Non-indigenous marine species of the Azores

Abstract

Marine benthic species introduced to the Azores are collated from scientific publications, internal reports and own data. Twelve algae and 21 invertebrates are classified as non-indigenous species, 18 as cryptogenic. Two species of algae and two ascidians are regarded as particularly invasive along the shores of this oceanic archipelago.

Introduction

As volcanic islands located close to the Mid-Atlantic Ridge (França et al. 2003), the Azores are geologically recent and separated from the nearest continental coasts by at least 1,300 km (Morton et al. 1998). Natural colonization for marine organisms occurs mainly through oceanic currents. At present, the prevailing sea-surface pathway to the Azores is a descending branch from the Gulf Stream running from NW towards SE (Santos et al. 1995). Nevertheless, the major affinities of the autochthonous marine flora and fauna are with the continental coasts of Europe and Africa, the Mediterranean Sea and the other Macaronesian archipelagos of Madeira and Canary islands (Santos et al. 1995; Tittley and Neto 1995; Ávila 2000, 2005). Birds can also be vectors of introductions. This may be the case of the caenogastropod Assiminea sp. found at Praia da Vitória (Ávila 2005). Factors conditioning the natural and human-mediated marine colonization of the Azores are discussed by Cornelius (1992) and Morton and Britton (2000). Besides natural pathways, various anthropogenic factors presently concur as additional vectors of entrance for marine species in areas outside their natural biogeographic range (Bax et al. 2003). Of these, hull fouling, ballast water, solid ballast, recreational boating and dive practices, fisheries and aquaria trade may be relevant for the Azores.

Little is known on marine species introductions and invasions to the Azores. However, the potential for introductions is high, considering that the transatlantic leisure boat-traffic stopping over at the islands has significantly increased over the last decade. Scattered literature (Monniot 1971; Monniot C 1974; Monniot F 1974; Cornelius 1992; Wirtz and Martins 1993; Tittley and Neto 1994, 1995; Neto 1997; Morton et al. 1998; Southward 1998; Ávila 2000, 2005; Morton and Britton 2000) together report 51 taxa as exotic marine species for the coastal areas in this NE Atlantic archipelago. The aim of this paper is to provide a commented list of these species, to delete misidentifications, to add new records and to indicate the invasive status.

Methods

A literature review and a database query were conducted. The “DOP Database” is a computerized species list, which compiles information from 575 SCUBA dives carried out to study assemblages of conspicuous species in the Azores archipelago. During these surveys, species that could not be identified in situ were collected and preserved for later identification. Samples of new records were stored in the Department of Oceanography and Fisheries of the University of the Azores (DOP). The marine mollusc database [Department of Biology of the University of the Azores (DBUA)] of one of the authors (S. Ávila) is also included. The DBUA database contains information on geographic distribution, mode of development and other pertinent details of the shallow (<50 m) marine molluscs of the Azores. The data are based on 880 samples collected in about 660 dives around all of the islands of the Azores. Species with disjunct geographic distributions (e.g., Azores and Mediterranean) as well as those commonly found nearby harbours were studied in detail in order to assess whether their occurrence was natural or human mediated. Planktonic organisms have not been considered.

In the present paper, criteria given by Boudouresque and Verlaque (2002) to consider a species as “introduced” are applied: (1) it colonizes a new area where it was not recorded previously; (2) the extension of its range is linked, directly or indirectly, to human activity; (3) widely disjunct dispersion; (4) new generations of non-native species are produced in situ without human assistance, thus constituting self-sustaining populations. To decide upon the introduction to the Azores, we adapted these criteria: (1) the species is new to the Azores; (2) occurrence in the Azores constitutes a geographic discontinuity to the species’ known range; (3) a new occurrence is at first very localized and (4) further spread within the archipelago follows a consistent pattern; (5) the species has established a persisting population. If according to these criteria there are doubts about the introduction status, populations are classified as cryptogenic (sensu Carlton 1996).

Results

Fifty-five taxa have been pointed as introduced in the Azores (Table 1). Eighteen are now classified as cryptogenic and 33 as established introduced species. Two taxa are rejected: the gastropod Engina turbinella and the crab Carcinus maenas previous records for the Azores are most likely misidentifications. The hydrozoan Ventromma halecioides may not yet be established. Pollia dorbigny is mentioned as an introduced species for the first time. Caulerpa webbiana (introduced) and Bugula cf. dentata (cryptogenic) are mentioned for the first time for the Azores archipelago.

Table 1 Species, which have been reported as introduced to the Azores. Names of species accepted as established non-indigenous taxa are presented in bold

Algae

Asparagopsis armata is a well-known invasive species that has its origin in the southern hemisphere and was first recorded in the northern hemisphere in 1923 (summarized in Verlaque et al. 2004). This species is widely spread throughout the Azores, in rocky habitats between 0 and 20 m (DOP Database), displaying a biomass maximum during spring (Neto 1997). Asparagopsis taxiformis is cosmopolitan in warm-temperate to tropical waters (Chualain et al. 2004) and was first recorded for the Azores as A. delilei by Schmidt (1931). It was not recorded in the Faial (Tittley and Neto 1994) and Flores islands 1989 expeditions (Neto and Baldwin 1990), Flores 1994/1995 expeditions (Tittley et al. 1998) and Santa Maria 1990 expedition (Neto et al. 1990), where it occurs nowadays. It presently occurs in Santa Maria, São Miguel, Faial, Pico, Flores, and Graciosa islands (DOP Database) and probably São Jorge due to proximity to Pico and Faial. It occupies a depth stratum similar to A. armata and co-occurs with the latter but its niche seems to extend to more sheltered places. According to Tittley and Neto (2005) A. taxiformis is now less common in São Miguel island possibly due to competition with A. armata. Contrastingly, unsystematic observations around Faial and Pico seem to show an expansion of the distribution and an increase in the abundance over the last decade. This variation in abundance needs further explanation.

Caulerpa webbiana is an invasive species recently collected in Horta harbour. It has colonized several sites around Horta harbour after its first record in 2002.

Codium fragiletomentosoides is a potentially invasive species for the Azores. It was first recorded by Neto (1997) for São Miguel island and then for Corvo island. Despite its capacity for spreading and replacing the indigenous species elsewhere (Nyberg and Wallentinus 2004), this has not yet been observed in the Azores.

Ascidiacea

Clavelina oblonga is more widespread in Faial and Pico islands (DOP Database) than C. lepadiformis, but the occurrence of the former is so far limited to those two islands. It covers large areas with hundreds of individuals per m², especially at vertical and slightly overhanging surfaces. Due to limited distance (in the order of a few tens of km) separating the three islands of the “Triangle” and the frequent boat traffic among them, there is a possibility that it may occur at São Jorge as well but no surveys have been done there recently.

Distaplia corolla is invasive in the Azores and is recorded for all the islands, although its abundance is low at Corvo, Flores and Santa Maria islands (DOP Database). The species was probably introduced by sailing yachts (Monniot and Monniot 1983) travelling from the Antilles. It occurs both on well-lit and shaded areas down to 35 m.

Discussion

The low number of introduced species compared to other areas (e.g., Coles et al. 1999) is probably a consequence of the geographic isolation of the Azores, comparatively low commercial shipping, scarcity of shallow lagoons and absence of marine aquaculture and of estuarine habitats. The low number of scientific studies on the biogeography of Azorean marine species may have also affected the results. As for Bugula cf. dentata and Cinachyrella cf. alloclada, the identification of species is doubtful due to the lack of taxonomic expertise. Molecular work should be conducted in order to clarify the origin of several species (e.g., Sabella spallanzanii in Morton and Britton 2000).

The genus Caulerpa, mentioned by Lowe et al. (2000) as a particularly invasive taxon, is present in the Azores. Several healthy mats of C. webbiana have now been identified outside Horta harbour and deserve special attention in future studies.

The bivalve Mytilus edulis has been occasionally reported for the Azores. Ávila et al. (1998) reported small populations inside the harbour of Ponta Delgada (São Miguel island) but recent surveys did not find live specimens (Ávila 2005). Transient mussels were also found in Santo Cristo Lagoon, São Jorge island (Morton et al. 1998). This species arrives at the Azores with floating objects (e.g., adrift floats with ropes hanging on the water column). Shells found inside harbours may have been discarded after meals. No self-sustaining populations have ever been recorded and this species is not considered to have established.

Several species in the northern hemisphere display a northward expansion of their distribution area due to the increase of water temperature (Elliot 2003; Perry et al. 2005). For the Azores, this seems to be the case for the fish species Canthigaster capistrata according to Wirtz (2005). Scorpaena canariensis is a rare species in the Azores and Wirtz (2005) admits this as a possible case of a northward expansion. As no direct human vector seems to be applicable to these species, they were not considered as introduced.

Other coastal fish species, such as Chaetodon sedentarius, Aluterus monoceros, Fistularia petimba (Santos et al. 1997; Wirtz 2005; Afonso et al. unpublished data) and Mycteroperca phenax (Morato et al. 2004) occur occasionally in the Azores but no stable populations seem to have established. Apparently, the same is applicable to the hydroid V. halecioides which was recorded only once in the Azores, in Horta’s marina at the island of Faial (Cornelius 1992). In this particular case, more surveying should be carried out.