Submitted 10 September 2015Accepted 16 December 2015Published 14 January 2016

Corresponding authorNancy Cabanillas-Teraacutennanchamexgmailcom

Academic editorFabiano Thompson

Additional Information andDeclarations can be found onpage 12

DOI 107717peerj1578

Copyright2016 Cabanillas-Teraacuten et al

Distributed underCreative Commons CC-BY 40

OPEN ACCESS

Trophic ecology of sea urchins incoral-rocky reef systems EcuadorNancy Cabanillas-Teraacuten1 Peggy Loor-Andrade1 Ruber Rodriacuteguez-Barreras2 andJorge Corteacutes3

1Departamento Central de Investigacioacuten Universidad Laica Eloy Alfaro de Manabiacute Ciudadela UniversitariaViacutea San Mateo Manta Manabiacute Ecuador

2Department of Biology University of Puerto Rico at Bayamoacuten Puerto Rico3Centro de Investigacioacuten en Ciencias del Mar y Limnologiacutea (CIMAR) and Escuela de BiologiacuteaUniversidad de Costa Rica San Pedro San Joseacute Costa Rica

ABSTRACTSea urchins are important grazers and influence reef development in the EasternTropical Pacific (ETP) Diadema mexicanum and Eucidaris thouarsii are the mostimportant sea urchins on the Ecuadorian coastal reefs This study provided a trophicscenario for these two species of echinoids in the coral-rocky reef bottoms of theEcuadorian coast using stable isotopes We evaluated the relative proportion of algalresources assimilated and trophic niche of the two sea urchins in the most southerncoral-rocky reefs of the ETP in two sites with different disturbance level Bayesianmodels were used to estimate the contribution of algal sources niche breadth andtrophic overlap between the two species The sea urchins behaved as opportunisticfeeders although they showed differential resource assimilation Eucidaris thouarsiiis the dominant species in disturbed environments likewise their niche amplitudewas broader than that of D mexicanum when conditions were not optimal Howeverthere was no niche overlap between the species The Stable Isotope Analysis in R(SIAR) indicated that both sea urchins shared limiting resources in the disturbed areamainly Dictyota spp (contributions of up to 85 for D mexicanum and up to 75for E thouarsii) The Stable Isotope Bayesian Ellipses in R (SIBER) analysis resultsindicated less interspecific competition in the undisturbed site Our results suggesteda trophic niche partitioning between sympatric sea urchin species in coastal areas ofthe ETP but the limitation of resources could lead to trophic overlap and strongerhabitat degradation

Subjects Ecology Marine BiologyKeywords Diadema mexicanum Eucidaris thouarsii Stable isotopes Rocky reefs Niche breadthEastern Tropical Pacific

INTRODUCTIONAs a consequence of increasing human pressure coastal ecosystems are facing a widerange of threats such as resource exploitation and habitat modification (Wilkinson 1999Dumas et al 2007 Costello et al 2010 Rossi 2013) Several studies have evaluated thedevelopment of rocky bottom disturbances by analyzing the densities of echinoids andthe development stage of habitats (Phillips amp Shima 2006 Alvarado Corteacutes amp Reyes-Bonilla 2012 Hereu et al 2012) Some of these studies have correlated different phases ofbenthic substrate degradation considering sea urchin density and their association with

How to cite this article Cabanillas-Teraacuten et al (2016) Trophic ecology of sea urchins in coral-rocky reef systems Ecuador PeerJ4e1578 DOI 107717peerj1578

functional algae groups (Steneck 1983 Steneck amp Dethier 1994) Another approach todecipher benthic dynamics is through the trophic relationships between consumers andresources using stable isotopes (Behmer amp Joern 2008) Stable isotope analysis (SIA) hasbeen a powerful tool to study trophic ecology especially for those species with foraginghabits for which it is difficult to use traditional techniques such as stomach contentanalyses Several studies have focused on sea urchins from a stable isotope approach(egMinagawa ampWada 1984 Tomas et al 2006 Vanderklift Kendrick amp Smith 2006Wing et al 2008 Cabanillas-Teraacuten 2009 Rodriacuteguez-Barreras et al 2015)

Stable carbon and nitrogen isotope ratios provide time-integrated information regardingfeeding relationships and energy flow through food webs (DeNiro amp Epstein 1981 Petersonamp Fry 1987 Vander-Zanden amp Rasmussen 2001 Carabel et al 2006) Stable isotopes canbe used to study the trophic niche of a species due to the lsquolsquoδ-spacersquorsquo This is comparable tothe n-dimensional space that ecologists refer to as a niche because an animalrsquos chemicalcomposition is directly influenced by what it consumes as well as the habitat in which itlives (Newsome et al 2007 Parnell et al 2010 Boecklen et al 2011)

Carbon is a conservative tracer used to track energy sources in food webs whilenitrogen helps determine the trophic position (Minagawa ampWada 1984 Vander-Zandenamp Rasmussen 2001 Post 2002 Phillips 2012 Phillips et al 2014) Carbon (δ13C) andnitrogen (δ15N) stable isotopes have been used in marine ecosystems to determine the foodhabits of species (Peterson amp Fry 1987) nutrient migrations within food webs the trophicposition of organisms and their contribution at every level (Vander-Zanden amp Rasmussen1996) the origin and transformation of the ingested organic matter (Peterson Howarthamp Garrett 1985) or how some ecosystems have organisms that occupy similar trophicpositions coexisting in high densities (Vanderklift Kendrick amp Smith 2006) Moreover SIAare useful to assess the ecosystem health (egCole et al 2004Hamaoka et al 2010Karubeet al 2010) For example human influence on lake ecosystems were studied by Karube etal (2010) and those authors found that signatures of δ13C and δ15N in macroinvertebratesof the littoral zone are indicators of anthropogenic impacts from the watershed Inorganicnitrogen loading from the watershed was recorded in δ15N of snails

Reef degradation currently has significant consequences for morpho-functionalityof marine environments (Hoegh-Guldberg 1999 Mumby Foster amp Fahy 2005) and theEcuadorian reefs are no exception (Glynn ampWellington 1983 Glynn 1993 Guzmaacuten ampCorteacutes 1993 Glynn 2003) Anthropogenic stressors can have synergistic effects on reefssuch as the harmful algae blooms that are becoming increasingly important drivers ofvariation in the sea urchin populations as seen in other areas (Hunter amp Price 1992Lapointe et al 2005 Lapointe et al 2010)

Coral-rocky reefs have rarely been studied along the Ecuadorian mainland despite theserious threat by eutrophication fisheries and other anthropogenic impacts (Guzmaacutenamp Corteacutes 1993 Corteacutes 1997 Corteacutes 2011) Ecuadorian coral communities are importantbecause they represent the southernmost distribution in the Eastern Tropical Pacific (ETP)Ecuador has no extensive reef systems as the majority of reefs are small rocky patches withsome coral colonies Nevertheless those areas are characterized by high biodiversityincluding more than a quarter of the Ecuadorian continental fishes and a great number of

Cabanillas-Teraacuten et al (2016) PeerJ DOI 107717peerj1578 220

echinoderms sea fans and scleractinian corals (Glynn et al 2001 Glynn 2003 Rivera ampMartiacutenez 2011)

Sea urchins have the capability to modify the community structure through foragingas several authors have previously mentioned (eg Carpenter 1981 Carpenter 1986 Hay1984 Hay amp Fenical 1988 Sala Boudouresque amp Harmelin-Vivien 1998) and we need toelucidate what occurs in areas where there are more than one sea urchin species whichdominate the substratum and their role in controlling fleshy macroalgae The sea urchinsDiadema mexicanum (Agassiz 1863) and Eucidaris thouarsii (Agassiz amp Desor 1846) aretwo of the most dominant benthic grazers in the ETP (Guzmaacuten amp Corteacutes 1993) Thesetwo echinoids exert a strong influence on the community structure (Lawrence 1975Glynn Wellington amp Birkeland 1979 Andrew 1989 Underwood 1992) In the ETP thesea urchin E thouarsii could be described as a major herbivore in rocky reef bottoms Itspreferential resource appeared to be benthic algal turf and macroalgae but if those werenot available it feeds on other organisms such as the corals Pavona clavus Pocilloporaspp and Porites lobata (Glynn Wellington amp Birkeland 1979 Glynn ampWellington 1983Reaka-Kudla Feingold amp Glynn 1996)

The ratios of δ15N and δ13C in consumers are strongly influenced by their food resources(Phillips et al 2014) and it is necessary to identify their ecological role not only by theircapacity to structure the environment but to understand the dynamics of coexistence of thesea urchin populations along the Ecuadorian coast The relative position of δ13C vs δ15Nechinoids species can be displayed in a bi-plot and help to understand food web structureand organism responses to niche shifts diet variability and human impact (Layman et al2007) The aimof this studywas to improve the knowledge and understanding of the trophicbiology of D mexicanum and E thouarsii in Ecuadorian rocky reefs We determined thestable isotopes of carbon and nitrogen isotope for both sea urchin species The complexityof the littoral zone was analyzed using stable isotopes to understand the trophic interactionsof these two echinoids in areas with different degree of human impact We assume that themore developed rocky-reef and substrate associated to coral coverage will favor habitatswith complex trophic interactions (see Duffy et al 2007 Alvarez-Filip et al 2009 Grahamamp Nash 2013) resulting in wider isotopic echinoids niche breadth

MATERIAL amp METHODSSite descriptionsThis study was conducted between May to September of 2013 at two localitiesLos Ahorcados (LA 0140prime42

primeprime

S 8051prime58primeprime

W) and Perpetuo Socorro (PS 055prime40primeprime

S8044prime25

primeprime

W) in Manabiacute province Ecuador (Fig 1) The LA site was a small group ofrocky islets located near Machalilla National Park Although this area was not considereda protected area it had a very high diversity of scleractinians and octocorals (Rivera ampMartiacutenez 2011) LA presented a rocky bottom with clear geomorphologic differencesbetween the leeward and windward areas The leeward area were 25 m depth and thewindward side was mainly build by octocorals (22 species) and hexacorals such as Pavonaspp the branching corals Pocillopora spp and solitary corals The PS site is located in front

Cabanillas-Teraacuten et al (2016) PeerJ DOI 107717peerj1578 320

Figure 1 Study area and sampling sites in the coast of Ecuador Los Ahorcados (LA) and Perpetuo So-corro (PS)

of the Port of Manta (15 km) one of the most important ports in Ecuador for large pelagicfisheries (Villoacuten amp Beltraacuten 1998a Villoacuten amp Beltraacuten 1998b Martiacutenez-Ortiz et al 2007) andgreatly impacted by anthropogenic activities (see details in Table 1) PS rocky reef is ahomogenous bottom of 7ndash9 m depth and had a substrate consisted mainly of a mixtureof rock and sand with scarce scleractinian corals (Pavona spp and Pocillopora spp) andgorgonians (mainly Leptogorgia alba)

In order to distinguish both sites a coral-rocky reef category was used for this studywhich was developed taking into account habitat complexity and type of disturbance toestablish two categories namely disturbed and undisturbed (Table 1) The distance ofhuman impact to the sites size of the fleet and type of human disturbance were consideredThe rugosity index (RI) which is the ratio of a length of chain following the reef contourto the linear distance between its start and end point (modified of Risk 1972) was usedTo calculate the RI we used a three-meter chain five times equitably-distributed along 15transects (20 m) The average RI obtained with transects was used to determine the rugositylevel per site where larger numbers indicate higher complexity following Alvarez-Filip etal (2009) and Alvarez-Filip et al (2011) Therefore values of RIlt 15 were considered lowcomplexity and RIgt 15 were defined as complex

Cabanillas-Teraacuten et al (2016) PeerJ DOI 107717peerj1578 420

Table 1 Category of coral-rocky reef sites and source of human impact

Site Source of human impact Human populationdensity (ind kmminus2)

Distance from samplingsite to Source of humanimpact (km)

Rugosityindex (RI)

Category

Los Ahorcados (LA) Artesanal fishery+ hotel zone 5455 1724 232 UndisturbedPerpetuo Socorro (PS) Artesanal and industrial Fishery+

hotel zone+ industry discharge104634 343 110 Disturbed

Collecting and processing dataWe collected algal samples for identification to calculate biomass and to carry out SIAAlgal biomass was measured using twelve 50times 50 cm quadrats per site The quadrats werelocated randomly within the sea urchin habitat The substrate inside each quadrat wasscrapped carefully removed collected in bags and frozen for later analysis Macroalgaewere identified to the lowest possible taxonomic level using the available keys (Abbottamp Hollenberg 1976 Afonso-Carrillo amp Sansoacuten 1999 Littler amp Littler 2010) The sampledinvertebrate and algal species for this study are not threatened The necessary permits wereobtained from the Ministry of Environment of Ecuador (014AT-DPAM-MAE)

In areas where the algal cover was dominated mainly by turf species (following themorpho-functional category of Guidetti 2006) we used a sniffer with a dense mesh bagcoupled to a compressed air tank In the laboratory individuals were separated into speciesand gently washed with distilled water and dried in an oven at 50 C for 24 h to measurethe dry weight

We collected four individuals of D mexicanum and six of E thouarsii in LA and twelveindividuals of D mexicanum and eight of E thouarsii in PS at the same depth range(8ndash10 m) Only individuals greater than 50 cm in test diameter were collected to avoidany effect of the development stage The samples were frozen shortly after collection andprocessed at the laboratory The muscles of Aristotlersquos lanterns were removed carefullyand washed from the stomach contents to estimate algal assimilation by D mexicanumand E thouarsii This tissue provides a time-integrated measure of assimilated sources(eg Michener amp Schell 1994 Ben-David amp Schell 2001 Polunin et al 2001 Phillips ampKoch 2002 Rodriacuteguez 2003 Tomas et al 2006)

The algal and echinoids muscle samples were rinsed with filtered water dried at 50 Cduring 36 h ground to a fine powder and placed in glass vial for isotope analyses Toremove carbonates from some algal species (Lobophora variegata and Polysiphonia spp)the samples were washed with diluted HCl at 1 N prior to drying to avoid disturbance inthe mass spectrometer reading A subsample was taken of each alga and muscle (sim1 mg)to evaluate the 13C12C and 15N14N ratios using a Thermo Electron Delta V AdvantageMass Spectrometer Carbon and nitrogen samples were analyzed in a dual isotope mode atthe Geology Department University of Florida Gainesville Florida

The isotope samples were loaded into Eppendorf capsules and placed in a 50-positionautomated Zero Blank sample carousel on a Carlo Erba NA1500 CNS elemental ana-lyzer After combustion in a quartz column at 1020 C in an oxygen-rich atmosphere thesample gas was transported in a He carrier stream and passed through a hot reduction

Cabanillas-Teraacuten et al (2016) PeerJ DOI 107717peerj1578 520

column (650 C) consisting of elemental copper to remove oxygen The effluent streamthen passed through a chemical (magnesium perchlorate) trap to remove water followedby a 3 m Gas chromatography (GC) column at 45 C to separate N2 from CO2 Thesample gas next passed into a ConFlo II preparation system and into the inlet of a massspectrometer running in continuous flowmode where the sample gaswasmeasured relativeto laboratory reference N2 and CO2 gases The carbon isotopic results were expressed instandard delta notation relative to Vienna Pee Dee Belemnite (VPDB) The nitrogenisotopic results were expressed in standard delta notation relative to atmospheric air Thestandard deviations of δ13C and δ15N replicate analyses were estimated the precision valueswere 0074 and 0148 for carbon and nitrogen isotope measurements respectively Carbonand nitrogen samples were analyzed in a dual isotope mode Ratios are expressed as

δX(h)= [(RsampleRstandard)minus1]times1000where X = 13C or 15N and

Rsample=13C12C or 15N14N

Data analysisThe relative contribution of algae to the diet of the sea urchins D mexicanum andE thouarsii was estimated with a Bayesian isotopic mixing model (SIAR Parnell amp Jackson2013) which included the isotopic signatures fractionation and variability to estimate theprobability distribution of the contribution of the food source to a mixture This proceduresupplied accurate information about the contribution of algal species to the sea urchintissues recognized the main components of the diet under different conditions (Peterson1999 Fry 2006 Wing et al 2008) Lipid extraction in sea urchins was not necessary sinceAristotle lanternrsquos muscle is low in lipids on the other hand when the CN ratios are lowerthan 35 it is not recommended (Post et al 2007) see Table S1 The isotopic discriminationfactor values used to run the model were 24 plusmn 16h (mean plusmn SD) for δ15N and 04plusmn 13h for δ13C (Fry amp Sherr 1984 Minagawa ampWada 1984 Michener amp Schell 1994Moore amp Semmens 2008) The results of the mixing model showing the calculated seaurchin dietary proportions were represented as box plots indicating the 25 75 and95 of credibility intervals (Fig 2)

The niche width and overlap for the sea urchins were estimated with Stable IsotopeBayesian Ellipses in R (SIBER) (Jackson et al 2011) from the SIAR package (Parnell ampJackson 2013) This analysis uses metrics based on ellipses and provides the standardellipse corrected area (SEAc) used as the trophic niche breadth and the overlap betweenellipses where values close to 1 represent a higher trophic overlap

Prior to the statistical analysis the homogeneity and normality of variance were tested byperforming a KolmogorovndashSmirnov and a Cochranrsquos test (Zar 2010) Statistical differencewas performed comparing δ15N and δ13C values between species In addition the algalbiomass between sites was evaluated with a one-way ANOVA with site as a fixed factorThe statistical analyses were performed using R with an alpha of 005 (R Core Team 2014)

RESULTSThe benthic communities in Ecuadorian rocky reefs ranged between habitats dominated bymacroalgae and live corals (LA) and habitats dominated by turf and coral skeletons (PS)

Cabanillas-Teraacuten et al (2016) PeerJ DOI 107717peerj1578 620

Figure 2 Contribution rates of algae to the diet of the two sea urchin species Results are shown as 2575 and 95 of credibility intervals (A) Represents the contribution for Diadema mexicanum in Los Ahor-cados (LA) (B) for Eucidaris thouarsii in LA (C) D mexicanumin Perpetuo Socorro (PS) and (D)E thouarsii in PS

Site estimates for perturbation and complexity are outlined in Table 1 LA is a site withstructural complexity and dominance of branched erect algae while PS has low structuralcomplexity and dominance of turf (Table 1)

The algae collected in LA were Asparagopsis armata Dictyota dichotoma Lobophoravariegata Polysiphonia spp and Sargassum spp while in PS were D dichotomaL variegata and Polysiphonia spp The greatest algal biomass was recorded for L variegataat both sites while D dichotoma was the algae with the lowest biomass at both localities(Table 2) Overall the biomass average values ranged from 358 plusmn 973 g (dry weight)mminus2 for PS to 14300 plusmn 2067 g mminus2 in LA We found significant differences between bothsites (ANOVA df = 1 F = 360 plt 001) The overall algal δ15N fluctuated from 505to 949h (Table 3) PS displayed the highest mean values of nitrogen with D dichotoma(760 plusmn 053h) At LA Polysiphonia spp exhibited the highest mean value for nitrogen(719 plusmn 113h) We found significant differences in δ15N between sites (ANOVA df =1 F = 529p= 002) taking into account all the algae isotopic signatures As for δ13Cratios fluctuated from minus2365 to minus690h with LA displaying the most negative values(A armata) There was no significant difference in δ13C among sites (ANOVA DF = 1F = 141pgt 005)

Cabanillas-Teraacuten et al (2016) PeerJ DOI 107717peerj1578 720

Table 2 Average algal biomass in grams (dry weight) mminus2plusmn standard deviation at Los Ahorcados (LA)and Perpetuo Socorro (PS)

Species LA PSA armata 3432plusmn 1698 ndashD dichotoma 469plusmn 190 060plusmn 020L variegata 6677plusmn 2452 2326plusmn 1261Polysiphonia spp 3073plusmn 1282 1638plusmn 626Sargassum spp 594plusmn 309 ndash

Table 3 Meanplusmn standard deviation values of δ13C and δ15N of algal genus considered in the mixing model analysis taken from Los Ahorcadosand Perpetuo Socorro

Los Ahorcados Perpetuo Socorro

Species δ13C δ15N Species δ13C δ15NA armata (n= 4) minus2363plusmn 010 568plusmn 002 ndash ndash ndashD dichotomaa (n= 4) minus1730plusmn 194 665plusmn 0791 D dichotoma (n= 3) minus1527plusmn 305 760plusmn 053L variegata (n= 4) minus1573plusmn 3331 589plusmn 0638 L variegata (n= 3) minus1202plusmn 060 706plusmn 108Polysiphonia spp (n= 6) minus933plusmn 1759 719plusmn 1129 Polysiphonia spp (n= 4) minus1472plusmn 304 738plusmn 036Sargassum spp (n= 4) minus1830plusmn 007 697plusmn 006 ndash ndash

Values of δ15N were particularly different between the two species of sea urchins(ANOVA df = 1 F = 2010plt 0001) The isotopic value of δ15N for D mexicanumranged from 1138 to 1299h whereas E thouarsii displayed values from 1231 to 1415hThe average values of δ13C and δ15N estimated forD mexicanum in LA wereminus1667plusmn 004and 1153 plusmn 014h respectively while E thouarsii displayed minus1546 plusmn 016h and 1284plusmn 040h respectively In PS the D mexicanum isotopic signals wereminus1625plusmn 039h forδ13C and 1262 plusmn 022h for δ15N while E thouarsii displayed minus1541 plusmn 043h for δ13Cand 1354 plusmn 047h for δ15N We found significant differences in δ13C between species(ANOVA df 1 F = 4931plt 00001) and the most negative values were found at LA Theδ15N showed the same patterns as those algae (higher values for PS) δ15N ratios of both seaurchins differed between the study sites as LA reported lower values than PS (ANOVA df1 F = 759plt 001) The most notorious difference was due to D mexicanum (ANOVAdf 1 F = 8241plt 00001)

The mixing models provided evidence for the contribution of different algal resourcesfor both sites and species The SIAR analysis showed that Sargassum spp was the mostimportant resource for D mexicanum in LA (up to 43) followed by D dichotoma and Aarmata as secondary resources (up to 37 for both) Likewise Sargassum spp was the mainalgal resource for E thouarsii in the same locality (up to 44) followed by Polysiphoniaspp (up to 41) (Table 4) Contrasting at PS the main macroalgal contributor was Ddichotoma for both sea urchins (Fig 2) with up to 85 of the proportional contributionfor D mexicanum and close to 75 for E thouarsii Table 5 shows data on isotopic nichebreadth as measured by the corrected standard ellipse area (SEAc) The main difference inthe trophic niche breadth was caused by E thouarsii with a difference probability of 52overlap between species isotopic niches was not found in any case (Fig 3) but the SEAcwas higher for E thouarsii in both sites with 025 in LA and 046 in PS (Table 5)

Cabanillas-Teraacuten et al (2016) PeerJ DOI 107717peerj1578 820

Table 4 Average percentage () contribution of algal species to the diet of the sea urchinsD mexi-canum and E thouarsii at Los Ahorcados (LA) and Perpetuo Socorro (PS) produced by the SIARmodelusing isotope values from algae Minimum and maximum values for each algae are shown in parenthe-ses

Diadema mexicanum Eucidaris thouarsii

Species LA PS LA PSA armata 21 (2ndash37) ndash 14 (0ndash28) ndashD dichotoma 20 (0ndash37) 52 (21ndash85) 19 (0ndash37) 44 (13ndash75)L variegata 16 (0ndash32) 9 (0ndash23) 15 (0ndash31) 19 (0ndash38)Polysiphonia spp 20 (04ndash35) 38 (3ndash67) 28 (15ndash41) 38 (4ndash66)Sargassum spp 23 (1ndash43) ndash 24 (1ndash44) ndash

Table 5 Trophic niche breadth of sea urchins calculated by SIBER analysis of muscle values SEAc cor-rected standard ellipse area The right column shows statistical differences in SEA

Species SEAc Ellipses areasgroup differencesprobability ()

D mexicanum (LA) 0005D mexicanum (PS) 0218 1 vs 2 (104)a

E thouarsii (LA) 0250E thouarsii (PS) 0457 1 vs 2 (520)a

NotesaGroup 1 Los Ahorcados (LA) Group 2 Perpetuo Socorro (PS)

Figure 3 Isotope niche breadth of the echinoidsD mexicanum (circles) and E thouarsii (triangles) inLos Ahorcados (white symbols and solid line) and Perpetuo Socorro (black symbols and dotted line)

Cabanillas-Teraacuten et al (2016) PeerJ DOI 107717peerj1578 920

DISCUSSIONThere is very little information on the ecology of the Ecuadorian coast and no datapertaining to trophic relationships among sea urchins apart from this study The majorityof the available information on Ecuador came from studies conducted on Galapagos reefs(Glynn Wellington amp Birkeland 1979Glynn ampWellington 1983Glynn 2003Glynn 2004Glynn et al 2009) The rocky reefs examined in this study were selected to establish thebaseline of the trophic ecology of two rocky reef areas with different disturbance levels inthe Ecuadorian mainland coast The presence of D mexicanum was related to the rockybottoms of LA where algal presence were more frequent than in the disturbed site (PS)The population density of E thouarsii was higher at the disturbed site (N Cabanillas-Teraacuten2013 unpublished data) This study demonstrated that algal abundance is not alwaysequivalent to assimilation by the consumer For instance L variegata displayed the lowestdietary contribution at PS and LA for both sea urchins although it exhibited the highestaverage biomass at both sites Grazing preference by D mexicanum and E thouarsii wasnot related to algal biomass

The isotopic results characterized different algal assemblages that were specific to eachrocky reef bottom (branched macroalgae for LA and turf for PS) The values of δ15N inalgae in this study ranged from 505h to 949h This result agreed with the ranges ofvariation reported in other studies (Owens 1987) The values of δ13C fluctuated fromminus2365 to minus690h and agreed with data from Fry amp Sherr (1984) who reviewed the δ13Cdata of benthic algae noting that values ranged between minus30 and minus5h The differentalgae species constituting the community of LA showed isotopic values that were closertogether but with a broader cloud distribution in the C vs N biplot of points relative towhat was observed in PS This suggests a more complex trophic net and shows how primaryconsumers interact with their resources (McClanahan 1988 Phillips amp Gregg 2003)

The isotopic ratios of δ15N could be influenced by two main factors One factorpertains to changes in dissolved nitrogen although these changes primarily affect themicroscopic algal communities or communities living near upwelling zones (Jennings etal 1997 Polunin amp Pinnegar 2002) The other factor is the anthropogenic impact (BodeAlvarez-Ossorio amp Varela 2006) affecting the communities near the coastline In this casethe community most affected by urban impact was PS located in front of Manta PortIn this port human density is higher than 1000 indkmminus2 and artisanal and industrialfishery contribute to nitrogen input as well as the hotel zone and discharges from tunaprocessing

For algae found in both sites (D dichotoma L variegata and Polysiphonia spp) theaverage δ15N were higher in PS This agrees with other areas with high anthropogenicinfluence where δ15N values tended to be higher (Wada Kadonaga amp Matsuo 1975Michener amp Schell 1994) Although both localities shared species the isotopic values forboth localities were different because each system had its own structure The erectedbranched algae A armata and Sargassum spp (not found in PS) contributed to thestructural complexity founded in LA

Cabanillas-Teraacuten et al (2016) PeerJ DOI 107717peerj1578 1020

Variations in carbon and nitrogen ratios gave us information on trophic spectruminherent to each site and the contribution of algal species to the sea urchin tissues displayinformation about how consumers assimilate the resources when they inhabit disturbedandor undisturbed sites Although both sea urchin species can share the same foodresources we found that their ecological roles were different and there are differencesbetween species in terms of assimilation This could explain the fact that δ15N values inthe muscle of E thouarsii were higher for both localities even though both sea urchinspecies showed a preference for the same species D dichotoma No overlap of isotopeniche breadth of the echinoids was found between the two species (Fig 3) but the isotopicvalues between species at PS were closer suggesting increased competition due to the lackof resources This result coincided with the mixing model because the two species of seaurchins preferentially consumed similar proportions of the same species Moreover theSEAc was larger for E thouarsii at both sites and in LA the niche trophic distance betweenD mexicanum and E thouarsii was very conspicuous while in PS the two species of seaurchins are closer (Fig 3) A low degree of feeding specialization suggests that the seaurchins adapt their foraging behavior to algae availability being most evident forE thouarsii that exhibits a broader trophic niche

The grazing behavior of these sea urchins agreed with the findings by Glynn Wellingtonamp Birkeland (1979) in the Galaacutepagos Islands as their grazing was stronger in those areaswith 30 or less coral cover Previous studies highlighted that E thouarsii limited coralgrowth as this echinoid interfered with the development of the reef frame and with theability to modify the habitat structure (Bak 1994 Carpenter 1981 Sonnenholzner Ladahamp Lafferty 2009) We considered D mexicanum to be an important grazer for the rockybottoms ecosystems considering that changes in its population caused significant changesin the algal cover of those areas

Our results supported the evidence that D mexicanum and E thouarsii were coexistentspecies that play a significant role as herbivores Nevertheless they apparently eat whateverthey find and the food items are incorporated differentially between the species Diademamexicanum grazing effect on algal diversity and community structure is important in theprocess of formation andmaintenance of rocky reefs in Ecuador This has also been observedin other areas of the ETP where D mexicanum has a relevant role in the recruitment ofcorals (Alvarado Corteacutes amp Reyes-Bonilla 2012) This was also observed in Caribbean reefswith D antillarum (Macintyre Glynn amp Hinds 2005 Mumby et al 2006 Idjadi Haringamp Precht 2010 Sandin amp McNamara 2012) and in shaping the sublittoral ecosystems ofthe Canary Islands with D africanum (Alves et al 2003 Tuya et al 2004 Hernaacutendez et al2005 Hernaacutendez et al 2008 Sangil et al 2014 Cabanillas-Teraacuten et al 2015)

The standard ellipses areas values (Table 5) indicated that niche partitioning may varydepending on different disturbance levels between sites however the diets ofD mexicanum and E thouarsii not only depend on the disturbance condition For instanceDictyota dichotoma was an important component of the diet of D mexicanum and Ethouarsii in the disturbed and undisturbed sites while Polysiphonia spp was important indisturbed bottoms where isotopic algal signals are closer to each other This could lead toa greater number of resource overlap at PS than at LA

Cabanillas-Teraacuten et al (2016) PeerJ DOI 107717peerj1578 1120

Differential assimilation and niche partitioning are just snapshots It is importantto depict how the shape of the food web varies in time and space (Layman et al 2007Schmidt et al 2007) so it is necessary to carry out more extensive spatial and temporalresearch Likewise it is necessary to deepen research to analyze if the narrower nicheamplitude (SEAc) of D mexicanum and its associated presence to scleractian corals (at LA)is consistent to what is happening in the Caribbean where its presence provides suitablehabitat for coral recruitment The feeding success of herbivores is associated with thecompetition level for resources therefore sympatric species are exposed to a potentialtrophic overlap The most pristine zone (LA) exhibited smaller SEAc (considering valuesper species) and nitrogen values which indicate a trophic niche partitioning between themain sea urchins on the Ecuadorian coast However the limitation of resources could leadto trophic overlap and stronger habitat degradation

ACKNOWLEDGEMENTSThe first author is grateful to Limber Alcivar and Jorge Figueroa for their scientific divinglogistic help during fieldwork and laboratory work Thanks to the Departamento Central deInvestigacioacuten-Universidad Laica Eloy Alfaro de Manabiacute We want to acknowledge NormanMercado and Joseacute Luis Varela for their valuable comments

ADDITIONAL INFORMATION AND DECLARATIONS

FundingThis study was funded by project Anaacutelisis de los Ecosistemas de los fondos rocososde Ecuador continental proyecto CUP 917400000000375395 of DCI-ULEAM Thefunders had no role in study design data collection and analysis decision to publish orpreparation of the manuscript

Grant DisclosuresThe following grant information was disclosed by the authorsAnaacutelisis de los Ecosistemas de los fondos rocosos de Ecuador continental917400000000375395

Competing InterestsThe authors declare there are no competing insterest

Author Contributionsbull Nancy Cabanillas-Teraacuten conceived and designed the experiments performed theexperiments analyzed the data contributed reagentsmaterialsanalysis tools wrotethe paper prepared figures andor tables reviewed drafts of the paperbull Peggy Loor-Andrade Ruber Rodriacuteguez-Barreras and Jorge Corteacutes analyzed the datawrote the paper prepared figures andor tables reviewed drafts of the paper

Cabanillas-Teraacuten et al (2016) PeerJ DOI 107717peerj1578 1220

Field Study PermissionsThe following information was supplied relating to field study approvals (ie approvingbody and any reference numbers)

Ministerio de Medio Ambiente de Ecuador014AT-DPAM-MAE

Data AvailabilityThe following information was supplied regarding data availability

Data S1

Supplemental InformationSupplemental information for this article can be found online at httpdxdoiorg107717peerj1578supplemental-information

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Glynn PW 2004High complexity food webs in low-diversity Eastern Pacific reefndashcoralcommunities Ecosystems 7358ndash367

Glynn PWMateacute JL Baker AC CalderoacutenMO 2001 Coral bleaching and mortality inpanama and Ecuador during the 1997ndash1998 El NintildeondashSouthern Oscillation Eventspatialtemporal patterns and comparisons with the 1982ndash1983 event Bulletin ofMarine Science 6979ndash109

Glynn PW Riegl B Romanski AMS Baums IB 2009 Rapid recovery of a coral reef atDarwin Island Galapagos Islands Galapagos Research 666ndash13

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Guidetti P 2006Marine reserves reestablish lost predatory interactions andcause community effects in rocky reefs Ecological Applications 16963ndash976DOI 1018901051-0761(2006)016[0963MRRLPI]20CO2

GuzmaacutenHM Corteacutes J 1993 Los arrecifes coralinos del Paciacutefico Oriental Ecuatorialrevisioacuten y perspectivas Revista de Biologiacutea Tropical 41535ndash557

Hamaoka H Okuda N Fukumoto T Miyasaka H Omori K 2010 Seasonal dynamicsof a coastal food web stable isotope analysis of a higher consumer In OhkouchiN Tayasu I Koba K eds Earth life and isotopes Kyoto Kyoto University Press161ndash181

HayME 1984 Predictable spatial escapes from herbivory how do these affect the evolu-tion of herbivore resistance in tropical marine communities Oecologia 64396ndash407DOI 101007BF00379139

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Hereu B Garcia-Rubies A Linares C Navarro L Bonaviri C Cebrian E Zabala M2012 Impact of the Sant Esteversquos storm (2008) on the algal cover in infralittoralrocky photophilic communities Final report Proyecto Intramural EspecialCofinanciado CEAB-CSIC PIEC 200430E599 123ndash134

Hernaacutendez JC Clemente S Brito A Falcon JM Garciacutea N Barquin J 2005 Estado de laspoblaciones de Diadema antillarum (Echinoidea Diadematidae) y del recubrimientode macroalgas en las Reservas Marinas de Canarias patrones de distribucioacuten espacialVieraea 33367ndash383

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Hoegh-Guldberg O 1999 Climate change coral bleaching and the future of the worldrsquoscoral reefsMarine and Freshwater Research 50839ndash866 DOI 101071MF99078

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Jackson AL Inger R Parnell AC Bearhop S 2011 Comparing isotopic niche widthsamong and within communities SIBERndashStable Isotope Bayesian Ellipses in RJournal of Animal Ecology 80595ndash602 DOI 101111j1365-2656201101806x

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Rodriacuteguez-Barreras R Cuevas E Cabanillas-Teraacuten N Sabat AM 2015 Potentialomnivory in the sea urchin Diadema antillarum Regional Studies in Marine Science211ndash18 DOI 101016jrsma201508005

Rossi S 2013 The destruction of the lsquoanimal forestsrsquo in the oceans towards an over-simplification of the benthic ecosystems Ocean and Coastal Management 8477ndash85DOI 101016jocecoaman201307004

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Cabanillas-Teraacuten et al (2016) PeerJ DOI 107717peerj1578 2020