Fish diversity of a southwestern Atlantic coastal island : aspects of distribution and conservation in a marine zoogeographical boundary

Despite the increase of knowledge about the southwestern Atlantic ichthyofauna, there is still a lack of information along extensive marine areas. The Espírito Santo state (ES) coast, considered a zoogeographic boundary and a transitional zone between tropical and subtropical realms, is still largely unknown. Here is provided a checklist containing 221 fish species at Franceses Island (south coast of ES), which was attained with data from 2000 to 2010 by means of underwater observations, specimen collections and fisheries monitoring. Abundance, habitats and threat risks of each species are shown and discussed. The number of reef fish species found at Franceses Island corresponds approximately to 35% of all fishes present in the Brazilian Province. The conservation of the Franceses Island and surrounding areas would protect a mosaic of environments that can support a high diversity of fish species.


INTRODUCTION
Although studies on the Caribbean reef fish fauna began in the 1950s (Hixon 2011), the ichthyofauna of southwestern Atlantic reefs remained largely unknown until the beginning of the 1990s.However, since then, the use of SCUBA for research has contributed for a huge amount of information about Brazilian reef fishes, mainly in respect to taxonomy, community structure, ecology, biogeography and phylogenetics (e.g., Floeter et al. 2001;Joyeux et al. 2001).
Sheltering a large proportion of endemic species (10 %; Floeter et al. 2008), Brazilian reefs constitute a distinct zoogeographic province (Floeter and Gasparini 2000;Floeter et al. 2008) separated of the others by semi-permeable biogeographic filters (Rocha 2003;Luiz et al. 2012).This singularity, associated with the relatively small area that the Brazilian reef environments represent in the Atlantic, turns it as a priority area for studies and conservation programs (Moura 2000).
During the last decade, the number of studies about reef fishes in Brazilian waters extensively increased.Many studies aimed to understand the relationship of community dynamics for distinct environmental factors (Ferreira et al. 2001;Floeter et al. 2007), fishing effects (Floeter et al. 2006) and management rules (Francini-Filho andMoura 2008a, 2008b).Ecological analysis (Sazima et al. 2000;Bonaldo et al. 2006;Ferreira and Gonçalves 2006;Francini-Filho and Sazima 2008;Francini-Filho et al. 2010) and behavioral patterns (Gibran 2002;Sazima 2002;Sazima et al. 2003;Gibran 2004) were also largely performed in different sites of the Brazilian shore.However, regardless the increase in research, an enormous part of the reef environments of Brazil are still lacking basic knowledge (Mendonça-Neto et al. 2008) and protection (Floeter et al. 2006), suffering impacts from population growth, industrial development, fishing activities and inordinate tourism.
In this context, the Espírito Santo state, a faunal biogeographical marine boundary zone situated in the central Brazilian coast (Floeter et al. 2001;Martins et al. 2007), until recently had received few attention by marine researchers and conservation initiatives.Consequently, most coastal reef environments of the state became highly overfished without a basic preterit Pinheiro et al. | Fish diversity in a marine zoogeographical boundary 20°55′ S, 040°45′ W), a coastal island located in Espírito Santo southern coast.The island, formed by a crystalline base, is situated 4 km from the coastline.It has an area of 0.135 km² and perimeter of 1,700 m, where its largest axis (500 m of length) is disposed parallel to coastline.The rocky shore has a strong difference in declivity and horizontal extension among its sides.In the western side, sheltered from winds and waves, the rocky shore is narrow and highly abrupt, arising 5 m from its deepest part.In this side the interface is composed of sand and mud.The seascape of the area between the isle and the continent is very shallow (<4 m), and is formed by a mosaic of sand bottoms, macro-algae beds and biogenic reefs and patch-reefs.
In the eastern side, facing the open ocean, the rocky shore is broader and deeper (ca.120 m and 12 m deep).The interface is constituted by rhodoliths, gravels, bioclastic material and sand.There are also patch reefs few meters from interface of this side.The infralittoral of the island shows an enormous variation of structural complexity due to the presence of big boulders and holes.The isle also has exposed and submersed reefs in northeast face.
knowledge about its fauna (Pinheiro et al. 2010a).Thus, this study contribute with information about reef fishes of a poorly studied area of the central coast of Brazil, analyzing the composition and distribution of fish species that occur in and surrounding Franceses Island´s reefs.Moreover, this is regionally a priority area for a MPA creation and this research raises important data and discussion to contribute for this process.

MATERIAL AND METHODS
The Espírito Santo state (18°22′ S -21°19′ S), central coast of Brazil, is located in a transitional tropicalsubtropical area, where tropical oligotrophic waters of Brazilian current coming from the north predominate, but also with the occurrence of a seasonal coastal upwelling from the south (Schmid et al. 1995).Additionally, the state lies in a boundary area between coral reef ecosystems in the north (00°52′ N -19° S) and rocky reefs ecosystems in the south (19° S -28° S) (Floeter et al. 2001).The climate is inter-tropical, with intensive and prolonged rains in summer and dry weather in winter.Predominant winds are from the east and northeast.However, south and southeast winds occur predominantly in the winter (Nimer 1989).
This study was conducted on the rocky shores, reefs and surrounding habitats of Franceses Island (Figure 1; Turf algae and soft bottom have the highest cover, followed by red algae, brown algae, sponges, briozoans, gorgonians and zoanthids.However, the benthonic cover shows a significant change between sheltered and highly exposed zones.Costa (2009) stated that corals, zoanthids and urchins have the highest cover in sheltered zones, while gorgonians, hydrozoans and macroalgae preferred the higher exposure face.
Additionally, Franceses Island is influenced by two hydrographic basins: Benevente (Anchieta) and Itapemirim rivers (between Marataízes and Itapemirim).These rivers, in raining periods or strong winter winds, contribute to promote turbidity and suspension of particulate material in the island surrounding waters.In the southwest of the island, in a bottom composed of sand, gravel (rhodolith and bioclastic material) and mud, fishermen practice trawl fishing for shrimps (Pinheiro and Martins 2009).The ichthyofauna of this environment was sampled between 2003 and 2004 (see details in Pinheiro et al. 2009a).In the present work this environment is called the soft bottom adjacent to the island (SBA).
Moreover, Franceses Island is situated in an area proposed for creating a MPA.The Brazilian government considers this region as a biological highly important area with an extremely high priority for action (studies and management) (MMA 2007).
The Franceses Island fish checklist results from underwater observations, photographic records and voucher specimens obtained between 2000 and 2010, where about 70 expeditions and 200 days in the field were conducted.Fishing activities were monitored from 2003 to 2006, when bottom trawls (12 embarkments; 30 hours of trawl), seine trawls (15 trawls) and recreational activities (75 fishermen) were studied, and the species caught identified.Recreational activities constituted angling and spearfishing, and both occur in all surrounding island (for details see Pinheiro et al. 2010a), catching specimens in the rocky reefs (RR), interface (IF) and water column (WC) habitats.The bottom trawl was performed by local boats of the shrimp fishery fleet in a fishing ground located between 500 and 1500 m southwest of the island (for details see Pinheiro et al. 2009a andPinheiro andMartins 2009) in the habitat denominated SBA.The seine trawls were performed from the island and had as target schools of seasonal fishes.The nets used were nearly 400 m long and 5 m high, seining and catching every fish that occurred in the sheltered zone of the island, involving IF, WC and soft bottom of the island (SBI) habitats.Other professional fishing activities, such as gill nets and trolling, were not evaluated.
Families and genera within families are listed in alphabetical order.Some recent taxonomic revisions were adopted, i.e., Epinephelidae separated from Serranidae and Scarinae subsumed in Labridae (Westneat and Alfaro 2005;Craig et al. 2011).Thus, the checklist contains the following information of each species (modified from Luiz et al. 2008): Abundance: an indicator of the relative abundance based in the several observations realized in each distinct habitat described above; where: AB = abundant (several sightings of many individuals -at least 50 -are expected at nearly every dive or fishing catch), VC = very common (several sightings are expected, but not necessarily of many individuals), CO = common (sights are frequent, but not necessarily expected on every dive or fishing activity monitored), OC = occasional (sightings are not unusual, but are not expected on a regular basis), UN = unusual (sights occurs less than occasionally), and RA = rare (sighted on reefs or in the fishing activities only one time).
Habitat: a particular place where a species lives and was sighted.The habitats were defined by physiographic features as substrate type and depth, of which: RR=rocky reefs (shallow and mid-depth areas of the shores and reefs; ranging from 0 to 12 m deep), IF=interface (interface between reef and adjacent soft bottom; 3 to 12 m deep); SBI=soft bottom of the island (consists mainly of sand, mud or bioclastic material near of the isle, although rhodolith patches are also found; < 100 m from the rocky shore or reefs); WC=water column (pelagic environment of the island from 0 to 8 m of depth); SBA=soft bottom adjacent to the island (composed by sand, mud and gravel ground from the surroundings of the isle to 1.5 km away; 4 to 6 m of depth).
Threat: species registered in fishing activities or in red lists of endangered species: PF=species caught by professional fishing activities monitored; RF=species caught by recreational fishing activities monitored; EN=species considered endangered (at risk of extinction, present in the Brazilian list of endangered species; MMA 2014); RO=species considered at risk of over-exploitation (present in the Brazilian list of over-exploited species; IBAMA 2003a, 2003b); IU= species evaluated and considered threatened by the IUCN red list (Critically Endangered, Endangered or Vulnerable); DD=data deficient by IUCN evaluation; NR= species not at risk (those not considered to be threatened by red lists and weren't caught by any fishing activity).
Record type: how the species was registered, where: COL=collected, MUS=museum voucher, LIT=literature, PHO=photograph/video and SIG=sighting.For specimens deposited in museum collections, the institution and voucher number are provided in the Appendix 1.
A cluster analysis of the habitat-types based on a species presence/absence matrix was performed.The Bray-Curtis similarity index was used, and habitats were clustered according to the UPGMA method (Pielou 1984).SIMPROF analysis was performed in order to test for multivariate structure within the data.Cluster and SIMPROF analysis were made in the software PRIMER v6 (Clarke and Gorley 2006).

RESULTS
A total of 221 species was recorded at Franceses Island and adjacent habitats (Table 1).One hundred sixty-four species (74%) were registered by underwater observations, 77 (35%) being recorded exclusively by this method.On the other hand, 145 species (65%) were registered by fishing activities, 57 (26%) being exclusive by this method.
The richest family was Sciaenidae, with 18 species, followed by Carangidae with 15, Labridae with 13, Haemulidae with nine, Gobiidae with eight and Epinephelidae with seven.Richest genera were Lutjanus and Sparisoma with five species, followed by Gymnothorax, Caranx, Haemulon, Cynoscion and Sphoeroides with four each.
Habitat dissimilarity analysis shows that the composition of species of each habitat differs strongly from each other (Figure 8; SIMPROF, Global R=11.8, p=0.001).The WC habitat shows the most different composition, while RR and IF have 41 species in common, and SBI and SBA share 17 in common.The highest richness is found in the RR (95 species), followed by IF (67), SBA (63), WC (46) and SBI (45) (Table 1).The RR habitat also has the highest exclusive species richness with 49 species, followed by WC (36), SBA (36), SBI (13) and IF (7) (Figure 8).

DISCUSSION
Along the Brazilian coast, at least 437 fish species occur in reef environments (Floeter et al. 2008), and the reef fishes found at Franceses Island and adjacent habitats (154 species, sensu Floeter et al. 2008) represent about 35% of the Brazilian province reef fish species.Although species diversity is influenced by biogeographic and latitudinal gradients (Floeter et al. 2004(Floeter et al. , 2008)), it also shows a close relation with the local habitat diversity in each area (Cornell and Karlson 2000).Franceses Island,   even with a small and shallow reef area, displays a large diversity of micro-habitats, such as rocky shores, one beach, emerged and submerged reefs and patch reefs, rhodolith and bioclastic material beds, sand and mud bottoms, and macroalgae beds, distributed in areas sheltered and exposed to winds and waves.This diversity of habitats can contribute to the high species richness found in the Franceses Islands.Additionally, some oceanographic features of Espírito Santo State (Schmid et al. 1995) make this region a transitional zone between Brazilian Northeastern (tropical) and Southern (subtropical) coast (Martins et al. 2007), can be related with the geographical proximity and habitat plasticity of species.The similarity of SBI and SBA, even not too high, suggest that many species found in demersal unconsolidated bottoms, even not characterized as reef fishes, can explore and be recorded in island surroundings habitats, increasing the local richness.Else, WC habitat has the most distinct fauna, showing high exclusive species richness.The majority of species of this habitat used to occur in schools and have a seasonal presence in the area (Froese and Pauly 2014; personal observation).Thus, the mosaic of seascape, habitat plasticity of many species and seasonal visitant species can also contribute to the high fish diversity found in the studied island.Moura and Francini-Filho (2005) state that due to the high endemism and large risks Brazilian reefs can be considered a hotspot inside the Atlantic Ocean, so, in need of an immediate attention from scientists and conservationists.Espírito Santo coast, considered a marine transitional zone and a faunal boundary (Floeter et al. 2001;Martins et al. 2007), should receive a special care.Boundary regions are normally very sensitive to climate and environmental changes (Peters 1994), and depend on the preservation of natural areas for the maintenance of its communities.
Apart of the fact that it contains a representative portion of the Brazilian reef fish diversity (35%), Franceses Island also hosts endangered and over-exploited species, as well as several species of commercial and recreational importance.However, the isle has suffered different kinds of impacts, such as increase of sedimentation from two hydrographic basis, uncontrolled tourism and overfishing (Pinheiro et al. 2009b(Pinheiro et al. , 2010a(Pinheiro et al. , 2010b)).These impacts threaten reef areas worldwide and have a high potential to change reef fish community structure.Moreover, some species registered at Franceses Island deserve further attention for an adequate classification of risk.Eight species are considered endangered by Brazilian red list but not by IUCN evaluations.Four species, including a Brazilian endemic, are considered threatened by IUCN but not for Brazilian red lists (  in Table 1, are common but have been recently target of local fishing since the collapse of bigger and more valuable species, so deserve attention and monitoring by managers in Espírito Santo and Brazil.
Although there is a necessity of improvement of catch regulations, the full protection of habitats has been essential for resource recovery and biodiversity conservation.In this context, Brazilian Environmental Ministry has tried to implement a policy of MPAs creation targeting the goals of the Aichi Convention.
Despite that, Brazil has less than 2% of its marine area effectively protected, and in many cases the establishment of MPAs looks like a political deal or exchange by the aggressive and accelerate industrial growth that is happening and impacting several Brazilian coastal areas (pers.obs.).Presently, management organizations and NGOs are working towards the creation of a MPA in the southern coast of Espírito Santo.The inclusion of Franceses Island and adjacent habitats in a no-take zone can collaborate to the protection of a high biodiversity

NOTE
The Brazilian Red List was recently upgraded (IBAMA 2014), with many species added.Regarding reef fishes, four species we considered in the present work to be highly endangered in the Espírito Santo state (L.cyanopterus, S. trispinosus, G. altavela and Z. brevirostris) had their endangered status updated to either vulnerable or critically endangered.On the other hand, Gramma brasiliensis, highly targeted for the ornamental trade but rare at Franceses Island, dropped out the Red List.The official status of the other species did not change.

Figure 1 .
Figure 1.Map of Franceses Island, Espírito Santo state, southeastern Brazil.SH=shelter; LE=Low exposure; IE=intermediate exposure; HE=high exposure to winds and waves.
Pinheiro et al. | Fish diversity in a marine zoogeographical boundary

Figure 8 .
Figure 8. Cluster analysis (Bray Curtis dissimilarity) of habitats found in the Franceses Island and adjacent area.The total number and exclusive number of species are shown for each habitat.RR=rocky reefs; IF=interface; SBI=soft bottom of the island; WC=water column; SBA=soft bottom adjacent to the island.
Pinheiro et al. | Fish diversity in a marine zoogeographical boundary area, sustainability of surrounding artisanal fishing and management and valorization of the local tourism.
ContinuedPinheiro et al. | Fish diversity in a marine zoogeographical boundary
Continued Pinheiro et al. | Fish diversity in a marine zoogeographical boundary
* Species considered at risk in Espírito Santo state by the authors (see discussion); # Species targeted of a redirection of local fishery activities (due to the collapse of bigger and more valuable species).

Table 1 )
Bender et al. 2012)ns 2009;Pinheiro et al. 2009aea for nine endangered species(E.marginatus,G.cirratum,L.analis,L.cyanopterus,M.bonaci,S. trispinosus, S.  amplum, S. axillare, S. frondosum), all targeted by local fishing activities (Table1).Three endangered elasmobranchs, G. altavela, R. horkelii and Z. brevirostris, have been highly threatened around Franceses Island, as well in other areas of the ES, as by-catch by trawling activities(Pinheiro and Martins 2009;Pinheiro et al. 2009a).Summing to these examples, there are other 12 species (highlighted in Table1) found at Franceses Island that are not considered threatened neither by IUCN nor by Brazilian lists, but that have populations in risk at Espírito Santo state (pers.obs.), thus deserving a special attention for analysis and classification of risk (six of these are predicted to have a high extinction risk in Brazil;Bender et al. 2012).Other ten species, also pointed

Table 2 .
Species name, institution and voucher number of specimens collected in Franceses Island (Espírito Santo state, Brazil) and deposited in museum collections.