Studies of Cystoseira assemblages in Northern Atlantic Iberia

García-Fernández, A. & Bárbara, I. 2016. Studies of Cystoseira assemblages in Northern Atlantic Iberia. Anales Jard. Bot. Madrid 73(1): e035. The Iberian Peninsula contains 24 specific and infraespecific taxa of the genus Cystoseira, but only 6 inhabit in Northern Iberia: C. baccata, C. foeniculacea, C. humilis var. myriophylloides, C. nodicaulis, C. tamariscifolia, and C. usneoides. The Cystoseira assemblages exhibit a complex structure and stratification that allows the presence of a large associate biota and a rich epiphytic flora. Although in the Mediterranean Sea several species have been analyzed in depth, the Atlantic ones are less studied. A revision of the literature (1931-2014) and grey information was made to know the diversity of the North Atlantic Iberian Cystoseira assemblages. The community of C. baccata harbors the biggest number of species (215), followed by C. tamariscifolia (162) and C. usneoides (126), whereas the community with fewest species was the C. foeniculacea one (34). More than 70 species were present in the majority of the Cystoseira assemblages. In this article, are revised also environmental issues in the Cystoseira assemblages, as pollution and anthropogenic pressures or disturbances that cause regression in their communities, and effects of biological invasions by non-native species. As a conclusion, it will necessary to study the Cystoseira assemblage in depth, starting by research of C. baccata along Northern Iberia, as it is an exclusive and widely distributed Atlantic species with very scarce information concerning its role in structuring the communities.


DIVERSITY AND DISTRIBUTION OF THE GENUS CYSTOSEIRA
The genus Cystoseira C. Agardh was described in 1820, including 37 species, although its taxonomy and nomenclature has suffered many changes since then, because of variability within the genus occurs not only among species but also among individuals of a single species and, seasonally, within a single individual.Moreover, in some species, no holotype was designated in species description, and lectotypes have yet to be chosen (Furnari & al., 1999).To complete the knowledge of Cystoseira (taxonomy and evolutionary origin), Draisma & al. (2010) made a phylogenetic analysis of the Sargassaceae and found out that Bifurcaria, Cystoseira, Halidrys, and Sargassum (as currently recognized) are polyphyletic and should each be split into two or more genera.The genus Cystoseira was originated in the Thetis Sea during the Mesozoic, afterwards, some species stayed in the Indo-Pacific Ocean and others should have entered into the Mediterranean Sea from the Atlantic Ocean during the Cenozoic, starting a speciation process that continues nowadays (Oliveras Plá & Gómez Garreta, 1989).
According to the literature (Gómez Garreta & al., 2000;Cormaci & al., 2012) Cystoseira species are plants about 1 meter high with a single primary axis or several primary axes in caespitose thalli, attached to the substratum by a conical disc or haptera.Its apex is smooth or spinous and its ramification in branches is abundant, radial or distichous, sometimes with small spine-like or filiform appendages.These branches could exhibit a characteristic greenish-blue iridescence.Some species present conical or ovoid tophules, arranged along the axis or grouped in the apical zone; and aerocysts, isolated or arranged in chains at the apices of the terminal branchlets.Receptacles are developed usually at the upper parts of higher order branchlets, but they are variable in shape, sometimes bifurcate or branched and with spine-like appendages.Conceptacles are generally hermaphrodite, although they can be unisexual at least during some periods of the year.Cryptostomata are present in most species, normally sunk into the branchlets and, only occasionally, pedicellate.
Among the 51 specific and infraespecific taxa of Cystoseira (Guiry & Guiry, 2014;Thibaut & al., 2014), 36 are present in the Mediterranean Sea, and 30 are endemic of this Sea.The Iberian Peninsula contains 24 species (31 taxa, table 1) and 14 taxa are exclusive of the Mediterranean Sea, 1 taxa of the Atlantic Ocean, and 9 taxa are present in both, Mediterranean Sea and Atlantic Ocean.In Northern Iberian coasts (table 2, figs.1-2) inhabit 6 specific and infraespecific taxa: C. baccata, C. foeniculacea, C. humilis var. myriophylloides, C. nodicaulis, C. tamariscifolia, and C. usneoides.The diversity of the genus Cystoseira is relevant and necessary to protect and manage of their populations, but at present, it has been studied unevenly between regions and issues.Thus, although several species in the Mediterranean Sea have been analyzed in depth (morphology, taxonomy, diversity, assemblages, etc.), the Atlantic ones are less studied, especially in Northern Iberian Peninsula.

Taxa
Although there is a basic knowledge on the habitat preferences of Cystoseira species, there are no much studies about the environmental factors affecting their distribution in the Mediterranean.In this way, Sales & Ballesteros (2009) obtained values of 14 environmental parameters in 103 coves surveyed in Menorca Island, which were added sequentially in a model in order to predict Cystoseira assemblages' composition.They detected significant relationships between great part of the factors and Cystoseira spp.composition and abundance, what show a high predictability of Cystoseira distribution departing from environmental variables.
The Atlantic Iberian Cystoseira species typically inhabits in the subtidal forming the canopy of the community, from wave exposed to sheltered areas.Some common subtidal species are C. baccata and C. usneoides, and other such as C. humilis inhabits from upper to middle intertidal rocky pools (Gómez Garreta & al., 2000).In this region, according to Templado & al. (2012) the Cystoseira species play an escort role and they could be dominant when the other species are not present.Below the C. tamariscifolia band there are present other species as C. mauritanica, C. nodicaulis, and, deeper, C. usneoides.In the Cantabrian coasts, there is a characteristic community dominated by Gelidium corneum in exposed rocks, which could be accompanied by C. baccata and other species as Mesophyllum lichenoides, Zanardinia typus, Pterosiphonia complanata, Corallina officinalis, Rhodymenia pseudopalmata, and Cryptopleura ramosa (Gorostiaga & al., 1998;Templado & al., 2012).Bermejo (2014) studied the genetics of C. amentacea, C. tamariscifolia, and C. mediterranea in the south of the Iberian Peninsula and found that individuals previously identified as C. amentacea in Alboran Sea would be closer related to C. tamariscifolia from the Atlantic Ocean than to Mediterranean specimens of C. mediterranea or C. amentacea.Furthermore, the genetic patterns along southern Iberian Peninsula show an important genetic flux between Atlantic and Mediterranean populations in western and central Alboran.Therefore, the results suggest that all specimens of these three species found along Alboran Sea can be considered one specific entity, probably C. tamariscifolia, so the morphological differences observed between C. tamariscifolia and C. amentacea from southern Iberian Peninsula lack a genetic basis.Moreover, Bermejo (2014) results revealed that the highest distances occur between sites instead between groups of populations.The study of the genetic structure of threatened species with reduced dispersion such as C. tamariscifolia, which play an important role in the maintaining of the biodiversity and ecosystem functioning in littoral communities of the Mediterranean and the proximate coast of the Lusitanian provinces, could yield important information to favor the resilience of littoral communities or to develop a suitable restoration.
In the sublittoral seaweed vegetation on the Basque coast (Gorostiaga, 1995;Díez, 1997;Gorostiaga & al., 1998;Díez & al., 1999;Santolaria, 2014), C. baccata is a very common species that inhabits in a wide range of depth, exposure and sedimentation conditions.Gorostiaga (1995) compared the vegetation in the shallow zone of the French Basque coast, which is very similar, although with a greater abundance of Gelidium corneum and C. tamariscifolia.Gorostiaga & al. (1998) explains that, although the macroalgal cover was very homogeneous flostically, Plocamium cartilagineum, Pterosiphonia complanata, Asparagopsis armata, C. baccata, Halopitys incurvus, and Corallina officinalis were the most abundant macrophytes.However, under sedimentation increasing, Gelidium corneum cover decreased while the macrophytes C. baccata and Zanardinia typus become more abundant.The sedimentation was a determining factor in seaweed distribution and the main trends were: (i) the maximum algal cover corresponded to Gelidium corneum beds.At the same time as the sediment increased to moderate levels, the first change detected was the reduction of crustose and epiphytic layers, due to the decrease of Mesophyllum lichenoides, Plocamium cartilagineum, and Dictyota dichotoma.(ii) The most abundant species along the vegetation gradient presented patterns of distribution associated with sedimentation.Pterosiphonia complanata and C. baccata were well adapted to sedimentation, showing an optimum development at moderate to high levels.In habitats highly exposed to wave action without sediment, Pterosiphonia complanata is displaced by Gelidium corneum.In contrast, C. baccata does not tolerate heavy hydrodynamics and only competes with Gelidium corneum in semiexposed conditions.
The species of Cystoseira generally supports a considerable epiphytic flora (Belegratis & al., 1999).The epiphytes in two Mediterranean species (C.compressa and C. spinosa) were studied by Belegratis & al. (1999) by transplanting plants to different sites.Epiphytic seasonality was generally observed in the sites, what suggests the absence of host-specific epiphytes.Moreover, the distinct zonation pattern of epiphytes covering only certain host areas was not observed.Most floristic and vegetation studies carried out on Northwestern Spain list epiphytic species, but these are not used to characterize differences among communities, as there are not much researches focused on the Cystoseira epiphytes.According to Rull Lluch & Gómez Garreta (1989), Morales-Ayala & Viera-Rodríguez (1989), Arrontes (1990), andOtero-Schmitt &Pérez-Cirera (1996), an epiphytic stratification with three strata can be considered: (i) attaching discs, (ii) main axes and branches and (iii) branchlets and phylloids.However, the host plants occur in different vegetation belts and wave exposure and these factors may be more important in characterizing epiphytism on Cystoseira rather than the own structure of the host.In addition, the fall of phylloids and branchlets usually occurs in winter, causing important variations in epiphytic species that can be found in some parts of the hosts, so the perennial axes allow a more stable flora.
Otero-Schmitt & Pérez-Cirera (1996) studied the epiphytism on four species of Cystoseira (C.baccata, C. tamariscifolia, C. humilis var.myriophylloides, and C. usneoides), that develop large and differentiated communities in the Galician coast.According to these authors, the generic specificity is small: of 125 epiphytic species, nearly half where only found on a single Cystoseira species.Rodophyta were the most abundant epiphytic group and Cyanophyta were the scarcest.Most epiphytic species were Ephemerophytes or Hypnophytes (Otero-Schmitt & Pérez-Cirera, 1996).The cover of epiphytic species was maximal on C. tamariscifolia and C. humilis var.myriophylloides, whereas C. usneoides were much lower.The cover in C. baccata was also quite high, but less than in C. tamariscifolia.The greater number of epiphytic species on C. tamariscifolia could be in part explained because of its position in the littoral zone.On the other hand, the mechanical activity of sand grains among the fronds, mainly in winter, results in a lower abundance of epiphytes in C. humilis var.myriophylloides (Otero-Schmitt & Pérez-Cirera, 1996).The presence of epiphytes in C. tamariscifolia is more or less regular, with a higher abundance in spring and summer, except in C. humilis var.myriophylloides.By contrast, C. baccata and C. usneoides presented the lowest variations, probably because of their optimal development in the subtidal, with a maximum in summer and a minimum at the end of autumn (Morales-Ayala & Viera-Rodríguez, 1989;Otero-Schmitt, 1993;Otero-Schmitt & Pérez-Cirera, 1996).

DISTURBANCES IN THE CYSTOSEIRA ASSEMBLAGES
In the literature (Belegratis & al., 1999;Sales & al., 2011;Sales & Ballesteros, 2012;Templado & al., 2012) is reported that assemblages of Cystoseira have regressed considerably during the last decades in several Mediterranean localities, a fact attributed mainly to the negative impact of pollution and other anthropogenic pressures in the most of species of the genus Cystoseira.Moreover, five Cystoseira taxa  convention (2010).Moreover, all the Mediterranean Cystoseira species are under surveillance by international organizations such as the IUCN, the RAC/ASP and MedPan (Thibaut & al., 2014).Monitoring studies generally suggest pollution as the main factor influencing the disappearance of Cystoseira spp., however, there are not much studies providing experimental evidences for the disappearance of Cystoseira species related to pollution.Belegratis & al. (1999) pointed out that one of the most negative effects is the eutrophication, as high nutrient levels trigger growth of epiphytes and phytoplankton, that concurrently inhibiting host growth through shading and, as a consequence, hostepiphyte complexes ultimately decline and are replaced by phytoplankton dominated systems.However, other factors like inorganic chemical pollution increased turbidity levels, overgrazing and climate change could be other possible causes (Sales & Ballesteros, 2009).In addition, their data shows a positive relationship of rich and well developed Cystoseira assemblages to urbanization distance and low levels of nutrient concentration (Sales & Ballesteros, 2009) and the results of the study of Sales & al. (2011) suggest that heavy metal pollution could be negatively affecting survival and growth of Cystoseira species with species-specific responses.In their study, individuals of three Cystoseira species were transplanted from non-polluted to slightly polluted and heavily polluted areas, in places known to have Cystoseira spp.populations before pollution increased one century ago.Effects of pollution were species-specific: negative effects in survival of C. barbata and growth of C. crinita were detected in specimens transplanted to the high polluted area.The pollution could have been the cause that led to the disappearance of Cystoseira species in the past; however, neither survival nor growth of any of the Cystoseira species was negatively affected at the slightly polluted area, and growth was favored for C. barbata (Sales & al., 2011).
Although great efforts are directed in the EU to improve water quality by the implementation of the Water Framework Directive and Cystoseira species are used as indicators of good water quality, no recovery of Cystoseira populations after improvement of water quality has been detected.Therefore, some authors (Belegratis & al., 1999;Sales & al., 2011;Bermejo & al., 2012;Sales & Ballesteros, 2012;Templado & al., 2012) claim for alternative management of measures that facilitates the re-establishment of Cystoseira populations in areas where water quality has improved.In the Balearic Island, Sales & Ballesteros (2007) found nine taxa of Cystoseira, some of them widely distributed around the island but other ones scarcely spread.Although these differences are probably due to physical causes more than pollution or anthropogenic disturbances, as sheltered Cystoseira assemblages are strongly determined by geomorphological features of the coast, Sales & Ballesteros (2007) proposed to used Cystoseira assemblages as ecological indicators in biological monitoring for water quality assessment according to the EEC Water Framework Directive since they are very good indicators.
Because of the sedentary condition of attached microalgae that integrates the effects of long-term exposure to nutrients and/or other pollutants, the use of these benthic organisms as bioindicators to assess pollution values in the marine environment was proved successful in many ecological studies (Gorostiaga & Díez, 1996;Díez & al., 1999;Bermejo & al., 2012;Santolaria, 2014).As macroalgal communities provide habitat and harbor for a wide variety of organisms, changes in these communities will have significant effects on shore ecosystems (Bermejo & al., 2012).Hernández & al. (2011) studied the vegetation in the intertidal zone of the port of Tarifa, (South Iberia).Some of the species were found in the catalogue of endangered species and can be used as bioindicators and should have a special attention, so recently the Cystoseira species have been included in the list of endangered species of the Mediterranean (Hernández & al., 2011).
In Northeastern Atlantic Iberia was detected regression of the Cystoseira assemblages (Gorostiaga & Díez, 1996;Díez, 1997;Díez & al., 2009;Santolaria, 2014) pointed out that, the Cystoseira species are sensitive to contamination, as C. baccata and C. tamariscifolia were not present in polluted areas.Gorostiaga & Díez (1996) found that in these unstable environments the community responds by simplifying its structure: reducing the number of layers, reducing vegetal cover and allowing a proliferation of opportunistic species with simple morphology, especially ceramiaceous algae.There is also proliferation of sciaphilous and sedimentation-resistant species.The crustose layer, made up of species having these characteristics, shows strong development in polluted environments.Díez & al. (2009) found that only the most degraded assemblages experienced a significant increase in algal cover, revealing that this structural community parameter is not relevant in distinguishing between moderately degraded and unaltered vegetation.These results suggest that a significant reduction in algal cover takes place when a threshold of pollution intensity is exceeded.Likewise, the degree of water motion, depth, salinity and the nature of the pollution discharged seem to play major roles in algal cover response.The conclusion of this study is that following pollution abatement there was a partial recovery of intertidal phytobenthic assemblages.Intertidal vegetation at the degraded sites has become progressively more similar to that of the reference site, characterizing five succession stages.The Cystoseira species only appears in the last recovery stages, the reference stage, so the first sign of degradation of natural communities is the loss of large perennial macrophytes as Cystoseira.In this way, Santolaria (2014) pointed out that where the contamination were worse, the macrophytes as Cystoseira spp.were absent and replaced by caespitose algae as Gelidium pusillum and Caulacanthus ustulatus; however, with the progressive recovery of the water quality, the Cystoseira species appear again, so it would indicate the full biological recuperation of the station.
The biological invasions is another disturbance in the Cystoseira assemblages, as in marine ecosystems they have been increasing all around the world, mainly due to human activities such as international shipping, aquaculture and aquarium activity.The brown macroalgae Sargassum muticum, native to East Asia, is considered an invasive species around the world, being distributed mainly in sheltered or semi-exposed rocky shores, and regularly invades the habitats of algal species from the genus Cystoseira (Vaz-Pinto & al., 2014).Previous studies (Sánchez & Fernández, 2005;Olabarria & al., 2009) showed the impact of the invasive Sargassum muticum on native assemblages, with a limited impact on native assemblages in northern Spain.Native species of Cystoseira can be displaced by Sargassum muticum (Critchley & al., 1986;Viejo, 1997;Engelen & Santos, 2009) and it causes changes in the structure of the native communities (Britton-Simmons, 2014).This could be explained because, although Sargassum muticum has a small basal disc, its bigger branches outshine the basal strata and compete for light and nutrients (Critchley & al., 1986;Viejo, 1997;Britton-Simmons, 2004;Sánchez & Fernández, 2005).Furthermore, the normal growth of Sargassum results in higher growth rates during shorter periods of time than those of Cystoseira (Rico & Fernández, 1997) and the productivity is higher than in native species as C. baccata or Saccorhiza polyschides (Fernández & al., 1990).In southwestern Portugal, Engel & Santos (2009) found out that the progression of the Sargassum muticum invasion modulates the environment to its own requirements and the combination of K-selected traits and an increase in population growth rate when Sargassum muticum became more dominant suggested that competition with the native species C. humilis was an important biotic filter for the establishment phase of Sargassum muticum invasion.However, Arenas & al. (1995) suggested that reproductive investment was higher in C. nodicaulis, so the successful colonization of Sargassum muticum in northern Spain shores is likely to be due to the large production of embryos.In addition, Vaz-Pinto & al. (2014) suggested a better nutritional strategy of C. humilis than Sargassum muticum to cope with limiting nutrient conditions of intertidal rocky pools, contrary to the expectations.In conclusion, Sargassum muticum has little effect in the native communities that are poorly invaded (Viejo, 1997;Sánchez & Fernández, 2005) but exhibits an important effect under high density and size of the nonnative species (Britton-Simmons, 2004).
Undaria pinnatifida, another non-native species, quickly colonizes the substrata and in some geographic areas is the dominant species, triggering decreasing in abundance of the native species.It is an opportunistic species with a high capacity to colonize new substrata, but, as it appears in empty spaces, it is not very competitive in natural and stable conditions (Eno & al., 1997).In Galicia it appears in the C. baccata assemblage, having not important impact in the community (Cremades & al., 2006).
The non-native species Codium fragile is affects the native species as Codium tomentosum because it is very competitive and aggressive.An empty space in the substrata due to exploitation or the damage of the habitats, make easier that Codium fragile colonizes the substrata, making changes in the benthic communities and affecting the sedimentation process (Harris & Tyrrel, 2001;Levin & al., 2002).

FUTURE RESEARCHES FOR THE CYSTOSEIRA ASSEMBLAGES IN THE NORTH ATLANTIC IBERIA
Taking into account that there is not much known about Cystoseira communities in the Atlantic Iberian coast, especially in the North coasts, it will be necessary to study their assemblages in depth concerning the habitat, the structure, the diversity, the seasonally changes, disturbing effects, nonnative and invasive species, long term changes, protected areas, etc.At the present, the more urgent study will be making an extensive research about C. baccata in Northern Iberia, as it is an exclusive Atlantic species that is widely distributed along the coast it is very little known about how its communities work, although it plays a key role structuring the communities.Furthermore, it is accompanied by the highest number of species and it has the highest number of epiphytes.In addition, C. baccata inhabits together with other four Cystoseira species so while studying the C. baccata communities we will obtain information of more species of Cystoseira.The necessity of making a study the Cystoseira communities in the North Atlantic Iberian coasts could be noticed reading Templado & al. (2012), since they stablish that, in general, the Cystoseira species play an accompanied role, while in the literature the Cystoseira assemblages exhibit an important role in the North Atlantic Iberian coasts communities, more than only escort species.What is more, Templado & al. (2012) only mentioned C. baccata in a sole paragraph as a species that sometimes appear in the Gelidium corneum communities.However, C. baccata is one of the most important species and widely distributed one in the North Atlantic Iberian coasts, developing their own communities, which have the highest diversity in the Cystoseira communities in these coasts.In addition, there are a several biological invasions that disturb the habitat by occupying the substrata and shading the Cystoseira canopy (Arenas & al., 1995;Sánchez & Fernández, 2005), so it is importante to know the distribution of non-native species and their impacts, especially in Galicia as some rías are important hotspot of introduced marine species (Bárbara & al., 2008).

Fig. 2 .
Fig. 2. Northern Atlantic Iberian species of Cystoseira: a, C. nodicaulis with Sargassum muticum in sand covered subtidal rocks; b, c, detail of C. nodicaulis with aerocysts (b) and basal tophules (c); d, shallow subtidal assemblage of C. tamariscifolia with C. baccata; e, detail of C. tamariscifolia and its aerocysts; f, g, lower intertidal community of C. tamariscifolia; h, subtidal community of C. usneoides; i, j, detail of C. usneoides with tophules (i) and chains of small aerocysts (j); k, big subtidal thallus of C. usneoides.
(C. amentacea, C. mediterranea, C. sedoides, C. spinosa, and C. zosteroides) are currently listed as species strictly protected under the Berne Convention (Annex I, 1979) and all the Mediterranean species of the genus Cystoseira, except C. compressa, have been listed under Annex II of the Barcelona

Table 2 .
North Atlantic Iberian species of Cystoseira and their features ).

Table 3 .
Associate flora of Cystoseira assemblages in Northern Atlantic Iberian Peninsula

Table 4 .
Summary of the associate flora of Cystoseira assemblages in the Northern Atlantic Iberian Peninsula. C.

baccata C. foeniculacea C. humilis var. myriophylloides C. nodicaulis C. tamariscifolia C. usneoides
The number of exclusive species by Cystoseira assemblages varies between communities.Neither species were exclusive of the C. foeniculacea and the C. nodicaulis communities, whereas the C. humilis var.myriophylloides and the C. tamariscifolia communities exhibit Amphiroa vanbosseae and Jania longifurca as typical species, respectively.The C. usneoides community contained two species (Erythroglossum laciniatum and Brongniartella byssoides) not present in other Cystoseira assemblages.Cystoseira baccata community comprises great number of species (Table3) that are absent or scarce in other Cystoseira assemblages, such as Phyllariopsis brevipes subsp.