Frondose and Turf-Dominated Marine Habitats Support Distinct Trophic Pathways: Evidence from 15N and 13C Stable Isotope Analyses

Arquipelago - Life and Marine Sciences ISSN: 0873-4704

Frondose and turf-dominated marine habitats support distinct trophic pathways: evidence from 15N and 13C stable isotope analyses

CLÁUDIA HIPÓLITO, RAUL M.A. NETO, TARSO M.M. COSTA, MARIA A. DIONÍSIO, AFONSO C.L. PRESTES, JOSÉ M.N. AZEVEDO, GUSTAVO M. MARTINS AND ANA I. NETO

Hipólito, C., R.M.A. Neto, T.M.M. Costa, M.A. Dionísio, A.C.L. Prestes, J.M.N. Azevedo, G.M. Martins and A.I. Neto 2020. Frondose and turf-dominated marine habitats support distinct trophic pathways: evidence from 15N and 13C stable isotope analyses. Arquipelago. Life and Marine Sciences 37: 37 – 44. https://doi.org/10.25752/arq.23546

Marine vegetation plays an important structuring role, delivering key functions and services to coastal systems the extent of which depends on the foundation species and their architecture. In increasingly urbanised coastlines, turf-forming macroalgae are replacing frondose morphotypes. Trophic relationships within these systems can be studied through stable isotope analysis of the different food web compartments. In the present study, we investigated trophic pathways in two distinct macroalgal assemblages: one dominated by small brown frondose algae, and one dominated by low-lying turf-forming species. 15N and 13C isotopic signatures were determined for selected macroalgae and sedentary animals from distinct trophic levels, collected from two habitats on São Miguel Island (Azores, Portugal). In frondose habitats macroalgae appeared to make up the primary carbon source for the entire food web, whilst in turf-dominated habitats there was a decouple between macroalgae and higher trophic levels. Because canopy replacement by algal turf may affect the structure of the littoral food webs, coastal biodiversity conservation strategies should give priority to natural areas rich in canopy-forming algae.

Key words: Trophic pathways; Habitat; Macroalgae; Food web; Stable isotopes

Cláudia Hipólito1 R.M.A. Neto2, T.M.M. Costa2, M.A. Dionísio3, A.C.L. Prestes2, J.M.N. Azevedo2, G.M. Martins4 and A.I. Neto2. 1Regional Fund for Sciences and Technology, Rua do Mercado 21, 9500-326 Ponta Delgada, Portugal. 2Centre for Ecology, Evolution and Environmental Changes/Azorean Biodiversity Group (cE3c) & Faculty of Sciences and Technology, University of the Azores, Rua da Mãe de Deus, 13-A, 9500-321 Ponta Delgada, Portugal. 3MARE ULisboa, Faculdade de Ciências da Universidade de Lisboa, Campo Grande, 1749-016 Lisboa, Portugal. 4AQUAZOR, Rua da Pranchinha, 92, 9500- 331 Ponta Delgada, Portugal.

Author for Correspondence: Ana I. Neto, E-mail: [email protected]

INTRODUCTION element of coastal ecosystems (Steneck et al. 2002). Warmer temperate and/or subtropical The functioning and complexity of services communities are characterized by two algal provided by marine vegetated ecosystems depend morphotypes, a canopy type of growth composed on the assemblage and architecture of foundation by associations of two or more species of species. In temperate areas, for instance, large frondose algae, and algal turfs, which are forests of brown seaweeds are the structural complex assemblages of macroalgae with 37

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compact growth, about 5 cm in height, and well (e.g. limpets) suggesting that human exploitation developed entangled prostate axes (Lawson & may have shifted the community to an alternative Norton 1971; Price & Scott 1992; Neto 2001; stable state, and that continued exploitation of Wallenstein et al. 2009; Martins et al. 2016). limpets is the key driver allowing turfs to Canopy-forming algae modify several biotic and dominate (Martins et al. 2010). abiotic factors of rocky shore ecosystems, and are Stable isotopes of Nitrogen and Carbon have fundamental in creating and maintaining habitats been successfully used for a range of applications and their assemblages and ecological processes in marine ecology (Behringer & Butler IV 2006; (Bulleri et al. 2002; O’Brien et al. 2018). They Carvalho 2008; Gillies et al. 2012), such as are, however, considerably vulnerable to comparative studies of aquatic food chains anthropogenic disturbances, and are being (Cabana & Rasmussen 1996; Behringer & Butler increasingly replaced by turf-forming algae in IV 2006) and investigating human impact on urbanised coastlines (e.g. Benedetti-Cecchi et al. coastal ecosystems (e.g. Page et al. 2013; 2001), due to the latter’s rapid lateral vegetative Mancinelli & Vizzini 2015). Following growth (Airoldi 1998) and consequently high considerable methodological and technological rates of colonisation under high sedimentation advances in this rapidly growing field, stable and nutrient input (Worm et al. 2001). Along with isotopes have become reliable tools for studying the fact that this type of algal growth can hinder food chain structure (Peterson 1999; Phillips et al. the recruitment of its canopy-forming counterpart 2014). (Kennelly 1987), these characteristics enable turf- The Carbon-13 stable isotope may be forming algae to dominate urbanized coasts, effectively used to identify the food chain’s which poses a major threat to the biodiversity of carbon sources, as there is considerable variation those ecosystems (Gorgula & Connell 2004). in the ratio of 13C to 12C (δ13C) among producers, In the subtropical Azores archipelago, kelps and little variation once incorporated in the higher occur only in limited deep water habitats (Tittley levels of the trophic pathways (Layman et al. et al. 2001), and there are no records of seagrass 2011). The ratio of 15N to 14N (δ15N), on the other and other warm-water vegetated habitats. Instead, hand, increases predictably from one trophic level the Azorean shallow subtidal (up to 40 m depth) to the next (Post 2002), and may thus be supports extensive beds of frondose vegetation employed to infer an organism’s position in the generally dominated by associations of brown food chain. Therefore, the combined analysis of algae, namely Dictyota spp., Halopteris filicina Carbon and Nitrogen stable isotope ratios is an and, most commonly, Zonaria tournefortii (Neto effective approach to investigate trophic 2000a, 2000b, 2001; Tittley & Neto 2000). Even pathways and energy flow within marine food though these macroalgae have not traditionally webs (Lepoint et al. 2003). been designated as canopies, they can attain Here we employ stable isotopic analysis to substantial sizes (>30 cm) and effectively shadow investigate whether there are functional the understory assemblage (e.g. Martins et al. differences between two distinct habitats, one 2016). Comparatively little is known about the dominated by frondose and the other by turf- ecological and functional role of the habitats forming macroalgae, in order to better understand dominated by these smaller brown algae. Another the potential consequences of canopy replacement benthic coastal habitat in the Azores is structured on the dynamics and structure of coastal by low-lying multispecific turf-forming algae, ecosystems. such as the red seaweeds Ellisolandia elongata and Gelidium spp. (Martins et al. 2016). Thus the Azorean coastal habitats, which are increasingly MATERIALS AND METHODS subject to human pressure and activities, match the basic conditions for the dynamics of canopy Study site and sampling method replacement. For instance, the dominance of turf- This work was carried out on two distinct forming algae in the Azores intertidal was seen to shallow-water habitats in the south coast of São be related with the overexploitation of herbivores Miguel Island, Azores (Fig. 1), one dominated by 38

Trophic pathways in frondose and turf dominated habitats

Fig. 1. Map of Azores Archipelago (a), São Miguel Island (b) and sampling locations (c): two frondose-dominated (Feteiras and Lagoa, black triangles) and two turf-dominated habitats (Santa Clara and São Roque, black circles). small frondose macroalgae (Asparagopsis spp., Parmentier 2016), and carnivores by the Dictyota spp. and Halopteris spp.) and one predatory gastropod Stramonita haemastoma dominated by low-lying turf-forming red algae (Carriker 1981) and the ambush predator rockfish (corresponding to macroalgae with <5 cm height Scorpaena maderensis (La Mesa et al. 2007). forming dense mats), mostly short strands of Hermit crabs have a generalized omnivorous Ellisolandia elongata (see Martins et al. 2016 for mode of feeding on benthic particles, detritus and further description of the studied communities). moderately macroscopic material, depending, Two sites were chosen for each habitat, similar in therefore on a reasonable amount of scavenging depth (5-15 m), seawater temperature, wave (Kunze & Anderson 1979; Schembri 1982). S. exposure and other physical factors. The selection lurida maintains farms of turf-forming algae of species (biotic entities) for this study took into (personal observation), and like all the members consideration two main criteria; their sedentary of the Stegastinae subfamily feeds upon the algae, life style, which ensured habitat representation; as well as on the detritus and invertebrates caught and their abundance in both habitats, which up in them (Frédérich & Parmentier 2016). ensured trophic level representation and Macroalgae were scraped off from three facilitated specimen collection. Herbivores were haphazardly-selected 0.15 x 0.15 m replicate represented by the sea urchin Sphaerechinus quadrats into fine mesh net bags. Three granularis (Verlaque 1981), omnivores by the specimens of each invertebrate and fish species hermit crab Calcinus tubularis (Kunze & were collected, by hand and spearfishing, Anderson 1979; Schembri 1982) and the Canary respectively. damselfish Similiparma lurida (Frédérich & Sampling took place in May 2014, in a short 4-

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day period (9th – 13th) in order to reduce 3-way mixed model analysis of variance with the temporal variations in isotopic composition following factors: habitat (2 levels, fixed), site (2 (Heminga & Mateo 1996; Jennings et al. 1997). levels, random and nested within habitat) and Samples were stored on ice immediately after biotic entities (algal morphotypes and animal arrival on the boat and no later than 30 minutes species; 6 levels, fixed). Prior to analysis, after collection. Cochran's test was used to assess heterogeneity of At the laboratory, algae were gently rinsed with variances and transformations were applied when tap water in order to remove all visible necessary. When required, a posteriori Student- macrofauna and detrital fragments, and oven- Newman-Keuls (SNK) tests were used. All dried at 60ºC until constant weight (about 48 h). analyses were run using GMAV5 (University of Following the instructions of the certificated Sydney). At one of the sites (Santa Clara) only MARINNOVA Laboratories of Porto, Portugal two (instead of three) replicates of S. haemastoma where the stable isotope ratios were determined, were available. In order to keep the analysis sea urchin gonads, fish muscle and skin samples, balanced, the missing value was replaced by the and whole gastropods and crustaceans were mean of the other two replicates, and one degree frozen, accommodated, and sent for analysis. The of freedom was subtracted from the residual. isotope analysis results were expressed relative to the primary patterns, air N2 for nitrogen and the Peedee belemnite marine limestone (PDB) RESULTS standard for carbon. 15N:14N and 13C:12C ratios were calculated following Wieser & Schwieters Although no δ13C differences were observed (2005) and Bahlmann et al. (2010). between habitats, both the differences between biotic entities and the interaction of habitat and Data analysis biotic entities were significant (P<0.001 and The 15N and 13C isotopic compositions of P<0.01 respectively, Table 1) and are illustrated consumers and producers on frondose- and turf- in Fig 2. Although the signatures of S. dominated communities were compared using a maderensis, S. haemastoma and C. tubularis

Fig. 2 – Relationship between δ13C and δ15N (‰) of producers and consumers in frondose and turf-dominated communities.

Trophic pathways in frondose and turf dominated habitats show no variation, those of the macroalgae and S. As for δ15N, neither the difference between granularis were higher in the frondose habitat, habitats nor the interaction of habitat and biotic where they aligned with the previously entities was significant, but the difference enumerated entities, then in the turf habitat, between biotic entities was highly significant where they matched that of S. lurida. The δ13C (P<0.001, Table 1), which is clearly displayed in signature of the latter varied in the opposite Fig 2. Macroalgae exhibited the lowest δ15N direction, with higher values in turf than in signature, just below that of the herbivore S. frondose habitats, where it formed a separate granularis, which was followed by those of the group from the remainder of the biotic entities omnivore C. tubularis and the carnivores S. (Fig 2). SNK tests confirmed the significance of haemastoma and S. maderensis. The omnivore S. entity isotopic variations among habitats, and lurida had on average the highest δ15N values of yielded two isotopic groups for each habitat, all the biotic entities. This ordering was separating S. lurida from all other biotic entities confirmed by SNK analysis of δ15N among biotic in the frondose habitat, and grouping S. lurida, S. entities (Table 1). granularis and macroalgae apart from the remaining entities in the turf habitat (Table 1).

Table 1 - ANOVA testing the effects of habitat (frondose- versus turf-dominated) on the 15N and 13C isotopic composition of biotic entities (algal morphotypes and animal species). Significant differences noted in bolt. SNK pair-wise tests assessing the effects of habitat on the 13C isotopic composition of each biotic entity, and comparing the δ15N of the biotic entities.

δ13C δ15N Source df MS F P MS F P F-ratio Habitat 1 5.01 1.58 0.34 0.68 0.35 0.61 Site (Habitat) Site (Habitat) 2 3.17 4.46 0.02 1.95 13.20 <0.001 Residual Site (Habitat) x Biotic Biotic entities 5 39.62 32.75 <0.001 87.13 337.72 <0.001 entities Habitat x Biotic Site (Habitat) x Biotic 5 10.77 8.90 <0.01 0.21 0.80 0.57 entities entities Site (Habitat) x 10 1.21 1.70 0.11 0.26 1.75 0.10 Residual Biotic entities

Residual 47 0.71 0.15 Cochran´s test C = 0.21 (Not significant) C = 0.32 (P<0.01) δ13C δ15N Among habitats within biotic entities Among biotic entities S. maderensis Frondose = Turf S. lurida > S. maderensis > S. haemastoma > C. S. granularis Frondose > Turf tubularis > S. granularis > Algae S. lurida Frondose < Turf C. tubularis Frondose = Turf S. haemastoma Frondose = Turf Algae Frondose > Turf SNK Among biotic entities within habitats

Frondose habitat:

S. lurida < all other biotic entities Turf habitat: S. maderensis = S. haemastoma = C. tubularis

> S. granularis = S. lurida = Algae

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DISCUSSION ACKNOWLEDGMENTS

The significant macroalgal δ13C variation This research was supported by the European between habitats reflects their different species Commission BEST Preparatory Action, under the composition. The 15N isotopic signature of the sea project “ECOSUBVEG – Changes in submersed urchin is consistent with its strictly herbivorous vegetation: assessing loss in ecosystems services diet, and its 13C isotopic signature suggest that it from frondose to depauperate systems dominated feeds on the dominant macroalgal assemblage in by opportunistic vegetation”, ref. each habitat. In both habitats, the omnivore 07.032700/2012/635752/SUB/B2. The research damselfish S. lurida exhibited a 13C isotopic was also partially supported by Portuguese signature similar to that of the turf macroalgae, National Funds, through FCT – Fundação para a which is consistent with its diet of turf-forming Ciência e a Tecnologia, within the projects algae. Surprisingly, it showed the highest δ15N UID/BIA/00329/2013, 2015 - 2018, values, above even those of the carnivorous UID/BIA/00329/2019 and UID/BIA/00329/2020- rockfishes, with trophic shifts as high as +5.9‰. 2023. Logistic support was also provided by This apparently higher 15N accumulation rate may CIRN/UAc (Centre of natural Resources of arise from differential digestion or fractionation University of the Azores) and by CVARG during assimilation and metabolic processes (Centro de Vulcanologia e Avaliação de Riscos (McCutchan et al. 2003). Geológicos). GMM was supported by a post- The hermit crabs and the carnivorous doctoral grant awarded by FCT gastropods and fish exhibited no significant (SFRH/BDP/63040/2009 and variation in δ 13C or δ15N across habitats. In SFRH/BDP/108114/2015). Authors are grateful frondose habitats the 13C isotopic composition to Ruben Couto, João Faria, Nuno Álvaro, Marc was similar among all those species and the local Fernandez, Isadora Moniz, Eva Cacabelos, Carles macroalgae, suggesting that the latter provide the Mir, Anna Lloveras, Virginie Leyendecker, main carbon source for the remainder of the Jessica Coulon, Ana Sofia Carreiro, Filipe benthic food web. However, in turf-dominated Parreira, Rita Patarra and Emanuel Xavier who habitats there was a clear decouple between helped in the field and laboratory work. Thanks to macroalgae/sea urchins and the three species Nuno Álvaro for his assistance on map provision. mentioned above. This implies that the higher We appreciate the reviewer’s help in improving trophic levels in these habitats rely on exogenous the paper. carbon sources, possibly from the adjacent frondose habitats. It should be noted that the suspension- and deposit-feeding pathways were REFERENCES not considered in this study, and that sampling the particulate organic matter pool (POM) could Airoldi, L. 1998. Roles of disturbance, sediment stress, improve these results and explain part of the and substratum retention on spatial dominance in algal turf. Ecology 79: 2759–2770. observed decoupling. https://doi.org/10.1890/0012- These findings add to literature indicating that 9658(1998)079[2759:RODSSA]2.0.CO;2 habitats dominated by frondose macroalgae play an Bahlmann, E., S.M. Bernasconi, S. Bouillon, M. important ecological role in coastal ecosystems Houtekamer, M. Korntheuer, F. Langenberg, C. (Benedetti-Cecchi et al. 2001; Gorgula & Connell Mayr, M. Metzke, J.J. Middelburg, B. Nagel, U. 2004; Martins et al. 2016; Smale et al. 2013). Their Struck, M. Voß and K.C. Emeis 2010. Performance fundamental contribution to the energy flows on the evaluation of nitrogen isotope ratio determination food webs is not matched by that of the increasingly in marine and lacustrine sediments: An inter- dominant turf communities. Therefore, the current laboratory comparison. Organic Geochemistry 41: 3–12. trends of reduction of algal canopies pose a threat to https://doi.org/10.1016/j.orggeochem.2009.05.008 coastal biodiversity, which should be taken into Behringer, D.C. and M.J. Butler IV 2006. Stable consideration when devising conservation strategies. isotope analysis of production and trophic

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