Diversity and composition of macro- and meiofaunal carapace epibionts of the hawksbill sea turtle (Eretmochelys imbricata Linnaeus, 1822) in Atlantic waters

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Marine Biodiversity ISSN 1867-1616 Mar BiodivDOI 10.1007/s12526-013-0189-9

Diversity and composition of macro-and meiofaunal carapace epibionts ofthe hawksbill sea turtle (Eretmochelysimbricata Linnaeus, 1822) in AtlanticwatersG. V. V. Corrêa, J. Ingels,Y. V. Valdes, V. G. Fonsêca-Genevois,C. M. R. Farrapeira & G. A. P. Santos

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DIVERSITY OF MARINE MEIOFAUNA ON THE COAST OF BRAZIL

Diversity and composition of macro- and meiofaunal carapaceepibionts of the hawksbill sea turtle (Eretmochelys imbricataLinnaeus, 1822) in Atlantic waters

G. V. V. Corrêa & J. Ingels & Y. V. Valdes & V. G. Fonsêca-Genevois &

C. M. R. Farrapeira & G. A. P. Santos

Received: 12 April 2013 /Revised: 2 October 2013 /Accepted: 8 October 2013# Senckenberg Gesellschaft für Naturforschung and Springer-Verlag Berlin Heidelberg 2013

Abstract The presence of macro-epibionts on turtlecarapaces is a well-known phenomenon, whereby carapacesare occupied by dynamic and fully functional epibiontcommunities. However, meiofaunal organisms have beenlargely ignored in turtle shell studies despite theiromnipresence and higher abundances and diversity than themacrofauna. Epifauna from the hawksbill sea turtleEretmochelys imbricata was investigated during summer2010 with the aim to advance our knowledge on meiofaunalepibiont communities on turtle carapaces and gain insightsinto their interaction with settled macrofauna. Eighteenepibiont higher taxa were found (17 meiofauna, 5macrofauna), 5 of which are common for macro- andmeiofauna. Meiofauna was present on all turtle carapaces,but macrofauna occurred on only 8 out of 19 investigatedcarapaces, suggesting that carapace colonization bymeiofauna precedes macrofauna recruitment. In addition, themacrofauna embedded on the carapaces increased themicrohabitat complexity, favoring richer and more abundantmeiofauna communities. The significant positive correlations

between meiofauna and macrofauna taxa (up to 90 %)suggests the presence of mutual facilitating processes andindicates the positive effects between meio- and macrofaunalepibionts important for their recruitment and establishment.The hawksbill sea turtle carapaces were occupied by fullyfunctional and active epifaunal communities, with adult andreproductive stages for most meiofaunal and macrofaunaltaxa. Turtle carapaces can therefore be seen as a biologicalsubstrate that can serve as a platform for faunal dispersal, ashas been observed for barnacles, enhancing the geographicaldistribution of several species through sea turtle migration. Inaddition to the main focus of this paper on meio- andmacrofaunal epibiont communities, we provide an updatedlist of taxa found on carapaces of the hawksbill sea turtle anddiscuss the geographical scope and dispersion potential ofsome of these taxa.

Keywords Eretmochelys imbricata . Meiofauna .

Macrofauna . Bioengineering . Facilitation . Biologicalinteractions . Epifaunal recruitment

Introduction

The hawksbill sea turtle Eretmochelys imbricata Linnaeus,1822 is considered the most tropical among all sea turtlespecies, and occurs in the Atlantic, Indian and Pacific oceans(Witzell 1983). The turtles develop to the juvenile stage (inabout 11–15 years after birth) in oceanic regions to then returnto neritic zones, where they reach their sexual maturity(Bjorndal 1997). They spend a great part of their lifeassociated with coral reefs, but they can migrate over longdistances between feeding and breeding areas (Bjordnal1999). Considering that the Brazilian coastline harbors largeareas with great potential for sea turtle feeding, juvenilescoming from Brazilian oceanic islands tend to stay along the

Electronic supplementary material The online version of this article(doi:10.1007/s12526-013-0189-9) contains supplementary material,which is available to authorized users.

G. V. V. Corrêa :Y. V. Valdes :V. G. Fonsêca-Genevois :G. A. P. Santos (*)Departmento de Zoologia, CCB, Laboratorio de Meiofauna,Universidade Federal de Pernambuco,Av. Prof.Moraes Rego, 1235, 50670-901 Recife, Pernambuco, Brasile-mail: [email protected]

J. IngelsPlymouth Marine Laboratory, Prospect Place, The Hoe,Plymouth PL1 3DH, UK

C. M. R. FarrapeiraDepartamento de Biologia, Universidade Federal Rural dePernambuco, Rua Dom Manoel de Medeiros s/n,52171-900 Recife, Pernambuco, Brazil

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country’s coastline (Marcovaldi et al. 2006). This is differentfor sub-adult individuals, which are able to travel more than 4,000 km, across international barriers (Bellini et al. 2000).Taking in consideration these distribution patterns, there mustbe variable opportunities for the colonization of the carapacesby marine invertebrates, and colonization patterns themselvesmust be variable. The variability and community dynamics ofturtle epibiont communities were highlighted in the recentwork of Frick and Pfaller (2013), who proposed a conceptualscheme to elucidate the mechanisms of epibiosis on turtlecarapaces. The importance of geographic and ecologicaloverlap was put forward in this study, with the likelihood ofepibiosis also being the result of a trade-off between cost andbenefits of the epibionts involved (Frick and Pfaller 2013).

Epibiont studies focusing on sea turtle carapaces arereporting more widespread epibiont occurrences globally(Frazier et al. 1992, 1998; Dobbs and Landry 2004). Up tonow, this type of research along the Brazilian coastline is scantand mainly focused on epibiotic macrofauna (organisms>1 mm; Bugoni et al. 2001; De Loreto and Bondioli 2008).The presence of small, microscopic animals that usually liveon the bottom in aquatic habitats with sizes between 0.038 and1 mm, defined as the meiofauna, has only recently beendocumented in association with sea turtle carapaces, and thereal phyletic richness of epibionts is likely still underestimated(Schärer 2003). The microscopic metazoan epibionts (meio-epifauna; <1mm; coined by Raes and Vanreusel 2005 for coldwater corals) have a short life cycle, which facilitates theirecological succession and ability to colonize substrates(Gallucci et al. 2008). These characteristics render them asan excellent tool to evaluate ecological relationships from thein situ epibiont community.

The effects of macrofauna presence on meiofaunacommunity structure are highly diverse, and meiofaunastudies on consolidated substrates are scant. However, forsea turtle carapaces there are some reports of epibioticmeiofauna on turtle carapaces (Frick and Pfaller 2013).Differences in density, abundance, and composition of themeiofauna as a result of macrofauna presence are significantdue to various mediating effects, including predation,facilitation, competition, physical disturbance, and theincrease of habitat complexity (Oláfsson 2003; Norling andKautsky 2007), and different macrofauna species may havedifferent effects on different meiofauna groups (Sundelin andElmgren 1991). In this context, it has been suggested thatmacrofaunal epibiont recruitment follows the initial settlingof the smaller meiofauna-sized organisms on turtle carapaces(Frick and Pfaller 2013). Following colonization, meiofaunamay suffer from macrofauna predation (Dupuy et al. 2010;Austen et al. 1998) that comes in the form of settling larvae orforaging adults. In turn, the meiofauna may also affect themacrofauna through, for instance, predation on polychaetelarvae that are trying to settle (Watzin 1983, 1986).

Alternatively, macrofauna organisms may act as biologicalengineers, modifying the environment by generatingmicrohabitats (Koivisto et al. 2011), which can facilitate thegrowth of other species (Grzelak and Kuklinski 2010). Forinstance, macrofauna outer body structures (i.e.: exoskeleton)with sediment attached to them may be rich in meiofaunathemselves. Another example of macrofaunal bioengineeringare the Cirripedia (barnacles), which can alter water flow, andcreate troughs that enhance recruitment of small organisms,such as nematodes, whilst causing irregular distribution ofpotential food particles across the substrate (Abelson et al.1993; Snelgrove 1994; Fonsêca-Genevois et al. 2006).

The macrofauna can influence the composition of themeiofauna in several ways: negatively, through (1) directpredation, (2) competition for food, and (3) competition forspace, especially during the recruitment phase; and positively,through (4) the creation of microhabitats, (5) the supply ofsemi-digested organic matter present in the feces, and (6) theformation of micro-currents that enhance the dispersion andavailability of food in the water column (Meziane et al. 2002;Dahms and Qian 2005; Fonsêca-Genevois et al. 2006). Theseinteractions mediate the epibiotic community present on thesea turtle carapace, whilst the carapace is used as mobile-passive habitat for several species.

This work aimed to study the structure and diversity ofepibiotic meio- and macrofaunal communities present oncarapaces of the hawksbill sea turtle along Pernambucosouth-coast beaches (Brasil), and identify the possibleinteractions between organisms of these epibioticassemblages. There is evidence that meio- and macrofaunafunctional communities interact to a great extent, and thatmacrofauna has the ability to facilitate meiofauna throughniche establishment (Braeckman et al. 2011a, b). Wehypothesize that, despite negative interactions such ascompetition and predation, there will be clear evidence offacilitative effects in epibiont communities on the carapacesof the hawksbill sea turtle. Given what we know aboutepibiont community development from turtle carapaces(Frick and Pfaller 2013, and references therein), it is likelythat a progression of organism recruitment takes place thatstarts with the smaller meiofauna taxa, followed bymacrofauna and the subsequent increase of habitat andcommunity complexity. We therefore tested whether thepresence of macrofauna affects the associated epibiontmeiofauna communities.

In addition to the main focus of the meio- and macrofaunalepibiont communities, we provide an updated list of all taxafound on carapaces of the hawksbill sea turtle and discuss thegeographical scope and dispersion potential of some of thesetaxa. It is well acknowledged that sea turtles have the potentialto act as dispersion vectors for a diverse array of marineinvertebrates over broad geographic regions (Frick andPfaller 2013, and references therein) and the list of turtle

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epibionts has increased recently and rapidly. In addition, theinformation on certain epibionts and their reproductivebehavior and requirements may reveal migratory locationsand habitat preferences of the turtles (Frick and Pfaller 2013)

Materials and methods

Sampling area

The samples were taken from 19 turtles at 6 beaches from themunicipality of Ipojuca (08°30’26.82”S, 35°00’2.23”W) onthe south coast of Pernambuco, Brazil (Fig. 1). In total, 14 kmof beach coastline were monitored twice a day during 2 h atnight and 2 h early morning shifts, the total time of all shiftsbeing approximately 342 h of field monitoring at low tideperiod, during summer 2010 ( from September 10 2010 andMay 11 2011).

Sampling

When turtles were observed on the beach, their carapaceswere subdivided in 9 zones as defined by Pfaller et al.(2006), and 5 out of the 9 zones were randomly chosen(Urbaniak and Plous 2011) and sampled by scraping off10 cm2 for each of the 5 zones (Fig. 2). Nineteen adult turtleswere sampled and all the samples taken from each carapacewere homogenized and preserved with 8 % formalin; henceeach carapace was considered as one replicate. Macrofaunalorganisms were arbitrarily defined as those organisms retainedin a 1-mm sieve, while the meiofauna comprised all organismspassing through a 1-mm sieve and retained in a 38-μm sieve.Macro- and meiofauna were identified under a stereoscopicmicroscope (×50 magnification). The macrofaunal

invertebrates were classified to the lowest taxonomic levelusing specific taxonomic literature for each taxon: thedichotomous keys from Camargo and Lana (1995a), 1995b)and books (Fauchald 1977; San Martín 2003, and referencestherein) for Polychaeta, the pictorial keys from Young (1991)for barnacles (Cirripedia) and the key of Barnard andKaraman (1991) for Amphipoda to the lowest taxonomiclevel. The meiofauna organisms were identified to highertaxon level (mostly phylum level) following Higgins andThiel (1988).

Statistical analyses

To determine the differences in the structure of the meiofaunacommunity between samples with the presence and absenceof macrofauna for each replicate, analysis of similarity(ANOSIM) was performed using fourth-root-transformedabundance data and the Bray–Curtis similarity measure. Thegraphic representation was done using a non-metricmultidimensional scaling (nMDS), which shows thedifferences between the epibiont meiofauna communitiesbased on multivariate community composition. Thecontribution of the faunal groups to similarity anddissimilarity values among the samples was measured with asimilarity percentage test (SIMPER). A distance-basedredundancy analysis (dbRDA) was used to identify the groupsthat best explain the differences between the sample data.Spearman rank correlations were performed to explain theinfluence of the macrofauna on the emergence and persistenceof meiofauna taxa and to investigate the relationship betweenmacrofauna and meiofauna, as well as to see whether therelationship among epibiont groups was significantly positiveor negative.

Fig. 1 Region monitored duringthe nesting period of hawksbillsea turtles Eretmochelysimbricata . The dashed linesindicate the areas where sampleswere taken, including thebeaches: Muro Alto, Cupe,Merepe, Porto de Galinhas,Maracaípe and Pontal deMaracaípe

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All the analysis and graphs were performed using thestatistical software Primer 6.0+ PERMANOVA (Clarke andGorley 2006; Anderson and Gorley 2008), with the exceptionof the correlation tests which were performed using Statistica7.0 (StatSoft). Additionally, the global distribution of speciesthat were registered as hawksbill sea turtle carapace epibiontsfor the first time were included in a map with the help ofWoRMS (World Register of Marine Species ) and availableliterature records.

To compare and discuss the epibiont data, the meiofaunaand macrofauna densities were expressed in ind. 10 cm−2 andind. m−2, respectively, following internationally standardizedunits. The classification of organisms presence frequency wasdone following Bodin (1977), grouping the organismsaccording to their occurrence: 1 constant (75.1–100 %), 2frequent (50.1–75 %), 3 common (25.1–50 %), and 4 rare(0.1–25 %).

Results

Macro-epifauna

A total of 6 macrofauna phyla were observed, present on only11 carapaces and hence not as omnipresent as the meiofauna.Abundances averaged (ind. m−2±SE): Polychaeta (181.8±143), Amphipoda (158.2±78.9), Cirripedia (118.2±32.5),Bivalvia (21.8±13.4), Tanaidacea (9.09±6.3), and Turbellaria(1.8±1.8). The mean area size of the carapace covered bymacrofauna was 1.08 m2 per turtle.

The groups with higher incidence were Cirripedia(omnipresent), followed by Amphipoda (81.8 %), Polychaeta(63.6 %), Bivalvia (27.2 %), Tanaidacea (18.1 %) andTurbellaria (9.1 %). Several individuals from Tanaidacea werefound with eggs and different-sized bivalves were recovered.

Polychaete individuals belonged to five families:Hesionidae (Grube, 1850), Syllidae (Grube, 1850) (Syllisamica Quatrefages, 1866), Terebellidae (Malmgren, 1867),Lumbrineridae (Schmarda, 1861) (Lumbrineris magalhaensisKinberg, 1865; Lumbrineris inflata Moore, 1911) andEunicidae (Berthold, 1827) (Nematonereis hebes Verril,1900). For one turtle, several parasites (leeches) were foundattached to its body, but they were not included in the analysisbecause they are not considered carapace epibionts. On thecarapaces, there were several tubes made with algae, detritus,and sediment.

The Amphipods belonged to three different families:Hyallidae, Gammaridae, and Caprellidae. These crustaceanswere found in association with macro-algae present on theturtle carapace and several of them were carrying offspring intheir ventral region, in between their coxal plates.

Although Cirripedia were found on all carapaces colonizedby the macrofauna (11), this group was only the third most-abundant macrofauna taxon. The individuals were identifiedto the species level, whereby 82.3 % were adults, of which 1/3showed developed gonads and 2/3 were in a non-reproductivestage; the other 17.7 % were juveniles. All the individualsbelonged to Chelonibia caretta (Spengler, 1790), exhibiting adensity of 118.2 ind. m-2.

Meio-epifauna

Meiofauna epibionts were present on all sampled carapaces,with 17 higher taxa identified: Sarcomastigophora, Cnidaria,Turbellaria, Kinorhyncha, Gastrotricha, Nematoda, Tardigrada,Polychaeta, Oligochaeta, Gastropoda, Bivalvia, Acari,Ostracoda, Copepoda, Tanaidacea, Amphipoda, and Insecta.1

Nauplii (crustacean larvae) were also found in the samples.The groups Nematoda, Copepoda, and Ostracoda were

categorized as constant taxa. Polychaeta was the only frequenttaxon, whilst Tanaidacea, Bivalvia, Amphipoda,Kinorhyncha, Acari, Turbellaria, Gastrophoda, and Cnidariawere common, with similar presence frequencies. The othergroups (Sarcomastigophora, Gastrotricha, Oligochaeta,Insecta) were classified as rare.

Carapaces with average area size of 0.90 m2 were coveredby meiofauna and the total abundance of different groupsshowed considerable variability, ranging from only 1individual (Sarcomastigophora) up to 3,653 individuals(Ostracoda). Ostracoda was the most abundant group (38.5±18.8 ind. 10 cm-2) and was represented by differentmorphotypes and ontogenic stages. They were present innearly 80 % (78.9 %) of the samples, in direct relationship

1 As there are very fewmarine insects, it is suspicious to find this taxon inturtle carapaces. Although we have found this aquatic insect in thesamples taken from the carapaces, we cannot confirm whether the insectwas living on the carapace or whether it was a sample contamination.

Fig. 2 Imaginary zones used to scrap five randomly selected sub-areas of10 cm2 to compose one replicate, showing the nine different zones usedfor sampling (inset adapted from Pfaller et al. 2006)

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with micro- and macro-algae, as well as from detrital padsaccumulated on the carapace (personal observation).Copepoda, the second most abundant taxon, were present in90 % of the samples with an average density of 33.63±10.4ind. 10 cm-2. Most of the individuals belonged to the familyHarpaticoidea, with the exception of two specimens, whichwere considered planctonic (Ciclapoidea). A number ofovigerous females were observed. Crustacean nauplii larvaewere present in 52.6 % of the samples. Nematoda were thethird most abundant taxon with an occurrence frequency

equivalent to that of the Copepoda, reaching a density of21.6±8.6 ind. 10 cm-2.

Meio- and macro-epifauna interactions

Density- and taxon-dependence was observed between meioand macrofauna, whereby carapaces with macrofauna presentexhibited a higher meiofauna abundance (10,200 individuals)and richness (16 taxa) than carapaces without macrofauna(147 meiofauna individuals, 9 taxa; see Fig. 3). The ANOSIManalysis to test for differences in meiofauna communitystructure between carapaces with and without macrofaunawas significant (R global=0,76; p <0,05). Few meiofaunagroups (Ostracoda, Nematoda, Copepoda, Turbellaria,Oligochaeta, Polychaeta, Acari, and Tardigrada) with lowabundance were present on the carapaces without macrofaunacompared to the carapaces colonized by the macrofauna.Carapaces with macrofauna present were indeed distinct fromthose with macrofauna absent, with the formation of twosample groups based on the absolute abundance of allmeiofauna taxa (meiofauna taxon-based similarities of 40and 60 % among samples, respectively, with the exceptionof one outlier point (Fig. 4a)). We also noticed that the totalabundance of the rare taxa was higher for those carapaces thathad macrofaunal epibionts (Fig. 4a). In the nMDS plots ofFig. 4b–d, the influence of the abundance of the mainmeiofauna taxa are clearly illustrated, with the carapaces that

Fig. 3 Meiofauna total abundance (bars) and taxa richness (■) found insea turtle carapaces, in relation to the presence or absence of macrofaunagroups attached to their carapaces

Fig. 4 Non-metricmultidimensional scaling(nMDS) of all carapaces with thepresence (▲) and absence (▼) ofmacrofauna and based on the totalabundance of all identifiedmeiofauna taxa (Bray–Curtisresemblance). Circles representthe values from the analysis ofsimilarity (ANOSIM) withcontinuous lines (40 %) anddashed lines (60 %). a Numbersrepresent the total abundance ofthe rare taxa (Tardrigada,Gastrotricha, Oligochaeta,Insecta, and Sarcomastigophora).b–d Bubble size and numbersrepresent the total abundance ofthe main meiofauna groups (bOstracoda, c Copepoda, and cNematoda)

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exhibit high abundances for Ostracoda (Fig. 4b), Copepoda(Fig. 4c), and Nematoda (Fig. 4d) grouping together on theright hand side. The SIMPER results (Table 1) confirm thisobservation, with Copepoda, Nematoda, and Ostracoda as themost abundant taxa, explaining over 60 % of the similaritybetween turtle carapaces with macrofauna present and over50 % of similarity between turtle carapaces with macrofaunaabsent (Fig. 4b–d); other taxa had lower contributions(<10 %). The dbRDA (not shown), based on the fullmeiofauna dataset, also shows a clear difference betweencarapaces with macrofauna absent and present. No particularmeiofauna groups exhibited a clear distinct contribution to theobserved differences, but approximately 70 % of themeiobenthic variation among the carapaces of E . imbricatawas explained by the first two axes.

The Spearman rank correlation analyses revealed asignificantly positive relationship between macro- andmeiofauna abundance (r s=0.89, n =19, p <0.05). Themacrofauna abundance generally correlated positively withall the meiofauna groups, with most correlations significant

(Nematoda, Bivalvia, Polychaeta, Copepoda, Ostracoda,Amphipoda, Turbellaria, Tanaidacea, and Kinorhyncha).Negative correlations were rare, and, if present, they werelow and non-significant. The macrofaunal Turbellaria didnot correlate significantly with any of the meiofauna groups,and the meiofaunal Tardigrada, Gastrotricha, and Cnidaria didnot correlate significantly with any macrofauna taxon; thesetaxa were therefore omitted from Table 2.

Discussion

Turtle carapaces as substrates and their associated fauna

The behavioral patterns of hawksbill sea turtles and theircontact with various marine habitats from which epibiontscan transfer to the carapace suggests substantial geographicaland ecological overlap (sensu Frick and Pfaller 2013). It istherefore not surprising that a large amount of organisms havebeen recovered from their carapaces. In addition, the proposed

Table 1 Contribution percentage(90 %) of meiofaunal taxa athawksbill sea turtlesEretmochelys imbricatacarapaces with the presence ofmacrofauna (group presence) andwith turtle carapaces without thepresence of macrofauna (groupabsence) for the averagesimilarity and dissimilarity, asdetermined by SIMPER; taxa arelisted according to theircontribution for 4th root averagesimilarity within each group

Av. S. average similarity, Av. Dis.average dissimilarity

Species 4th root average abundances Contribution (%) Cumulative (%)

Presence Absence

Av. S. 60.57%

Copepoda 3.79 27.46 27.46

Nematoda 3.18 19.87 47.34

Ostracoda 3.19 17.11 64.45

Polychaeta 1.59 7.65 72.10

Bivalve 1.14 5.36 77.46

Amphipoda 1.07 4.77 82.23

Acari 0.98 4.55 86.78

Turbellaria 0.99 4.16 90.94

Av. S. 50.29%

Copepoda 1.46 45.57 45.57

Nematoda 1.17 43.40 88.97

Ostracoda 0.77 9.74 98.71

Av. Dis. 66.42%

Copepoda 3.79 1.46 15.52 15.52

Ostracoda 3.19 0.77 14.58 30.09

Nematoda 3.18 1.17 11.37 41.46

Polychaeta 1.59 0.13 8.43 49.89

Bivalve 1.14 0.00 6.70 56.59

Amphipoda 1.07 0.00 6.37 62.96

Cnidaria 1.01 0.00 5.94 68.89

Acari 0.98 0.13 5.68 74.58

Turbellaria 0.99 0.15 5.23 79.81

Gastrophoda 0.75 0.27 4.62 84.43

Tanaidacea 0.72 0.00 3.99 88.41

Kynorincha 0.64 0.00 3.36 91.78

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facilitation between epibiont macro- and meiofaunacommunities may enhance the ecological suitability of turtlecarapaces for new colonizers. The succession from pioneeringcolonizing species to more complex communities that are insome respect similar to complex sedimentary of hard substratehabitats supports the ecological overlap concept proposed byFrick and Pfaller (2013).

Most of the works on sea turtle-associated epifauna havefocused on the macrofauna group (Frick et al. 2002, andreferences therein) and did not take into account themeiofauna component and hence the true phylum richnessassociated with sea turtles. Since the work of Frick et al.(2002), new sea turtle associations with mollusks, bryozoans,echinoderms, cnidarians (Pfaller et al. 2006), crustaceans(Fuller et al. 2010), and algae (Frick et al. 2003) have beenreported. The epifauna associated with E . imbricata wasdescribed for the first time on the coastline of Puerto Rico,where by means of qualitative sampling 12 different epibioticanimal phyla were recorded together with some algae groups(Schärer 2003). In this study, the metazoanmeiofauna showeda similar dominance pattern compared to the present study.However, here, we report for the first time, the epifaunalassociation of the meiofauna taxa Acari, Kinorhyncha,Tardigrada, Gastrotrich, Oligochaeta, and Sarcomastigophorawith sea turtle carapaces. Two possible reasons why these taxamay not have been reported previously are samplingtechnique and effort. Manual sampling of carapaces with toolssuch as spatulas may depend on the accuracy and diligence ofthe researcher and may vary between different studies. Also,the complete removal of epibiont communities on randomly

chosen sectors of the carapace, followed by sieving as done inthe present study, is likely to enhance sampling efficiencycompared to manual selection and removal of individualorganisms. Moreover, as more carapaces are sampled, andhence research effort increases, the inventory of epibiontspecies is likely to increase. The observation of 17 phylaassociated with hawksbill sea turtles in the our study impliesthat this species hosts the most diverse epibiotic communities(at least on the phylum level) observed for sea turtles thus far(Frick et al. 2000; Schärer 2003).

It has been suggested that the structure of the epibioticcommunity associated with sea turtle carapaces is directlyrelated to submerged structures located in areas adjacent tonesting beaches and reef environments which are used asfeeding areas by this species (Frick et al. 2003). In ameiofauna study investigating beach rocks in the BrazilianNortheast (Silva 2012), 6 taxa were found in common withour observations. Of these, Copepoda and Nematoda were themost abundant, followed by Polychaeta, Ostracoda,Turbellara, and Acari. Another study in the same region, butfocusing on sandstone reefs, pointed out the dominance ofNematoda and Copepoda, and a total of 12 meiofauna taxawere found in the study area (Maranhão 2003). All thosegroups were also identified on the hawksbill sea turtlecarapaces in the present study, with the exception of Nemerteaand Rotifera (Maranhão 2003). Compared to the sandstonehard substrates, the turtle carapaces harbored 6 additionaltaxa: Cnidaria, Kinorhyncha, Tanaidacea, Insecta, Bivalvia,and Gastropoda. More conclusive evidence for theresemblance of epibiont meiofauna communities on hawksbill

Table 2 Spearman rank correlation values between the total abundance of meiofauna taxa, macrofauna taxa, meiofauna richness, macrofauna richness,total macrofauna, and total meiofauna

Macrofauna total Macrofaunarichness

Amphipoda Cirripedia Polychaeta Tanaidacea Bivalvia

Meiofauna total +0.89*** +0.55* +0.82*** +0.82*** +0.77*** 0.40 0.42

Meiofauna richness +0.56** +0.90*** +0.54* +0.54* 0.41 0.43 0.36

Bivalvia +0.85*** +0.47* +0.87*** +0.78*** +0.88*** +0.55* +0.47*

Ostracoda +0.72*** 0.36 +0.71*** +0.64** +0.63** 0.18 0.43

Acari +0.50* +0.46* 0.35 +0.46* 0.28 −0.01 0.19

Tanaidacea +0.46* 0.38 +0.52* 0.32 0.33 0.24 0.13

Nematoda +0.87*** +0.57* +0.81*** +0.74*** +0.81*** 0.40 +0.56*

Amphipoda +0.67** 0.13 +0.65** +0.72*** +0.57* +0.51* 0.27

Gastropoda 0.30 0.35 0.28 0.31 0.35 0.45 0.20

Copepoda +0.79*** +0.59** +0.70*** +0.75*** +0.57** 0.40 0.16

Polychaeta +0.82*** +0.51* +0.83*** +0.67** +0.84*** 0.34 +0.56*

Kinorhyncha +0.46* 0.37 0.45 0.31 0.41 −0.20 0.45

Turbellaria +0.66** +0.56* +0.61** +0.53* +0.66** 0.30 0.36

Oligochaeta 0.23 0.33 0.30 0.18 0.38 −0.14 +0.63**

Insecta 0.22 0.18 0.28 0.22 0.34 −0.08 +0.47*

Significant differences are represented by: *p <0.05, **p <0.01, ***p <0.001

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sea turtle carapaces and reef environments is given bySarmento et al. (2011), who investigated effects of humantrampling (as a result of tourism activities) on the meiofaunaof reefs. Sarmento et al. (2011) reported that reefenvironments harbored a meiofauna community that wasdominated by Copepoda, Nematoda, and Ostracoda, a similardominance pattern as found on the sea turtle carapaces. Of allthe rare taxa described by Sarmento et al. (2011), onlyPolyplacophora was not found as an epibiont on hawksbillsea turtle carapaces. The dominance of the three meiofaunataxa, Copepoda, Nematoda, and Ostracoda, seems to becommon for reef environments, and also for consolidatedsubstrates in general and for sea turtle carapaces. Theresemblance between the structure of meiofauna communitiesassociated to sea turtle carapaces and those found on coralreefs and consolidated substrates is substantial and suggeststhe likely exchange of meiofauna organisms between thesedifferent environments.

Interactions between macrofauna and meiofauna

Epibiont studies focusing on both macro- and meiofauna arerare, and investigations of the interaction between thesegroups are even scarcer, especially with regards to theirfacilitation effects (Meadows et al. 2012). The presence ofseveral rare taxa and the high abundances and richness ofepimeiofaunal communities were observed only in thosesamples (carapaces) with macrofauna present. The presenceof unilateral or reciprocal facilitation effects between both sizeclasses and their members is suggested here by the high andsignificant Spearman rank correlation values.

In this study, some carapaces were colonized by meiofaunain the absence of macrofauna, but not the other way around.The most likely explanation for this is that the meiofauna (bothin terms of their size and functional identity) are the firstinvertebrates to colonize the sea turtle carapaces. The carapacescolonized only by the meiofauna are therefore most likely in anearly stage of succession. Recruitment by the meiofauna priorto the macrofauna was also observed by Fônseca-Genevoiset al. (2006) in a colonization experiment using aluminiumplates, whereby Copepoda were the first to colonize the platesafter only 1 day, soon followed by Nematoda after the secondday, and Ostracoda after day 13. Our results stand in agreementwith these observations, and, despite the lack of temporal dataon different colonization stages, suggest that colonization onhard substrates, in this particular case, turtle carapaces, isinitiated by the meiofauna in an early recruitment phase, withmacrofauna colonization following later.

Colonization of hard substrates is generally sequentialthrough time with first the production of molecular films thatattract microbes, which, in turn, may facilitate the settlementof meio- and macrofauna, the latter usually as meio-sizedpropagules (e.g., Wahl 1989; Fonsêca-Genevois et al. 2006).

That indicates that our findings not only correspond with theliterature but also that meiofauna versus macrofaunainteractions can be beneficial for the abundance and richnessof the carapace community. At the same time, negativeinteractions (e.g,. competition and predation) between bothmeio- and macrofauna may regulate the colonization processand define the assemblages resulting from it (Oláfsson 2003).Noteworthy here is our observation during the sample sortingthat some macrofauna organisms showed stomach contentsthat resembled meiofauna hard structures under lightmicroscopy without macrofauna dissection (data not shown).

For both meio- and macrofauna, we found predators aswell as organisms that are good competitors (e.g., nematodesand polychaetes). Even if these organisms exhibit verydifferent feeding strategies, it is an indication that predationand competition were present during the communitysettlement. Competition and predation have been reported asimportant interactions regulating faunal assemblages withinthe meio- and macrofauna. Amphipoda, for instance, havebeen shown to negatively affect the abundance of Nematodaand Ostracoda (Sundelin and Elmgren 1991). Copepods canprey on specific polychaete larvae during the initial stages ofthe succession (Dahms et al. 2004), and so can certainnematode taxa and turbellarians (Danovaro et al. 1995).Hence, there is evidence that negative or bottleneck effectsfor meiofauna on macrofauna recruitment exist, but theregulatory processes remain debated (Zobrist and Coull1992). However, our observations suggest that the positiveeffect of facilitation processes may prevail over negativemeio- or macro-interactions such as competition andpredation.

Our results suggest that the presence of macrofaunaorganisms on hawksbill sea turtle carapaces influences thetotal abundance of meiofauna positively and is likely to allowthe appearance of rare taxa (Sarcomastigophora, Gastrotrich,Tardigrada, Oligochaeta, and Insecta). This facilitation mayhave occurred from the moment that the macrofauna alters thehabitat complexity, by creating microhabitats and allowing theaccumulation of micro- and macro-algae as well as detritusand sediments (Dos Santos, unpublished observations),subsequently attracting a richer meiofauna community (Frickand Pfaller 2013). Such faunal associations may also be theresult of the production of bio-deposits and the regeneration ofnutrients provided by the macrofauna, with a positive effect onthe richness, biomass, and abundance of the meiofaunacommunity. This has also been demonstrated for the foulingcommunity at the Swedish west coast in the North Sea(Norling and Kautsky 2007) and in the estuarine environmentof Rio de la Plata in Argentina (Spaccesi and RodriguesCapítulo 2012). Unfortunately, studies on the associationsbetween macrofauna and meiofauna in coral reefs or hardsubstrates are still in their infancy, and completely lackingfor sea turtle carapaces.

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Epifauna geographic scope and dispersion capacity

Records of turtle epibionts may provide crucial information ongeographical spread and dispersion potential for a broad arrayofmarine invertebrates (Frick and Pfaller 2013, and referencestherein). Such information may also reveal migratorylocations and habitat preferences of the turtles (Frick andPfaller 2013) which is of crucial importance in marineconservation management. For this study, we have compileda list of all taxa that have been recorded from carapaces of thehawksbill sea turtle (including new taxa found in the presentstudy; see supplementary material, Table S1).

Among the macrofauna organisms, Cirripedia or barnacleswere the most constant sessile invertebrates, agreeing with Fulleret al. (2010) and Pfaller et al. (2006). The species Chelonibiacaretta has already been found in association with the hawksbillsea turtle in the Pacific Ocean (Loop et al. 1995; Dobbs andLandry 2004), Indian Ocean (Jones et al. 2000), theMediterranean Sea (Badillo 2007), and the Atlantic Ocean(Frick et al. 2003; present study) (Table S1). This barnacle hasalso been found in association with other turtle species, the greenturtle (Chelonia mydas) and the loggerhead turtle (Carettacaretta) (Epibiont Research Cooperative 2007). The majorityof these crustaceans are hermaphrodites which do not practiceself-fertilization, and are therefore generally found in compactaggregations (Anderson 1994). In the present study, thepresence of adult barnacle clusters with developed gonadsindicates the ability of reproduction and dispersion of theseorganisms, even on what seems an inhospitable substrate. Ithas been shown that the population structure of barnacles isdirectly linked to their host (in this case, sea turtle carapaces) asthey are considered their primary habitat (Torres-Pratts et al.2009, and references therein). As such, they seem tightlyconnected with sea turtles and may depend on them fordispersal purposes (Frick and Pfaller 2013). Little researchhas so far described reproductive aspects of Cirripediaassociated with sea turtles, especially due to the samplingdifficulties, but such information is important to advance ourunderstanding of their dispersion and biogeography (Frick andPfaller 2013).

The Amphipoda recovered from the carapaces belonged tothe families Gammaridae, Hyalidae, and Caprellidae.Amphipod diversity for the Pernambuco region that has beenstudied so far is low, with these three families being restrictedto the sampling area (Sarmento et al. 2011). The occurrence ofGammaridae is more frequent in July, September, November,and December (Santos and Soares 1999). More than 90 % ofthese animals are benthic and the rest occur in pelagic habits(Barnard and Karaman 1991). The family Hyalidae was thesecond-most abundant amphipod taxon, similar to what hasbeen described by Santos and Soares (1999) for consolidatedsubstrates, with higher occurrences in January and Augustwhen compared with Gammaridae. Individuals of different

sizes were found, and females with juveniles within theircoxal cavities. This indicates that there is the potential toreproduce on the turtle carapaces, which sheds new light onthe dispersion ability for this group. The samples were takenfrom the turtle carapaces in the period between September andMarch, encompassing the period of previous recordings ofthese families along the coastline of Pernambuco (Santos andSoares 1999). The third family found was Caprellidae,previously described in association with Chelonia mydas(Loreto and Bondioli 2008), Caretta caretta (Frick et al.1998), and Lepidochelys olivacea (Vivaldo et al. 2006). Thepresent study reports, for the first time, the association of thisfamily with carapaces of the hawksbill sea turtle.

Within the phylum Annelida, Syllidae was the mostabundant family, similar to rocky shore habitats where algaeare present (Serrano et al. 2006). In Brazil, the Polychaetaspecies Syllis amica has so far been restricted to the states ofSão Paulo (SP) and Rio de Janeiro (RJ). The polychaetespecies Lumbrineris inflata occurs from intertidal zones(Camargo and Lana 1995a, b) to deeper than 100 m waterdepth (Attolini 1997) and in different sediment types (Lana1987) (e.g., rocky shores (Camargo 1993), associated withalgae, bryozoans, and corals; Nogueira 2000). Until now, thisspecies had only been found in the states RJ, Santa Catarina(SC), Espírito Santo (ES), Paraná (PR), Alagoas (AL), Bahia(BA), and SP (Amaral et al. 2010). The geographicaldistribution of Lumbrineris Magalhaensis has so far beenrestricted to the states SP, RJ, ES, and SC. This species occursbetween 0 and 100 m depth on intertidal zones (Camargo1993), sediments and continental shelves (Paiva 1990). Thespecies Nematonereis hebes , on the other hand, had only beenreported in the states of BA and SP (Amaral et al. 2010), andhas been described as endofauna associated with sandbankscreated by the reef-building polychaete Phragmatopomalapidosa (Souza 1989) and as fauna associated with coralreefs (Santa-Isabel et al. 2000). In Cuba, this species wasfound associated with marine sponges (Rullier 1974) as wellas in intertidal (Reis 1995) and infralittoral (Morgado 1980)zones. For all the polychaetes species mentioned above, thepresent study reports their occurrence in the state ofPernambuco (PE) for the first time, hence expanding theirknown geographical distribution. In addition, all thesepolychaete species are reported for the first time in associationwith sea turtle carapaces.

Acknowledgements This work was financially supported by FACEPE(Fundação de Amparo a Ciência e Tecnologia) grant (IBPG-0027-2.04/10) to the first author and by Federal University of Pernambuco for thelaboratory support and the ONG Ecoassociados for the essential help inthe field. JI is supported by a Marie Curie Intra-European Fellowshipwithin the 7th European Community Framework Programme (GrantAgreement FP7-PEOPLE-2011-IEF No 300879). The authorsacknowledge the Guest Editor, Gustavo Fonseca, and anonymousreferees for their valuable comments on earlier versions of themanuscript.

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