Macrobenthic fauna from an upwelling coastal area of Peru (Warm Temperate South-eastern Pacific province -Humboldtian ecoregion)

Abstract Background A total of 162 species and subspecies of marine macroinvertebrates were recorded in the submerged soft and hard substrates around the PERU LNG marine terminal and surrounding area, in the central coast of Peru, 167 km south of Lima, Peru. The collection of specimens was carried out from June 2011 to June 2015 as part of the research studies conducted by the Biodiversity Monitoring and Assessment Program (BMAP) around the marine terminal. The area is part of the Humboldt Current Large Marine Ecosystem, one of the most important upwelling systems in the world. New information We identified specimens belonging to 83 families and seven phyla. The list was assembled from the taxonomic identifications made by the BMAP. We identified species and subspecies belonging to phyla Annelida, Arthropoda, Brachiopoda, Cnidaria, Echinodermata, Bryozoa and Mollusca. Phyla Annelida (60 spp.), Arthropoda (47 spp.)and Mollusca (45 spp.) exhibited the largest number of species.


Introduction
Marine studies along the coastline of Peru are largely focused on species of economic importance (Tarazona et al. 2003). Species without economic importance or smaller size species, but of great importance for the maintenance and functioning of the marine ecosystem, remain poorly studied and understood. Marine invertebrates, particularly the coastal macrobenthic fauna, are known in Peru, but the information about them arises from studies focused on the effect of El Nino Southern Oscillation (ENSO) and largely limited to the fauna from deepest areas (Tarazona 1990, Tarazona et al. 1996, Arntz et al. 2006. This is understandable because, in deeper areas, the impact of ENSO on macrobenthic communities is more evident compared to shallow areas (Tarazona et al. 2003). This has resulted in a gap of information about the diversity and dynamics of the macrobenthos inhabiting shallow coastal areas (i.e. less than 15 metres). After the collapse of the anchovy fishery in the 1970s, research on marine biodiversity became more inclusive towards species without commercial importance (Arntz and Tarazona 1990). Preliminary research was focused on taxonomic groups already reported in lists and catalogues (Chirichigno and Vélez 1998, Del Solar et al. 1970, Mendez 1981, Alamo and Milla 1997, Paredes et al. 1988), but it eventually started to include less studied groups. Now, there is a greater record of research in biodiversity for different groups including decapods and stomatopods (Moscoso 2012), holothurians (Prieto 2010), asteroidea (Morales 2011), molluscs (Ramírez et al. 2003, Cardoso et al. 2016, sponges (Azevedo et al. 2015), nudibranchs (Schrödl and Hooker 2014) and echinoids (Hooker et al. 2012). This remarkable increase of biodiversity information helps understanding the general macrobenthonic diversity and encourages the compilation of geographicallyfocused lists to improve our understanding about species range distribution and for monitoring temporal changes.
Here, we have assembled a taxonomic list of macrobenthic species present in the shallow coastal area near the international marine terminal of company PERU LNG (PLNG), in Pampa Melchorita, on the central coast of Peru, in the southeast Pacific. The area where the terminal is located is part of the Humboldt Current Large Marine Ecosystem (HCLME), an important upwelling system encompassing submerged habitats from the southern tip of Chile to northern Peru. The HCLME is considered amongst the most productive marine ecosystems in the world and knowledge about the diversity and natural processes characterising it are in great need, given its importance in global fisheries economy (Sherman 1991, Bakun andWeeks 2008). This taxonomic list focuses both on the species inhabiting the hard and soft bottoms at intertidal and subtidal levels in the area of direct influence of the marine terminal and control sites.

Study area
The checklist of benthic macrofauna species was assembled using data collected by the Biodiversity Monitoring Assessment Program (BMAP). This programme is carried out in collaboration with the Smithsonian Conservation Biology Institute and PLNG. The area of study is the area of influence of PLNG marine terminal (13°15,15'S; 76°18,5'W), situated 167 km south of Lima, Peru. The submerged area is characterised by sediment flats with scattered patches of hard bottom and new artificial hard bottom created after establishment of an 800 m-long breakwater. Sampling was carried out close to the PLNG marine terminal and surroundings from June 2011 to June 2015, with a biennial periodicity. Samples were taken in three replicates both from soft and hard substrates (Suppl. material 1). Soft substrate samples were obtained from the resurgence and saturated zone from the intertidal (Salvat 1964) and from the subtidal at depths of 8, 10, 12 and 15 m (Fig. 1a). Samples collected from artificial hard substrates (breakwaters and piles) were obtained from the intertidal level (0 m) and subtidal levels (depths of 5 to 10 m) (Fig. 1b). To collect samples from intertidal soft substrate, an 18 cm-diameter benthos hand corer was used while, for the subtidal soft substrate, a 0.05 m Van Veen grab was used. Samples were sieved through a bag of 0.5 mm mesh size and the retained material was fixed with 4% formaldehyde in seawater. To facilitate later triage work and taxonomic analysis, the samples were stained with 1% rose bengal. To collect samples from hard substrate, a 25 cm x 25 cm quadrat was used and samples were obtained by clearing all specimens within the quadrat using a chisel and hammer.

Identification of species and data analysis
The taxonomic identifications of collected specimens were made by the team of taxonomists from The Environment Management S.A.C (TEM). In this study, we only considered taxa identified at species or subspecies levels. Names of higher taxa as well as names of species and subspecies within them are listed alphabetically. For each of the species, we provide information about its original combination, the type of substrate (soft or Study area around the PERU LNG marine terminal including location of sampling sites. Sites are identified by a unique code followed by depth at which that site is located. Grey-shaded area at the centre is the area of direct influence of the marine terminal while grey-shaded areas at the north and south of the terminal are control sampling sites. a: Soft bottom sites. b: Hard bottom sites. hard), depth or bathymetric range, code of station where it was reported (with the name of transect and the depths in parentheses). We include remarks when necessary, particularly in the case of identified non-native species. Voucher specimens were deposited at the scientific collection of Laboratorio de Biología y Sistemática de Invertebrados Marinos (LabSIM) at Universidad Nacional Mayor de San Marcos (UNMSM).

Nomenclature:
Nerine cirratulus chilensis Hartmann-Schröder, 1962 Notes: Material examined: Fig. 2. Prostomium elongated and distally pointed, continuing posteriorly as caruncle to end of setiger 1. Peristomium well developed, forming lateral wings that sometimes cover half of the prostomium. Setiger 1 reduced. Branchiae from setiger 7, fused with the dorsal lamella, leaving free only the tips of both; from the setigero 22-25, the fusion only covers half of the branchiae and lamella.

Fissurella latimarginata Sowerby, 1835
Notes: Material examined: Fig. 2. Conical shell and sharpened in the front end, medium-sized apical foramen oval, the external surface is ornamented with thin and little spaced radial striae in a dark purple background. The shell is white from the inside, with thick, uniform and purple border. The sides of the foot and mantle are of an intense black colour, with yellow prolongations in the border of the mantle. Its tentacles are deep yellow. Types of substrate: hard bottom. Depth / bathymetric range: 0-10 m. Station code: D1(0, 5); D2(0, 10).

Analysis
We recorded 162 species and subspecies of marine macroinvertebrates in the submerged soft and artificial hard substrates around the PERU LNG marine terminal and surrounding area between June 2011 and June 2015 (Suppl. material 2). In soft-substrate sampling sites, we recorded 71 species. For these sites, the accumulation curve appeared asymptotic (Suppl. material 3) and the richness estimator Chao2 estimated that 89.9% of expected species were detected in our sampling (Chao2=78.892, 89.99%). In hardsubstrate sampling sites, we recorded 131 species during the five years of surveys. The accumulation curve appeared nearly asymptotic (Suppl. material 4) and the richness estimator indicated that 89.7% of expected species were detected by our sampling effort (Chao2=145.933, 89.76%).
The Polychaeta was the group with the highest number of species (61 spp.), followed by Crustacea and Mollusca with 47 and 45 species, respectively. Less numerous in species, but present in the study area, were the phyla Brachiopoda, Bryozoa, Cnidaria and Echinodermata (one to five species). The photographs for some of the species listed in this study are presented in Fig. 2.

Discussion
This study reports the diversity of macrobenthonic species associated with the coastal soft and hard bottom habitats around PERU LNG marine terminal in central Peru. In general, species richness and taxonomic composition observed in our study area are similar to other upwelling areas, north of the terminal, like Ancon Bay (Tarazona et al. 1988, Tarazona 1990) and Chancay (L. Quipúzcoa, pers. comm.) in Peru and south of the terminal, like Independence Bay in Peru (Tarazona et al. 1996) and Coloso Bay (Carrasco 1997) and Mejillones Bay (Laudien et al. 2007) on the coast of Chile. We observed, however, a slight increase in richness in the sampling sites immediately adjacent to the marine terminal, compared to the rest of the sampling sites. This was due to the presence of infrastructure. In general, large coastal marine infrastructure like docks, piers and breakwaters, have an important role in attracting benthic fauna, just like artificial reefs do (Lincoln-Smith et al. 1994). The three-dimensionality of the structures creates different types of microhabitats likely to be colonised by species with different habitat preferences. Similar to what other studies have observed for coastal macroinvertebrate communities, species richness decreased with depth (Tarazona et al. 1996, Tarazona 1990).
We highlight the report of a new Polychaeta species, Myrianida paredesi, described from specimens obtained from biofouling from main pier piles at PERU LNG marine terminal (Aguirre et al. 2015). Areas with regular maritime traffic, as is the case for our study area, are likely to be colonised by non-native biofouling species given the spatial range of microhabitats that offer these artificial structures. In this study, we have been able to report eight species considered as non-native (Caprella scaura, Elasmopus rapax, Monocorophium insidiosum, Monocorophium acherusicum, Polydora websteri, Ancinus brasiliensis, Hepatus lineatus, Bugula neritina). The most likely vector of introduction may be the maritime traffic occurring along the coast of Peru.
We detected species in our study area (but not listed here) that were challenging to identify because their presence was limited to individuals at early developmental stages (i.e. juveniles), they were present in low numbers or because of taxonomic complexity. These putative species include Abarenicola affinis chilensis, Capitella capitata, Cirratulus megalus , Dodecaceria opulens, Eunice pelamidis, Hemipodia simplex, Kinbergonuphis microcephala, K. multidentata, Lumbrineris annulata, Magelona phyllisae, Paleanotus chrysolepis, Phymactis clematis, Pisione oerstedii, Polydora pygidialis, Scoletoma tetraura, Syllis gracilis, Thoracophelia mucronata and Spiophanes norrisi. We recommend an increased sampling effort as well as an extensive review to confirm their presence in the area. Further, the application of molecular tools (i.e. barcode sequencing) could be integrated into the analyses to help improving biodiversity assessments (e.g. Rosas et al. 2018) and for resolving taxonomic conflicts (e.g. Hebert and Gregory 2005). Molecular tools offer additional benefits like the effective detection of non-indigenous species (e.g. Zaiko et al. 2015) and improving assessment of the health of marine ecosystems (Sigamani et al. 2016). Considering the high complexity, variability and productivity of the Peruvian coastal upwelling system, this study helps to increase the understanding of the local marine biodiversity and serves as a baseline for monitoring of the spatial and temporal changes in the diversity and composition of coastal macrobenthic communities.