquipelago - Life and Marine Sciences ISSN: 0873-4704

Estimates of biomass and potential yield for the deep- water red crab, Chaceon affinis and the toothed rock crab, Cancer bellianus (: Brachyura) off the Azores (Mid-North Atlantic)

MÁRIO PINHO, RÉGIS SANTOS, OCTÁVIO MELO, EDUARDO ISIDRO, ANA NOVOA-PABON, WENDELL SILVA AND JOÃO GONÇALVES

Pinho, M., R. Santos, O. Melo, E. Isidro, A. Novoa-Pabon, W. Silva and J. Gonçalves 2020. Estimates of biomass and potential yield for the deep-water red crab, Chaceon affinis and the toothed rock crab, Cancer bellianus (Decapoda: Brachyura) off the Azores (Mid-North Atlantic). Arquipelago. Life and Marine Sciences 37: 21 – 36. https://doi.org/10.25752/arq.23645

Available information on the deep-water red crab, Chaceon affinis and the toothed rock crab, Cancer bellianus, resulting from exploratory research surveys and commercial experiments carried out in the Azorean Exclusive Economic Zone (EEZ), were summarized to estimate the biomass and potential yield (Maximum Sustainable Yield – MSY) for both resources. The fishery potential was estimated through empirical methods usually applied when available information is scarce in line with the precautionary approach principle. Results suggest modest MSY values (considered as precautionary Total Allowable Catch – TAC), around 2,205 t for the deep-water red crab (2,159 t year-1 at seamounts and 46 t year-1 at coastal areas), and 471 t for the toothed rock crab (281 t year-1 at offshore seamounts and 189 t year-1 at coastal areas). Considering the limited available data and high uncertainty associated with these estimations, it is suggested that only a reduced number of vessels should be allowed to fish in the aggregated areas, namely coastal and areas. The exploitation of these resources should be started in a very limited way followed by an ad hoc observer programme, aiming to collect reliable data that will allow, if it is the case, to raise in the future the exploitation level in a gradual and sustainable way.

Key words: Chaceon affinis; Cancer bellianus; abundance; fishery potential; deep-sea; Azores.

Mário Pinho1,2,3, Régis Santos1,2 (email:[email protected]), Octávio Melo1,2, Eduardo Isidro1,2,3, Ana Novoa-Pabon2,3, Wendell Silva1,2, João Gonçalves1,2,3. 1IMAR Institute of Marine Research, University of the Azores, 9901-862, Horta, Portugal. 2Okeanos R&D Centre, University of the Azores, 9901-862, Horta, Portugal. 3Faculty of Science and Technology, Department of Oceanography and Fisheries, University of the Azores, 9901-862, Horta, Portugal.

Corresponding author: Régis Santos (email:[email protected])

INTRODUCTION as virgin or poorly exploited resources. In fact, only the toothed rock crab, Cancer bellianus J. Y. The deep-sea from the Azores Johnson, 1861, has been sporadically exploited archipelago (Mid-North Atlantic) can be considered for local consumption in three of the nine islands

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that form the archipelago, i.e. Terceira (65% of the potentially sustainable levels for the reported landings), São Miguel (16%) and Pico exploitation of these resources to guide (14%) islands, reaching annual average values of management. In fisheries terms, populations eight tons between 1997 and 2018 (Lotaçor S.A., need to be maintained within safe biological commercial landings database). limits, i.e. the maximum sustainable yield (MSY) Studies on Azorean deep-sea crabs, C. that is the highest theoretical equilibrium yield bellianus and Chaceon affinis A. Milne-Edwards that can be continuously taken (on average) from and Bouvier, 1894, began in 1994 with sporadic a stock under existing (average) environmental cruises and "opportunistic" actions (i.e. fishing conditions without affecting significantly the and sampling on cruises not directed to reproduction process (FAO 1997; ICES 2018a). crustaceans) (Gonçalves 1994; Gonçalves & This work aims to review and summarize all Pinho 1994; Gonçalves et al. 1995). More the available information for C. affinis and C. detailed knowledge about the biology and fishing bellianus in the Azorean region (Mid-North aspects of these species were obtained from the Atlantic) to estimate the biomass and potential European project "Biology of some Macaronesian yield as MSY proxies to guide management deep-sea commercial species" (González et al. advices. 1998) and the regional project "CRUSTAÇO" (Pinho et al. 2001a; Santos et al. 2019). As the results obtained in the preliminary MATERIALS AND METHODS studies (above referenced) suggested that these resources had the potential to develop a small Azores archipelago fishery, experiments were The Azores archipelago is placed in the Mid- carried out using two coastal closed-deck vessels North between 33.5° – 43° N, of around 14 m length (Pinho et al. 2001a). These and 21° – 35.5° W, and its Exclusive Economic vessels operated primarily in coastal areas of Zone (EEZ) has approximately 1,000,000 km2. Terceira, , São Jorge, Pico and Faial The Azores archipelago is constituted of nine islands (central group of the Azores archipelago) islands (: Flores and Corvo; and the results showed that there was indeed central group: Terceira, Graciosa, São Jorge, potential for both species to be exploited and that Pico and Faial; eastern group: São Miguel and this potential was greater for the toothed rock Santa Maria), several islets and many seamounts crab than for the deep-water red crab (Pinho et al. and banks of volcanic origin (Figure 1). 2001 a, b, c). Muddy sediments are the most extensive At this stage, some limiting factors for substrate types in the Azores (ICES 2019). exploitation were also identified, namely: (a) Continental shelves are quite narrow (ca 1,500 Lack of established local or external markets at km2) and the average depth in the Azorean EEZ stimulating prices; (b) Aggregate distribution or is about 3,000 m, 0.8% of the total EEZ area has "patches" of the resource (not uniform and very depths < 600 m and 6.8% is between 600 and dependent on specific habitat available) 1,500 m (ICES 2018b). The North Atlantic introducing great variability of abundance from Central Water (NACW) at depths shallower than site to site; and (c) Technological difficulties 600-700 m, the North Atlantic Deep Water related to the operation of the artisanal fleet, (NADW) below 2000 m depth, and the Subarctic namely those related to the power of the hauler Intermediate Water (SAIW), Labrador Sea and the necessary space to work with ropes and Water (LSW) and Antarctic Intermediate Water traps. (AAIW) at intermediate depths are the main There is nowadays a growing interest in the water masses in the Azorean region exploitation of crab resources as an alternative or (Bashmachnikov & Martins 2007). a complement to the traditional demersal Mediterranean Water can also occur resources intensely exploited. However, there approximately between 650-1,200 m depth is a requirement for scientific studies reporting (Bashmachnikov & Martins 2007).

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Estimates of biomass and potential yield for deepwater crabs off the Azores

Fig. 1. The Azores archipelago (mid-North Atlantic Ocean) with depth contours layers and location of the nine islands (in bold), major seamounts, and the limit of the Exclusive Economic Zone (EEZ).

Data collection sex and carapace length were also recorded whenever The primary data used in this study were obtained possible. The landing by weight was subsequently in: registered for each trip. Survey data (item "b") were obtained mainly in (a) commercial experimental trap fishing coastal areas of the central group (Faial, Pico and operations targeting the deep-water red crab São Jorge). Of the banks, only the Princess Alice during 2003. These data were collected by Bank was sampled. This study area was stratified observers on board of an Azorean industrial into depth strata with 100 m intervals (i.e. the first vessel, with enough autonomy and power to stratum represented 0-100 m, the second 100-200 operate in the offshore banks and seamounts. m and so on) down to 1,200 m. Within each stratum, random sets were allocated, guaranteeing (b) exploratory research surveys using traps a minimum of two sets per stratum. For each set, targeting the deep-water red crab and the information was collected on fishing (start and toothed rock crab from 1994 to 2000 (Pinho et retrieval dates, time, geographical position, depth, al. 2001a, b, c). number of dropped and lost traps, catch in In each set carried out by the aforementioned number of individuals per trap, etc.) and biology commercial vessels (items "a"), information on start (length and carapace width, weight, sex, etc.). and retrieval dates, time, geographical position, depth, The bait was ca 1 kg of salted Atlantic chub number of dropped and lost traps, as well as the mackerel Scomber colias. For details of the capture per trap in number of individuals were sampling methodology see Pinho et al. (2001b, c). obtained. In addition, information on the vessel and For this study, we selected data corresponding gear characteristics was recorded. For crustaceans only to sets made with benthic bottom traps. (the deep-water red crab and the toothed rock crab), Although different types of bottom traps (Fathom

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Plus® and the homemade crab trap “Josué”; see software (Thematic Mapping System, Golden Melo (2009) for technical specifications) were Software, Inc.). For mapping details of banks and used, abundance was considered to be seamounts of the Azores, see Machete et al. independent of the trap because no (2005). significant differences (α = 0.05) were found in abundance between traps (t-test, t = 1.24, p = Estimates of biomass and potential yield 0.22). The biomass (abundance) of each species was Assuming that depths of greatest abundance estimated according to the methodology of the correspond to the preferential habitat of the theoretical attraction (influence) area for traps species, the depths of 500-900 m for the deep- (Eggers et al. 1982). This methodology, similar to water red crab and 200-600 m for the toothed the swept area procedure used in the case of rock crab were adopted based on the survey bottom trawls, has been proposed and largely available information. It was considered that the employed to evaluate other trapped crab resources species distribution in the Azorean EEZ along the (Miller 1975; McElman & Elner 1982; Melville- respective bathymetric is identical to that of the Smith 1986; Defeo et al. 1991; Arana 2000; sampled areas. For coastal zones of the islands, Cores et al. 2019). the average catch per unit of effort (CPUE - For the approximate biomass estimation, the estimated number of individuals per trap) follow expression was used: estimated for each species based on the survey data was used as abundance index (Pinho et al. N = A*D*q 2001b, c). For bank area and the deep-water red crab, the average CPUE was estimated from the where: N – biomass (abundance) of the resource in data collected by the observers throughout the number; A – total area of distribution of the resource in experimental commercial fishing operation. For the Azorean EEZ; D – average density of the resource the toothed rock crab, the average CPUE value (number of individuals per km2); and q – catchability estimated for the Princess Alice Bank using coefficient (proportion of individuals that are trapped in survey data was extrapolated for all bank areas. the catchment area and actually captured). Only the complete records, i.e. those containing catch, fishing effort and georeferenced The mean density of the resource was estimated information, were used in the analysis. The data as follows: corresponding to a group of strata, due to the displacement of the fishing gear, were eliminated D = C/a1 from the analysis. The CPUE in number was Where: C – average number of individuals caught per converted to weight, using the average weight for trap; and a1 – theoretical area of attraction of a trap each species estimated by Pinho et al. (2001b, c). (km2).

Areas of occurrence The theoretical attraction area of the trap was Areas of probable occurrence of these resources considered to have a circular shape, assuming a in the Azorean EEZ were estimated from Smith null or minimal underwater current. Thus, and Sandwell (1997) according to Eggers et al. (1982), the effective (http//topex.ucsd.edu/sandwell/sandwell.html) theoretical mean attraction area of a trap in an bathymetric mapping and assuming an amplitude overlapping configuration of successive traps in line was calculated as: of bathymetric distribution of 200 to 600 m for the toothed rock crab and 500 to 900 m for the deep-water red crab. na −1 The bathymetric mapping was first constructed a t = a1 − * L through the kriging method for data interpolation na © using the Surfer 7.05 software (Surface Mapping Where: at – effective mean theoretical attraction area System Golden Software, Inc.). The areas were of a trap in overlapping configuration; a1 – theoretical © then estimated using the Map Viewer 4.0 attraction area of a trap; na – total number of traps per 24

Estimates of biomass and potential yield for deepwater crabs off the Azores fishing gear (line); and L – overlapping area of 5% of the population reaches the maximum age influence (attraction) of two adjacent traps, calculated 20 years if only natural mortality acts), and as: Rikhter & Efanov (1976) (assuming that the  1  length of first maturation estimated for these 2 2  −1  s  2 s  2 s   species in the Azores, between 80 and 85 mm of L = 2* cos  *R − *R −    2R  2  4   carapace length, corresponds to 10 years of age;   Pinho et al. 2001b,c). This value also corresponds Where: s – distance between adjacent traps along a to the estimated value used by other authors for line of traps; and R – radius of the attraction area of a deep-water crab species (Cayre et al. 1979; trap. Melville-Smith 1988; Defeo et al. 1991; Arana 2000). The virgin biomass (B0) corresponded to Biomass was estimated for combined sexes and the biomass estimated since the resources are by species, for radius of attraction of a trap pristine. varying between 25 and 45 m (intervals of five metres). In the case of data from the research surveys, the first radius (25 m) corresponds to a RESULTS non-interaction configuration between adjacent traps while the following ones correspond to an Distribution and catches interaction configuration. The distance between adjacent traps along a line was approximately 50 Cancer bellianus was found distributed in the m in the research surveys and 45 m in Azores between 100 and 800 m depth, with commercial fishing experience. The commercial higher catches at coastal areas, approximately 5 used on average 60 traps per line, individuals (ca 2.73 kg) trap-1 between 200 and while approximately 10 traps per line were used 600 m (Table 1). The results showed a great in the research survey (Pinho et al. 2001 b, c). variability in abundance in all depth strata The potential yield for each species was (catches at coastal zones and in the 200-600 m estimated using Gulland's empirical formula for stratum vary from ca 1 to 10 individuals trap-1), estimating the maximum sustainable yield (MSY) meaning that the distribution of the species was of unexploited (virgin) populations (Gulland not uniform. The estimated CPUE for the 1971, 1983): Princess Alice Bank for this species was very low and had a great variability (Table 1). P = x*M*B0 Chaceon affinis was found distributed in the Azores between 400 and 1,100 m depth with Where: P – potential yield; M – natural mortality; B0 – higher catches between 600 and 900 m depth virgin biomass; and x – constant (related to growth and (Pinho et al. 2001c) (Table 2). The catch mortality characteristics). variability was very significant particularly in the survey data, evidencing the distribution Gulland (1971) proposed the value of 0.5 for "x", characteristics of the species by "patches". The while Garcia & Le Reste (1981), Beddington & CPUE value at coastal zones estimated from the Cooke (1983), and Garcia et al. (1989) suggested research surveys and commercial fishing were using more conservative values (x < 0.5). Thus, in very similar, revealing that the occurrence of the this study, potential yields were estimated with species at coastal zones was relatively scarce values of "x" varying between 0.1 and 0.5. For (Table 2). The estimated CPUE from the the natural mortality was adopted the value M = commercial fishing experience during the year 0.15, which corresponds to the mean value of 2003 was very high, meaning that only areas of mortality for the species estimated by empirical high concentration of the species were probably methods, such as Tanaka (1960) (assuming that of covered.

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Table 1. Estimated average catches for the toothed rock crab Cancer bellianus per trap and per depth stratum, for the Azorean coastal zones and Princess Alice Bank. The mean values for the 200-600 m stratum adopted for the fishery potential estimation are also presented in the table. CPUE - Catch per Effort Unit (number of ind. per trap); SD - Standard deviation; n - number of sets; na - not sampled. Coastal zones Princess Alice Bank Depth strata (m) CPUE SD n CPUE SD n 100 0.50 0.00 3 0.00 0.00 6 200 5.89 4.92 22 1.52 1.75 5 300 4.91 3.36 24 1.97 2.57 22 400 8.41 5.18 17 2.45 3.61 11 500 4.71 3.13 17 1.66 1.18 4 600 3.08 2.02 17 0.75 0.12 2 700 1.01 0.98 12 0.48 0.26 3 800 0.79 0.70 6 na na na 200-600 5.39 4.19 97 1.95 2.61 44

Table 2. Estimated average catches for the deep-water red crab Chaceon affinis per trap and per depth stratum, for the Azorean coastal zones and seamounts. The mean values for the 500-900 m stratum are also presented, with the values adopted for the fishery potential estimation in bold. CPUE - Catch per Effort Unit (number of ind. per trap); SD - Standard deviation; n - number of sets; na - not sampled.

Commercial fishery Research surveys Depth strata (m) Seamounts Coastal zones Coastal zones CPUE SD n CPUE SD n CPUE SD n 400 5.43 1 na na na 0.01 0.03 14 500 5.07 1.57 4 0.80 1 0.27 0.63 14 600 5.30 3.32 10 0.83 0.21 2 0.33 0.46 22 700 5.45 2.28 15 1.37 0.59 6 0.42 0.44 18 800 5.81 2.12 13 1.01 0.37 4 1.06 1.22 19 900 0.43 - 1 na na na 0.80 1.24 17 1,000 na na na na na na 0.78 0.83 13 1,100 na na na na na na 0.25 0.35 2 500-900 5.37 2.49 43 1.13 0.49 13 0.79 1.30 90

Areas of occurrence The total areas available in the Azorean EEZ for habitat available in the Azorean EEZ for the depths considered optimal for the distribution of toothed rock crab and 13% for the deep-water the species were summarized in Table 3. These red crab). Offshore (banks and seamounts) areas represented approximately 1.4% of the habitat areas available for these species in the Azorean EEZ in the case of Cancer bellianus and Azorean EEZ were also very scarce, especially 3.4% in the case of Chaceon affinis. Coastal for the toothed rock crab, meaning that the habitat areas available for both species were number of banks and seamounts with depth scarce(representing approximately 24% of the total strata between 200-600 m was relatively small.

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Estimates of biomass and potential yield for deepwater crabs off the Azores

Table 3. Coastal zone and bank and seamount areas on the value of the radius of attraction adopted for identified in the Azorean EEZ as potential habitats for a trap. These values corresponded to a mean the toothed rock crab Cancer bellianus (200-600 m) density between 0.5 and 2 individuals per 1000 and the deep-water red crab Chaceon affinis (500-900 m2. At coastal zones, estimated average biomass m). values varied between 1,952 and 6,296 t, Habitat Depth (m) Area (km2) corresponding to mean densities between 2 and 6 individuals per 1,000 m2 (Table 4). Coastal zones 200-600 2,694 The potential yield (MSY) varied considerably according to the combination of 500-900 4,247 each radius of attraction area (R) and Banks and seamounts 200-600 11,106 exploitation rate (constant of empirical equation, x) (Tables 5 and 6). In the most 500-900 32,775 pessimistic scenario, it was estimated a MSY (considered as precautionary TAC) of 44 t of

the toothed rock crab at banks and seamounts, Estimates of biomass and potential yield and 704 t in the most optimistic scenario (Table Cancer bellianus 5). On coastal zones, values of 29 t in a The estimated average biomass for banks/seamounts pessimistic scenario and 472 t in an optimistic ranged from approximately 2,912 to 9,392 t, depending one was estimated (Table 6).

Table 4. Average biomass of the toothed rock crab Cancer bellianus estimated at banks/seamounts and coastal zones of the Azorean EEZ. The table shows the lower (LCI) and upper (UCI) limits of the estimates for a 95% confidence interval. R - radius of attraction area of a trap; at - effective theoretical mean area of attraction of a trap in overlapping configuration; Area - total area of the 200-600 m stratum available in the Azorean EEZ; CPUE - Catch per Effort Unit (number of ind. per trap); W - average weight in the catch.

R (m) 25* 30 35 40 45 2 Habitat at (m ) 1,963 1,164 2,032 2,880 3,755 Area (km2) CPUE Biomass (t) LCI 1.18 3,367 5,678 3,253 2,295 1,760

11,106 1.95 5,570 9,392 5,381 3,797 2,912 Banks and seamounts UCI 2.72 7,773 13,106 7,509 5,299 4,064 LCI 4.56 3,156 5,322 3,049 2,152 1,650

Coastal zones 2,694 5.39 3,734 6,296 3,607 2,545 1,952 UCI 6.22 4,312 7,270 4,166 2,939 2,254 * Non-interaction condition between traps. W = 0.505 kg

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Table 5. Maximum sustainable yield (MSY) of the toothed rock crab Cancer bellianus estimated for the aggregated bank and seamount areas of the Azorean EEZ. The table shows the lower (LCI) and upper (UCI) limits of the estimates for a 95% confidence interval. R – radius of attraction area of a trap; x – constant. Bold values correspond to the base option.

x R (m) Biomass (t) 0.1 0.2 0.3 0.4 0.5 LCI 3,367 51 101 152 202 253 25* Mean 5,570 84 167 251 334 418 UCI 7,773 117 233 350 466 583 LCI 5,678 85 170 255 341 426 30 Mean 9,392 141 282 423 564 704 UCI 13,106 197 393 590 786 983 LCI 3,253 49 98 146 195 244 35 Mean 5,381 81 161 242 323 404 UCI 7,509 113 225 338 451 563 LCI 2,295 34 69 103 138 172 40 Mean 3,797 57 114 171 228 285 UCI 5,299 79 159 238 318 397 LCI 1,760 26 53 79 106 132 45 Mean 2,912 44 87 131 175 218 UCI 4,064 61 122 183 244 305 * Non-interaction condition between traps.

Table 6. Maximum sustainable yield (MSY) of the toothed rock crab Cancer bellianus estimated for the aggregated coastal areas of the Azorean EEZ. The table shows the lower (LCI) and upper (UCI) limits of the estimates for a 95% confidence interval. R – radius of attraction area of a trap; x – constant. Bold values correspond to the base option. x R (m) Biomass (t) 0.1 0.2 0.3 0.4 0.5 LCI 3,156 47 95 142 189 237 25* Mean 3,734 56 112 168 224 280 UCI 4,312 65 129 194 259 323 LCI 5,322 80 160 239 319 399 30 Mean 6,296 94 189 283 378 472 UCI 7,270 109 218 327 436 545 LCI 3,049 46 91 137 183 229 35 Mean 3,607 54 108 162 216 271 UCI 4,166 62 125 187 250 312 LCI 2,152 32 65 97 129 161 40 Mean 2,545 38 76 115 153 191 UCI 2,939 44 88 132 176 220 LCI 1,650 25 50 74 99 124 45 Mean 1,952 29 59 88 117 146 UCI 2,254 34 68 101 135 169 * Non-interaction condition between traps.

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Estimates of biomass and potential yield for deepwater crabs off the Azores

Table 7. Average biomass of the deep-water red crab Chaceon affinis estimated at banks/seamounts and coastal zones of the Azorean EEZ. The table shows the lower (LCI) and upper (UCI) limits of the estimates for a 95% confidence interval. R - radius of attraction area of a trap; at - effective theoretical mean area of attraction of a trap in overlapping configuration; Area - total area of the 500-900 m stratum available in the Azorean EEZ; CPUE - Catch per Effort Unit (number of ind. per trap); W - average weight in the catch. R (m) 25 30 35 40 45 2 at (m ) – Commercial fishery 468 1,286 2,025 2,770 3,548 Habitat 2 at (m ) – Research surveys 1,963* 1,164 2,032 2,880 3,755 Area (km2) CPUE Biomass (t) LCI 4.63 170,324 62,004 39,394 28,794 22,480

32,775 5.37 197,721 71,978 45,731 33,425 26,096 Banks and seamounts UCI 6.12 225,119 81,951 52,067 38,057 29,712 LCI 0.52 596 1,006 576 407 312

Coastal zones 4,247 0.79 902 1,521 871 615 472 UCI 1.06 1,207 2,036 1,167 823 631 * Non-interaction condition between traps. W = 0.526 kg

Table 8. Maximum sustainable yield (MSY) of the deep-water red crab Chaceon affinis estimated for the aggregated bank and seamount areas of the Azorean EEZ. The table shows the lower (LCI) and upper (UCI) limits of the estimates for a 95% confidence interval. R – radius of attraction area of a trap; x – constant. Bold values correspond to the base option.

x R (m) Biomass (t) 0.1 0.2 0.3 0.4 0.5 LCI 170,324 2,555 5,110 7,665 10,219 12,774 25* Mean 197,721 2,966 5,932 8,897 11,863 14,829 UCI 225,119 3,377 6,754 10,130 13,507 16,884 LCI 62,004 930 1,860 2,790 3,720 4,650 30 Mean 71,978 1,080 2,159 3,239 4,319 5,398 UCI 81,951 1,229 2,459 3,688 4,917 6,146 LCI 39,394 591 1,182 1,773 2,364 2,955 35 Mean 45,731 686 1,372 2,058 2,744 3,430 UCI 52,067 781 1,562 2,343 3,124 3,905 LCI 28,794 432 864 1,296 1,728 2,160 40 Mean 33,425 501 1,003 1,504 2,006 2,507 UCI 38,057 571 1,142 1,713 2,283 2,854 LCI 22,480 337 674 1,012 1,349 1,686 45 Mean 26,096 391 783 1,174 1,566 1,957 UCI 29,712 446 891 1,337 1,783 2,228 * Non-interaction condition between traps.

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Table 9. Maximum sustainable yield (MSY) of the deep-water red crab Chaceon affinis estimated for the aggregated coastal areas of the Azorean EEZ. The table shows the lower (LCI) and upper (UCI) limits of the estimates for a 95% confidence interval. R – radius of attraction area of a trap; x – constant. Bold values correspond to the base option.

x R (m) Biomass (t) 0.1 0.2 0.3 0.4 0.5 LCI 596 9 18 27 36 45 25* Mean 902 14 27 41 54 68 UCI 1,207 18 36 54 72 91 LCI 1,006 15 30 45 60 75 30 Mean 1,521 23 46 68 91 114 UCI 2,036 31 61 92 122 153 LCI 576 9 17 26 35 43 35 Mean 871 13 26 39 52 65 UCI 1,167 17 35 52 70 87 LCI 407 6 12 18 24 30 40 Mean 615 9 18 28 37 46 UCI 823 12 25 37 49 62 LCI 312 5 9 14 19 23 45 Mean 472 7 14 21 28 35 UCI 631 9 19 28 38 47 * Non-interaction condition between traps.

Chaceon affinis DISCUSSION The estimated average biomass at banks/seamounts ranged from approximately 26,096 to 197,721 t, Distribution and catches depending on the value of the radius of attraction The results showed two important facts: a) the adopted for a trap. These values corresponded to a abundance of the studied resources seems to vary mean density between 2 and 12 individuals per 1,000 considerably in their spatial distribution, although m2. at coastal zones, estimated average biomass the depth range of the species can be well values varied between 472 and 521 t, corresponding defined; and b) there seems to be areas/strata of to mean densities between 0.2 and 0.7 individuals dominance for each species with Cancer per 1,000 m2 (Table 7). The potential yield varied bellianus being more abundant in coastal zones considerably according to the combination of and Chaceon affinis on banks/seamounts (Tables each radius of attraction area (R) and exploitation 1 and 2). rate (constant of empirical equation, x) (Tables 8 The variability of abundance for the two and 9). In the most pessimistic scenario, MSY species within each area can be explained by was estimated to 391 t of the deep-water red crab several factors. However, it is likely that different on banks and seamounts, and 14,829 t in the most bottom types from site to site or at the same site optimistic one (Table 8). In coastal zones, values from stratum to stratum is the main factor (Pinho of 7 t in a pessimistic scenario and 114 t in an et al. 2001b, c; Biscoito et al. 2015; Triay-Portella optimistic one, were estimated (Table 9). et al. 2017; Santos et al. 2019). This

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Estimates of biomass and potential yield for deepwater crabs off the Azores appears to be more evident for Chaceon affinis size, structure, and abundance. However, to that showed a clear aggregate distribution identify the essential habitat can be a difficult task ("patches"), possibly reflecting the preference for since the same species can use different habitat specific habitats, e.g. muddy bottom with some types for different purposes related to their life rocks. Variable abundance may also be explained cycle or life history (e.g. spawning in one area by sampling bias due to seasonal changes, for and foraging in another). instance in migration movements and spawning. The reason why the abundance of Chaceon The differences in density observed between affinis is considerably lower in coastal areas than coastal areas and banks/seamounts are more in banks/seamounts is unclear, but the difference difficult to explain. A possible ecological may have been magnified by bias sampling. significance of the dominance of each species in Samples from bank areas were obtained from a particular habitats should be explored. The lower commercial fishing vessel that concentrated its abundance of Cancer bellianus on fishing activity in areas of greater abundance, banks/seamounts appears to be due to the depths while data from coastal areas resulted from a available, which makes the habitat area for this stratified random sampling (research surveys). species considerably smaller (Pinho et al. 2001c). The total areas available in the Azorean EEZ It should be noted that in coastal areas, where all for depths considered optimal for species depth strata are present the habitat can be defined distribution are relatively scarce (Figure 1). These continuously, although in some areas the strata areas, defined as habitats, also have the may be wider or narrower than in others. For peculiarity of being spatially discontinuous banks/seamounts, on the contrary, the (islands and banks/seamounts). For the purposes discontinuity predominates due to diversity of of estimating the fishery potential, areas were sizes, shapes, elevations and inclinations between aggregated at local (coastal) and offshore these structures, or even within the same structure (banks/seamounts) zones due to the importance (see Machete et al. 2005). Another explanation they have for management purposes related to may be that the catches used for this analysis do fishing technology and vessel characteristics not reflect indices of abundance in these offshore necessary for the exploitation at each area. The areas because the sampling coverage may not be interactions among different areas related to the representative of the total area. In this study, 83 dynamics of each population are unknown and banks/seamounts were identified in the Azorean therefore, it is not yet known if each of these EEZ. Among them, only 35% were considered to areas should be managed as a management unit. have C. bellianus, although only 7% of the cases A research programme with implementation detected the occurrence of the entire habitat priorities to better understand the approach to be (areas with depths between 200 and 700 m). The followed in the management of these fisheries, abundance index used for C. bellianus came only would be necessary. However, considering that from an area partially covered by research they are fragile habitats, any development of a surveys, the Princess Alice Bank. However, it fishery must take these uncertainties into must be asked if the result of sampling of a consideration to avoid local depletion or even bank/seamount should be extrapolated to other overexploitation because of connectivity areas of identical characteristics or not. The mechanisms between areas and subpopulations. abundance index used for Chaceon affinis came Catches approximately equal to 5 individuals from samples taken from four banks/seamounts, per trap for each species in dominance areas but 70% of the samples were taken from Princess (coastal areas for Cancer bellianus and Alice bank. The representativeness of these banks/seamounts for Chaceon affinis) can be samples is an issue that future studies should considered reasonable. In the case of Chaceon confirm. affinis, catches in the Azores (global average of 3 Further studies are needed to clarify the kg trap-1) agreed with the minimum and essential habitat for these species and to maximum catch values found in other world areas understand how habitat limits population for similar species (see Arana 2000).

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Estimates of biomass and potential yield traps per day and 200 annual fishing days, the average catch per vessel would be approximately Biomass and potential yield results showed a -1 considerable variability depending on the values 98 t year . In these areas, it would be sustainable adopted for the trap radius of attraction (R) and to develop an initial fishery with approximately the exploitation rate (x) (Table 4-9). Similar three vessels. results are expected for a range of different Chaceon affinis catchability values that may be adopted. The total average biomass of C. affinis estimated for It should be noted that the estimated values the Azorean EEZ, considering an optimum average R correspond to estimates in data-poor situations (in of 30 m, was 73,499 t (Table 7). However, this this case, virgin, i.e. not exploited resources). density varied considerably with the habitat, Thus, the results are valid as short-term approximately 4 individuals per km2 at indicators, for example for a fishery banks/seamounts and approximately 0.7 individuals implementation, and should not be confused as per km2 in coastal areas. These densities are within indicators of MSY for a long-term fishery, which the limits of mean densities estimated for deep-water should be estimated after the start of exploration. crab species in other world areas (see Arana 2000). Cancer bellianus Considering the base values of x = 0.2 and R = The total average biomass of C. bellianus 30 m, the average annual MSY for the Azorean EEZ was estimated to approximately 2,205 t year- estimated as most likely for the Azorean EEZ, 1 -1 -1 considering an optimal average R of 30 m, was (2159 t year at banks/seamounts and 46 t year 15,688 t, corresponding to a total mean density of in coastal areas). Assuming an average CPUE of -1 -1 approximately 2.3 individuals per km2 (Table 4). 0.7 kg trap (computed as the average kg trap However, this density varied spatially, being for the combined trap sets for coastal depth strata much more abundant in coastal areas, range of 500-900 m), a total of 200 traps to fish approximately 5 individuals per km2, than in per day (three lines with approximately 66 traps bank/seamount zones, approximately two each) and 200 annual fishing days per year, the individuals per km2. Although estimates of average catch per vessel would be approximately -1 abundance for these species are not reported in 32 t year in coastal areas. Considering the the literature, these values can be considered quite fishery potential of the resource in these areas (46 -1 reasonable and particularly high in coastal areas. t year ), it would be sustainable to develop an Considering the base values of x = 0.2, as initial fishery with approximately one vessel. For suggested by Beddington & Cooke (1983), and R bank/seamount areas, assuming a CPUE of 2.8 kg -1 -1 = 30 m, it was estimated as the average annual trap (computed as the average kg trap for the MSY for the Azorean EEZ approximately 471 t combined trap sets for bank/seamount depth strata year-1 (282 t year-1 at banks/seamounts and 189 t range of 500-900 m), a total of 500 traps per day -1 and 200 annual fishing days, the average catch year at coastal areas). Assuming an average -1 CPUE for coastal areas of 2.7 kg trap-1 (computed per vessel would be approximately 283 t year . In as the average kg trap-1 for the combined trap sets these areas, it would be sustainable to develop an for coastal depth strata range of 200-600 m), a initial fishery with approximately seven vessels. total of 200 traps to fish per day (three lines with approximately 66 traps each) and 200 annual Methodology fishing days per year, the average catch per vessel The effective trapping area method (Miller 1975; would be approximately 109 t year-1. Considering Eggers et al. 1981) is only an approximation the fishery potential of the resource in these areas whose quality depends on several basic (189 t year-1), it would be sustainable to develop assumptions of the model indirectly related to the an initial fishery with approximately two vessels. fixed gear capture process (Fernö & Olsen 1994) For bank/seamount areas, assuming a CPUE of and more directly with the degree of reliability of 0.98 kg trap-1 (computed as the average kg trap-1 the values of some variables used, such as for the combined trap sets for bank/seamount average CPUE, radius of attraction of a trap, total depth strata range of 200-600 m), a total of 500 size of the estimated area, etc.

32

Estimates of biomass and potential yield for deepwater crabs off the Azores

Soak time and gear saturation, for example, are depths available, bottom type). However, results considered the variables of the fixed gear capture from commercial fishery directed to C. affinis process that most affect the abundance estimation during 2003 also showed low abundances of C. (Murphy 1960; Rothschild 1967; Sigler 2000; bellianus in bank/seamount areas, estimating for Bacheler et al. 2013). The operational regime of the 200-800 m stratum a CPUE of 0.31 ± 0.47 data used in the analyses of the abundance individuals trap-1. It should be noted, however, estimates is more or less standardized (24 h that the industrial vessel that operated in 2003 immersion, similar standard gears with during this fishing experience made the sets approximately the same space between them and primarily at banks and at depths usually below with the same average branch line; Pinho et al. 600 m, which is considered to be the limiting 2001b, c). However, the soak time and gear depth of C. bellianus. Also, the population saturation effects were not analysed in the present structure can vary seasonally with depth, as study. suggested by Pinho et al. (2001c). The optimal radius of attraction of a trap is The estimation of the total area available for another factor affecting the abundance estimation. each species was based on a planar estimation For example, the use of a radius smaller than the using available bathymetric information. optimum, can considerably underestimate the However, imprecision of these bathymetric data biomass. The method assumes that each trap has a can introduce great errors in the strata size fixed catch field with a circular shape centred in estimation, especially on bank/seamount zones the trap. Optimum values for radius of attraction which are still insufficiently mapped. have been reported as between 27 and 33 m Additionally, some areas, such as the Menez (Miller 1975; Cayre et al. 1979; McElman & Gwen hydrothermal vent, have not been Elner 1982; Defeo 1991). However, Sigler (2000) considered in this study. However, hydrothermal considered that the radius of attraction of a trap is vents have been identified as areas with the not fixed, and it is not valid to estimate its value highest catches of C. affinis when compared to from experiments with variable spaces between other seamounts and coastal regions, being traps, since the field of attraction increases possible areas to be protected although their considerably with the concentration of traps. For ecological role in the distribution of this resource this reason, different values of radius of attraction remains unknown (Pinho et al. 2001b; Santos et varying between 25 and 45 m were used in this al. 2019). study, in order to analyse the sensitivity of The methodology used to estimate the MSY for abundance variability with this parameter. virgin resources suggested by Gulland (1971) is However, the value of 30 m was considered as empirical, and there is no explicit scientific optimal for purposes of comparison with other justification for that mathematical expression. studies. However, it is considered reasonable in the The abundance index (CPUE) used to calculate assumptions that the natural growth of biomass biomasses may not be representative of the actual follows the production model of Schaefer (1954) abundance of the stocks, since it was estimated and that fishing mortality corresponding to MSY from non-standardized exploratory research is equal to the natural mortality (for details, see surveys with samples taken at different times of Gulland 1971; Die & Caddy 1997). In the present the year in a reduced area of distribution of the study, different values for exploitation rate (x) resource or from commercial fishing experiences were used in order to analyse the sensitivity of the probably carried out only in areas of high MSY variability with this parameter. concentration of resources. For example, the In view of these inaccuracies, our results CPUE of Cancer bellianus estimated from the should be considered preliminary and interpreted Princess Alice Bank survey data (Table 1) may as guides on the species abundances and for not be representative of species abundance on all management and development of possible banks and seamounts because the sampling area fisheries (precautionary approach principle). We may not be representative of the abundance in consider that more important than the precision of banks/seamounts of different characteristics (e.g. the estimates is the order of potential catches 33

Pinho et al.

values estimated, which suggests that the Final considerations exploitation of these resources, if desired, should The scientific knowledge of these resources in the always be on a very small scale and highly Azorean EEZ until the present moment went controlled. This is the most important through three initial phases: 1) preliminary contribution of this study and it may be observation of the species occurrence; 2) extrapolated to other remote insular areas. preliminary collection of biological information and

fisheries technology; and 3) hypotheses formulation Management about the distribution and abundance of resources The implementation and management of a spatial and prediction of potential yields (MSY) from these exploitation scheme for these resources should be hypotheses. The next step should be to identify key considered, despite the current limitations of variables to evaluate and to test these predictions. knowledge, especially on the mobility of individuals This objective involves several studies that integrate and connectivity between adjacent areas. the abundance estimation by areas and analysis of Although it is convenient to manage these the population structure according to the resources by island and bank/seamount, the environmental characteristics (resource-environment difficulties of implementing, managing and analysis); growth and reproduction studies, supervising a complex exploration design, suggest including early life-history stages characterization; that it may be more appropriate to implement species- and theoretical modelling of the impacts of the based fisheries with licensing by aggregated areas, implementation of different commercial exploration such as coastal and bank/seamounts. strategies on population dynamics, including Measures for statistical collection on fisheries and multispecies and multiarea spatiotemporal biological information should be promoted by dynamics. In this perspective, it is recommended introducing for example the fishing logbook and to that all results obtained be presented, discussed and condition the license renewal to its proper completion validated in working groups within international and delivery, and the on-board observers or landings scientific forums. control under a sampling programme. Ovigerous females of Cancer bellianus are not generally captured (Pinho et al. 2001c) which in itself ACKNOWLEDGMENTS can function as a conservation measure. However, the introduction of a minimum landing size (MLS) of 13 We are grateful to Gui Menezes, Helen Martins, cm carapace width (8.5 cm carapace length), Nagib Souza and Ricardo Medeiros for their corresponding to the size of first maturation, is support. We thank all the crew members of R/V recommended in order to preserve the juveniles. “Arquipélago”, and “Três Rosas”, “Alexa Marie”, Ovigerous females of Chaceon affinis occur “Garcia Miguel” and “Pescatum” commercial approximately between October and March (Pinho et vessels, for all assistance during the data al. 2001b; Biscoito et al. 2015). These months collection. Régis Santos was supported by the correspond to the period of reduced fleet activity in IMAR Institute of Marine Research, through a the Azorean EEZ due to the meteorological post-doc fellowship (ref. conditions, and a design of seasonal exploitation with IMAR/DEMERSAIS/001-2018). Wendell Silva a fishing stop during this period should be considered. was funded by the IMAR Instituto do Mar, The aim would be to control fishing effort and avoid through a scholarship (ref. local depletion effects, especially at bank/seamount IMAR/UNI/MAR/04292/2013 MARE/001-2018). areas. It is also suggested that an MLS of 8.5 cm Ana Novoa-Pabon was funded by an FCT Ph.D. carapace length should be introduced to protect fellowship (ref. SFRH/BD/124720/2016). juveniles.

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Estimates of biomass and potential yield for deepwater crabs off the Azores

REFERENCES Fisheries No. 4: . Rome, FAO, 82 pp. Fernö, A. and S. Olsen 1994. Marine fish behaviour in Arana, P.M. 2000. Estimación de abundancia y capture and abundance estimation. Oxford, Fishing biomasa del cangrejo dorado (Chaceon chilensis), New Books, 221 pp. en el archipiélago de Juan Fernández, Chile. Garcia, S. and L. Le Reste 1981. Life cycles, dynamics, Investigaciones Marinas 28: 53-68. exploitation and management of coastal penaeid Bacheler, N.M., Z.H. Schobernd, D.J. Berrane, C.M. shrimp stocks. FAO Fisheries Technical Paper Schobernd, W.A. Mitchell and N.R. Geraldi 2013. 203: 1-215. When a trap is not a trap: converging entry and exit Garcia, S., P. Sparre and J. Csirke 1989. Estimating rates and their effect on trap saturation of black sea surplus production and maximum sustainable yield bass (Centropristis striata). ICES Journal of from biomass data when catch and effort time series Marine Science 70: 873-882. are not available. Fisheries Research 8: 13-23. Bashmachnikov, I. and A. Martins 2007. Water masses, Gonçalves, J.M. 1994. “Lucky Strike”, outras fontes circulation patterns and oceanographic data density hidrotermais, escorrências frias e relatório de of the subtropical NE Atlantic, Presentation, 1st participação na 2ª parte da campanha “Diva-2”. DEECON meeting, Horta, Azores, 29-31 Oct. Arquivos do DOP, Série Estudos 3/94, 26 pp. 2007. Gonçalves, J.M., H.R Martins and M.R. Pinho 1995. Beddington, J.R. and J.G. Cooke 1983. The potential Deep water crabs, Chaceon affinis, a new fisheries yield of fish stocks. FAO Fisheries Technical resource in the Azores? ICES CM 1995/K:43. Paper 242: 1-47. Gonçalves, J.M. and M.R. Pinho 1994. Relatório da Biscoito, M., M. Freitas, J.G. Pajuelo, R. Triay- campanha nº17/94 do N/I Arquipélago (ensaio de Portella, J.I. Santana, A.L. Costa, J. Delgado and pesca de crustáceos de profundidade com covos, J.A. González 2015. Sex-structure, depth manutenção do DCP da Graciosa e arrastos de bongo). distribution, intermoult period and reproductive Arquivos do DOP, Série Cruzeiros, 1/94, 7 pp. pattern of the deep-sea red crab Chaceon affinis González, J.A., I.J. Lozano, J.M. Lorenzo, L.J. López- (Brachyura, Geryonidae) in two populations in the Abellán, J.M. Bautista, D.M. Carvalho, M.J. north-eastern Atlantic. Deep-Sea Research Part I: Biscoito and G. Menezes 1998. Biology of some Oceanographic Research Papers 95: 99-114. Macaronesian deep-sea commercial species. Final https://doi.org/10.1016/j.dsr.2014.10.010. report of the UE-DG XIV Study contract 95/032. Cayré, P., P. Le Loeuff and A. Intès 1979. Geryon Telde, Las Palmas, Instituto Canario de Ciencias quinquedens, le crab rouge profond : biologie, Marinas, 356 pp. pêche, conditionnement, potentialities Gulland, J.A. 1971. The fish resources of the ocean. d`exploitation. La Pêche Maritime 1210: 1-8. West By-fleet, Surrey, Fishing News (Books), Ltd., Cores, C., M. Gaspar and K. Erzini 2019. Estimating for FAO, 255 pp. rev. ed. of FAO Fisheries the density of Pennant's swimming crab, Technical Paper 97: 1-425. Portumnus latipes (Pennant, 1777) in the swash Gulland, J.A. 1983. Fish stock assessment: a manual of zone using baited stakes and area of attraction. basic methods. New York, Wiley, 223 pp. Journal of the Marine Biological Association of the ICES 2018a. Advice basis. In Report of the ICES United Kingdom 99(4): 887-890. Advisory Committee, 2018. ICES Advice 2018, doi:10.1017/S002531541800067X Book 1, Section 1.2. Defeo, O., V. Little and L. Barea 1991. Stock https://doi.org/10.17895/ices.pub.4503 assessment of the deep-sea red crab Chaceon ICES 2018b. Report of the Working Group on the notialis in the Argentinian-Uruguayan Common Biology and Assessment of Deep-sea Fisheries Fishing Zone. Fisheries Research 11: 25-39. Resources (WGDEEP), 11–18 April 2018, ICES Die, D.J. and J.F. Caddy 1997. Sustainable yield HQ, Copenhagen, Denmark. ICES CM indicators from biomass: are there appropriate 2018/ACOM:14, 771 pp. reference points for use in tropical fisheries? ICES 2019. Azores ecoregion – Ecosystem overview. In Fisheries Research 32: 69-79. Report of the ICES Advisory Committee, 2019. Eggers, D.M., N.A. Rickard, D.G. Chapman and R.R. ICES Advice 2019, Section 3.1. Whitney 1982. A methodology for estimating area https://doi.org/10.17895/ices.advice.5753. fished for baited hooks and traps along a ground Machete, M., T. Morato and G. Menezes 2005. line. Canadian Journal of Fisheries and Aquatic Modeling the distribution of two fish species in Sciences 39: 448-453. seamounts of the Azores. FAO Fisheries FAO, 1997. FAO Technical Guidelines for Responsible Proceedings 3/1: 182-195.

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McElman, J.F. and R.W. Elner 1982. Red crab (Geryon 2001a. Pesca experimental de crustáceos de quinquedens) trap survey along the edge of the profundidade dos Açores (CRUSTAÇO). Arquivos Scotian shelf, September 1980. Canadian do DOP, Série Relatórios internos, Nº2/2001. Technical Report of Fisheries and Aquatic Sciences Rikhter, V.A. and V.N. Efanov 1976. On one of the 1084: 1-12. approaches to estimation of natural mortality of Melo, O.E.B.M. 2009. Biologia e abundância do fish populations. ICNAF Research Documents camarão Plesionika edwardsii (Brandt, 1851) nos 76/VI/8: 12 pp. Açores. (Dissertação de Mestrado em Estudos Rothschild, B.J. 1967. Competition for gear in a Integrados dos Oceanos). Horta: Universidade dos multiple-species fishery. ICES Journal of Marine Açores, 67 pp. Science 31: 102-110. Melville-Smith, R. 1986. Red crab (Geryon maritae) Santos, R., M. Pinho, O. Melo, J. Golçalves, A. density in 1985 by the technique of effective area Leocádio, A. Aranha, G. Menezes and E. Isidro fished per trap on the northern fishing grounds of 2019. Biological and ecological aspects of the South West Africa. South African Journal of deep-water red crab populations inhabiting isolated Marine Science 4: 257-263. seamounts to the west of the Azores (Mid‐Atlantic Melville-Smith, R. 1988. The commercial fishery and Ridge). Fisheries Oceanography, https population dynamics of red crab Geryon maritae ://doi.org/10.1111/fog.12454. off South West Africa, 1976-1986. South African Schaefer, M. 1954. Some aspects of the dynamics of Journal of Marine Science 6: 79-95. the populations important to the management of the Miller, R.J. 1975. Density of the commercial spider commercial marine fisheries. Inter-American crab, Chionoecetes opilio, and calibration of Tropical Tuna Commission Bulletin 1(2): 23-56. effective area fished per trap using bottom Sigler, M.F. 2000. Abundance estimation and capture photography. Journal of the Fisheries Research of sablefish (Anoplopoma fimbria) by longline Board of Canada 32: 761-768. gear. Canadian Journal of Fisheries and Aquatic Murphy, G.I. 1960. Estimating abundance from Sciences 57: 1270-1283. longline catches. Journal of the Fisheries Research Smith, W.H.F. and D.T. Sandwell 1997. Global seaflor Board of Canada 17: 33-40. topography from satellite altimetry and ship depth Pinho, M.R. 2000. Pesca experimental de crustáceos de soundings. Science 277: 1957-1962. profundidade nos Açores (CRUSTAÇO). Relatório Tanaka, S. 1960. Studies on the dynamics and de progresso. Arquivos do DOP, Série Relatórios management of fish populations. Bulletin of Tokai internos, nº4/2000, 31 pp. Regional Fisheries Research Laboratory 28: 1-200. Pinho, M.R., J.M. Gonçalves, H.R. Martins and G.M. [in Japanese]. Menezes 2001b. Some aspects of the biology of the Triay-Portella, R., J.G. Pajuelo and J.A. González deep-water crab, Chaceon affinis (Milne-Edwards 2017. Spatio‐temporal variation in biomass of the and Bouvier, 1984) off the Azores. Fisheries deep-sea red crab Chaceon affinis in Gran Canaria Research 51: 283-295. Island (, Eastern-Central Atlantic). Pinho, M.R., J. Gonçalves and H. Martins 2001c. Marine Ecology 38(5): 1-14. Biology and abundance of Cancer bellianus https://doi.org/10.1111/maec.12462 (Decapoda, Brachyura) around the Azores. ICES Journal of Marine Science 58: 896-903. Submitted 6 Dec 2019. Accepted 7 Apr 2020. Pinho, M.R., O. Melo, J. Gonçalves and H. Martins Published online 30 Jun 2020.

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Arquipelago - Life and Marine Sciences ISSN: 0873-4704

Frondose and turf-dominated support distinct trophic pathways: evidence from 15N and 13C stable isotope analyses

CLÁUDIA HIPÓLITO, RAUL M.A. NETO, TARSO M.M. COSTA, MARIA A. DIONÍSIO, AFONSO C.L. PRESTES, JOSÉ M.N. AZEVEDO, GUSTAVO M. MARTINS AND ANA I. NETO

Hipólito, C., R.M.A. Neto, T.M.M. Costa, M.A. Dionísio, A.C.L. Prestes, J.M.N. Azevedo, G.M. Martins and A.I. Neto 2020. Frondose and turf-dominated marine habitats support distinct trophic pathways: evidence from 15N and 13C stable isotope analyses. Arquipelago. Life and Marine Sciences 37: 37 – 44. https://doi.org/10.25752/arq.23546

Marine vegetation plays an important structuring role, delivering key functions and services to coastal systems the extent of which depends on the foundation species and their architecture. In increasingly urbanised coastlines, turf-forming macroalgae are replacing frondose morphotypes. Trophic relationships within these systems can be studied through stable isotope analysis of the different food web compartments. In the present study, we investigated trophic pathways in two distinct macroalgal assemblages: one dominated by small brown frondose algae, and one dominated by low-lying turf-forming species. 15N and 13C isotopic signatures were determined for selected macroalgae and sedentary from distinct trophic levels, collected from two habitats on São Miguel Island (Azores, Portugal). In frondose habitats macroalgae appeared to make up the primary carbon source for the entire food web, whilst in turf-dominated habitats there was a decouple between macroalgae and higher trophic levels. Because canopy replacement by algal turf may affect the structure of the littoral food webs, coastal biodiversity conservation strategies should give priority to natural areas rich in canopy-forming algae.

Key words: Trophic pathways; Habitat; Macroalgae; Food web; Stable isotopes

Cláudia Hipólito1 R.M.A. Neto2, T.M.M. Costa2, M.A. Dionísio3, A.C.L. Prestes2, J.M.N. Azevedo2, G.M. Martins4 and A.I. Neto2. 1Regional Fund for Sciences and Technology, Rua do Mercado 21, 9500-326 Ponta Delgada, Portugal. 2Centre for Ecology, Evolution and Environmental Changes/Azorean Biodiversity Group (cE3c) & Faculty of Sciences and Technology, University of the Azores, Rua da Mãe de Deus, 13-A, 9500-321 Ponta Delgada, Portugal. 3MARE ULisboa, Faculdade de Ciências da Universidade de Lisboa, Campo Grande, 1749-016 Lisboa, Portugal. 4AQUAZOR, Rua da Pranchinha, 92, 9500- 331 Ponta Delgada, Portugal.

Author for Correspondence: Ana I. Neto, E-mail: [email protected]

INTRODUCTION element of coastal ecosystems (Steneck et al. 2002). Warmer temperate and/or subtropical The functioning and complexity of services communities are characterized by two algal provided by marine vegetated ecosystems depend morphotypes, a canopy type of growth composed on the assemblage and architecture of foundation by associations of two or more species of species. In temperate areas, for instance, large frondose algae, and algal turfs, which are forests of brown seaweeds are the structural complex assemblages of macroalgae with 37

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compact growth, about 5 cm in height, and well (e.g. limpets) suggesting that human exploitation developed entangled prostate axes (Lawson & may have shifted the community to an alternative Norton 1971; Price & Scott 1992; Neto 2001; stable state, and that continued exploitation of Wallenstein et al. 2009; Martins et al. 2016). limpets is the key driver allowing turfs to Canopy-forming algae modify several biotic and dominate (Martins et al. 2010). abiotic factors of rocky shore ecosystems, and are Stable isotopes of Nitrogen and Carbon have fundamental in creating and maintaining habitats been successfully used for a range of applications and their assemblages and ecological processes in marine ecology (Behringer & Butler IV 2006; (Bulleri et al. 2002; O’Brien et al. 2018). They Carvalho 2008; Gillies et al. 2012), such as are, however, considerably vulnerable to comparative studies of aquatic food chains anthropogenic disturbances, and are being (Cabana & Rasmussen 1996; Behringer & Butler increasingly replaced by turf-forming algae in IV 2006) and investigating human impact on urbanised coastlines (e.g. Benedetti-Cecchi et al. coastal ecosystems (e.g. Page et al. 2013; 2001), due to the latter’s rapid lateral vegetative Mancinelli & Vizzini 2015). Following growth (Airoldi 1998) and consequently high considerable methodological and technological rates of colonisation under high sedimentation advances in this rapidly growing field, stable and nutrient input (Worm et al. 2001). Along with isotopes have become reliable tools for studying the fact that this type of algal growth can hinder food chain structure (Peterson 1999; Phillips et al. the recruitment of its canopy-forming counterpart 2014). (Kennelly 1987), these characteristics enable turf- The Carbon-13 stable isotope may be forming algae to dominate urbanized coasts, effectively used to identify the food chain’s which poses a major threat to the biodiversity of carbon sources, as there is considerable variation those ecosystems (Gorgula & Connell 2004). in the ratio of 13C to 12C (δ13C) among producers, In the subtropical Azores archipelago, kelps and little variation once incorporated in the higher occur only in limited deep water habitats (Tittley levels of the trophic pathways (Layman et al. et al. 2001), and there are no records of seagrass 2011). The ratio of 15N to 14N (δ15N), on the other and other warm-water vegetated habitats. Instead, hand, increases predictably from one trophic level the Azorean shallow subtidal (up to 40 m depth) to the next (Post 2002), and may thus be supports extensive beds of frondose vegetation employed to infer an organism’s position in the generally dominated by associations of brown food chain. Therefore, the combined analysis of algae, namely Dictyota spp., Halopteris filicina Carbon and Nitrogen stable isotope ratios is an and, most commonly, Zonaria tournefortii (Neto effective approach to investigate trophic 2000a, 2000b, 2001; Tittley & Neto 2000). Even pathways and energy flow within marine food though these macroalgae have not traditionally webs (Lepoint et al. 2003). been designated as canopies, they can attain Here we employ stable isotopic analysis to substantial sizes (>30 cm) and effectively shadow investigate whether there are functional the understory assemblage (e.g. Martins et al. differences between two distinct habitats, one 2016). Comparatively little is known about the dominated by frondose and the other by turf- ecological and functional role of the habitats forming macroalgae, in order to better understand dominated by these smaller brown algae. Another the potential consequences of canopy replacement benthic coastal habitat in the Azores is structured on the dynamics and structure of coastal by low-lying multispecific turf-forming algae, ecosystems. such as the red seaweeds Ellisolandia elongata and Gelidium spp. (Martins et al. 2016). Thus the Azorean coastal habitats, which are increasingly MATERIALS AND METHODS subject to human pressure and activities, match the basic conditions for the dynamics of canopy Study site and sampling method replacement. For instance, the dominance of turf- This work was carried out on two distinct forming algae in the Azores intertidal was seen to shallow-water habitats in the south coast of São be related with the overexploitation of herbivores Miguel Island, Azores (Fig. 1), one dominated by 38

Trophic pathways in frondose and turf dominated habitats

Fig. 1. Map of Azores Archipelago (a), São Miguel Island (b) and sampling locations (c): two frondose-dominated (Feteiras and Lagoa, black triangles) and two turf-dominated habitats (Santa Clara and São Roque, black circles). small frondose macroalgae (Asparagopsis spp., Parmentier 2016), and carnivores by the Dictyota spp. and Halopteris spp.) and one predatory gastropod Stramonita haemastoma dominated by low-lying turf-forming red algae (Carriker 1981) and the ambush predator rockfish (corresponding to macroalgae with <5 cm height Scorpaena maderensis (La Mesa et al. 2007). forming dense mats), mostly short strands of Hermit crabs have a generalized omnivorous Ellisolandia elongata (see Martins et al. 2016 for mode of feeding on benthic particles, detritus and further description of the studied communities). moderately macroscopic material, depending, Two sites were chosen for each habitat, similar in therefore on a reasonable amount of scavenging depth (5-15 m), seawater temperature, wave (Kunze & Anderson 1979; Schembri 1982). S. exposure and other physical factors. The selection lurida maintains farms of turf-forming algae of species (biotic entities) for this study took into (personal observation), and like all the members consideration two main criteria; their sedentary of the Stegastinae subfamily feeds upon the algae, life style, which ensured habitat representation; as well as on the detritus and invertebrates caught and their abundance in both habitats, which up in them (Frédérich & Parmentier 2016). ensured trophic level representation and Macroalgae were scraped off from three facilitated specimen collection. Herbivores were haphazardly-selected 0.15 x 0.15 m replicate represented by the sea urchin Sphaerechinus quadrats into fine mesh net bags. Three granularis (Verlaque 1981), omnivores by the specimens of each invertebrate and fish species tubularis (Kunze & were collected, by hand and , Anderson 1979; Schembri 1982) and the Canary respectively. damselfish Similiparma lurida (Frédérich & Sampling took place in May 2014, in a short 4-

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day period (9th – 13th) in order to reduce 3-way mixed model analysis of variance with the temporal variations in isotopic composition following factors: habitat (2 levels, fixed), site (2 (Heminga & Mateo 1996; Jennings et al. 1997). levels, random and nested within habitat) and Samples were stored on ice immediately after biotic entities (algal morphotypes and arrival on the boat and no later than 30 minutes species; 6 levels, fixed). Prior to analysis, after collection. Cochran's test was used to assess heterogeneity of At the laboratory, algae were gently rinsed with variances and transformations were applied when tap water in order to remove all visible necessary. When required, a posteriori Student- macrofauna and detrital fragments, and oven- Newman-Keuls (SNK) tests were used. All dried at 60ºC until constant weight (about 48 h). analyses were run using GMAV5 (University of Following the instructions of the certificated Sydney). At one of the sites (Santa Clara) only MARINNOVA Laboratories of Porto, Portugal two (instead of three) replicates of S. haemastoma where the stable isotope ratios were determined, were available. In order to keep the analysis sea urchin gonads, fish muscle and skin samples, balanced, the missing value was replaced by the and whole gastropods and crustaceans were mean of the other two replicates, and one degree frozen, accommodated, and sent for analysis. The of freedom was subtracted from the residual. isotope analysis results were expressed relative to the primary patterns, air N2 for nitrogen and the Peedee belemnite marine limestone (PDB) RESULTS standard for carbon. 15N:14N and 13C:12C ratios were calculated following Wieser & Schwieters Although no δ13C differences were observed (2005) and Bahlmann et al. (2010). between habitats, both the differences between biotic entities and the interaction of habitat and Data analysis biotic entities were significant (P<0.001 and The 15N and 13C isotopic compositions of P<0.01 respectively, Table 1) and are illustrated consumers and producers on frondose- and turf- in Fig 2. Although the signatures of S. dominated communities were compared using a maderensis, S. haemastoma and C. tubularis

Fig. 2 – Relationship between δ13C and δ15N (‰) of producers and consumers in frondose and turf-dominated communities.

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Trophic pathways in frondose and turf dominated habitats show no variation, those of the macroalgae and S. remaining entities in the turf habitat (Table 1). granularis were higher in the frondose habitat, As for δ15N, neither the difference between where they aligned with the previously habitats nor the interaction of habitat and biotic enumerated entities, then in the turf habitat, entities was significant, but the difference where they matched that of S. lurida. The δ13C between biotic entities was highly significant signature of the latter varied in the opposite (P<0.001, Table 1), which is clearly displayed in direction, with higher values in turf than in Fig 2. Macroalgae exhibited the lowest δ15N frondose habitats, where it formed a separate signature, just below that of the herbivore S. group from the remainder of the biotic entities granularis, which was followed by those of the (Fig 2). SNK tests confirmed the significance of omnivore C. tubularis and the carnivores S. entity isotopic variations among habitats, and haemastoma and S. maderensis. The omnivore S. yielded two isotopic groups for each habitat, lurida had on average the highest δ15N values of separating S. lurida from all other biotic entities all the biotic entities. This ordering was in the frondose habitat, and grouping S. lurida, S. confirmed by SNK analysis of δ15N among biotic granularis and macroalgae apart from the entities (Table 1).

Table 1 - ANOVA testing the effects of habitat (frondose- versus turf-dominated) on the 15N and 13C isotopic composition of biotic entities (algal morphotypes and animal species). Significant differences noted in bolt. SNK pair-wise tests assessing the effects of habitat on the 13C isotopic composition of each biotic entity, and comparing the δ15N of the biotic entities.

δ13C δ15N Source df MS F P MS F P F-ratio Habitat 1 5.01 1.58 0.34 0.68 0.35 0.61 Site (Habitat) Site (Habitat) 2 3.17 4.46 0.02 1.95 13.20 <0.001 Residual Site (Habitat) x Biotic Biotic entities 5 39.62 32.75 <0.001 87.13 337.72 <0.001 entities Habitat x Biotic Site (Habitat) x Biotic 5 10.77 8.90 <0.01 0.21 0.80 0.57 entities entities Site (Habitat) x 10 1.21 1.70 0.11 0.26 1.75 0.10 Residual Biotic entities

Residual 47 0.71 0.15 Cochran´s test C = 0.21 (Not significant) C = 0.32 (P<0.01) δ13C δ15N Among habitats within biotic entities Among biotic entities S. maderensis Frondose = Turf S. lurida > S. maderensis > S. haemastoma > C. S. granularis Frondose > Turf tubularis > S. granularis > Algae S. lurida Frondose < Turf C. tubularis Frondose = Turf S. haemastoma Frondose = Turf Algae Frondose > Turf SNK Among biotic entities within habitats

Frondose habitat:

S. lurida < all other biotic entities Turf habitat: S. maderensis = S. haemastoma = C. tubularis

> S. granularis = S. lurida = Algae

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DISCUSSION ACKNOWLEDGMENTS

The significant macroalgal δ13C variation This research was supported by the European between habitats reflects their different species Commission BEST Preparatory Action, under the composition. The 15N isotopic signature of the sea project “ECOSUBVEG – Changes in submersed urchin is consistent with its strictly herbivorous vegetation: assessing loss in ecosystems services diet, and its 13C isotopic signature suggest that it from frondose to depauperate systems dominated feeds on the dominant macroalgal assemblage in by opportunistic vegetation”, ref. each habitat. In both habitats, the omnivore 07.032700/2012/635752/SUB/B2. The research damselfish S. lurida exhibited a 13C isotopic was also partially supported by Portuguese signature similar to that of the turf macroalgae, National Funds, through FCT – Fundação para a which is consistent with its diet of turf-forming Ciência e a Tecnologia, within the projects algae. Surprisingly, it showed the highest δ15N UID/BIA/00329/2013, 2015 - 2018, values, above even those of the carnivorous UID/BIA/00329/2019 and UID/BIA/00329/2020- rockfishes, with trophic shifts as high as +5.9‰. 2023. Logistic support was also provided by This apparently higher 15N accumulation rate may CIRN/UAc (Centre of natural Resources of arise from differential digestion or fractionation University of the Azores) and by CVARG during assimilation and metabolic processes (Centro de Vulcanologia e Avaliação de Riscos (McCutchan et al. 2003). Geológicos). GMM was supported by a post- The hermit crabs and the carnivorous doctoral grant awarded by FCT gastropods and fish exhibited no significant (SFRH/BDP/63040/2009 and variation in δ 13C or δ15N across habitats. In SFRH/BDP/108114/2015). Authors are grateful frondose habitats the 13C isotopic composition to Ruben Couto, João Faria, Nuno Álvaro, Marc was similar among all those species and the local Fernandez, Isadora Moniz, Eva Cacabelos, Carles macroalgae, suggesting that the latter provide the Mir, Anna Lloveras, Virginie Leyendecker, main carbon source for the remainder of the Jessica Coulon, Ana Sofia Carreiro, Filipe benthic food web. However, in turf-dominated Parreira, Rita Patarra and Emanuel Xavier who habitats there was a clear decouple between helped in the field and laboratory work. Thanks to macroalgae/sea urchins and the three species Nuno Álvaro for his assistance on map provision. mentioned above. This implies that the higher We appreciate the reviewer’s help in improving trophic levels in these habitats rely on exogenous the paper. carbon sources, possibly from the adjacent frondose habitats. It should be noted that the REFERENCES suspension- and deposit-feeding pathways were not considered in this study, and that sampling the Airoldi, L. 1998. Roles of disturbance, sediment stress, particulate organic matter pool (POM) could and substratum retention on spatial dominance in improve these results and explain part of the algal turf. Ecology 79: 2759–2770. observed decoupling. https://doi.org/10.1890/0012- These findings add to literature indicating that 9658(1998)079[2759:RODSSA]2.0.CO;2 habitats dominated by frondose macroalgae play an Bahlmann, E., S.M. Bernasconi, S. Bouillon, M. important ecological role in coastal ecosystems Houtekamer, M. Korntheuer, F. Langenberg, C. (Benedetti-Cecchi et al. 2001; Gorgula & Connell Mayr, M. Metzke, J.J. Middelburg, B. Nagel, U. 2004; Martins et al. 2016; Smale et al. 2013). Their Struck, M. Voß and K.C. Emeis 2010. Performance evaluation of nitrogen isotope ratio determination fundamental contribution to the energy flows on the in marine and lacustrine sediments: An inter- food webs is not matched by that of the increasingly laboratory comparison. Organic Geochemistry 41: dominant turf communities. Therefore, the current 3–12. trends of reduction of algal canopies pose a threat to https://doi.org/10.1016/j.orggeochem.2009.05.008 coastal biodiversity, which should be taken into Behringer, D.C. and M.J. Butler IV 2006. Stable consideration when devising conservation strategies. isotope analysis of production and trophic

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Arquipelago - Life and Marine Sciences ISSN: 0873-4704

Stock assessment prioritization in the Azores: procedures, current challenges and recommendations

RÉGIS SANTOS, WENDELL MEDEIROS-LEAL AND MÁRIO PINHO

Santos, Régis, W. Medeiros-Leal and M. Pinho 2020. Stock assessment prioritiza- tion in the Azores: procedures, current challenges and recommendations. Ar- quipelago. Life and Marine Sciences 37: 45 - 64. https://doi.org/10.25752/arq.23647

To implement the Marine Strategy Framework Directive (MSFD) of the European Union (EU) in order to achieve the Sustainable Development Goals (SDGs) of the United Nations (UN) regarding the biological sustainability of marine fisheries, it is fundamental to apply a framework for prioritizing stocks. This process helps the regional managers to make the best use of data and resources for management. The present study describes and applies a standard framework for prioritization of stock assessment in the Azores. The current state of the selected stocks is identified and the main issues and gaps for assessment are presented and discussed. A total of 138 species were landed in the region during the period 2009-2019. Twenty-two (18 fishes, 2 molluscs and 2 crustaceans) were selected as priority stocks according to the Food and Agriculture Organization of the United Nations (FAO) and International Council for the Exploration of the Sea (ICES) criteria. Most of these showed a decreasing trend in their abundances. Only four stocks are currently assessed using data- limited approaches: Pagellus bogaraveo, Aphanopus carbo, Raja clavata, and Trachurus picturatus. No biological reference points are defined and stock and exploitation status relative to Maximum sustainable yield (MSY) are not assessed. The main issues identified were the lack of information regarding catches and population structure and validated analytical methods. Future studies should evaluate which methods for assessment may be suitable for each stock and identify what additional data are needed to improve the analyses.

Key words: Sustainable Development Goals; Marine Strategy Framework Directive; fishery resources, management; Azores archipelago

Régis Santos1,2 (e-mail: [email protected]), Wendell Medeiros-Leal1,2, Mário Pinho1,2,3. 1IMAR Institute of Marine Research, University of the Azores, 9901-862, Horta, Portugal. 2Research Institute in Marine Sciences – Okeanos-UAc, University of the Azores, 9901-862, Horta, Portugal. 3Faculty of Science and Technology, Department of Oceanography and Fisheries, University of the Azores, 9901-862, Horta, Portugal.

INTRODUCTION required to produce the maximum sustainable yield (MSY) as determined by their biological Member States of the European Union (EU) are characteristics, at the latest by 2030. committed, through the implementation of the Stock assessment involves the application of Common Fisheries Policy (CFP), the Marine various statistical and mathematical calculations Strategy Framework Directive (MSFD) and the to estimate current and historical status and trends United Nations (UN) 2030 Agenda for of a fish stock, including abundance, mortality Sustainable Development and its Sustainable and productivity (Hilborn & Walters 1992). Full Development Goals (SDGs), to keep exploitable assessments utilize information on life history, marine stocks at biomass levels above those fishery-dependent data and stock abundance from

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Santos et al. fishery-independent surveys. These data feed Service - Lotaçor S.A. online database statistical models that fit available information to (https://lotacor.pt/pescado-descarregado) for the provide simplified representations of population period 2009-2019. For each species, taxonomic and fishery dynamics (Cadrin & Dickey-Collas classification (Fricke et al. 2020; WoRMS 2020), 2015). Therefore, if an assessment is based on common name in Portuguese and English (Froese & weak, inaccurate or outdated data, it might Pauly 2019; Palomares & Pauly 2019), FAO stock provide guidance that leads to or code (http://www.fao.org/fishery/collection/asfis/en), reduces available fishing opportunities. and landings in weight (t) and commercial value (€) Resources for providing accurate and timely were provided. Habitat information (habitat zone and assessment for all stocks on a regional or national depth range) was extracted from FishBase (Froese & scale are insufficient. The International Council Pauly 2019), SeaLifeBase (Palomares & Pauly 2019) for the Exploration of the Sea (ICES) and the and Santos et al. (2019a, 2020). Technical sheets of Food and Agriculture Organization of the United commercial marine species from the Azores (Lotaçor Nations (FAO) have discussed and proposed 2019) were used to classify the main fishing gear criteria for selecting exploitable stocks to be associated with capture of each species. Fishing gear assessed according to environmental status codification was based on FAO’s International descriptors and sustainable development Standard Statistical Classification of Fishing Gear indicators, namely the MSFD Descriptor 3 (ISSCFG) by adding a category for fishing without “Populations of all commercially exploited fish gear (i.e. HPD: hand picking and diving). Stocks were and shellfish are within safe biological limits, ranked based on landing value. exhibiting a population age and size distribution The selection of priority stocks for regional that is indicative of a healthy stock” and the SDG assessment was in line with the procedures proposed Indicator 14.4.1 “Proportion of fish stocks within by FAO (FAO 2018) and ICES (ICES 2011). This biologically sustainable levels” (ICES 2011; FAO stock selection was based on the ranking of landings 2018). by commercial value excluding stocks that migrate Identification of stocks that are important for through, or occur in, more than one Exclusive small-scale/local fisheries should be conducted at Economic Zone (EEZ) (i.e. straddling stocks). These a regional level and EU Member States should straddling stocks should be assessed under add them to their national list of commercial international agencies, as is the case of tuna and tuna- stocks to be assessed and monitored (ICES 2011). like species, which are assessed under the In this context, this study aims to apply a standard International Commission for the Conservation of framework for prioritization of stock assessment Atlantic Tunas (ICCAT). When clearly defined stock in the Portuguese Autonomous Region of the units were not known, we used species and/or group Azores (ICES Subdivision 27.10.a.2) aligned with as units in order to report the information at the the ICES and FAO recommendations, collecting regional level. The reference list includes stocks that information on each stock from available represent 90% of total landing value during the period databases and identifying the current stock status. 2009-2019 and stocks of major importance in terms Case studies like this are of major importance for of ecosystem role and social/cultural considerations. the purpose of clearly describing the process of The latter evaluation was performed based on stock prioritization adopted by the region to available information and regional expert opinion respond with international commitments, and for (Fig. 1). identifying gaps in data and knowledge. For each selected stock, information was provided on jurisdictional distribution (fishing areas; ICES 2020), stock category (ICES classification of stocks MATERIAL AND METHODS into six main categories based on the available knowledge; ICES 2019a) and assessment (if the A taxonomic list of commercially exploited marine species is assessed or not, biological reference points stocks in the Azores was constructed based on the and current stock status), including MSFD Descriptor official landings obtained from the Azores Auction 3 (D3) criteria (D3C1 – pressure level of fishing -

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Stock assessment prioritization in the Azores

Fig. 1. Overview of the stock assessment prioritization process in the Azores. activity, D3C2 - reproductive capacity of the stock and D3C3 - population age and size distribution) of Good Environmental Status (GES) (EU 2017). When stock status could not be determined, trend analyses of the Azorean annual spring bottom longline survey-derived abundance indices for the recent period (2017-2019) were used to estimate the current stock size. The analyses were performed only for stocks which had data based on research surveys reliable for management advice (Santos et al. 2019b; Pinho et al. 2020). For species assessed under ICES working groups, the stock size information from ICES Advice sheet was used (ICES 2018a, b; 2019b, c).

RESULTS

Landings composition A total of 138 species of algae, molluscs, crustaceans, echinoderms and fishes (teleost and elasmobranch species) have been landed annually in the Azores during the period 2009-2019 (Table 1 Fig. 2. Annual landings by (A) weight and (B) com- and Table 2). Total landings have varied between mercial value for all straddling and non-straddling 6,203 t and 19,029 t and 25.9 M € and 39.6 M € per stocks in the Azores during 2009-2019. Table 1 and year considering the studied period (Fig. 2). Table 2 detail which species belong to each category.

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1758; Scomber colias Gmelin, 1789; Serranus atricauda Günther, 1874; Pontinus kuhlii (Bowdich, 1825); Seriola spp. Cuvier, 1816; Mora moro (Risso, 1810); Aphanopus carbo Lowe, 1839; and Raja clavata Linnaeus, 1758), 2 molluscs (Loligo forbesii Steenstrup, 1856 and Patella aspera Röding, 1798) and 2 crustaceans (Palinurus elephas (Fabricius, 1787) and Scyllarides latus (Latreille, 1803)). According to available scientific evidence, half of the selected stocks have their distribution inside the Azores EEZ (ICES Subdivision 27.10.a.2) but the other half has no clearly defined distribution (Table 3).

Assessment information and stock status Twelve stocks were classified as ICES category 5, i.e. stocks for which only landings or a short series of catches are available, and 10 stocks were classified as ICES category 3, i.e. stocks for

Fig. 3. Proportion of landings by commercial value for which survey-based assessments or exploratory (A) non-straddling and (B) straddling stocks pooled by assessments indicate trends (Table 3). Among all the main species categories in the Azores for the period these, only four stocks are assessed using data- 2009-2019. Table 1 and Table 2 detail which species limited approaches: P. bogaraveo, A. carbo, and belong to each category. R. clavata (category 3) and T. picturatus (category 5). However, no biological reference Non-straddling species represented on average points are defined and stock status relative to 64% of these landings in value (50% in weight) maximum sustainable yield (MSY) are not and were mainly represented by demersal fishes assessed for any of these stocks (Table 3). (Fig. 3). The main gear used to capture these Since the reference points for all selected species were mechanized lines and pole-and- stocks are not known, the MSFD D3 criteria of lines, and set longlines (Table 1). Straddling GES has not been possible to estimate (Table 3). species represented on average 36% of the total The current stock size was available for 11 landings in value. Overall, the main species stocks, and most of them (P. bogaraveo, H. caught were tuna and tuna-like species (Fig. 3) by dactylopterus, P. pagrus, C. conger, B. splendens, the hand-operated pole-and-line fishery (Table 2). and R. clavata) showed decreasing abundance trend (Table 3). Priority stocks Twenty-two stocks were selected as priorities for local assessment and monitoring (Table 3). The DISCUSSION reference list is composed of 18 fish species (Pagellus bogaraveo (Brünnich, 1768); Prioritizing stock assessment is important in order Trachurus picturatus (Bowdich, 1825); to provide a transparent and objective process for Helicolenus dactylopterus (Delaroche, 1809); determining which are the appropriate assessment Pagrus pagrus (Linnaeus, 1758); Phycis phycis targets and how to best achieve them (Methot Jr. (Linnaeus, 1766); Conger conger (Linnaeus, 2015). The reference list of priority stocks (Table 1758); Beryx decadactylus Cuvier, 1829; B. 3) should remain unchanged for a number of splendens Lowe, 1834; Sparisoma cretense years to allow for comparability and monitoring (Linnaeus, 1758); Lepidopus caudatus the effectiveness of the adopted management (Euphrasen, 1788); Scorpaena scrofa Linnaeus, measures (FAO 2018). Therefore, it is essential to 48

Table 1. Checklist of the species officially landed in the ports of the Azores during the period 2009-2019 excluding straddling stocks. Main fishing gear: LHM - Mechanized lines and pole-and-lines, LLS - Set longlines, LHP - Handlines and hand-operated pole-and-lines, LLD - Drifting longlines, FPO – Pots, PS - Purse seines, GNS - Set gillnets (anchored), GEN - Gillnets and entangling nets (nei), LNP - Portable lift nets, LNB - Boat-operated lift nets, LN - Lift nets (nei), HPD - Hand picking and diving. MAL: mean annual landing. Species are listed in descending order of landed commercial value. Species representing 90% of the landings by value and species of major importance in terms of ecosystem role and social/cultural considerations are highlighted with a flag.

Main % Ranking % Common name FAO Depth MAL MAL Ranking Category Scientific name Common name (PT) Habitat fishing Total* in Total* (EN) code range (m) (t) (M €) in Value gear (t) Weight (€)

Pagel- Carapau / Goraz / LHM, Teleost lus bogaraveo (Brünnich, Blackspot seabream SBR Demersal 150 - 700 631.54 12.47 2 6.40 31.13 1 Peixão LLS  1768) Loligo forbesii Steenstrup, Mollusc Veined squid Lula SQF Demersal 68 - 431 LHP 462.64 9.13 3 2.85 13.85 2 1856  PS, Trachu- LNB, Chicharro / Teleost rus picturatus (Bowdich, Blue jack mackerel JAA Pelagic 305 - 370 LNP, 845.82 16.70 1 1.37 6.65 3 Chicharro-do-alto  1825) LHM, LLS Heli- Teleost colenus dactylopterus (Delar Blackbelly rosefish Boca-negra BRF Demersal 50 - 1100 LLS 245.39 4.85 6 1.25 6.07 4  oche, 1809) Pagrus pagrus (Linnaeus, LHM, Teleost Red porgy Pargo / Parguete RPG Demersal 0 - 250 85.63 1.69 15 0.87 4.23 5 1758) LLS  Phycis phycis (Linnaeus, LHM, Teleost Forkbeard Abrótea FOR Demersal 13 - 614 226.80 4.48 8 0.80 3.91 6 1766) LLS  Conger conger (Linnaeus, LHM, Teleost European conger Congro / Safio COE Demersal 0 - 1171 407.56 8.05 4 0.72 3.52 7 1758) LLS  Beryx decadactylus Cuvier, LHM, Teleost Alfonsino Imperador BXD Demersal 110 - 1000 39.96 0.79 21 0.63 3.05 8 1829 LLS  LHM, Teleost Beryx splendens Lowe, 1834 Splendid alfonsino Alfonsim BYS Demersal 25 - 1300 145.36 2.87 11 0.51 2.46 9 LLS  Sparisoma cretense (Linnae- Teleost Parrotfish Veja PRR Demersal 20 - 50 GNS 209.48 4.14 10 0.46 2.24 10 us, 1758)  Lepidopus caudatus (Eu- Teleost Silver scabbardfish Peixe-espada-branco SFS Demersal 42 - 620 LLS 216.27 4.27 9 0.45 2.21 11 phrasen, 1788)  49

Main % Ranking % Common name FAO Depth MAL MAL Ranking Category Scientific name Common name (PT) Habitat fishing Total* in Total* (EN) code range (m) (t) (M €) in Value gear (t) Weight (€)

Scorpaena scrofa Linnaeus, Teleost Red scorpionfish Rocaz SER Demersal 20 - 500 LLS 28.03 0.55 25 0.39 1.88 12 1758  LNB, Scomber colias Gmelin, Atlantic chub macke- Teleost Cavala MAZ Pelagic 0 - 300 LHM, 306.73 6.06 5 0.36 1.76 13 1789 rel  LLS GNS, Serranus atricauda Günther, Teleost Blacktail comber Garoupa WSA Demersal 0 - 150 LHM, 56.74 1.12 17 0.29 1.39 14 1874  LLS Pontinus kuhlii (Bowdich, LHM, Teleost Offshore rockfish Cântaro / Bagre POI Demersal 100 - 600 54.10 1.07 18 0.27 1.33 15 1825) LLS  LHM, Teleost Seriola spp. Cuvier, 1816 Amberjacks nei Írio / Lírio AMX Demersal 1 - 360 40.31 0.80 20 0.26 1.25 16 LLD  Melga / Escamuda- LHM, Teleost Mora moro (Risso, 1810) Common mora RIB Demersal 450 - 2500 92.52 1.83 14 0.25 1.21 17 branca LLS  Palinurus elephas (Fabricius, Common spiny lob- HPD, Lagosta SLO Benthic 5 - 200 8.94 0.18 39 0.24 1.18 18 1787) ster FPO  Aphanopus carbo Lowe, Teleost Black scabbardfish Peixe-espada-preto BSF Demersal 200 - 2300 LLS 94.45 1.86 13 0.24 1.14 19 1839  Epinephelus marginatus LHM, Teleost Dusky grouper Mero GPD Demersal 8 - 300 25.58 0.50 26 0.22 1.07 20 (Lowe, 1834) LLS Pseudocaranx dentex (Bloch LHM, Teleost White trevally Encharéu TRZ Demersal 10 - 238 35.31 0.70 23 0.18 0.86 21 & Schneider, 1801) LLS Sphyraena viridensis Cuvier, Yellowmouth barra- LHM, † Bicuda YRU Pelagic 0 - 100 66.74 1.32 16 0.16 0.80 22 Teleost 1829 cuda LLS Mollusc Patella aspera Röding, 1798 Azorean limpet Lapa-brava LQY Benthic 0 - 10 HPD 21.20 0.42 29 0.13 0.65 23  LHM, Teleost Zeus faber Linnaeus, 1758 John dory Peixe-galo JOD Demersal 5 - 400 12.21 0.24 33 0.13 0.64 24 LLS Diplodus sargus (Linnaeus, LHM, Teleost White seabream Sargo / Sarguete SWA Demersal 0 - 50 39.60 0.78 22 0.13 0.63 25 1758) GNS LHM, Elasmobranch Raja clavata Linnaeus, 1758 Thornback ray Raia RJC Demersal 5 - 1020 98.96 1.95 12 0.11 0.54 26 LLS  Mullus surmuletus Linnaeus, GNS, Teleost Surmullet Salmonete MUR Demersal 5 - 409 11.66 0.23 36 0.11 0.53 27 1758 FPO 50

Main % Ranking % Common name FAO Depth MAL MAL Ranking Category Scientific name Common name (PT) Habitat fishing Total* in Total* (EN) code range (m) (t) (M €) in Value gear (t) Weight (€)

Octopus vulgaris Cuvier, Mollusc Common octopus Polvo OCC Demersal 0 - 347 HPD 12.04 0.24 34 0.09 0.42 28 1797 LHM, Muraena helena Linnaeus, Teleost Mediterranean moray Moreia-pintada MMH Demersal 1 - 801 LLS, 49.35 0.97 19 0.07 0.34 29 1758 FPO Mollusc Patella spp. Linnaeus, 1758 Limpets nei Lapa LPZ Benthic 0 - 10 HPD 9.77 0.19 38 0.07 0.34 30 Teleost Sarda sarda (Bloch, 1793) Atlantic bonito Serra BON Pelagic 80 - 200 LHM 14.46 0.29 32 0.07 0.32 31 Pagellus acarne (Risso, LHM, Teleost Axillary seabream Besugo SBA Demersal 0 - 500 16.93 0.33 30 0.06 0.31 32 1827) LLS Chelon labrosus (Risso, Teleost Thicklip grey mullet Tainha / Muja MLR Pelagic 0 - 50 GNS 24.61 0.49 27 0.05 0.24 33 1827) Molva macrophthalma (Raf- Teleost Spanish ling Pescada-dos-açores SLI Demersal 30 - 1000 LLS 15.97 0.32 31 0.05 0.22 34 inesque, 1810) Sardina pilchardus (Wal- Teleost European pilchard Sardinha / Petinga PIL Pelagic 10 - 100 PS 23.89 0.47 28 0.04 0.19 35 baum, 1792) Scyllarides latus (Latreille, Mediterranean slip- HPD, Crustacean Cavaco YLL Benthic 4 - 100 1.37 0.03 62 0.04 0.17 36 1802) per lobster FPO  Labrus bergylta Ascanius, GNS, Teleost Ballan Bodião-vermelho USB Demersal 1 - 50 10.65 0.21 37 0.03 0.17 37 1767 LHM Schedophilus ovalis (Cuvier, LHM, Teleost Imperial blackfish Choupa HDV Demersal 70 - 700 3.38 0.07 52 0.03 0.13 38 1833) LLS Isurus oxyrinchus Raf- † Shortfin mako Rinquim/Anequim SMA Pelagic 0 - 750 LLS 8.22 0.16 40 0.02 0.10 39 Elasmobranch inesque, 1810 Boops boops (Linnaeus, Teleost Bogue Boga BOG Demersal 0 - 350 LN 30.24 0.60 24 0.02 0.08 40 1758) Megabalanus azoricus (Pils- Crustacean Azorean Craca ? Benthic 0 - 20 HPD 5.51 0.11 44 0.02 0.08 41 bry, 1916) Epigonus telescopus (Risso, Escamuda / Es- LHM, Teleost Black cardinal fish EPI Demersal 75 -1200 4.98 0.10 46 0.01 0.07 42 1810) camuda-preta LLS Diplodus vulgaris (Geoffroy Common two-banded LHM, Teleost Safia CTB Demersal 0 - 160 6.71 0.13 41 0.01 0.07 43 Saint-Hilaire, 1817) seabream GNS

51

Main % Ranking % Common name FAO Depth MAL MAL Ranking Category Scientific name Common name (PT) Habitat fishing Total* in Total* (EN) code range (m) (t) (M €) in Value gear (t) Weight (€)

Teleost Not idendified Several fish Diversos Peixes ? ? ? ? 5.51 0.11 43 0.01 0.06 44 Cancer bellianus Johnston, Crustacean Toothed rock crab Sapateira KCB Benthic 37 - 750 FPO 6.21 0.12 42 0.01 0.05 45 1861 Ruditapes decussatus (Lin- Mollusc Grooved carpet shell Amêijoa CTG Benthic 0 - 1 HPD 0.55 0.01 74 0.01 0.05 46 naeus, 1758) Lophius piscatorius Linnae- LHM, Teleost Angler (= Monk) Tamboril MON Demersal 20 - 1000 4.16 0.08 49 0.01 0.04 47 us, 1758 LLS Bodianus scrofa (Valenci- LHM, Teleost Barred hogfish Peixe-cão / Gaio IVD Demersal 20 - 200 2.25 0.04 59 0.01 0.03 48 ennes, 1839) LLS (Lowe, LHM, Teleost Island grouper Badejo MKF Demersal 1 - 200 1.23 0.02 64 0.01 0.03 49 1838) LLS Ruvettus pretiosus Cocco, Escolar / Chocolate / LHM, Teleost Oilfish OIL Demersal 100 - 800 2.66 0.05 57 0.01 0.03 50 1833 Peixe-chocolate LLS LHM, Labrus mixtus Linnaeus, Teleost Cuckoo wrasse Peixe-rei-do-alto USI Demersal 2 - 200 LLS, 1.70 0.03 60 0.00 0.02 51 1758 GNS Clupea harengus Linnaeus, Teleost Atlantic herring Arenque HER Pelagic 0 - 364 ? 3.96 0.08 50 0.00 0.02 52 1758 Sarpa salpa (Linnaeus, Teleost Salema Salema SLM Demersal 5 - 70 GNS 4.48 0.09 48 0.00 0.02 53 1758) LHM, Kyphosus incisor (Cuvier, Teleost Yellow sea chub Patruça / Preguiçosa KYI Demersal 1 - 15 LLS, 3.46 0.07 51 0.00 0.02 54 1831) GNS Centrophorus lusitanicus Elasmobranch Barbosa du Bocage & de Lowfin gulper shark Tubarão-lusitano CPL Demersal 300 - 1400 LLS 2.29 0.05 58 0.00 0.02 55 Brito Capello, 1864 Sargassum spp. Agardh, Algae Sargassum Sargaço QWX ? ? HDP 11.86 0.23 35 0.00 0.02 56 1820 LHM, Teleost Trachinotus ovatus Pompano Prombeta / Pombeta POP Pelagic 50 - 200 5.22 0.10 45 0.00 0.02 57 PS LHM, Gymnothorax unicolor (De- Teleost Brown moray Moreão AGK Demersal 0 - 20 LLS, 2.96 0.06 55 0.00 0.01 58 laroche, 1809) FPO 52

Main % Ranking % Common name FAO Depth MAL MAL Ranking Category Scientific name Common name (PT) Habitat fishing Total* in Total* (EN) code range (m) (t) (M €) in Value gear (t) Weight (€)

Chaceon affinis (Milne- Crustacean Deep-sea red crab Caranguejo-real KEF Benthic 130 - 2047 FPO 1.21 0.02 65 0.00 0.01 59 Edwards & Bouvier, 1894) Maja brachydactyla Balss, Atlantic spinous Crustacean Santola JDV Benthic 0 - 80 FPO 0.77 0.02 68 0.00 0.01 60 1922 spider crab Caranx crysos (Mitchill, LHM, Teleost Blue runner Írio-de-serra RUB Pelagic 0 - 100 0.60 0.01 73 0.00 0.01 61 1815) LLD Holothuria spp. Linnaeus, Echinoderm Sea Cucumber Pepino-do-mar WBX Benthic ? HPD 3.30 0.07 53 0.00 0.01 62 1767 Sphaerechinus granularis Echinoderm Violet sea urchin Ouriço-do-mar FKG Benthic 2 - 130 HPD 0.75 0.01 69 0.00 0.01 63 (Lamarck, 1816) Chromis limbata (Valenci- LHM, Teleost Azores chromis Castanheta-amarela HZL Demersal 5 - 45 0.50 0.01 75 0.00 0.01 64 ennes, 1833) GNS Algae Porphyra spp. Agardh, 1824 Nori nei Erva-patinha FYS Benthic ? HPD 0.12 <0.01 88 0.00 0.01 65 Lepidorhombus whiffiagonis Teleost Megrim Areeiro MEG Demersal 100 - 700 LLS 0.19 <0.01 83 0.00 0.01 66 (Walbaum, 1792) Zenopsis conchifer (Lowe, LHM, Teleost Silvery John dory Galo-branco JOS Demersal 50 - 600 0.39 0.01 76 0.00 0.01 67 1852) LLS Serranus cabrilla (Linnaeus, LHM, Teleost Comber Garoupa-do-alto CBR Demersal 5 - 500 0.63 0.01 71 0.00 0.01 68 1758) LLS Hexaplex trunculus (Linnae- HPD, Mollusc Banded dye-murex Búzio FNT Benthic 1 - 100 0.75 0.01 70 0.00 0.01 69 us, 1758) FPO Patella candei d'Orbigny, Mollusc Limpet Lapa-mansa ? Benthic 0 - 3 HPD 0.12 <0.01 87 0.00 0.01 70 1839 Chelidonichthys cuculus Teleost Red gurnard Cabra / Ruivo GUR Demersal 15 - 400 LLS 1.26 0.02 63 0.00 <0.01 71 (Linnaeus, 1758) Dalatias licha (Bonnaterre, LHM, Elasmobranch Kitefin shark Gata-lixa SCK Demersal 37 - 1800 2.72 0.05 56 0.00 <0.01 72 1788) LLS Polymixia nobilis Lowe, LHM, Teleost Stout beardfish Salmonete-do-alto PXV Demersal 100 -770 0.14 <0.01 85 0.00 <0.01 73 1836 LLS Brama brama (Bonnaterre, LHM, Teleost Atlantic pomfret Xaputa POA Pelagic 0 - 1000 0.31 0.01 79 0.00 <0.01 74 1788) LLS Centracanthus cirrus Raf- LLS, Teleost Curled picarel Boqueirão EHI Demersal 0 - 464 0.82 0.02 67 0.00 <0.01 75 inesque, 1810 GNS 53

Main % Ranking % Common name FAO Depth MAL MAL Ranking Category Scientific name Common name (PT) Habitat fishing Total* in Total* (EN) code range (m) (t) (M €) in Value gear (t) Weight (€)

Thalassoma pavo (Linnaeus, LHM, Teleost Ornate wrasse Rainha TMP Demersal 1 - 150 0.32 0.01 78 0.00 <0.01 76 1758) GNS Pterocladiella capillacea Algae (S.G.Gmelin) Santelices & Spanish agar Agar OKQ Benthic 0 - 15 HPD 230.73 4.56 7 0.00 <0.01 77 Hommersand, 1997 LHM, Muraena augusti (Kaup, Teleost Mediterranean moray Moreia-preta MWK Demersal 0 - 250 LLS, 1.68 0.03 61 0.00 <0.01 78 1856) FPO Dasyatis pastinaca (Linnae- LHM, Elasmobranch Common stingray Ratão / Uge JDP Demersal 5 - 200 0.60 0.01 72 0.00 <0.01 79 us, 1758) GNS Plesionika spp. Spence Bate, Plesionika shrimps Crustacean Camarão XKX Benthic 4 - 910 FPO 0.07 <0.01 90 0.00 <0.01 80 1888 nei Centrophorus granulosus Barroso / Xara- LHM, Elasmobranch Gulper shark GUP Demersal 50 - 1440 0.84 0.02 66 0.00 <0.01 81 (Bloch & Schneider, 1801) Branca LLS Grapsus grapsus (Linnaeus, Crustacean Lightfoot crab Caranguejo-fidalgo GSQ Benthic 0 - 5 HPD 0.04 <0.01 95 0.00 <0.01 82 1758) Symphodus trutta (Lowe, Bodião-verde / Bod- LHM, Teleost Emerald wrasse JCN Demersal 5 - 15 0.19 <0.01 82 0.00 <0.01 83 1834) ião-azul GNS Charonia lampas (Linnaeus, HPD, Mollusc Trumpet shell Buzina ? Benthic 0 - 200 0.17 <0.01 84 0.00 <0.01 84 1758) FPO Haliotis tuberculata Linnae- Mollusc Tuberculate abalone Lapa-burra / Abalone HLT Benthic 0 - 200 HPD 0.02 <0.01 102 0.00 <0.01 85 us, 1758 Bothus podas (Delaroche, LHM, Teleost Wide-eyed flounder Carta OUB Demersal 15 - 400 0.03 <0.01 98 0.00 <0.01 86 1809) LLS Centrostephanus longispinus Ouriço-castanho-de- Echinoderm Needle spined urchin ? Benthic 40 - 363 HPD 0.05 <0.01 92 0.00 <0.01 87 (Philippi, 1845) espinhos-longos Arbacia lixula (Linnaeus, Echinoderm Black sea urchin Ouriço-do-mar-negro UKB Benthic 0 - 50 HPD 0.02 <0.01 105 0.00 <0.01 88 1758) Callista chione (Linnaeus, Mollusc Smooth callista Ameijola KLK Benthic 10 - 180 HPD 0.03 <0.01 99 0.00 <0.01 89 1758) Gaidropsaurus guttatus LHM, Teleost Spotted rockling Viúva ? Demersal 5 - 10 0.04 <0.01 96 0.00 <0.01 90 (Collett, 1890) LLS Elasmobranch Deania profundorum (Smith Arrowhead dogfish Sapata SDU Demersal 205 - 1800 LLS 0.38 0.01 77 0.00 <0.01 91 54

Main % Ranking % Common name FAO Depth MAL MAL Ranking Category Scientific name Common name (PT) Habitat fishing Total* in Total* (EN) code range (m) (t) (M €) in Value gear (t) Weight (€)

& Radcliffe, 1912) Gephyroberyx darwinii Teleost Darwin's slimehead Peixe-vidro GXW Pelagic 9 - 1210 ? 0.01 <0.01 110 0.00 <0.01 92 (Johnson, 1866) Similiparma lurida (Cuvier, LHM, Teleost Canary damsel Castanheta-azul AUU Demersal 0 - 25 0.02 <0.01 103 0.00 <0.01 93 1830) GNS Promethichthys prometheus Teleost Roudi escolar Peixe-coelho PRP Demersal 80 - 800 LLS 0.05 <0.01 94 0.00 <0.01 94 (Cuvier, 1832) Synodus saurus (Linnaeus, LHM, Teleost Atlantic lizardfish Lagarto-da-costa SDR Demersal 1 - 400 0.24 <0.01 81 0.00 <0.01 95 1758) GNS Dardanus calidus (Risso, Crustacean Great red hermit crab Caranguejo-eremita ? Benthic 3 - 30 FPO 0.06 <0.01 91 0.00 <0.01 96 1827) Macroramphosus scolopax PS, Teleost Longspine snipefish Trombeteiro SNS Demersal 25 - 600 0.01 <0.01 108 0.00 <0.01 97 (Linnaeus, 1758) LNB Pomadasys spp. Lacepède, Teleost Grunts Roncador BGX ? ? ? 0.02 <0.01 101 0.00 <0.01 98 1802 Etmopterus spp. Rafinesque, LHM, Elasmobranch Lanternsharks nei Lixinha-da-fundura SHL Demersal 100 - 1200 0.01 <0.01 109 0.00 <0.01 99 1810 LLS Belone belone (Linnaeus, LLD, Teleost Garfish Peixe-Agulha GAR Pelagic 0 - 20 0.03 <0.01 97 0.00 <0.01 100 1760) GNS Apogon imberbis (Linnaeus, LHM, Teleost Cardinal fish Folião OGT Demersal 10 - 200 0.02 <0.01 107 0.00 <0.01 101 1758) GEN Alepocephalus rostratus Teleost Risso's smooth-head Celindra PHO Demersal 300 - 2250 LLS 0.05 <0.01 93 0.00 <0.01 102 Risso, 1820 Enchelycore anatina (Lowe, LHM, Teleost Fangtooth moray Víbora AWM Demersal 3 - 60 0.02 <0.01 104 0.00 <0.01 103 1838) LLS Anthias anthias (Linnaeus, LHM, Teleost Swallowtail seaperch Canário-do-mar AHN Demersal 0 - 300 0.02 <0.01 100 0.00 <0.01 104 1758) GNS Elasmobranch Deania calcea (Lowe, 1839) Birdbeak dogfish Sapata-áspera DCA Demersal 60 - 1490 LLS 0.14 <0.01 86 0.00 <0.01 105 Pachygrapsus marmoratus Crustacean Marbled rock crab Moura YGM Benthic 0 - 5 HPD 0.00 <0.01 111 0.00 <0.01 106 (Fabricius, 1787) Coryphaenoides rupestris Teleost Roundnose grenadier Peixe-rato RNG Demersal 180 - 2600 LLS 0.02 <0.01 106 0.00 <0.01 107 Gunnerus, 1765 55

Main % Ranking % Common name FAO Depth MAL MAL Ranking Category Scientific name Common name (PT) Habitat fishing Total* in Total* (EN) code range (m) (t) (M €) in Value gear (t) Weight (€)

Acantholabrus palloni (Ris- Teleost Scale-rayed wrasse Bodião-vidrão AKL Demersal 30 - 500 ? 0.00 <0.01 112 0.00 <0.01 108 so, 1810) Capros aper (Linnaeus, Teleost Boarfish Pimpim BOC Demersal 40 - 700 GNS 0.07 <0.01 89 0.00 <0.01 109 1758) Asparagopsis spp. Monta- Algae Harpoon seaweeds - ASR Benthic ? HPD 4.60 0.09 47 0.00 <0.01 110 gne, 1840 Gelidium spinosum Algae (S.G.Gmelin) P.C.Silva, Spiny straggle weed - ? Benthic ? HPD 3.20 0.06 54 0.00 <0.01 111 1996 Halopteris scoparia (Lin- Algae Sea flax weed - ? Benthic ? HPD 0.26 0.01 80 0.00 <0.01 112 naeus) Sauvageau, 1904 Note: * Total landings excluding straddling stocks. † Classified as large pelagic fish.

56

Table 2. List of the species officially landed in the ports of the Azores during the period 2009-2019 considered as straddling stocks. Main fishing gear: LHM - Mechanized lines and pole-and-lines, LLS - Set longlines, LHP - Handlines and hand-operated pole-and-lines, LLD - Drifting longlines, GNS - Set gillnets (anchored). MAL: mean annual landing. Species are listed in descending order of landed commercial value.

FAO Depth range Main fishing MAL MAL Category Scientific name Common name (EN) Common name (PT) Habitat code (m) gear (t) (M €)

LHP, LHM, † Thunnus obesus (Lowe, 1839) Bigeye tuna Atum-patudo BET Pelagic 0 - 1500 2429.83 5.19 Teleost LLD Teleost† Katsuwonus pelamis (Linnaeus, 1758) Skipjack tuna Bonito / Gaiado SKJ Pelagic 0 - 260 LHP 2901.41 3.38 Teleost Polyprion americanus (Bloch & Schneider, 1801) Wreckfish Cherne WRF Demersal 40 - 600 LLS 177.70 2.32 LHP, LHM, † Thunnus alalunga (Bonnaterre, 1788) Albacore Atum-voador ALB Pelagic 0 - 600 331.70 0.68 Teleost LLD Teleost† Xiphias gladius Linnaeus, 1758 Swordfish Espadarte / Agulhão SWO Pelagic 0 - 2878 LHM, LLS 91.19 0.43 Teleost Balistes capriscus Gmelin, 1789 Grey triggerfish Peixe-porco TRG Demersal 0 - 55 LHM, GNS 77.05 0.11 Elasmobranch Galeorhinus galeus (Linnaeus, 1758) Tope shark Cação GAG Demersal 0 - 1100 LHM, LLS 52.30 0.10 Teleost Pomatomus saltatrix (Linnaeus, 1766) Bluefish Anchova BLU Pelagic 0 - 200 LHM 17.89 0.05 LHP, LHM, † Thunnus albacares (Bonnaterre, 1788) Yellowfin tuna Atum-Albacora / Galha-à-ré YFT Pelagic 1 - 250 21.99 0.05 Teleost LLD Teleost Phycis blennoides (Brünnich, 1768) Greater forkbeard Juliana / Abrótea-do-alto GFB Demersal 10 - 1200 LLS 11.96 0.04 Elasmobranch Prionace glauca (Linnaeus, 1758) Blue shark Tintureira BSH Pelagic 1 - 1000 LHM, LLS 66.94 0.03 Teleost Coris julis (Linnaeus, 1758) Rainbow wrasse Peixe-rei COU Demersal 0 - 120 LHM, GNS 3.23 0.02 Teleost Coryphaena hippurus Linnaeus, 1758 Common dolphinfish Dourado DOL Pelagic 0 - 85 LHP, LHM 6.71 0.02 LHP, LHM, † Thunnus thynnus (Linnaeus, 1758) Atlantic bluefin tuna Atum-rabilho / Rabilo BFT Pelagic 0 - 985 0.76 0.01 Teleost LLD Elasmobranch Sphyrna zygaena (Linnaeus, 1758) Smooth hammerhead Cornuda / Tubarão-martelo SPZ Pelagic 0 - 200 LHM, LLS 0.85 0.00 Teleost† Makaira nigricans Lacepède, 1802 Blue marlin Espadim-azul BUM Pelagic 0 - 1000 LHM, LLD 0.23 0.00 57

FAO Depth range Main fishing MAL MAL Category Scientific name Common name (EN) Common name (PT) Habitat code (m) gear (t) (M €)

Teleost† Auxis rochei (Risso, 1810) Bullet tuna Judeu BLT Pelagic 0 - 200 LHM 0.13 0.00 Teleost† Acanthocybium solandri (Cuvier, 1832) Wahoo Cavala-da-índia / Uau WAH Pelagic 0 - 20 LHM, LLS 0.08 0.00 Elasmobranch Centroscymnus owstonii Garman, 1906 Shortnose velvet dogfish Xara-preta-de-natura CYY Demersal 100 - 1500 LHM, LLS 0.80 0.00 Teleost† Kajikia albida (Poey, 1860) Atlantic white marlin Espadim-branco WHM Pelagic 0 - 150 LHM, LLD 0.07 0.00 Elasmobranch Heptranchias perlo (Bonnaterre, 1788) Sharpnose sevengill shark Bico-doce HXT Demersal 0 - 1000 LLS 0.20 0.00 Elasmobranch Hexanchus griseus (Bonnaterre, 1788) Bluntnose sixgill shark Tubarão-albafar SBL Demersal 1 - 2500 LHM, LLS 0.22 0.00 Elasmobranch Alopias superciliosus Lowe, 1841 Bigeye thresher Tubarão-raposo-olhudo BTH Pelagic 0 - 730 LLS 0.07 0.00 Teleost Hoplostethus atlanticus Collett, 1889 Orange roughy Peixe-relógio ORY Pelagic 180 - 1809 LLS 0.00 0.00 Centroscymnus crepidater (Barbosa du Bocage & de Brito Elasmobranch Longnose velvet dogfish Sapata-preta CYP Demersal 230 - 1500 LLS 0.08 0.00 Capello, 1864) Elasmobranch Centrophorus squamosus (Bonnaterre, 1788) Leafscale gulper shark Lixa / Xara GUQ Demersal 145 - 2400 LHM, LLS 0.00 0.00 Note: † Classified as tuna and tuna-like species.

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Table 3. Reference list of the species landed in the ports of the Azores during the period 2009-2019 that represent 90% of total landings in value excluding landings from straddling stocks which were selected as priority stocks. This list also includes species of major importance in terms of ecosystem role and social/cultural considerations. Current stock status for each stock is reported based on the ICES Advice and Marine Strategy Framework Directive (MSFD) Descriptor 3 criteria. ICES data category: 3 – stocks for which survey-based assessments or exploratory assessments indicate trends. 5 – stocks for which only landings or a short series of catches are available. NA: not available. ?: Unknown or undefined. ARQDAÇO: Azorean annual bottom longline survey.

Stock jurisdic- ICES MSFD FAO Stock Stock Category Scientific name tional distri- Data Assessed spe- Reference Source code D3C1 D3C2 D3C3 status size bution category cies point Teleost Pagellus bogaraveo (Brünnich, 1768) SBR 27.10* 3 Yes ? ? ? ? ? ↘ ICES (2019b) Mollusc Loligo forbesii Steenstrup, 1856 SQF ? 5 No ? ? ? ? ? ? NA Teleost Trachurus picturatus (Bowdich, 1825) JAA 27.10.a2 5 Yes ? ? ? ? ? ? ICES (2018a) Teleost Helicolenus dactylopterus (Delaroche, 1809) BRF 27.10.a2 3 No ? ? ? ? ? ↘ ARQDAÇO (2017-2019) Teleost Pagrus pagrus (Linnaeus, 1758) RPG 27.10.a2 3 No ? ? ? ? ? ↘ ARQDAÇO (2017-2019) Teleost Phycis phycis (Linnaeus, 1766) FOR 27.10.a2 3 No ? ? ? ? ? ↗ ARQDAÇO (2017-2019) Teleost Conger conger (Linnaeus, 1758) COE ? 3 No ? ? ? ? ? ↘ ARQDAÇO (2017-2019) Teleost Beryx decadactylus Cuvier, 1829 BXD 27† 5 No‡ ? ? ? ? ? ↗ ARQDAÇO (2017-2019) Teleost Beryx splendens Lowe, 1834 BYS 27.10.a2 3 No‡ ? ? ? ? ? ↘ ARQDAÇO (2017-2019) Teleost Sparisoma cretense (Linnaeus, 1758) PRR ? 5 No ? ? ? ? ? ? NA Teleost Lepidopus caudatus (Euphrasen, 1788) SFS ? 5 No ? ? ? ? ? ? NA Teleost Scorpaena scrofa Linnaeus, 1758 SER ? 5 No ? ? ? ? ? ? NA Teleost Scomber colias Gmelin, 1789 MAZ ? 5 No ? ? ? ? ? ? NA Teleost Serranus atricauda Günther, 1874 WSA 27.10.a2 5 No ? ? ? ? ? ? NA Teleost Pontinus kuhlii (Bowdich, 1825) POI 27.10.a2 3 No ? ? ? ? ? → ARQDAÇO (2017-2019) Teleost Seriola spp. Cuvier, 1816 AMX ? 5 No ? ? ? ? ? ? NA

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Stock jurisdic- ICES MSFD FAO Stock Stock Category Scientific name tional distri- Data Assessed spe- Reference Source code D3C1 D3C2 D3C3 status size bution category cies point Teleost Mora moro (Risso, 1810) RIB ? 3 No ? ? ? ? ? ↗ ARQDAÇO (2017-2019) Crustacean Palinurus elephas (Fabricius, 1787) SLO ? 5 No ? ? ? ? ? ? NA Teleost Aphanopus carbo Lowe, 1839 BSF 27† 3 Yes ? ? ? ? ? → ICES (2018b) Mollusc Patella aspera Röding, 1798 LQY 27.10.a2 5 No ? ? ? ? ? ? NA Elasmobranch Raja clavata Linnaeus, 1758 RJC 27.10.a2 3 Yes ? ? ? ? ? ↘ ICES (2019c) Crustacean Scyllarides latus (Latreille, 1803) YLL ? 5 No ? ? ? ? ? ? NA Note: * Stock is considered a management unit for Subdivision 10.a.2 but ICES advice is currently provided for Subarea 10. † Stock unit is not clearly defined. ‡ Stocks assessed by ICES as a single group (Beryx spp.).

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Stock assessment prioritization in the Azores include representative stocks of different the long-term dynamics of populations and their categories of marine resources which are response to historical exploitation rates and to exploited locally. define biological reference points. Biological The reference list comprises the main species reference points provide guidance to decision of small-pelagic and demersal fishes, crustaceans makers in determining whether populations are and molluscs targeted by the main fisheries that too small, or fishing pressure is too high (Cooper take place in the Azorean region. The demersal 2006). However, for almost all priority stocks in (handline and longline) fishery is one of the most the Azores region, the exploitation and stock important in terms of value, weight and number status are unknown. Two main issues that may be of vessels (Santos et al. 2019a). It is a small-scale related to these knowledge gaps are the fishery, whose vessels (mostly less than 12 m in deficiency of information regarding catches and length) operate throughout the year around the population structure and lack of validated islands and in banks/seamounts targeting analytical methods for local stock assessment. demersal/deep-water species such as blackspot Fishery-independent data have been collected seabream Pagellus bogaraveo, blackbelly annually in the Azores over the past c. 25 years rosefish Helicolenus dactylopterus, and (Santos et al. 2019a). The Azorean spring bottom alfonsinos Beryx spp. (Santos et al. 2019a). Part longline survey (ARQDAÇO) has as main of this fleet occasionally changes its fishing objectives to: (i) provide annual fishery activity for targeting the veined squid Loligo independent estimates of abundance and size forbesi between November and February when composition for commercially important demersal the latter appears in large quantities in the region fish species, (ii) collect information for biological (cyclical resource; Martins 1982; Porteiro 1994). studies on growth and reproduction, and (iii) In the pelagic zone, a small coastal purse-seine obtain information for ecological studies, such as fleet catches blue jack mackerel Trachurus distribution and community structure (Santos et picturatus, which is used for human consumption al. 2019b). This information has been used for and as live bait in the tuna fishery. Other coastal stock assessment and advice for management of fisheries use gillnets, pots and traps, or hand- commercially exploited species but picking to target coastal fishes (e.g. parrotfish has certain limitations. The survey is considered Sparisoma cretense, blacktail comber Serranus reliable for conducting management advice for 10 atricauda), lobsters (e.g. common spiny lobster species (Santos et al. 2019b), although abundance Palinurus elephas and Mediterranean slipper indices better reflect populationabundance of lobster Scyllarides latus), and limpets (e.g. species mainly distributed down to 800 m (i.e. P. Azorean limpet Patella aspera). phycis, P. bogaraveo, P. pagrus, H. Most of these Azorean fishery resources are dactylopterus, R. clavata, B. splendens, and P. considered to be intensively exploited (ICES kuhlii; Pinho et al. 2020). Nevertheless, the linear 2018c) and, just as the survey-derived stock sizes relationship between longline catch rate and are decreasing (Table 3), commercial landings density of these species (i.e. effect of factors such also exhibit a decreasing pattern for some species as soak time, gear saturation and competition for (Santos et al., 2019a, 2020). These results should hooks on the longline catching process; Sigler be interpreted with caution as the observed trends 2000) should be assessed to reliably apply may reflect a variation in the survey catch process longline catch rates for management advice (e.g. soak-time, gear saturation) or commercial (Santos et al. 2019b). fleet operational regime (e.g. changes in targeted Another issue is that some demersal fish stocks species and fishing area as consequence of are not fully sampled throughout their distribution fisheries regulations such as introduction of range and population dynamic aspects (e.g. restricted areas, total allowable catches and reproductive and growth parameters) are not fully closed period) and not a variation of stock known. This issue is mostly related to the abundances caused by fishing exploitation difficulty of defining local management units, (Santos et al. 2019a). Thus, it is through stock given that most stocks have a spatial distribution assessments that scientists attempt to understand that goes far beyond the Azores EEZ and detailed 61

Santos et al. data is only available for the Azorean sub-region since 1990 within the European Commission’s (ICES Subdivision 10.a.2). Beryx splendens and Data Collection Framework (DCF; EU 2008). B. decadactylus, for example, are currently The structured interviews of captains of the local assessed by the ICES working group on biology fleet have been carried out in the main ports of and assessment of deep-sea fisheries resources the Azores during landings. Differently from the (WGDEEP) as a single stock comprising both research surveys, fishing data have been collected species in the North Atlantic Ocean (ICES on a monthly basis, which allows a more robust 2018c). Recent studies have shown, at least for B. assessment of the exploitable populations. On the splendens, that the Azorean stock can be other hand, degradation in data quality can occur considered a local management unit (Santos et al. when fishermen do not trust stock assessments 2019c). However, discrepancies in some life- and believe that these interviews (inquiries) are history parameters indicate that its stock structure responsible for increasingly restricted quotas and needs to be better studied. reduced fishing opportunities. This degradation Small pelagic fishes (e.g. blue jack mackerel can cause serious errors in stock assessments, as a Trachurus picturatus, Atlantic chub mackerel reduction in fishing pressure and Red-Listing of Scomber colias), veined squid Loligo forbesii and healthy and commercially important stocks (Helle some coastal resources (e.g. common spiny et al. 2015). Therefore, even with legal lobster Palinurus elephas, Mediterranean slipper requirements, reported fishing data cannot lobster S. latus, Azorean limpet Patella aspera) necessarily be assumed to be accurate (NRC are not being currently assessed under directed 1998). Thus, in addition to application of and continued research surveys. For most of these techniques and diagnostics to standardize fishing resources only landings or a short series of data to minimize confounding effects (Maunder catches are available and advice on that basis & Punt 2004), it is essential to promote (when performed) needs to be applied on a perception and understanding of fishermen about precautionary basis (ICES 2012). Populations the management mechanisms and procedures for with insufficient data to conduct a conventional stock assessment (Mauser et al. 2013), seeking to stock assessment are assessed using methods resolve conflicts and improve their participation applicable to data-limited stocks (ICES 2012). and involvement in these processes. Although a wide range (over 85) of data-limited The main contribution of this study is to help methods have been described (Carruthers & ensure effective and transparent decision-making Hordyk 2020), suitable methods to be used for related to stock assessment planning within the specific stocks in the Azorean region need to be Azorean region. Once the reference list of priority studied. This evaluation should be performed stocks is defined, the next step should involve exploring available dataset and requires both first-time assessments for previously not assessed simulation testing (e.g. Carruthers et al. 2014; stocks, updating existing assessments using Wiedenmann et al. 2019) and validation (e.g. established methods and data, and upgrading Kokkalis et al. 2017; Sagarese et al. 2019). assessments using new types of data and methods. Besides that, analyses should be carried out on For this, it is necessary to catalogue and which additional data are needed to run better- document available information for assessment performing methods and so inform future data on life history, fishery monitoring and stock collection priorities. abundance data for each of the selected stocks Stock assessments are often done using both and propose new studies to collect them when fishery-independent (research surveys) and necessary. All information should be validated, fishery-dependent data (Hilborn & Walters 1992; and adequate analytical methods for stock Cadima 2003). These two sources may provide assessment should be defined based on the data different types of information with additional quality. Exploratory analyses should be details. Fishery-dependent data (e.g. catch, effort, performed to improve the assessments. Some of time, fishing area, gear, biological samples of these analyses involves, for example, target species landed for reproduction and growth standardization of fishery abundance indices and studies) have been collected in the Azores EEZ effort unit, analyses of the effects of competition, 62

Stock assessment prioritization in the Azores gear saturation and soak time on the survey data 21–24 November 2017. FAO Fisheries and to better understand the reliability of abundance Report, R1222. 30 pp. indices for assessment, and analyses of the Fricke, R., W. N. Eschmeyer and R. Van der Laan reproductive biology and spatial distribution of (eds) 2020. Eschmeyer's : genera, species, references. Available from: the species. http://researcharchive.calacademy.org/research/icht hyology/catalog/fishcatmain.asp (cited 18 April 2020). ACKNOWLEDGMENTS Froese, R. and D. Pauly (Eds) 2019. FishBase. World Wide Web electronic publication. This study is part of the PESCAz project (ref. www..org (version 12/2019). MAR-01.03.02-FEAMP-0039) financed by the Helle, K., M. Pennington, N.-R. Hareide and I. Fossen European Maritime and Fisheries Fund (EMFF) 2015. Selecting a subset of the commercial catch through the Regional Government of the Azores data for estimating catch per unit effort series for ling (Molva molva L.). Fisheries Research 165: under the MAR2020 operational program. 115-120. doi: 10.1016/j.fishres.2014.12.015. Hilborn, R. and C.J. Walters 1992. Quantitative fisheries stock assessment: choice, dynamics and REFERENCES uncertainty. New York, Chapman & Hall. 570 pp. ICES, 2011. Report of the Workshop on Marine Cadima, E.L. 2003. Fish stock assessment manual. Strategy Framework Directive1 - Descriptor 3+ FAO Fisheries Technical Paper 393: 1-161. (WKMSFD1 D3), 4-8 July 2011, ICES Cadrin, S.X. and M. Dickey-Collas 2015. Stock Headquarters, Denmark. ICES CM assessment methods for sustainable fisheries. ICES 2011/ACOM:58. 44 pp. Journal of Marine Science 72: 1–6. ICES, 2012. ICES Implementation of Advice for Data- doi:10.1093/icesjms/fsu228 limited Stocks in 2012 in its 2012 Advice. ICES Carruthers, T.R., A.E. Punt, C.J. Walters, A. MacCall, CM 2012/ACOM 68. 42 pp. M.K. McAllister, E.J. Dick and J. Cope 2014. ICES, 2018a. Blue jack mackerel (Trachurus Evaluating methods for setting catch limits in data- picturatus) in Subdivision 10.a.2 (Azores grounds). limited fisheries. Fisheries Research 153: 48–68. In Report of the ICES Advisory Committee, 2018. Carruthers, T.R., and Hordyk, A. 2020. DLMtool: ICES Advice 2018, jaa.27.10a2. doi: Data-Limited Methods Toolkit. http://cran.r- 10.17895/ices.pub.4499 project.org/web/packages/DLMtool/index.html. ICES, 2018b. Black scabbardfish (Aphanopus carbo) in Cooper, A.B. 2006. A Guide to Fisheries Stock subareas 1, 2, 4–8, 10, and 14, and divisions 3.a, Assessment: From Data to Recommendations. Sea 9.a, and 12.b (Northeast Atlantic and Arctic Grant College Program, University of New Ocean). In Report of the ICES Advisory Hampshire. 44 pp. Committee, 2018. ICES Advice 2018, bsf.27.nea. EU, 2008. Council Regulation (EC) 2008/199 of 25 doi: 10.17895/ices.pub.4403 February 2008 concerning the establishment of a ICES, 2018c. Report of the Working Group on the Community framework for the collection, Biology and Assessment of Deep-sea Fisheries management and use of data in the fisheries sector Resources (WGDEEP), 11–18 April 2018, ICES and support for scientific advice regarding the HQ, Copenhagen, Denmark. ICES CM Common Fisheries Policy. Official Journal of the 2018/ACOM:14. 771 pp. European Union L 60: 1–12. ICES, 2019a. Advice basis. In Report of the ICES EU, 2017. Commission Decision (EU) 2017/848 of 17 Advisory Committee, 2019. ICES Advice 2019, May 2017 laying down criteria and methodological Section 1.2. doi: 10.17895/ices.advice.5757. standards on good environmental status of marine ICES, 2019b. Blackspot seabream (Pagellus waters and specifications and standardised methods bogaraveo) in Subarea 10 (Azores grounds). In for monitoring and assessment, and repealing Report of the ICES Advisory Committee, 2019. Decision 2010/477/EU. Official Journal of the ICES Advice 2019, sbr.27.10. doi: European Union L 125: 43–74. 10.17895/ices.advice.4820 FAO, 2018. Report of the Technical Workshop on ICES, 2019c. Rays and skates (Rajidae), mainly “Best-practices for the implementation and thornback ray (Raja clavata) in subareas 10 and 12 reporting of SDG Indicator 14.4.1 – Percentage of (Azores grounds and north of Azores). In Report of biologically sustainable fish stocks”, Rome, Italy, the ICES Advisory Committee, 2019. ICES Advice

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2019, raj.27.1012. doi: 10.17895/ices.advice.4832. Sagarese, S.R., W.J. Harford, J.F. Walter, M.D. Bryan, ICES, 2020. Definition and rationale for ICES J.J. Isely, M.W. Smith, D.R. Goethel, A.B. Rios, ecoregions. In Report of the ICES Advisory S.L. Cass-Calay, C.E. Porch, T.R. Carruthers and Committee, 2020. ICES Advice 2020, Section 1.4. N.J. Cummings 2019. Lessons learned from data- doi: 10.17895/ices.advice.6014. limited evaluations of data-rich reef fish species in Kokkalis, A., A.M. Eikeset, U.H. Thygesen, P. the Gulf of Mexico: Implications for providing Steingrund and K.H. Andersen 2017. Estimating fisheries management advice for data-poor stocks. uncertainty of data limited stock assessments. ICES Canadian Journal of Fisheries and Aquatic Journal of Marine Sciences 74: 69–77. doi: Sciences 76: 1624-1639. doi: 10.1139/cjfas-2017- 10.1093/icesjms/fsw145. 0482 Lotaçor, 2019. Fichas técnicas de espécies marinhas Santos, R.V.S., A.M. Novoa-Pabon, H.M. Silva and comerciais dos Açores. Version April 2019. M.R. Pinho 2019c. Can we consider the stocks of Lotaçor, S.A., Departamento de Segurança alfonsinos Beryx splendens and Beryx decadactylus Alimentar e Certificação. Available from: from the Azores a discrete fishery management https://lotacor.pt/uploads/docs/9419.Biblioteca%20 unit? Journal of Fish Biology 94: 993-1000. doi: de%20esp%C3%A9cies%20abril%202019.pdf 10.1111/jfb.13937 (cited 15 May 2020). Santos, R., M. Sigler, A. Novoa-Pabon, W. Silva, E. Martins, H.R. 1982. Biological Studies of the Exploited Isidro, O. Melo, M. Larose, M. Rosa, J. Miodonski, Stock of Loligo forbesi (: Cephalopoda) in L. Rodrigues and M. Pinho 2019b. ARQDAÇO – the Azores. Journal of the Marine Biological Recommendations of the Working Group on Association of the United Kingdom 62: 799-808. research surveys in the Ocean Governance in doi: 10.1017/s002531540007034x Archipelagic Regions International Conference. Maunder, M.N. and A.E. Punt 2004. Standardizing Arquivos Okeanos, Relatórios Internos, nº1/2019. catch and effort data: a review of recent 10 pp. ISSN: 2184-7568. doi: approaches. Fisheries Research 70: 141-159. doi: 10.13140/RG.2.2.13371.85288 10.1016/j.fishres.2004.08.002. Santos, R.V.S., W.M.M.L. Silva, A.M. Novoa-Pabon, Mauser, W., G. Klepper, M. Rice, B.S. Schmalzbauer, H.M. Silva and M.R. Pinho 2019a. Long-term H. Hackmann, R. Leemans and H. Moore 2013. changes in the diversity, abundance and size Transdisciplinary global change research: the co- composition of deep sea demersal teleosts from the creation of knowledge for sustainability. Current Azores assessed through surveys and commercial Opinion in Environmental Sustainability 5: 420– landings. Aquatic Living Resources 32: 25. doi: 431. 10.1051/alr/2019022 Methot Jr., R.D. (Ed.) 2015. Prioritizing fish stock Santos, R., A. Novoa-Pabon, H. Silva and M. Pinho assessments. United States Department of 2020. Elasmobranch species richness, fisheries, Commerce, NOAA Technical Memorandum, abundance and size composition in the Azores NMFS-F/SPO152. 31 pp. archipelago (NE Atlantic). Marine Biology NRC, 1998. Improving Fish Stock Assessments. Research 16: 103-116. Washington DC, The National Academies Press. Sigler, M.F. 2000. Abundance estimation and capture doi: 10.17226/5951. of sablefish, Anoplopoma fimbria, by longline gear. Palomares, M.L.D. and D. Pauly (Eds) 2019. Canadian Journal Fisheries and Aquatic Sciences SeaLifeBase. World Wide Web electronic 57: 1270-1283. publication. www.sealifebase.org (version Wiedenmann, J., C.M. Free and O.P. Jensen 2019. 12/2019). Evaluating the performance of data-limited Pinho, M., W. Medeiros-Leal, M. Sigler, R. Santos, A. methods for setting catch targets through Novoa-Pabon, G. Menezes and H. Silva 2020. application to data-rich stocks: A case study using Azorean demersal longline survey abundance Northeast U.S. fish stocks. Fisheries Research 209: estimates: Procedures and Variability. Regional 129–142. Studies in Marine Science, doi: WoRMS 2020. World Register of Marine Species. 10.1016/j.rsma.2020.101443. Available from http://www.marinespecies.org at Porteiro, F.M. 1994. The present status of the squid VLIZ. Accessed 2020-05-29. fishery (Loligo forbesi) in the Azores archipelago. Fisheries Research 21: 243-253. doi: Submitted 15 Jun 2020. Accepted 13 Oct 2020. 10.1016/0165-7836(94)90107-4. Published online 30 Oct 2020.

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Arquipelago - Life and Marine Sciences ISSN: 0873-4704

SHORT COMMUNICATION

Life goes on: Oblada melanura (Linnaeus, 1758) (, Sparidae), the saddled seabream, expands its distribution range westwards to the Azores

JOSÉ M.N. AZEVEDO AND RAUL M.A. NETO

Azevedo, José M.N. and R.M.A. Neto 2020. Life goes on: Oblada melanura (Linnaeus, 1758) (Perciformes, Sparidae), the saddled seabream, expands its distribution range westwards to the Azores. Arquipelago. Life and Marine Sciences 37: 65 - 70. https://doi.org/10.25752/arq.23650

A group of 10 individuals of the saddled seabream, Oblada melanura (Linnaeus, 1758), was photographed at Lajes do Pico Bay, on , Azores. This finding represents a significant westward expansion of the known range of this species and may be linked to global warming. A call is therefore made for a monitoring program of the coastal fish fauna of the Azores which would improve the understanding of the effects of climate change and other anthropogenic stressors on marine communities.

Key words: Oblada melanura, new record, Azores

José M.N. Azevedo1 (e-mail: [email protected]) and Raul M.A. Neto, 1Centre for Ecology, Evolution and Environmental Changes/Azorean Biodiversity Group (cE3c) & Faculty of Sciences and Technology, University of the Azores, Rua da Mãe de Deus, 13-A, 9500-321 Ponta Delgada, Portugal.

On August 9th 2020 a school of 10 silver-grey jaw not extending backward beyond a vertical fish, less than 20 cm in total length and with a line through middle of eye; long, continuous conspicuous black spot surrounded by a white ; forked caudal fin; single, well ring on the caudal peduncle, was observed inside developed and continuous lateral line extending Lajes do Pico bay (Pico Island, Azores, Portugal, backward to base of caudal fin; pelvic fin inserted approximately 38°23'55.8"N 28°15'21.2"W) (Fig. just behind a vertical line through base of pectoral 1). The group was observed while the authors fin, which is long and pointed. However, were snorkeling over a rocky bottom covered by a Haemulidae, Lethrinidae and are fish multispecific algal turf at about 2 m depth. The families similar to Sparidae (Parenti 2019), and encounter lasted for several minutes which made they cannot be distinguished by using only the it possible to take a number of pictures (Fig. 2) features visible on the images we captured. and make a short video. Therefore, all these four families were included in Observation of the images suggested that the searching for a species match. The procedure fish belong to the family Sparidae, with the consisted of browsing in FishBase (Froese & following visible diagnostic features (Carpenter Pauli 2019) and several other publications (see & Iwatsuki 2016): small size and fusiform body Table 1) for species with a silver-grey colouration with a large head; silver-grey colouration with and a dark spot on the caudal peduncle. The dark spots and lines; mouth small with the upper results are presented on Table 1. 65

Azevedo and Neto

Fig. 1. Observation site on Pico Island (top); Azores (bottom). We did not find any silver-grey species with a Therefore, the analysis shows that only the black spot on the caudal peduncle in the saddled seabream, Oblada melanura, belonging Lethrinidae and Lutjanidae families. In fact, no to the family Sparidae, has all the features visible species of Lethrinidae has a black spot on the in our images. In particular, the combination of a caudal peduncle, whereas the two Lutjanidae silver-grey general colouration with a white ring species which do have such a spot (one of them, surrounding the large black spot on the caudal the sailfin snapper Symphorichthys spilurus, even peduncle was found to be a diagnostic feature of has a white ring surrounding it) are rather this species among the families investigated. colourful fish, with conspicuous body The present record of O. melanura in the ornamentations which were obviously not present Azores represents a significant westward in our individuals. Furthermore, the only three expansion of the species range. The species has a species belonging to the family Haemulidae wide latitudinal distribution along the eastern which have a black spot lack a white ring Atlantic shores (from the Bay of Biscay, into the surrounding it, and two of them have clear yellow Mediterranean and southward to Angola), but it longitudinal lines, not present on the observed had not yet been recorded west of the Madeira individuals. Islands (Froese & Pauli 2019).

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Oblada melanura (Linnaeus, 1758), new record for Azores

The continuous rise in anthropogenic greenhouse (Schäfer et al. 2019) and the Canary Islands gas emissions is increasing global ocean (Espino et al. 2019). The Azores coastal fish temperatures (Pörtner et al. 2019). One of its fauna is also undergoing a process of effects is the tropicalization of temperate marine tropicalization, characterized by the growing communities (Vergés et al. 2014), observable in number of records of species with tropical or the Northeastern Atlantic, from the UK coasts subtropical affinities, which have their (Stebbing et al. 2002) down to the Iberian northernmost distribution limit on this Peninsula (Encarnação et al. 2019), Madeira archipelago. (Afonso et al. 2013).

Fig. 2. Part of the Oblada melanura school observed (top) with detail of one of the indivudals (bottom).

However, the present record of O. melanura on Nevertheless, there may also be a link between these isolated islands does not fit this south to this east to west expansion and climate change, north tropicalization pattern because the species exemplified by the colonization of D. vulgaris. was already present at higher latitudes. Instead, it This species was first caught in the Azores in corresponds to a westward colonization process 1997 (Afonso et al. 2013). However, Steffani et similar to that of several species with northeastern al. (2015), based on results from Approximate Atlantic and Mediterranean origin. Recent Bayesian Computation, indicated that D. vulgaris examples include new records of the roughtail could have inhabited the archipelago over a tingray Bathytoshia lata, the golden grey mullet century ago, and that its demographic expansion Liza aurata, and the two-banded seabream after the 1990s may have been facilitated by Diplodus vulgaris (Afonso et al. 2013). changing climatic conditions.

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Table 1. Features of the observed specimens compared with world-wide species of Sparidae and similar families with silver-grey coloration and a black spot on the caudal peduncle, based on Fisher & Bianchi 1984 (1); Randall 1996 (2); Carpenter 2002 (3); Jiménez Prado & Béarez 2004 (4); Carpenter & Iwatsuki 2016 (5) and Froese & Pauli 2019 (6).

Species Features Distribution Observed Caudal Body ob- Head profile Faint dark Azores (this publication) specimens peduncule long/ elon- straight longitudinal with a black gated, slight- lines spot sur- ly ventrally rounded by a compressed white ring Sparidae Diplodus annularis NO (5) NO (5) YES (5) NO (5) Eastern Atlantic: Canary Islands, from Portugal to the Bay of Biscay, Mediterranean. Black Sea and Sea of Azov. (6) Diplodus capensis NO (5) NO (5) NO (5) NO (5) Southeastern Atlantic and Western Indian Ocean: Angola to Mozambique and southern Madagascar. (6) Diplodus NO (3) NO (3) YES (3) NO (3) Western Atlantic: Chesapeake Bay to holbrookii Florida and northeastern Gulf of Mexico. (6) Diplodus kotschyi NO (1) NO (1) YES (1) YES (1) Western Indian Ocean: Persian Gulf and Oman to India. (6) Diplodus noct NO (1) YES (1) YES (1) YES (1) Red Sea. (6) Diplodus sargus NO (5) NO (5) NO (5) NO (5) West African coast, from to the Straits of Gibraltar; Madeira and Canary Islands; Bay of Biscay. (6) Oblada melanura YES (5) YES (5) YES (5) YES (5) Eastern Atlantic: Bay of Biscay, Mediterranean, and from the Strait of Gibraltar to Angola; Madeira, Cabe Verde Islands, and Canary Islands. (6) Spicara melanurus NO (5) YES (5) NO (5) NO (5) Eastern Atlantic: Cabe Verde Islands and Senegal. (6) Haemulidae Haemulon NO (3) YES (3) NO (3) NO (3) From Chesapeake Bay and through the aurolineatum Gulf of Mexico to Brazil. (6) Haemulon NO (4) YES (4) YES (4) YES (4) Eastern Pacific: Baja California,

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Oblada melanura (Linnaeus, 1758), new record for Azores

Species Features Distribution maculicauda Mexico to Colombia (6) Haemulon NO (2,4) YES (2,4) YES NO (2,4) Western Atlantic: Panama to Santa steindachneri (2,4) Catarina, Brazil. Eastern Pacific: Mexico to Peru (6)

Given the current context of a climate emergency Purposes, Rome, FAO. 3124 pp. (Ripple et al. 2017), the MoniCO program to Encarnação, J., P. Morais, V. Baptista, J. Cruz, M.A. monitor coastal resources and habitats in the and Teodósio 2019. New evidence of marine fauna Azores (Afonso 2020) is particularly welcome. tropicalization off the Southwestern Iberian Peninsula (Southwest Europe). Diversity 11, 48. Considering Azores as a key point for the study Espino, F., F. Tuya, A. del Rosario, N.E. Bosch, J. of Atlantic biogeography (see the recent analysis Coca, A.J. González-Ramos, F. del Rosario, F.J. by Freitas et al. 2019), a long term monitoring Otero-Ferrer, Á.C. Moreno and R. Haroun 2019. program would have more than local relevance; it Geographical range extension of the spotfin would contribute (as emphasized, e.g., by burrfish, Chilomycterus reticulatus (L. 1758), in Sandström et al. 2005) more detailed data to the Canary Islands: A response to ocean warming? understand the effects on marine communities of Diversity 11, 230. climate change and other anthropogenic stressors. Fischer, W. and G. Bianchi (Eds) 1984. Western Indian Ocean (Fishing Area 51). FAO species 1984 identification sheets for fishery purposes. Prepared and printed with the support of the Danish REFERENCES International Development Agency (DANIDA). Rome, FAO, vols 1-6. Afonso, P. 2020. MoniCo – a new program to monitor Freitas, R., M. Romeiras, L. Silva, R. Cordeiro, P. coastal resources, species and habitats in the Madeira, J.A. González, P. Wirtz, J.M. Falcón, A. Azores. Ocean Governance in Archipelagic Brito, S.R. Floeter, P. Afonso, F. Porteiro, M.A. Regions. International Conference 2019, 7-10 Viera-Rodríguez, A.I. Neto, R. Haroun, J.N.M. October 2019, Horta, Azores, Portugal. Farminhão, A.C. Rebelo, L. Baptista, C.S. Melo, A. Arquipelago. Life and Marine Sciences. Martínez, J. Núñez, B. Berning, M.E. Johnson and Supplement 11: 17. S.P. Ávila 2019. Restructuring of the Afonso, P., F.M. Porteiro, J. Fontes, F. Tempera, T. ‘Macaronesia’ biogeographic unit: A marine multi- Morato, F. Cardigos and R.S. Santos 2013. New taxon biogeographical approach. Scientific reports and rare coastal fishes in the Azores islands: 9 (15792). occasional events or tropicalization process? Froese, R. and D. Pauly (Eds) 2019. FishBase. World Journal of Fish Biology 83(2): 272-294. Wide Web electronic publication. Carpenter, K.E. 2002. Sparidae. Pp. 1375-2127 in: www.fishbase.org, version (12/2019). Carpenter, K.E. (Ed.). The living marine resources Jiménez Prado, P. and P. Béarez 2004. Peces Marinos of the Western Central Atlantic, vol. 3. Bony fishes del Ecuador Continental / Marine fishes of part 2 (Opistognathidae to Molidae), sea turtles and continental Ecuador. SIMBIOE/NAZCA/IFEA. marine mammals. FAO Species Identification Tomo II. Quito. Guide for Fishery Purposes and American Society Parenti, P. 2019. An annotated checklist of the fishes of of Ichthyologists and Herpetologists Special the family Sparidae. FishTaxa 4(2): 47-98. Publication No. 5. Rome, FAO. 2127 pp. Pörtner, H.-O., D.C. Roberts, V. Masson-Delmotte, P. Carpenter, K.E. and Y. Iwatsuki 2016. Sparidae. Pp. Zhai, M. Tignor, E. Poloczanska, K. Mintenbeck, 2343-3124 in: Carpenter, K.E. and N. De Angelis A. Alegría, M. Nicolai, A. Okem, J. Petzold, B. (Eds). The living marine resources of the Eastern Rama, and N.M. Weyer (Eds) in press. IPCC Central Atlantic, vol. 4. Bony fishes part 2 Special Report on the Ocean and Cryosphere in a (Perciformes to Tetradontiformes) and sea turtles. Changing Climate. FAO Species Identification Guide for Fishery Randall, J.E. 1996. Caribbean reef fishes. T.F.H.

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Publications, Inc. Ltd., Hong Kong. 368 pp. Stefanni, S., R. Castilho, M. Sala-Bozano, J.I. Robalo, Ripple, W., C. Wolf, T. Newsome, P. Barnard, W. S.M. Francisco, R.S. Santos, N. Marques, A. Brito, Moomaw and P. Grandcolas 2017. World V.C. Almada and S. Mariani 2015. Establishment scientists’ warning to humanity: A second notice. of a coastal fish in the Azores: recent colonisation BioScience 67: 1026–1028. or sudden expansion of an ancient relict Sandström, O., Å. Larsson, J. Andersson, M. population? Heredity 115: 527–537. Appelberg, A. Bignert, H. Ek, H. and M. Olsson Vergés, A., P.D. Steinberg, M.E. Hay, A.G.B. Poore, 2005. Three decades of Swedish experience A.H. Campbell, E. Ballesteros, K.L. Heck Jr, D.J. demonstrates the need for integrated long-term Booth, M.A. Coleman, D.A. Feary, W. Figueira, T. monitoring of fish in marine coastal areas. Water Langlois, E.M. Marzinelli, T. Mizerek, P.J. Quality Research Journal, 40(3): 233-250. Mumby, Y. Nakamura, M. Roughan, E. van Schäfer, S., J. Monteiro, N. Castro, G. Rilov and J. Sebille, A.S. Gupta, D.A. Smale, F. Tomas, T. Canning-Clode 2019. Cronius ruber (Lamarck, Wernberg and S.K. Wilson 2014. The 1818) arrives to Madeira Island: a new indication tropicalization of temperate marine ecosystems: of the ongoing tropicalization of the northeastern climate-mediated changes in herbivory and Atlantic. Marine Biodiversity 49: 2699–2707. community phase shifts. Proceedings of the Royal Stebbing, A. R. D., S. M. T Turk, A. Wheeler and K.R. Society B 281 (1789): 20140846. Clarke 2002. Immigration of southern fish species to south-west England linked to warming of the North Submited 08 Nov 2020. Accepted 16 Dec 2020. Atlantic (1960–2001). Journal of the Marine Biological Published online 14 Jan 2021. Association of the United Kingdom 82 (2): 177-180.

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Arquipelago - Life and Marine Sciences

Book Review

The ecology, biogeography and speciation of the butterflies of the Azores, by Mark Payne. Hardback. World Natural History Publications, “The Lake District”, 2019, 370pp.

This is the second book in a planned series of numerous books covering all of the world’s butterflies. It opens with a detailed and lengthy account of the author, his supposed achievements and future plans. A prominent acknowledgement to Martin Wiemers, a highly respected European entomologist, is out of date. Martin has disassociated himself from the books and withdrawn co- authorship of a proposed volume on Macaronesian endemic butterflies advertised in the book. Following a misspelling of Alfred Russell [sic] Wallace’s name in connection with a quote, there is a rambling list of the contents, which are largely copied from other’s books and research papers, often inaccurately. Throughout the book, the largest city of the Azores, Ponta Delgada, is misspelled “Ponta Delgarda”. Tables figure prominently and are frequently either inaccurate or irrelevant. For example, Table 5 (p. 47), said to provide average monthly and annual precipitation in the Azores, doesn’t. There is no annual rainfall and no figures for three months of the year; other tables include pre- and post-monsoon larval instar duration and weight of larval faeces in laboratory rearing experiments in India! Fourteen pages of pictures (pp. 28-41) present 28 “Azorean Landscapes”, none identified by island. There is every indication that the author has never been to the Azores, and it is probable that he has no idea which islands are depicted. Very many text citations are lacking from the references, and some are cited inaccurately. For example (Chapter five: flora, p. 46), he declares “Marsden & Wright (1971) made interesting notes on cloud cover at two different altitudes on on 30 days of August 1965”. No, they didn’t. Marsden & Wright were on São Jorge, not Faial and data were collated on undisclosed days “between July and September 1965”. Table 6 (p. 49) is taken from “Elias et al. (2016)”, which appears in the references with only four of the six authors and the wrong volume of the journal in which it was published (“48(2)” [sic: recte 46(2)]). The author is swift to highlight trivial mistakes of others, overlooking – or perhaps being impervious to – his own failings. His own typographical errors (or ignorance) are numerous: “Pericalis [sic: recte Pericallis]” (p. 73); “Macronesian [sic: recte Macaronesian]” (p. 110); “Gomophocarpus [sic: recte Gomphocarpus]” (p. 114); “Asclepias curassavicai [sic: recte “Asclepias curassavica]” (p. 114); “Satyrid [sic: recte satyrine]” (pp. 118, 183 and elsewhere); “Campoplex turniculus [sic: recte turdiculus]” (p. 125); “Ichneumonmidae [sic: recte

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John Tennent

Ichneumonidae]” (p. 134); “Occum’s [sic: recte Occam’s] Razor …” (p. 184); “non-sequiteur [sic: recte non-sequitur]” (p. 215); “Urethesia [sic: recte Utetheisa]” (p. 361) … and so on. More significant gaffes are many and varied. For example (p. 63): “The largest number of total taxa [sic] found were [sic] in [sic] São Miguel …”. The reviewer suggests the author intended to say that the greatest number of taxa occur on São Miguel, but there are instances where his meaning is unclear and his clumsy syntax can be confusing. For example (p.224): “… males of H.miguelensis emerged, followed two days later by females of H.azorina jorgense. Pairings took place and over the course of the following few days 30 eggs were laid …”. The prose is extraordinarily laboured on occasions: for example, rather than ‘significant’ we see “can be of not a little significance” (p. 275). The author’s ignorance is also exposed: unfamiliar with the useful term ‘monotypic’, he declares “Lampides boeticus constitutes a genus by itself …” (p. 103). Throughout the book grammar and punctuation are poor, and there is a lack of important supporting information. For example, with spelling, punctuation and spacing reproduced here precisely (p.223: all square brackets are the reviewer’s): “It would appear that Motacill [sic: recte Motacilla] cinera [sic: recte cinerea] patriciae (Varie [sic: recte Vaurie] 1957) [the Azores Grey Wagtail] could use H.azorina as their diet includes insects. Predators [such] as Lacerta. spp. [a genus of lizards] do not occur in the habitats of the H.azorina complex …”. Chapter 10 (pp. 90-98) covers the study of butterflies in the Azores, which includes reproduction in full of many accounts published by previous visitors interspersed with extensive and gratuitous criticism. Butterfly accounts begin on p. 99. The first is Lampides boeticus, which includes lengthy passages copied from a paper by “Palem et al. (2015)”, spelled variously “Palem”, “Palim” (p. 101) or “Padem” (p. 103). The paper, absent from the references, relates to rearing boeticus in Andhra Pradesh, India, on a host-plant that apparently doesn’t occur in the Azores. This was an unsuitable paper to copy, since although Palem et al. believed they were dealing with L. boeticus, the 10 adults illustrating their work are Euchrysops cnejus, a species that occurs from India to the Pacific. This would have been spotted immediately by any schoolboy butterfly collector in Europe but, as the reviewer has remarked elsewhere in an assessment of the author’s book, his butterfly identification skills are hopeless. Danaus plexippus follows (pp. 108-116) and includes the claim “… with its larvae feeding on Asclepias G.fruticosus [sic: ‘Asclepias fruticosa’ is an outdated name for Gomphocarpus fruticosus] (Neves et al, [sic] 2001) and A.sericofera. [sic: in addition to misspelling sericifera, the implication is that this is a species of Asclepias; it belongs to the genus Araujia]”. Following entries include Danaus chrysippus (p. 117): with a groundless statement that “It is felt that D.chrysippus could in due course establish a breeding colony in the Azores, given appropriate climatic conditions, but first migrant individuals would most likely be seen over a period of some years” and Hypolimnas misippus (pp. 120-121): “First noted in the Azores by the late Ronny Leestmans … citing (incorrectly) Williams … but without noting the island on which it was captures [sic]”. The reality is there was no island to record: Williams reported seeing misippus out at sea. Vanessa atalanta occupies eight pages (pp. 122-130), mostly irrelevant to the Azores, including the bizarre statement that (p. 125): “Garcia-Barros et al [sic] (2013) reported that occasionally imagines are attacked and killed (and eaten) by the bee-killing Hymenopteran, Merops apiaster”. Since a ‘hymenopteran’ is a member of the insect order Hymenoptera, and M. apiaster is the European bee-eater (a passerine bird), the reviewer contacted Enrique Garcia-Barros (predictably, the text reference is not in the bibliography). The sentence is taken from p. 704 of Garcia-Barros’ multi-authored volume 37 of Fauna Ibérica (Lepidoptera, Papilionoidea): “It has occasionally been observed that adults are eaten by bee-eaters, Merops apiaster [translation]). The author’s opinions illustrate a tenuous grasp on reality; for example, following discussion of temperature 72

Arquipelago - Life and Marine Sciences development rates of V. atalanta published by others, he states (p. 126): “it would appear to this author that up to ten generations per annum could theoretically be feasible in Cabo Verde, while in the Canary Islands five generations each year could be feasible, in Madeira three or four, and in the Azores two or three”. Colias croceus (pp. 141-152) is dealt with in detail; it comprises substantial data copied from other people’s research, interspersed with criticism of others which serve no purpose and reflect badly on the author. A detailed paragraph on the occurrence of Colias hyale (p. 153), mapped as occurring throughout São Miguel (it doesn’t occur in the Azores), wilfully misinterprets a note by Vieira and Constancia. Pieris brassicae (pp. 154-160) is a combination of the copied work of others, missing references, and condescendingly arrogant opinion: “Some pseudo-scientific observers consider [Azorean brassicae] to be a separate sub-species …” (p. 154)). The author’s quintessential ignorance of entomological matters is confirmed in his reference to the “parasite[s] [sic: recte parasitoids]” Cotesia glomeratus and Apanteles glomerata in the same paragraph (p. 155) apparently without realising they are the same thing. He ends his treatment of P. brassicae with the note: “So extensive, not to say confusing, has been the nomenclature of this species in the Azores that it bears summarising here …”. He then provides a woefully incomplete ‘list’ of previous authors using ‘Pieris brassicae’ (6: between 1860-1982); ‘Pieris brassicae ab.chariclea’ (1: 1905); ‘Pieris brassicae brassicae’ (1: 1961) and ‘Pieris brassicae azorensis’ (8: 1917-1993), indicating if anything (inclusion of ‘P. brassicae’ is meaningless in this context) that nomenclatural history of brassicae in the Azores is, as presented, very straightforward. Pages 161-163 relate to “doubtful species” (sic: recte doubtful records; the species are not in doubt) and are followed by (pp. 164-175) illustrations of Azores butterflies, more than half the text references to which have the wrong page number. The bulk of these are taken from the website of Matt Rowlings (recorded as “Matt Rowlands [sic]” in the acknowledgements), who tells the reviewer he has never visited the Azores, raising the high probability that very few of the butterflies illustrated are actually from the islands. A double page spread (pp. 166-167) of D. chrysippus and H. misippus, neither of which occur in the Azores, is excessive, particularly as three male uppersides of misippus are much the same and were photographed in India. The six pictures of P. brassicae (p. 174) are without doubt not from the Azores and six undersides said to be of C. hyale, which has never occurred in the Azores, are impossible to identify. A voluminous and subjective section on Hipparchia (pp. 176-261) includes long-winded polemic, which seems particularly out of place coming from an ‘author’ whose own knowledge of butterflies generally is minimal. Whilst the two species of Hipparchia on the Azores are more interesting than any other group of butterflies on the islands, the author’s treatment of the subject over 85 pages is, in the opinion of the reviewer, unscientific and substandard. It includes extensive passages from an unpublished work and two long muddled sections that appear to be different drafts of the same thing (pp. 214, 216). He declares (p. 242): “Plates … show images of Hipparchia habitats in the Azores”. The seven pictures (pp. 258-261) do show Hipparchia habitat, although their geographical source is not recorded, possibly because the information was not known to the author. For the record, all were taken by Martin Wiemers on Terceira. This is followed (pp. 275-280) by a section on ghost islands and ghost species, which include (p. 275) the unsupported “reasoned observation that an Azorean Vanessid [sic] butterfly from geological history, and which is now extinct … may in fact have been the ancestor of V. vulcania”. A section titled “The Curious Case of Vanessa Vulcania [sic]” (pp. 281-298) presents pretentious views on a butterfly that does not and has never been suggested to occur on the Azores that include some very nice photographs of larvae and pupae (Mr Payne believes the singular of larvae is larvum) taken by ‘Rose-Marie Haccour’, not mentioned in the acknowledgments. The final

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John Tennent chapter describes where to see butterflies on the Azores. It consists of rough outlines of each island with some localities vaguely marked and a plea: “for future editions of this book this author would welcome receiving details of readers’ own ideas concerning noteworthy localities …”, no doubt necessitated by the author’s own lack of knowledge. There is no index. There is no logic to the presentation of references (pp. 315-365) and both the purpose and process of presenting references in a scientific work clearly elude the author. Literally dozens of text references are absent, whilst a plethora of his own “publications”, mostly with the wrong date of publication (all are dated 2019 and so far as the reviewer is aware, in early January 2020, only three of almost 30 planned titles have seen the light of day) and incorrect page numbers are listed. The references are a chaotic muddle. Fundamentally this book is a grimly unethical exercise in copying the work of others. The author has no background in science or Lepidoptera research and this is abundantly clear. In the opinion of the reviewer Mr Payne’s corrosive approach is unwelcome. The book is abysmal. It is not recommended. John Tennent 18 Feb 2020

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EDITORIAL NOTES

ARQUIPElAGO – Life and Marine Sciences

Forty years of natural sciences in the Atlantic Ocean

The journal has gone through several presentation changes since the first volume in 1980. At the 30 years anniversary in 2010, a narrative of the progress during those years was given. The present Editorial Board includes 10 scientists with experience in working in the Atlantic Ocean and Atlantic oceanic islands in different fields of marine and terrestrial biology, fishery science and biodiversity from Canada, France, Ireland, Netherlands, USA, Madeira and Azores. During the last years, articles have been published from Azores, Madeira, São Tomé e Principe, Cabo Verde, Canary islands, St. Helena, Ascension, Falkland islands and St. Peter and St. Paul archipelagos.

Since 2010 ten volumes and five more Supplements have been published:

8 - 2015 9 - 2016 10 - 2017 12 - 2020 01 - 2021

www.okeanos.uac.pt/arquipelago

Helen Rost Martins

The first issue of the Natural Sciences series of the Arquipelago journal was published in 1980, under the auspices of the Azores University Institute, the preparatory stage of the current University of the Azores. At the same time the series of Humanity was published and in the following years 7 more series, aiming to be an instrument for the researchers and teachers of this university to publish their results of research, planned to have an annual periodicity. As for the series of Natural Sciences annual issues continued for the next 5 years, followed by a suspension. There were no publications of the journal during four years and number 7, which was prepared, ended up without being printed. It was on this hiatus that the researcher Helen Rost Martins was invited by the rector of the University of the Azores to become the editor of this series of the Bulletin of the University of the Azores in order to revitalize it. Thus, this Archipelago series, become specialized in Life and Marine Sciences, opened up to the entire scientific community, modernized itself, having English as its preferred language, a graphically more compact and attractive format, and above everything started to have a peer review system composed by national and international experts. Not less relevant is the fact that it has reached the routine of being an annual publication since

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1990, since the number 8 to present, not counting with the supplement issues numbers dedicated to specific scientific events. I will never forget my participation in the graphic edition of number 8, which marked the transition from the original format to the current one. The level of scientific quality achieved in this journal is greatly due to the professionalism and obstinate persistence of its editor, who has always overcome the problems it faced over the years. Finding sources of funding was one of these chronic problems, but always solved. The exhaustive work of maintaining communication with the scientific reviewers selected for each paper, constituted the invisible part of the work Helen has carried out over the past three decades. A good example of this resilience is the fact that Life and Marine Science is the only series of the journal Arquipelago that continues to this day. Arquipelago - Life and Marine Sciences is a regular journal, with a solid peer review system, independent of large editorial groups, publishing open access papers and without costs to the authors, which is a great singularity today!

João Gonçalves

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EDITORIAL NOTES

We acknowledge with gratitude the financial support for nos. 35 and 36 given by Secretaria Regional do Mar, Ciência e Tecnologia e Direção Regional das Pescas, do Governo dos Açores, do IMAR – Instituto do Mar e do OKEANOS – Centro de I&D da Universidade dos Açores.

The Editor of Arquipelago – Life and Marine Sciences, sincerely thanks the scientists listed below who served as reviewers for the numbers 35 and 36.

35: 36: Marco Taviani, Italy Manuel Biscoito, Madeira, Portugal John Lawrence, Florida, USA Ronald Fricke, Germany Christopher Mah, Washington DC, USA João L. Gasparini, Espirito Santo, Brazil Simone Fattorini, Italy Daniel Golani, Israel Hanno Schaefer, Germany Bert W. Hoeksema, Netherlands Ronald Fricke, Germany James Reimer, Japan Peter Wirtz, Madeira, Portugal Joёl Bried, France Manuel Biscoito, Madeira, Portugal Charles Fransen, Netherlands John C. Briggs, California, USA † Katharina Peters, Australia Paulo A.V. Borges, Azores, Portugal Cláudia Oliveira, Azores, Portugal Rui Elias, Azores, Portugal Maria Capa, Majorca, Spain Artur Serrano,Portugal Gabriela Garcia-Soto, Alabama, USA Martin Collins, United Kingdom

ARQUIPELAGO – LIFE AND MARINE SCIENCES

EXCHANGE b) Reference to a chapter from a book: The Journal is distributed on exchange basis through the O’Dor, R., H.O. Pörtner and R.E. Shadwick 1990. Squid publisher. as elite athletes: locomotory, respiratory, and circulatory integration. Pp. 481-503 in: GILBERT, D. L., W. J. PURCHASE ADELMAN, JR. and J. M. ARNOLD (Eds). Squid As Hard copies can be purchased from the publisher. Experimental Animals. Plenum Press, New York- OFFPRINTS London. 516 pp. First authors receive a hard copy of the journal. c) Article from a journal: INSTRUCTIONS TO AUTHORS Bentley, M.G., P.J.W. Olive, P.R. Garwood and N.H. Wright 1984. The spawning and spawning mechanism General. MSS should be submitted to the Editor by e- of Nephtys caeca (Fabricius, 1780) and Nephtys mail: [email protected]. homebergi Savigny, 1818 (Annelida: Polychaeta). The text, in English, should be ready to go online and Sarsia 69: 63-68. carefully checked for all errors, including linguistic d) Electronic article, from online-only Journal: ones, before submission. Choose font Times New Roman, size 12, double spaced paragraph and insert Woo, K.L. 2006. Testing Visual Sensivity to the Speed page numbers. MSS that are not in accordance with the and Direction of Motion in Lizards. Journal of instructions will be returned for revision. All MSS will Visualized Experiments [Internet]. Available from: be peer-reviewed by two referees prior to their http://www.jove.com/index/details.stp?id=127 (cited 18 acceptance by the Editor. February 2007)

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E-mail Attachment. All text and images files formats References. (6) Should correspond with the examples are accepted. Attachments must be identified with the given below: author's last name followed by the file name and extension (e.g. Bianchi_text.doc, Bianchi_fig1.tif, a) Reference to a book: Bianchi_tab1.xls). Boyle, Peter 2009. Life in the Mid Atlantic. Bergen For instruction to authors consult our webpage at: Museum, University of Bergen. 240 pp. http://www.okeanos.uac.pt/arquipelago

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ISSN 0873-4704

ARQUIPELAGO - Life and Marine Sciences

No. 37 – 2019/2020 CONTENTS: PAGE

POLAINO-MARTIN, CLARA, R. GABRIEL, P.A.V. BORGES, R. CRUZ AND I.S. ALBERGARIA Bryophytes of Azorean parks and gardens (I): “Reserva Florestal de Recreio do Pinhal da Paz” - São Miguel Island 1

PINHO, M., R. SANTOS, O. MELO, E. ISIDRO, A. NOVOA-PABON, W. SILVA AND J. GONÇALVES Estimates of biomass and potential yield for the deep-water red crab, Chaceon affinis and the toothed rock crab, Cancer bellianus (Decapoda: Brachyura) off the Azores (Mid-North Atlantic) 21

HIPÓLITO, C., R.M.A. NETO, T.M.M. COSTA, M.A. DIONÍSIO, A.C.L. PRESTES, J.M.N. AZEVEDO, G.M. MARTINS AND A.I. NETO Frondose and turf-dominated marine habitats support distinct trophic pathways: Evidence from 15N and 13C stable isotope analyses 37

SANTOS, RÉGIS, W. MEDEIROS-LEAL AND M. PINHO Stock assessment prioritization in the Azores: procedures, current challenges and recommendations 45

AZEVEDO, JOSÉ M.N. AND R.M.A. NETO Life goes on: Oblada melanura (Linnaeus, 1758) (Perciformes, Sparidae), the saddled seabream, expands its distribution range westwards to the Azores 65

TENNENT, J. Book Review - The ecology, biogeography and speciation of the butterflies of the Azores, by Mark Payne. Hardback. World Natural History Publications, “The Lake District”, 2019, 370pp 71

Forty years of natural sciences in the Atlantic Ocean 75

EDITORIAL NOTES 77