Regional Studies in Marine Science Exploring Marine Invasions

Regional Studies in Marine Science 37 (2020) 101333

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Regional Studies in Marine Science

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Exploring marine invasions connectivity in a NE Atlantic Island through the lens of historical maritime traffic patterns

Nuno Castro a,⇤, Patrício Ramalhosa a,b, Jesús Jiménez a, José Lino Costa c, Ignacio Gestoso a,d, João Canning-Clode a,d a MARE - Marine and Environmental Sciences Centre, Agência Regional para o Desenvolvimento da Investigação Tecnologia e Inovação (ARDITI), Edifício Madeira Tecnopolo, Piso 0, Caminho da Penteada, 9020-105 Funchal, Madeira, Portugal b OOM - Oceanic Observatory of Madeira, Agência Regional para o Desenvolvimento da Investigação Tecnologia e Inovação, Edifício Madeira Tecnopolo, Piso 0, Caminho da Penteada, 9020-105 Funchal, Madeira, Portugal c MARE—Marine and Environmental Sciences Centre, Faculdade de Ciências, Universidade de Lisboa, Lisbon, Portugal d Smithsonian Environmental Research Center, 647 Contees Wharf Road, Edgewater, MD 21037, USA article info abstract

Article history: In recent decades, maritime traffic has been increasing globally. Introduction vectors involving ships, Received 20 January 2020 hull fouling and ballast water are often cited as having high risk for introducing marine non- Received in revised form 18 May 2020 indigenous species (NIS) worldwide. Due to its geographical location, Madeira Island (Portugal) had Accepted 28 May 2020 a significant role in past maritime connections, with the ability to serve as a ‘‘port of call’’ facility. Available online 1 June 2020 However, little is known about past temporal maritime traffic patterns in Madeira, and particularly its Keywords: relationship with NIS introductions. In this context, the present study was designed to create a first Marine traffic and comprehensive baseline for historical maritime traffic data for Funchal port, Madeira’s main port, Madeira island between 1936 and 2004. Official marine traffic data with stops in Funchal were documented, including Biological invasions information concerning last port, ship type, ship size, and residence time in port. In addition, a Introduction vectors comprehensive literature search of NIS detected in Madeira Island until 2004 was conducted. Based on Ballast water the frequency of ship arrivals from different origins five statistically different periods of maritime traffic Biofouling were determined. The most common maritime traffic origin arriving at Funchal was from Portugal (mainland), Great-Britain, Canary Islands and Spain mainland (Mediterranean). The most relevant IUCN bioregions of Madeira’s maritime traffic origins were in accordance with the frequency of the native distribution of the island’s marine NIS inventories until 2004. The present study reports for the first time a significant and positive relationship with native regions of NIS present in Madeira until 2004 with the most relevant maritime traffic routes, confirming maritime traffic as one of the main vectors for the introduction of these species in Madeira Island. Finally, a continuous monitoring, update, and analysis of maritime traffic, identifying invading corridors, needs to be maintained as a fundamental tool for management NIS introductions in Madeira Island. © 2020 Elsevier B.V. All rights reserved.

1. Introduction et al., 2018). There has been a large intensification in biological invasions, with an increase in the number of species (plants Biodiversity today faces unprecedented constraints as an- and animals) introduced into ecosystems far from their native thropogenic activities have been and are still continuing to al- range (Antunes et al., 2009). In the marine system, there are ter ecosystems on local and global scales (Hooper et al., 2005; several vectors that can transport NIS from their native range to Costello et al., 2010). Climate change, habitat destruction and the other locations (Bax et al., 2001). In this context, shipping has introduction of non-indigenous species (NIS) are key stressors been identified as a major introduction vector for NIS through ballast water and hull fouling (Chainho et al., 2015; Minton et al., that are affecting biodiversity and causing ecosystem disturbance 2015). Recreational boating is another important vector of NIS (Thuiller, 2007; Costello et al., 2010). These modifications are introduction through hull fouling. Firstly described as secondary causing dramatic changes in the biotic structure and compo- spreading vector or hubs (Zabin et al., 2014; Marchini et al., 2015), sition of ecological communities (Hooper et al., 2005; Gestoso recent research provided evidence that recreational boating is also responsible for primary introductions (Ferrario et al., 2017). ⇤ Corresponding author. However, there are other introduction vectors associated with E-mail address: [email protected] (N. Castro). human activities, such as aquaculture, live bait, aquarium trade https://doi.org/10.1016/j.rsma.2020.101333 2352-4855/© 2020 Elsevier B.V. All rights reserved. 2 N. Castro, P. Ramalhosa, J. Jiménez et al. / Regional Studies in Marine Science 37 (2020) 101333

(e.g. discards or releases) or marine debris (Padilla and Williams, should be at levels that do not adversely alter ecosystems. The 2004; Guedes et al., 2009; Afonso, 2011; Galil et al., 2015; Rech first commitment to minimize the problem should be to im- et al., 2016; Carlton et al., 2018). plement practices to control and manage the introductions of New non-indigenous estuarine and marine species (e.g. NIS by maritime traffic. Alongside the MSFD in September 2017 Caulerpa taxifolia (Vahl) C. Agardh 1822; Carcinus maenas (Lin- entered into force the Ballast Water Convention (BWC), where naeus, 1758); Ruditapes philippinarum (Adams & Reeve, 1850)) several standards need to be met to reduce NIS introduction by have been establishing worldwide (Ruiz et al., 2000; Papini et al., this vector (IMO, 2020). Moreover, the International Maritime 2013) at a rate that appears to be increasing (Sardain et al., 2019). Organization (IMO) have implemented the GloBallast program to Moreover, shipping in the past decades has increased globally, assist the implementation of the BWC (IMO, 2020). with 80% of global trade by volume and more than 70% of its In addition to these actions, it is essential to identify the main value being carried by ship (UNCTAD, 2017). Introduction vectors shipping routes and the likelihood for new species introductions involving the movement of ships and boats (e.g. biofouling and (Holeck et al., 2006). In the Macaronesia region studies related ballast water discharges) are often cited as having high risk for with NIS and maritime traffic are scarce (but see Canning-Clode the introduction of marine NIS and this concurs with the finding et al., 2013; Micael et al., 2014). Particularly in Madeira, there that NIS hotspots are usually located in areas with a high volume has been a growing interest in biological invasions with numer- of maritime traffic and people (Eno et al., 1997; Canning-Clode ous NIS detections in recent years, resulting from ongoing NIS et al., 2013; Seebens et al., 2013). In this context, Canning-Clode monitoring campaigns (Wirtz and Canning-Clode, 2009; Canning- et al. (2013) and Lacoursière-Roussel et al. (2016) verified that assemblages of NIS fouling species (e.g. Botryllus schlosseri (Pallas, Clode et al., 2013; Ramalhosa et al., 2017b, 2019). However, 1766); Distaplia corolla Monniot F., 1974) were consistently studies regarding shipping characterization in Madeira are only higher in areas with increased arrivals of ships and recreational found in the form of books, mostly associated to shipping compa- vessels. In North America, Ruiz et al. (2000) observed that ship- nies operating in the region (Correia, 2003, 2009). Consequently, ping accounted for 51% of the 298 initial invasions documented in little is known about past maritime traffic in Madeira, particularly their study. There are several features related to shipping/boating its patterns over time and its connection with species invasions. that may influence NIS introductions (i.e. intensity of propagule In this context, the present study conducted a first and base- pressure), namely the ship type (e.g. Container, Bulker, Tanker) line characterization of the historical maritime traffic into and size, their residence time in port and traffic patterns, among Madeira Island and its relationship with NIS detections over a 70- others (Davidson et al., 2006; Minton et al., 2015). For example, year-old period. Based on a comprehensive dataset of historical containerization of cargo has reduced the risk of invasions by NIS, maritime traffic, we further identified opportunity windows and because this ship type has a shorter residence time in ports and relevant invasion corridors for NIS, essential to control species faster sailing speeds, decreasing this way the opportunities for invasions particularly relevant in an insular context. colonization of hulls in ports and persistence on hulls (Davidson et al., 2006). 2. Material and methods Ever since humans began travelling in ships, they have carried diverse organisms, accidentally or deliberately (Bax et al., 2003). For example, wooden sailing ships were often heavily covered 2.1. Study area with fouling organisms, in the hull, dry ballast and anchor chain (Carlton, 1999). In the XV century, in Europe, Portuguese and The Madeira Archipelago (Portugal) is located in the North At- Spanish sailors started their overseas expansions years before lantic Ocean, 32240N, between 16160 and 17160W(Fig. 1). It lies others European nations (Garcia, 2017). Both Portuguese and in the Macaronesia region, together with the Azores, the Canary Spanish empires have used several Atlantic islands as strate- Islands and Cabo Verde archipelagos. The Madeira archipelago gic locations for their expansion operations. In this context, the comprises two populated islands, Madeira (resident population Macaronesia islands (comprised by the Azores, Madeira, Canary of 259,195) and Porto Santo (resident population of 5,173) (INE, Islands and Cabo Verde archipelagos) as well as other Atlantic 2019) and two smaller uninhabited group of islands (Desertas and islands provided ‘‘port of call’’ facilities for these ancient explor- Selvagens) that are Marine Protected Areas (MPA). The present ers (Garcia, 2017). In this period, Portuguese ships have likely study was focused on Madeira Island only, which is the largest played a relevant role in marine species introductions (Blakeslee, of the archipelago, with 63 km in length and 23 km in width 2015). For example, the Portuguese oyster (Crassostrea angulata at its maximum. The coastline offers only a reduced number of (Lamarck, 1819)) was recently discovered that had Asian origin small coves with only a few sandy beaches. There are some bays, and introduced to Portugal in the 16th century by Portuguese where geographical features allowed some protected areas and navigators (Blakeslee, 2015). Since the end of World War II, with where, as a logical consequence, the principal ports of the island the resulting technological innovations, there has been a marked emerged (Funchal and Caniçal). increase in human population, economic activity, production and According to the Madeira Port Authority (APRAM, 2019) the consumption, resource use, and transport and flow of people and exploration of the Funchal Port was established in 1756, under- goods (Fernandes, 2009). Currently, shipping is a complex network of movement patterns of different types of ships operating going several stages of construction and extension of the mooring at a global scale (Kaluza et al., 2010). berth. In 1961 this extension of the Funchal Port was completed, Nowadays several policy and regulatory instruments address where the fundamental structures of what is today Funchal port NIS introductions essentially focusing on preventive measures, by were created. In 2004, the Master Plan of the Port of Funchal ways of pathways and introduction vectors management was approved, which defined its future as a port exclusively (Chainho et al., 2015). One example is the Marine Strategy Frame- dedicated to cruise tourism and nautical activities, freeing the work Directive (MSFD), that requires all European Union State city of Funchal from handling and cargo transportation. In this Members to achieve the Good Environmental Status of marine context, during 2005, containers, freight and unloading services ecosystems by 2020, and where one of the 11 descriptors tar- were transferred to the Port of Caniçal, located in the eastern part geted for monitoring are NIS (Descriptor 2) (MSFD.EC, 2008). This of the island. Currently, Funchal Port serves as Madeira’s major descriptor establishes that NIS introduced by human activities hub for ferries and cruise ships (APRAM, 2019). N. Castro, P. Ramalhosa, J. Jiménez et al. / Regional Studies in Marine Science 37 (2020) 101333 3

Fig. 1. Location of the Madeira archipelago, with indication of Funchal Port (Portugal).

Fig. 2. Number of ship entries, by ship type, in Funchal Port (Portugal) from 1936 to 2004. Data between 1950 and 1959 and in the biennium 1986–1987 were missing and therefore were not included in the analysis.

Fig. 3. Hierarchical cluster analysis diagram, where is displayed the year of ship entries according to their origin arriving in Funchal Port (Portugal) from 1936 to 2004. The analysis showed the formation of five different periods with a cut-off line at the Euclidean distance of 178.25. 4 N. Castro, P. Ramalhosa, J. Jiménez et al. / Regional Studies in Marine Science 37 (2020) 101333

2.2. Data collection modified by Hewitt and Campbell (2010). For assessing species native distribution several research articles and databases (Hewitt Ships arriving at Funchal from 1936 to 2004 were analysed and Campbell, 2010; Hewitt et al., 2009, 2012; Froese and Pauly, using the official logbooks provided by the Madeira Port Authority 2019) were used. The relationship between NIS IUCN marine (Administração dos Portos da Região Autónoma da Madeira, S. A., bioregions frequency and vessels origins frequency, also consider- APRAM). These logbooks were handwritten, and as a result, all ing IUCN marine bioregions, was examined by a Spearman’s rank information had to be transferred to a digital format, standardized correlation test, using R (R Core Team, 2017). (terminology) and revised. For the purpose of our study, the All statistical analyses (except mentioned otherwise) were following shipping information were considered for the analyses: performed using PRIMER v6 software package (Clarke and War- arrival and departure date, ship type (Bulker, Containers, General wick, 2001) with the PERMANOVA add-on package (Anderson cargo, Passengers, Passengers and cargo, Ro-Ro, Reefer, Tanker, et al., 2008). Flow maps were developed to visualize maritime Recreational vessels and others (i.e. scientific, navy or any other traffic intensity arriving at Funchal Port. Maps were produced in type of ship), port of origin, Gross Tonnage (GT), and port of R(R Core Team, 2017) using ‘‘gdistance’’ (van Etten, 2018) and destination. Due to unforeseen reasons (stolen and/or lost), log- ‘‘sf’’ (Pebesma, 2018) packages. The number of ship trips from books with registered information between 1950 and 1959 and the origin port to Funchal was calculated, for both the whole- between 1986 and 1987 were missing and therefore were not time span and each significant period. A least-cost path analysis included in the database. In addition, logbooks between 1960 was performed to connect the origin port and the target port and 1974 only contained passenger ships information. Finally, (i.e. Funchal Port). The model assumes a higher cost (or lower a comprehensive literature search was conducted in scientific conductance values) for pixels in a raster surface representing documentation which included works in the format of scientific land areas, with respect to pixels over the sea surface. Therefore, articles, books, book chapters, theses and reports. This search was the path connecting ports, some of which are located inland, are conducted in English and Portuguese, between 1897 and 2004. All more prone to traverse sea than land pixels. Assuming an equal references were carefully examined for NIS records in Madeira cost for pixels in the same category (land or sea surface), the Island and relevant subsequent citations were also analysed. In route follows the great circle distance (shortest distance between total, 81 references were detected and 16 validated and were two points on the globe). To avoid unrealistic trips over the therefore included in our analyses. A species was considered poles, the globe was cut down in terms of geographical extension. NIS and therefore validated when one of the following criteria The log number of trips was used to plot the data due to the was met: (i) reference of its biogeographic status in literature presence of extreme values and mapped into a viridis colour or known biological invasions databases (e.g. NEMESIS, AquaNIS palette (Garnier, 2018). The legend shows the correspondence and WRIMS); (ii) indication that a species was found within ports between real values and those based on the log transformation. and/or marina areas as these locations have higher propagule The code is available in github (https://github.com/jesusjl/jesusjl- pressure and are considered NIS hotspots (Canning-Clode et al., maritime-traffic-least-cost). 2013; Seebens et al., 2013); (iii) species that underwent tropicalization processess (i.e. shifts in range distribuition induced by 3. Results climate change (Canning-Clode and Carlton, 2017). As previously stated, 2004 represents the last year that Fun- A total of 43,071 ships arrived at Funchal Port between 1936 chal Port was used as a cargo hub. For this reason, our literature and 2004 (Fig. 2). The most common origin was Lisbon port search for NIS in Madeira also ceased in 2004. (Portugal mainland), with 10,208 (23.70%) entries followed by Porto Santo (other ports of Madeira) with 3,676 entries. The 2.3. Data analysis highest number of records (1,491 entries, 3.46%) was observed in the year 1937 whilst the lowest number of entries occurred in To reduce the complexity of the dataset by grouping samples a 1942, with only 192 ships (0.44%). In a period of approximately Hierarchical Cluster Analysis was employed (Clarke and Warwick, 30 years (1940 to 1970) the number of entries was relatively 2001). This type of procedure is adequate to define groups ac- even, starting to grow around. cording to their degree of similarity (Clarke and Warwick, 2001). In what refers to ship types (Fig. 2), passenger’s ships were To determine identical periods in terms of origin, the analyses the most recorded for the duration of the study period, most included ‘origin port’ as a variable and the different years of likely due to the 14-year period with only passenger ship records arrival as samples, for each port entry. The ‘origin ports’ were between 1960 and 1973. During 1936 and 1939 these ships grouped into countries and/or regions in case of an island or recorded more than 500 entries per year. Throughout the 1940’s, archipelago (i.e. Canary Islands). Untransformed data and Eu- ship entries started to decrease, reaching a higher peak again clidean distance as similarity matrix were used in this analysis. in the early 1970’s. After this period, the respective numbers of The slicing in the Cluster Analysis was predefined by the PRIMER passenger’s ships dropped again and became more stable with v6 software (50% of the Euclidean distance). To test if the de- 150 to 200 entries per year. General cargo ships were the second fined periods in the previous analysis were statistically different ship type most observed. Most of these records were observed a Permutational Analysis of Variance (PERMANOVA) (Anderson, during the 1980s and 1990s, but with solid numbers also in the 2005) was performed. The main test and pair-wise comparisons 1930s and late 1940s. In the period between 1960 and 1974 were conducted with unrestricted permutations of raw data. A data did not account for this ship type as previously explained. SIMPER analysis (Clarke and Warwick, 2001) was also performed Ro-Ro carriers, Reefers, Tankers and Containers ships started to to identify which ‘origin ports’ most contributed for the similarity arrive later, most of them after 1974 (again, note that from 1960 of each established period. The ship’s average GT and average to 1974, only passenger ship data was available, and therefore residence time (in days) were calculated by period and ship type, entries of these ship types might have begun earlier). to assess if these characteristics changed over time and per ship Hierarchical Cluster analyses (Fig. 3) revealed the formation of type. five different periods according to the origin port of the different In addition, for each NIS the year of detection in the region and ships: Period A: 1936–1939; Period B: 1940–1973; Period C: the origin distribution was assigned using the 18 large-scale IUCN 1974–1989; Period D: 1990–1996: Period E: 1997–2004. PER- marine bioregions as defined by Kelleher et al. (1995) and later MANOVA confirmed that these five periods formed in the Cluster N. Castro, P. Ramalhosa, J. Jiménez et al. / Regional Studies in Marine Science 37 (2020) 101333 5

Table 1 Results of PERMANOVA test conducted to determine significant differences considering the periods formed in the Cluster, ‘‘Period’’ (5 levels, fixed) (1936–2004). Results of the PERMANOVA pairwise tests for the factor ‘‘Period’’ are also indicated. Bold values highlight significant effects (p < 0.05). Source of variation Degrees of freedom Sum of squares Mean squares Pseudo-F P (perms) Unique perms Period 4 1.6185E6 4.0461E5 83.525 0.001 999 Res 52 2.519E5 4844.2 Total 56 1.8704E6 Periods t P(perm) perms P(MC) A, B 7.297 0.001 980 0.001 A, C 6.517 0.001 857 0.001 A, D 6.319 0.005 310 0.001 Pair-wise A, E 10.190 0.006 438 0.001 B, C 7.985 0.001 998 0.001 B, D 9.050 0.001 997 0.001 B, E 14.567 0.001 997 0.001 C, D 5.215 0.001 992 0.001 C, E 11.957 0.001 996 0.001 D, E 4.973 0.002 927 0.001

Fig. 4. Flowmaps identifying which origin ports were more frequent for the ships that reached Funchal Port (Portugal) regarding the studied period (1936-2004). Black dots representing origin ports.

Fig. 5. Ship’s average GT (ton) by period and ship type that arrived at the Funchal Port (Portugal) from 1936 to 2004. analysis were significantly different and corresponding pairwise Islands (Spain) (W Africa bioregion). In Period C, Portugal main- tests showed that all periods were different from each other land, Canary Islands, Great Britain, and Spain (mostly Mediter- (Table 1). In addition, SIMPER analyses and flow maps for all ranean bioregion) were the most relevant origin ports reaching periods revealed that Portuguese mainland was the main origin Funchal. In Periods D and E Portugal mainland, other ports of Madeira (W Africa bioregion), Canary Islands and Spain (mostly of ships that arrived at Funchal in all periods (Table 2 and Fig. 4). Mediterranean bioregion) were the origin ports that contributed For Period A, Portugal mainland (NE Atlantic bioregion), Great the most for these periods. In the latter period the number of trips Britain (NE Atlantic bioregion), Brazil and Argentina (South At- from other ports of Madeira also became more frequent. lantic bioregion) were also major origin ports. The origins that In terms of average gross tonnage (GT), some variation was contributed more for Period B were Portugal mainland, Great observed over time (Fig. 5). In period C, gross tonnage reached Britain, and the Azores (Portugal) (W Africa bioregion) and Canary the lowest GT average and in Period E the opposite trend was 6 N. Castro, P. Ramalhosa, J. Jiménez et al. / Regional Studies in Marine Science 37 (2020) 101333

Table 2 SIMPER analyses performed to identify which origin ports contributed more to characterize each period (A to E) of maritime traffic in the Funchal Port (Portugal). Group A Average similarity: 83.32 Av. Abund Cum.% Portugal (mainland) 274.50 22.81 Great Britain 205.50 40.13 Brazil 131.25 51.18 Argentina 125.75 60.58 Canary Islands 106.75 68.03 South Africa 58.50 72.98 Cape Vert 53.25 77.20 Belgium 43.75 80.20 Group B Average similarity: 64.37 Portugal (mainland) 135.33 43.67 Great Britain 56.83 55.57 Azores 28.46 64.31 Canary Islands 47.04 73.04 Spain 30.25 81.10 Fig. 6. Daily average residence time (days s.d.) of the different ships over the ± Group C Average similarity: 80.73 different periods (n 43,017 s.d.) in Funchal Port (Portugal) from 1936 to = ± Portugal (mainland) 305.93 50.39 2004. Canary Islands 104.07 65.97 Great Britain 50.64 72.67 Spain 42.79 77.86 Azores 32.50 82.73 2004, and our analyses identified five different periods according to the most relevant ports of origin being connected to Funchal. Group D Average similarity: 84.22 The results clearly showed how intense was the evolution of the Portugal (mainland) 363.29 48.30 Madeira Island 155.29 65.61 maritime traffic in Madeira Island over the years (Bernal, 1992). Canary Islands 74.86 74.84 Since ballast water exchanges were implemented globally around Spain 43.57 79.97 the XIX century (Carlton and Geller, 1993), our study provides The Netherlands 31.86 83.61 new qualitative information on large amounts of ballast water Group E Average similarity: 88.73 discharged in Madeira waters. Taking advantage of its geographi- Portugal (mainland) 372.25 36.98 cal location, the port of Funchal has been used as strategic stop by Madeira Island 316.38 68.88 the maritime transport fleet, adding passenger transport, tourism Canary Islands 90.25 76.12 or port of call for emigrants on their way to South America or Africa (Bernal, 1992; Bosa, 2008). Consequently, the maritime traffic in the island has been always strongly conditioned by observed. Regarding average GT by ship type (Fig. 5), there was the fluctuations in the national and international socio-economic evidence of a growing tendency, especially in passenger ships. activities. The ecological implications that maritime traffic re- This ship type was present in all periods (A to E) and reached lated with tourism and trade, and other introduction vectors a maximum in Period E with more than 25,000 GT in average. (e.g. recreational boating and aquaculture), can have on local Reefers, Containers and Tankers appeared in the Period C and marine communities, especially in the context of an offshore is- their average GT built up after that. The minimum value of GT land, seemed overlooked over the years. Mostly because invasion was registered for recreational vessels. ecology is a recent discipline where a significant push in invasion The time that ships stayed at port (or residence time) was ecology publications only started in the 1990’s (Lockwood et al., related with ship type, with recreation vessels staying longer, 2008). In addition, only during the past decade there was an effort in average more than 7 days (Fig. 6). In contrast, all types of to start documenting the identity and the number of introduced Passengers have registered less port residence time (less than species in Madeira Island (Ramalhosa et al., 2017b, 2019; Riera half a day, in average). Whereas the remaining categories stayed et al., 2018; Souto et al., 2018). In this context, the current study around one and half days (Fig. 6). represents a pioneer contribution for the Madeira region by char- The literature survey conducted to obtain a comprehensive NIS acterizing for the first time the maritime traffic and its correlation inventory for Madeira Island between 1936 and 2004 listed 27 with NIS recorded in the island over a significant temporal scale. species (Table 3). The most frequent taxonomic groups amongst After the World War I (WWI, 1914–1918), there was an in- NIS were Gastropoda (7), Algae (4), Tunicata (5), Pisces (5) (Ta- crease in the maritime traffic at Funchal Port, with new compa- ble 3). Moreover, most NIS present at Madeira in that period were nies emerging, most of them related to the tourism sector (Vieira, native in the NE Atlantic, NW Atlantic and W Africa (all with 11%), 2012). According to this trend, the first period (A) identified in Mediterranean (10%) and Wider Caribbean (9%) (Fig. 7). Antarctica the present study (1936–1939) registered the highest number was the only bioregion with no NIS representatives in this list of entries in Funchal Port, mostly associated with passengers’ (Fig. 7). The detection of NIS increased constantly over time ships and cargo ships (general cargo and bulk). The dominant (Fig. 8), starting with a peak in period C (in the 70’s) and with origins were Portugal mainland, UK, and South America (Brazil the remaining species detected in period D and E. Finally, there and Argentina). An intense maritime traffic was also detected was a significant and strong positive correlation (p 0.00052, R2 0.73) between the native range frequency of NIS= and vessels during the time Portugal had its colonies in Africa (Cabo Verde, origins= frequency considering the IUCN bioregions (Fig. 9). Angola, São Tomé and Príncipe and Mozambique) with the cre- ation of the Navigation Colonial Company (Companhia Colonial 4. Discussion de Navegação (CCN)). This company was created to promote the trade and to explore the connections between Portugal mainland In the present study the historical maritime traffic to Funchal and the Portuguese African colonies. During this period, passen- Port in Madeira Island (Portugal) was examined from 1936 to gers and cargo liners, transporting people, cargo and postal mail N. Castro, P. Ramalhosa, J. Jiménez et al. / Regional Studies in Marine Science 37 (2020) 101333 7

Table 3 List of Non-Indigenous Species (NIS) detected between 1936 and 2004 in Madeira Island (Portugal). Species name, year of first detection, correspondent taxa and native distribution based on IUCN Bioregions (Kelleher et al., 1995) are indicated. For assign species native distribution it was used the several research articles and databases (Hewitt and Campbell, 2010; Hewitt et al., 2009, 2012; Froese and Pauly, 2019). Species Taxa Year of detection References Native bioregion (Fig. 7) Caulerpa cylindracea Sonder, 1845 Chlorophyta 2000 Verlaque et al. (2003) 10,11,12,13,18 Asparagopsis taxiformis (Delile) Trevisan de Saint-Léon, 1845 Rhodophyta 1974 Levring (1974) 7,9,10,11,12,13,15,17,18 Grateloupia turuturu Yamada, 1941 Rhodophyta 2002 Ferreira et al. (2012) 16 Melanothamnus sphaerocarpus (Børgesen) Díaz-Tapia & Rhodophyta 2000 Haroun et al. (2002)7 Maggs, 2017 Crambe crambe (Schmidt, 1862) Porifera 2004 Duran et al. (2004) 3,4,5,7,8 Vallicula multiformis Rankin, 1956 Ctenophora 1998 Wirtz (1998)8 Ectopleura crocea (Agassiz, 1862) Cnidaria 1995 Wirtz (1995) 4,7 Macrorhynchia philippina Kirchenpauer, 1872 Cnidaria 1978 Agís et al. (2001) 11,12,14 Pileolaria berkeleyana (Rioja, 1942) Polychaeta 1980 Knight-Jones and Knight-Jones (1980) 14,15,16 Spirorbis (Spirorbis) marioni Caullery & Mesnil, 1897 Polychaeta 1995 Knight-Jones and Knight-Jones (1995) 15,17 Aeolidiella sanguinea (Norman, 1877) Gastropoda 1995 Wirtz (1998)5 Antiopella cristata (Delle Chiaje, 1841) Gastropoda 1995 Wirtz (1998) 3,5 Bedeva paivae (Crosse, 1864) Gastropoda 1994 Houart and Abreu (1994) 18 Caloria elegans (Alder & Hancock, 1845) Gastropoda 1995 Wirtz (1998) 3,5 Hexaplex trunculus (Linnaeus, 1758) Gastropoda 1994 Houart and Abreu (1994)4 Placida dendritica (Alder & Hancock, 1843) Gastropoda 1995 Wirtz (1998) 2,4,5 Tonna pennata (Mörch, 1853) Gastropoda 1998 Wirtz (1998) 4,7,8,9 Botryllus schlosseri (Pallas, 1766) Tunicata 2004 Canning-Clode et al. (2008) 4,6,8,11,17 Clavelina dellavallei (Zirpolo, 1925) Tunicata 1995 Wirtz (1998) 3,5 Clavelina lepadiformis (Müller, 1776) Tunicata 1995 Wirtz (1998) 3,4,6,9 Microcosmus squamiger Michaelsen, 1927 Tunicata 1992 Turon et al. (2007) 11,12,1314 Pycnoclavella taureanensis Brunetti, 1991 Tunicata 1995 Wirtz (1995) 3,5 Abudefduf saxatilis (Linnaeus, 1758) Pisces 2004 Freitas and Araújo (2006) 4,7,8,9 Aluterus scriptus (Osbeck, 1765) Pisces 1970 Freitas and Biscoito (2002) 4,7,8,9,13,14b,16,17 Gnatholepis thompsoni Jordan, 1904 Pisces 2002 Araújo and Freitas (2002) 3,4,7,8,9 Sparus aurata Linnaeus, 1758 Pisces 2000 Alves and Alves (2002) 3,5,8 Vanneaugobius canariensis Van Tassell, Miller & Brito, 1988 Pisces 1996 Wirtz (1998)8 from Europe (mostly UK) to Africa and South America, were also Porto Santo (Madeira) as one of the main ports of origin. In 1995 very important. These shipping lines, making stops at Madeira there was a government contract tender for the route Funchal- and other Atlantic islands, maintained an intense activity until Porto Santo. Firstly, in a more ‘‘experimental’’ way, with the World War II (WW II, 1939–1942). At this time, two navigation use of charted ships, and later with a Ro-Ro ship built for this companies, ‘Union-Castle’ and ‘Elder Dempster’, were particular purpose, the ‘‘Lobo Marinho’’ ship, that entered into service in relevant, each making more than 100 annual trips to Madeira 1996 (Correia, 2003) initiating the route Funchal to Porto Santo each (Vieira, 2012). This high intensity traffic period had a high and vice-versa. Moreover, in these two periods, there was a risk of NIS introduction through hull fouling and ballast water significant increase in the cruise ships routes. In 1995, both the (Flagella et al., 2006; Campbell and Hewitt, 2011; Seebens et al., port authorities of Madeira and the Canary islands have promoted 2013). a cruise zone covering the two archipelagos, with attractive mea- Subsequently, WW II abruptly reduced the maritime traffic sures for the stopovers (Sousa, 2000). The two periods differed entering Madeira (Period B), reaching its lowest number of entries due to more intense maritime traffic between Madeira and Porto (192) in 1942. During this conflict period, it was risky to sail and Santo in recent years (period E) when the demand for this route travel in the Atlantic even for neutral countries. Moreover, certain increased. Once again with high risk of NIS introductions due to companies had their line’s ships requisitioned for service as troop high propagule pressure and consequently in these two periods ships or hospital ships (Gardiner, 1988). After WW II, maritime most species were registered. navigation recovered again reaching the levels of previous times, Our study reveals the massive importance that maritime traffic as the shipping companies (e.g. Union-Castle) started to resume had (and still has) to Madeira over the years where intense traffic their lines (Vieira, 2012). However, a very remarkable fact from periods generated windows of opportunity for marine biological this period (B) was the construction of the Madeira Airport in invasions. In parallel and being maritime traffic a major vector of 1964, which resulted in a decrease in maritime traffic after its NIS introductions, several marine species were likely introduced construction (Vieira, 2012). in Madeira through ballast water and biofouling. Several authors The start of Period C (1974–1989) was characterized by a change in the origin ports that reached Funchal. The Portuguese referred that the modern globalization of maritime trade is play- civil revolution (25th of April 1974) led to the fall of 48 years of an ing a key role in this accelerated spread of species (Hulme, 2016; established dictatorial regime in the country. As a result, Portugal Sardain et al., 2019). More than 3000 species are transported on a has withdrawn from its African colonies, leading some shipping daily basis throughout the world inside ships ballast water tanks companies to change their routes. In addition, in the beginning (Carlton and Geller, 1993). Large quantities of this ballast water of the 1970’s some shipping companies ended (Vieira, 2012). are pumped into ships at different ports of call and are released One example was the British Union-Castle line, which began in in different areas breaking natural barriers among geographically the early 19th century and ran until 1977, a victim of emerging separated areas (Gollasch, 2002; Cabrini et al., 2019), providing competition from jet aircraft, increasing fuel costs and container- connectivity. On the other hand, in the USA alone, 316 coastal ization of cargo (Roussel and Warwick, 2015). During this period, species introductions, 19% to 37%, were related with hull fouling container ships started to dock in Funchal Port, initiating a new transfers (Fofonoff et al., 2003). Prior to 2004, marine invasion modern maritime traffic in Madeira Island and the first records ecology studies in Madeira were almost non-existent, and this of NIS started to emerge. subject only started to get more attention in the last ten years The other two periods (D and E) identified in the present with NIS monitoring surveys in the whole archipelago, which led study represented more contemporary origins and ships, with to several NIS detections (e.g. Wirtz and Canning-Clode, 2009; 8 N. Castro, P. Ramalhosa, J. Jiménez et al. / Regional Studies in Marine Science 37 (2020) 101333

Fig. 7. Frequency of the origin of the Non-Indigenous Species (NIS) detected between 1936 and 2004 in the Madeira Island (Portugal). Native distribution based on IUCN Bioregions (Kelleher et al., 1995) and publications (Hewitt and Campbell, 2010; Hewitt et al., 2009, 2012) and also Froese and Pauly (2019). Note that some species have more than one native origin. (1 — Antarctica; 2 — Artic; 3 — Mediterranean including the Black and Azov sea; 4 — North West Atlantic (including region 19 North America Great Lakes); 5 — North East Atlantic; 6 — Baltic; 7 — Wider Caribbean Sea; 8 — West Africa; 9 — South Atlantic; 10 — Central Indian Ocean; 11 — Arabian Seas; 12 — East Africa; 13 — East Asian Seas; 14a&b — South Pacific including Hawaii; 15 — North East Pacific; 16 — North West Pacific; 17 — South East Pacific; 18 — Australia and New Zealand).

Fig. 8. Number of ship entries and cumulative number of Non-Indigenous Species (NIS) introduced species in Madeira Island (Portugal) from 1936 to 2004.

Canning-Clode et al., 2013; Ramalhosa et al., 2014, 2017a,b, 2019; Ramalhosa and Canning-Clode, 2015; Souto et al., 2015, 2018; Gestoso et al., 2018; Riera et al., 2018; Ferrario et al., 2020). The number of NIS in Madeira has increased, as well the number of ship entries (exception for period 1) and the GT of those ships. In European waters NIS numbers are increasing largely over the last 50 years (Tsiamis et al., 2019). This reflects an increase in propagule pressure, which is recognized as the primary determinant of invasion success (Ojaveer et al., 2014). With the available information, it is not possible to detailed in which period the translocations/introductions have occurred and from where the species arrived. There is an unquantifiable bias associated to the first record date, in which many of the listed species could have arrived much earlier (Chainho et al., 2015). Fig. 9. Spearman correlation test based on the frequency of vessel trips versus One factor that influences NIS distribution per country is the the frequency of native range by IUCN bioregions (Kelleher et al., 1995) of the variability in the monitoring and reporting effort (Katsanevakis Non-indigenous Species (NIS) present in Madeira Island (Portugal) between 1936 and 2004. Correlation between x and y was R 0.73 and p 0.00052. et al., 2013). Additionally, other vectors could account for some = = species presented in the current NIS listings. For example, the Gilt-head seabream (Sparus aurata Linnaeus, 1758) presence in Madeira is likely a consequence of open sea aquaculture escape N. Castro, P. Ramalhosa, J. Jiménez et al. / Regional Studies in Marine Science 37 (2020) 101333 9

(Alves and Alves, 2002), and currently is a common coastal fish CRediT authorship contribution statement in the region (Castro N., personal observation). The occurrence of other species may be due also to floating marine debris/litter Nuno Castro: Conceptualization, Methodology, Formal analy- (Rech et al., 2016; Carlton et al., 2018; Therriault et al., 2018). sis, Investigation, Writing - original draft, Visualization. Patrício In addition, the presence of new species might be related Ramalhosa: Validation, Investigation, Writing - review & editing. with climate change i.e. tropicalization which could promote the Jesús Jiménez: Data curation, Writing - review & editing. José establishment and or arrival of new tropical-affinity species or Lino Costa: Conceptualization, Writing - review & editing, Su- other species of temperate regions (Cuesta et al., 2016). The pervision. Ignacio Gestoso: Conceptualization, Writing - review consequences of these changes in the distribution limits can in & editing, Supervision, Project administration, Funding acquisi- some cases provoke the displacement or substitution of local tem- tion. João Canning-Clode: Conceptualization, Writing - review & perate species by tropical and temperate species (Vergés et al., editing, Supervision, Project administration, Funding acquisition. 2014; Cuesta et al., 2016). Recent work in Madeira recorded a new established crab species (Cronius ruber (Lamarck, 1818)) Declaration of competing interest evidencing that the arrival and establishment of this crab was due to ongoing tropicalization of the region (Schäfer et al., 2019). The authors declare that they have no known competing finan- There is evidence of similar occurrences on other Macaronesia cial interests or personal relationships that could have appeared archipelagos (Afonso et al., 2013; Brito et al., 2014). to influence the work reported in this paper. Although with low numbers in the present study, recreational vessels might also play an important role in NIS introductions by Acknowledgements hull biofouling (Marchini et al., 2015). One aspect of this vector is the high residence time of this type of boats in port (4 days in The authors gratefully thank to Administração dos Portos average for the present study), as some studies evidence that this da Região Autónoma da Madeira, S. A. (APRAM) for providing feature could enhance the invasion risk (Carlton, 1985; Lim et al., the dataset that allowed for this study. We further thank Nuno 2017). Jesus and Clube de Entusiastas de Navios (CEN) for supplying A six-year survey on Quinta do Lorde Marina (also in the some valid information on missing data and thank Filipa Paiva south coast of Madeira Island) demonstrated that the number and Manuel Biscoito for the indispensable help when gathering of NIS detections in the marina was correlated with increasing digital information on maritime traffic books. We thank Mark maritime traffic over the years (Canning-Clode et al., 2013). There Minton, Whitman Miller and Chad Hewitt for their help, in the is a positive and significant association of vessels origins by initial discussions, that resulted in this paper. Nuno Castro was bioregions with native range frequency of the NIS present in funded by a doctoral grant (SFRH/BD/146881/2019) awarded Madeira, until 2004. The most relevant maritime traffic arriving at by Fundação para a Ciência e Tecnologia (FCT). P. Ramalhosa Funchal in the present study period were Portugal, Great Britain was partially funded by the Project Observatório Oceânico da (NE Atlantic) and Canary Islands (W Africa) and mainland Spain Madeira-OOM (M1420-01-0145-FEDER-000001), co-financed by (Mediterranean) that was consistent with the bioregions of the the Madeira Regional Operational Programme (Madeira 14-20), NIS listing. This suggest that most NIS detected in Madeira until under the Portugal 2020 strategy, through the European Regional 2004 most likely came from those regions through maritime Development Fund (ERDF). I. Gestoso was financially supported traffic, likely through hull fouling and/or ballast water. Carlton by a post-doctoral grant in the framework of the 2015 ARDITI (1987) studied the patterns of marine species introduction in the Grant Programme Madeira 14-20 (Project M1420-09-5369-FSE- Pacific Ocean and verified that the maritime traffic, and shellfish 000001). JCC is funded by national funds through FCT – Fundação culture (especially oysters), were the main mechanisms of disper- para a Ciência e a Tecnologia, I.P., under the Scientific Employ- sal. Based on a similar methodology to the one employed in the ment Stimulus - Institutional Call - [CEECINST/00098/2018]. This present study, Carlton (1987) verified that 14 major transoceanic work was partially funded by projects Observatório Oceânica da routes were responsible for species dispersal in the Pacific Ocean. Madeira-OOM (M1420-01-0145-FEDER-000001), MIMAR (MAC/ Structural connectivity refers to physical linkages that could 4.6.d/066) and MIMAR+ (MAC2/4.6.d/249) INTERREG MAC 2014– facilitate movement (Tischendorf and Fahrig, 2000). In this case 2020 Programme. Finally, this study had the support of ‘‘Fundação maritime traffic, by ballast water and hull fouling, provides con- para a Ciência e Tecnologia (FCT)’’, through the strategic project nectivity between locations that otherwise were separated. UIDB/04292/2020 granted to MARE. Species with limited self-dispersal capacity can spread via maritime traffic (Zabin et al., 2014). The identification of ‘‘invasion References corridors’’ (i.e. significant traffic routes) is of major relevance to support the implementation of regulations that aims to improve Afonso, C.M.L., 2011. Non-indigenous Japanese oyster drill Pteropurpura (Ocine- ecosystems conservation (Carlton and Ruiz, 2015), such as the brellus) inornata (Récluz, 1851) (Gastropoda: Muricidae) on the south-west Maritime Strategic Framework Directive (MSFD) and support the coast of Portugal. Aquat. Invasions 6 (SUPPL.1), 85–88. http://dx.doi.org/10. effective control and inspection of ballast water management 3391/ai.2011.6.S1.019. Afonso, P., Porteiro, F.M., Fontes, J., Tempera, F., Morato, T., Cardigos, F., San- (i.e. Port State Control (PSC) developed by IMO). The present study tos, R.S., 2013. New and rare coastal fishes in the Azores islands: occasional details for the first time the maritime traffic arriving in Madeira events or tropicalization process?. J. Fish Biol. 83 (2), 272–294. over almost one century and verified that native regions of NIS Agís, J.A., Ramil, F., Vervoortt, W., 2001. Atlantic Leptolida (Hydrozoa, Cnidaria) of present in Madeira until 2004 were significant correlated with the families Aglaopheniidae, Halopterididae, Kirchenpaueriidae and Plumu- the most relevant maritime traffic routes. However, a continuous lariidae collected during the CANCAP and Mauritania-II expeditions of the National Museum of Natural History, Leiden, the Netherlands. Zool. Verh. update and analysis of the maritime traffic combined with a 333. more accurate determination of the biogeographical origin of Alves, F., Alves, C., 2002. Two new records of Seabreams (Pisces: Sparidae) from the detected NIS (i.e. DNA barcoding and Mitochondrial Gene the Madeira Archipelago. Arquipél. - Life Mar. Sci. 19, 107–111. Sequencing) (Verlaque et al., 2003; Rius et al., 2008; Lacoursière- Anderson, M.J., 2005. PERMANOVA: A FORTRAN Computer Program for Permuta- tional Multivariate Analysis of Variance. Department of Statistics, University Roussel et al., 2016) and predicting models (Seebens et al., 2016) of Auckland, New Zealand. should follow this current baseline study in order to effectively Anderson, M.J., Gorley, R.N., Clarke, K.R., 2008. PERMANOVA+ for PRIMER: Guide monitor and prevent NIS introductions in the region. to Software and Statistical Methods. PRIMER-E, Plymouth, UK. 10 N. Castro, P. Ramalhosa, J. 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