Introduction

Materials and methods

Study Area

The Azores are an oceanic group of islands located in the middle of the North Atlantic Ocean, roughly 1500 km from Europe and 1900 km from America (Fig. 1). The Archipelago is made up of nine islands roughly aligned along 615 km in a WNW-ESE trend, that are divided into three groups according to their geographical position. Although they are in geographical proximity, the Islands present unique features differentiating themselves from each other (Table 1), with different amounts of annual rainfall (Secretaria Regional do Ambiente e do Mar 2011) and distinct geological settings (e.g. Moore 1990, Azevedo and Portugal Ferreira 2006, Cole et al. 2008).

Table 1.

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Island characterisation. [1] Ávila et al. 2016, [2] Secretaria Regional do Ambiente e do Mar 2011, [3] Porteiro 2000, [4] Morton 2014, [5] Cruz and França 2006, [6] Secretaria Regional da Agricultura e Ambiente – Direção Regional do Ambiente 2015, [7] Ramsar 2013, [8] Morton et al. 1997.

Group	Island	Age (Ma)[1]	Area (Km2)[2]	Freshwater lakes (N)[3]	Permanent Streams (N)[6]	Coastal lakes (N)[4, 7, 8]	Thermal waters (N)[5]	Total lake area (km2)[3, 4, 7, 8]	Annual precipitation (mm)[2]
Eastern	São Miguel	4.00	744,6	33	6	-	14	8.34	1027.1
	Santa Maria	6.30	96,9	-	1	-	-	-	775.2
Central	Terceira	0.40	400,3	18	-	3	-	0.36	1125.6
	Pico	0.27	444,8	28	-	-	-	0.16	956.3
	Faial	0.85	173,1	-	-	-	2	-	974.0
	São Jorge	1.32	243,7	-	-	2	-	0.86	1194.3
	Graciosa	0.70	60,7	-	-	-	1	-	918.4
Western	Flores	2.16	141,0	8	2	-	2	0.72	1716.1
	Corvo	1.50	17,1	1	-	-	-	0.24	1144.6

Figure 1.  

Azores Archipelago location with an indication of the most represented aquatic habitats on each island.

The western group includes the Islands of Flores and Corvo, which are amongst the smallest islands of the Archipelago. Corvo and Flores are very rich in aquatic habitats despite their small size due to their higher annual precipitation (Secretaria Regional do Ambiente e do Mar 2011). The central group (Graciosa, Faial, Pico, São Jorge and Terceira Islands) comprise the youngest in the Archipelago (Ávila et al. 2016). The islands in the central group include a high diversity of inland aquatic habitats, including freshwater and saline lakes, streams and thermal waters (Morton et al. 1997, Porteiro 2000, Cruz and França 2006, Morton 2014). The eastern group, Santa Maria and São Miguel, includes the Archipelago’s oldest (Santa Maria) and the largest (São Miguel) islands. São Miguel is the island with most of the lakes and the larger area of water bodies (Porteiro 2000), whereas Santa Maria is the driest island of the Archipelago, with only 775.2 mm mean annual precipitation and no significant inland water habitats (Secretaria Regional do Ambiente e do Mar 2011).

The Azores are particularly rich in freshwater systems, with 88 lakes (Porteiro 2000), nine permanent streams, five saline lakes and several thermal springs (Table 1). Lakes are located between 230 and 1,050 m altitude and, according to Gonçalves 2008, could be classified into two main lake types: shallow lakes, with a maximum depth below five metres; and (ii) deep lakes, with maximum depths, greater than five metres. The insular lotic systems are small, narrow, with steep watersheds and are fed by lakes or springs, most of them having torrential or seasonal flowing regimes (Raposeiro et al. 2013).

Data resources

Analysis

The present work comprises 225 taxa, 179 identified species and 11 only to genus level, distributed by six orders (Chroococcales, Nostocales, Oscillatoriales, Pleurocapsales, Spirulinales and Synechococcales), 30 families and 79 genera (Table 4). Most species belong to the Nostocales (43.0%) and Synechococcales (21.2%) orders. Chroococcales and Oscillatoriales orders contributed almost with the same number of species (17.3% and 16.8%, respectively), despite their different genera contributions.

Table 4.

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Cyanobacteria taxa richness of the Azores Archipelago.

Order	Taxa	Family	Genus	Species		Habitat (by taxa)
				Nº	%	Freshwater	Thermal	Brackish	Marine
Chroococcales	36	5	8	31	17.3	34	2	-	-
Nostocales	95	11	34	77	43.0	85	9	1	4
Oscillatoriales	36	4	14	30	16.8	27	7	2	2
Pleurocapsales	4	1	2	2	1.1	-	-	-	4
Spirulinales	1	1	1	1	0.6	-	-	-	1
Synechococcales	53	8	20	38	21.2	47	5	-	2
Total:	225	30	79	179	100	193	23	3	13

A summary of cyanobacteria species richness found in the Azores and on each of the nine islands in the different types of habitats is given in Table 5. The number of recorded species was highest on São Miguel Island (115) and lowest on Graciosa Island (3). Freshwater systems were the most diverse habitats, comprising 193 taxa (85.7%), followed by thermal, with 23 species (10.2%), marine (13 species, 5.8%) and brackish systems (3 species, 1.3%).

Table 5.

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Cyanobacteria taxa richness in the Azores by island.

	Island	Taxa	Taxonomy				Habitat
			Order	Family	Genus	Species	Freshwater	Thermal	Brackish	Marine
Eastern	São Miguel	151	4	25	59	115	133	20	1	1
	Santa Maria	7	2	5	6	5	5	-	2	-
Central	Terceira	37	4	14	21	31	28	1	2	4
	Pico	43	4	16	27	31	43	-	-	-
	São Jorge	31	5	14	15	28	28	-	-	3
	Graciosa	3	3	3	3	3	3	-	-	-
	Faial	18	5	8	11	15	10	-	-	8
Western	Flores	56	4	18	33	43	56	-	1	-
	Corvo	21	4	11	16	16	20	-	-	1

A positive Pearson correlation coefficient (r = 0.86, n = 9, P = 0.003) was evident between species richness (S) and island area. This correlation is best described by a linear relationship (Fig. 2), where Pico and Flores seem to be outliers. Flores presented higher, while Pico has lower than expected species richness concerning its surface area.

Figure 2.  

Species-area relationship. Regression line indicates a significant linear relationship with P = 0.003 and R² = 0.86 (Pearson correlation). Dashed lines represent 95% interval confidence. COR: Corvo, FAI: Faial, FLO: Flores, GRA: Graciosa, PIC: Pico, SMR: Santa Maria, SJG: São Jorge, SMG: São Miguel, TER: Terceira.

Discussion

The cyanobacteria diversity in the Azores Archipelago is understudied compared to other European regions (Gkelis et al. 2016), despite being one of the best studied archipelagos in the North Atlantic (Cordeiro et al. 2020a). With its first records of cyanobacteria in Furnas, São Miguel Island, under the Challenger expedition, Moseley (1874) identified three genera: Chroococcus Nägeli, 1849, Nostoc Vaucher ex Bornet & Flahault, 1886 and Oscillatoria Vaucher ex Gomont, 1892. After that, as seen in Fig. 3, the contributions of the Cyanobacteria flora were sporadic, but significant, mainly with Bohlin (1901), Cedercreutz (1941), Bourrelly and Manguin (1946) and Johansson (1977). Their contributions were important, but geographically restricted to the larger islands, such as São Miguel and Terceira. From thereon, the number of recorded cyanobacteria species in the Azores has risen throughout the end of the 20^th century and the 21^st century and presently stands at 225 taxa with 179 identified species (Fig. 3). This boost in the 21^st century is mainly due to the implementation of the WFD (e.g. Santos et al. 2005, Santos et al. 2012, Luz et al. 2020) with 39 new described species, which makes 21.8% of the total described species. This programme has helped the continuous study of freshwater cyanobacteria present in the major lakes of the Azores, in Pico, Flores and São Miguel. The works of Luz (2018), Xavier et al. (2018) and Cordeiro et al. (2020b) significantly contributed to the records of cyanobacteria for the Azores, reporting 19 new species, 10.6% of all taxa recorded only through in-vitro cultivation methods. Using a cultivation approach, these studies were able to isolate strains from lakes, terrestrial and thermal habitats, increasing the ability to identify small or rare species normally not detected in regular monitoring works.

Figure 3.  

The number of described species through time from 1874 to 2020. Bars represent the number of species described per year, the line represents the cumulative number of described species.

Freshwater cyanobacteria are the most represented taxa in the Azores records, mainly from lakes. Although this result may reflect the abundance of this type of habitat in the Azores, it may also denote the less effort on diversity studies in other types of habitats. A much lower percentage of cyanobacteria was identified from thermal, marine and brackish habitats (10%, 6% and 1%, respectively), probably due to low sampling efforts. The availability of freshwater habitats in the Azores favours the establishment of incoming cyanobacteria in São Miguel, Flores, Terceira and São Jorge. These Islands have permanent streams, lakes, peat bogs and wetlands, providing highly diverse habitats for incomers, while these are absent in Faial, Graciosa and Santa Maria.

Several islands of the Azores have active volcanoes and present high numbers of fumarolic fields, geysers and hot springs (Cruz and França 2006) creating conditions for the growth of thermophilic cyanobacteria. Nevertheless, the current knowledge about thermal cyanobacteria in the Azores is low with few published works focusing on this habitat (Moseley 1874, Bohlin 1901, Luz 2018, Cordeiro et al. 2020b). The recent works by Luz (2018), with morphological identifications and Cordeiro et al. (2020b), that used both morphological and genetic characters for its identification, contributed to several new cyanobacteria taxa reports for the Azores from thermal habitats in São Miguel.

The cyanobacteria diversity and distribution in lotic systems in the Azores are much less known compared to other sites (Branco et al. 2001, Casamatta and Hašler 2016). Only a few works are available addressing this type of habitat in the Azores, with contributions mainly by Cedercreutz (1941), Bourrelly and Manguin (1946) and Johansson (1977), with no relevant works in the latest years. This is unusual as, in lotic systems, cyanobacteria are easily identified and sometimes even the dominant taxa (Schultz et al. 2013, Casamatta and Hašler 2016).

One of the most accepted explanations for regional biodiversity is the species-area relationship (SAR), according to which the number of species along the spatial scale increases with the area (e.g. Rosenzweig 1995, Drakare et al. 2006). This pattern was thoroughly studied on islands (e.g. Lomolino and Weiser 2001, Whittaker and Fernandez-Palacios 2007, Triantis et al. 2012), where the number of species from different taxonomic groups increases with the increase in island size (Triantis et al. 2012). In our data, a positive relationship between the island area and the number of species was observed (Fig. 3). This increase in cyanobacteria species richness with increasing island area in the Azores is consistent with the work of Borges et al. (2005), for arthropods and bryophytes and Raposeiro et al. (2009) for chironomids with an exception from Flores and Corvo Islands. A possible explanation for these exceptions is the higher percentage that water bodies represent in the total island area (Porteiro 2000) and also the higher precipitation (Secretaria Regional do Ambiente e do Mar 2011, Reichwaldt and Ghadouani 2012, Haakonsson et al. 2017). Compared to Pico Island, the percentage of land covered with water is double in Corvo and almost six times higher in Flores (Porteiro 2000). This suggests that, for cyanobacteria in the Azores, habitat diversity is an important factor in determining the SAR, as shown for other taxonomic groups and islands (Hortal et al. 2009, Chase et al. 2019).

Compared to other North Atlantic islands, the Azores present the highest species richness (Table 6). The overall distribution of species richness in the different cyanobacteria orders on the North Atlantic archipelagos generally follows the same pattern as the total world species, with Nostocales and Oscillatoriales being the richest orders. However, Nostocales represents a much higher contribution to the regional species richness in the Azores and Madeira Archipelagos, which could reflect their longer dispersion capabilities (Ribeiro et al. 2018). Nostocacean cyanobacteria are able to produce akinetes that can resist long periods of unfavourable conditions (Sarma 2012), enabling them to survive during long dispersion routes and colonise remote oceanic archipelagos, such as the Azores and Madeira. The absence of some orders, such as the Chroococcidiopsidales and Thermostichales, in the Azores and the other Macaronesia Archipelagos, suggests that they probably have a more restricted geographic distribution. Although biological, geographical and climatic factors may contribute to cyanobacteria regional species richness (Moreira et al. 2013, Walter et al. 2017, Ribeiro et al. 2018), the differences amongst islands are most probably related to different sampling efforts (Cordeiro et al. 2020b) and, between Azorean Islands, the distribution of planktic cyanobacteria seems to be mainly related to lake typology rather than environmental parameters (Cordeiro et al. 2020c). For instance, the reduced richness of Oscillatoriales in the Azores could be related to their preference for terrestrial and benthic habitats that are less studied in this Archipelago. With the increase in sampling campaigns covering all types of habitats, the reports of new cyanobacteria in the Azores are expected to increase and the representation of the different orders can become similar to the global pattern.

Table 6.

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Cyanobacteria species richness in the Azores compared to world-known species richness (World's order and species number retrieved from Guiry and Guiry (2022); Canary Islands, Madeira and Cuba numbers retrieved from Cordeiro et al. (2020a)).

Order	Azores		Madeira		Canary Islands		Cuba		World
	Nº	%	Nº	%	Nº	%	Nº	%	Nº	%
Chroococcales	31	17.32	2	8.33	4	6.35	28	19.05	649	13.20
Chroococcidiopsidales	0	0	0	0	0	0	2	1.36	37	0.75
Gloeobacterales	0	0	0	0	0	0	0	0	3	0.06
Gloeomargaritales	0	0	0	0	0	0	0	0	1	0.02
Nostocales	77	43.02	11	45.83	20	31.75	44	29.93	1547	31.46
Oscillatoriales	30	16.76	8	33.33	18	28.57	30	20.41	1397	28.41
Pleurocapsales	2	1.12	1	4.17	6	9.52	3	2.04	223	4.53
Spirulinales	1	0.56	0	0	4	6.35	5	3.40	56	1.14
Synechococcales	38	21.23	2	8.33	11	17.46	35	23.81	995	20.23
Thermostichales	0	0	0	0	0	0	0	0	10	0.20
Total:	179		24		63		147		4918

The hereby presented taxonomic list of cyanobacteria in the Azores represents a valuable resource for biodiversity research and awareness of described cyanobacteria tracked through years that, in the future, will allow the identification of possible invader species and studies of the influence of temperature changes in the World. Besides that, knowing the biodiversity of a specific archipelago enriches its value and allows future works in ecology and, in a more practical way, in biotechnology or pharmaceutical if found to be of increased value.

Acknowledgements

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