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Home , Alpheus armatus, Ancylomenes, Ancylomenes pedersoni, Condylactis, Condylactis gigantea, Fungiidae

Marine Biodiversity (2019) 49:2609–2620 https://doi.org/10.1007/s12526-019-00993-5

ORIGINAL PAPER

Comparative diversity of anemone-associated fishes and decapod in a Belizean reef and seagrass system

Rohan M. Brooker1,2 & William E. Feeney3,4 & Tiffany L. Sih5,6 & Maud. C. O. Ferrari7 & Douglas P. Chivers2

Received: 16 April 2019 /Revised: 5 July 2019 /Accepted: 12 July 2019/Published online: 19 August 2019 # Senckenberg Gesellschaft für Naturforschung 2019

Abstract Within tropical coastal habitats such as coral reefs and seagrass meadows, sea anemones (Actiniaria) provide microhabitats for a diverse range of fauna. However, the mechanisms that enable these interactions, and how actiniarian diversity and abundance mediates associate assemblages, remains poorly understood. Here, we compared richness and abundance with that of their associated decapod crustaceans and teleost fishes across adjacent and seagrass habitats at Carrie Bow Cay, Belize. At least 16 decapod and seven fish species were associated with anemones across both habitats, including several previously undocumented associations. While overall anemone-associate richness did not differ between habitats, seagrass anemones had the greatest mean abundance and diversity of both decapod and fish associates. This suggests that the importance of anemones as microhabitat reflected broader benthic complexity and shelter availability, with species aggregating on sea anemones when access to alternative shelter, such as , was limited. Patterns of associate distributions on anemones were also highly structured, in terms of both associate and anemone species, with these patterns likely reflecting a combination of associate specialization, intraspecific competition, and anemone morphology and toxicity. The diverse multi-species associate complexes observed suggest that sea anemones provide an important refuge for both specialized and generalist species and so have the potential to increase faunal diversity and abundance within tropical coastal habitats.

Keywords Actiniaria . Sea anemone . Caribbean . Habitat complexity . Predation risk

Introduction

Marine sessile are common ecosystem engi- Communicated by B. W. Hoeksema neers, providing microhabitat for complex assemblages of as- sociated species (Jones et al. 1994; Gutiérrez et al. 2003; Bell * Rohan M. Brooker 2008; Bos and Hoeksema 2015). With most marine ecosys- [email protected] tems now threatened by climate change and overexploitation, the global contribution of sessile invertebrates to broader hab- 1 Centre for Integrative Ecology, School of Life and Environmental itat quality has received increasing recognition, with substan- Sciences, Deakin University, Geelong, Victoria, Australia tial effort devoted to determining their ecosystem role, 2 Department of Biology, University of Saskatchewan, preventing their decline, and facilitating regeneration and re- Saskatoon, Saskatchewan, Canada silience (Beck et al. 2011; Gillies et al. 2018). Sessile inverte- 3 Environmental Futures Research Institute, Griffith University, brates can create habitat heterogeneity and structural complex- Brisbane, Australia ity that may otherwise be limited (Tews et al. 2004); for ex- 4 School of Biological Sciences, University of Queensland, ample, the occurrence of bivalves on soft sediment can affect Brisbane, Queensland, Australia surrounding biodiversity (McLeod et al. 2014). Therefore, the 5 College of Science and Engineering, James Cook University, relative availability of microhabitat-forming invertebrates can Townsville, Queensland, Australia facilitate overall community composition and biodiversity, as 6 ARC Centre of Excellence for Coral Reef Studies, James Cook well as the distribution, abundance, and population structure University, Townsville, Queensland, Australia of associated fauna (Jones et al. 1994). For associated and 7 Department of Biomedical Sciences, WCVM, University of symbiotic species, sessile invertebrates can influence key Saskatchewan, Saskatoon, Saskatchewan, Canada 2610 Mar Biodiv (2019) 49:2609–2620 factors such as trophic dynamics, mediating predator-prey in- 2018). However, individuals or colonies are generally stable teractions by providing shelter, limiting sensory acuity or enough to support the reproductive cycle of associates, which movement, or reducing the likelihood of attack (Lima and are usually also short-lived (O’Reilly et al. 2018). Associative Dill 1990). hosts can also increase associate fit- relationships range from facultative to obligate, often varying ness, providing food resources and protection from abiotic with ontogeny (Baeza and Stotz 2001;Feeneyetal.2019)and extremes and mediating exploitative or interference competi- reflecting the degree of reliance on anemones for food or shelter. tion (Almany 2004; McKeon and O’Donnell 2015). However, The most specialized symbionts, such as the Amphiprion and while they can play a critical role, these invertebrates are usu- Premnas anemonefishes, normally associate with specific anem- ally themselves specialized to specific habitats or abiotic pa- one species and have evolved a suite of innate and acclimation rameters. As such, many are at risk from environmental mechanisms that make them impervious to their host’s feeding change, habitat loss, and exploitation, compromising their and defensive responses (Fautin 1991;Crawford1992;Mebs ecological function and ability to support associated species 2009; Feeney and Brooker 2016). While facultative species usu- (Duke et al. 2007; Hughes et al. 2017). It is therefore essential ally lack these specializations, they could theoretically remain that we quantify the relationship between microhabitat- capable of associating with anemones by avoiding the stinging forming invertebrates and their associated fauna, to identify tentacles or associating with less aggressive or toxic hosts. their ecosystem role, how these interactions are mediated, and Patterns of microhabitat use, host specificity, and distribution the potential impacts of their decline on future biodiversity. on the anemone may be indicative of niche partitioning by as- On tropical reefs, the most ubiquitous ecosystem engineers sociates, reducing competition and increasing diversity are scleractinian corals, with colonial and solitary species (Robertson and Polunin 1981;ElliotandMariscal2001;Khan supporting complex micro- and macrofaunal assemblages et al. 2003;Campetal.2016). Irrespective of the degree of (Stella et al. 2011;Hoeksemaetal.2012; Coker et al. 2014) reliance, relationships between anemones and associates appear and declines associated with decreased biodiversity, habitat to primarily evolve in response to predation risk, with anemones complexity, and resilience (Hughes et al. 2018). However, a providing a protective refuge to small-bodied species or individ- range of other invertebrates, such as , bivalves, and uals within species (Huebner et al. 2012; Feeney et al. 2019). soft corals, also produce microhabitat that can support distinc- However, these interactions are mostly mutualistic, with various tive species assemblages, both on reefs and in adjacent sys- fish and invertebrate associates known to defend their host from tems such as seagrass meadows (Goh et al. 1999;Wulff2006; potential predators or increase aeration and nutrient availability, Neo et al. 2015). While the ecological role of non- leading to greater anemone growth, survival, and reproductive scleractinian invertebrates is often overlooked, their role as rates (Spotte 1996; Holbrook and Schmitt 2005; Porat and microhabitat may become increasingly important if global Chadwick-Furman 2004; Roopen and Chadwick 2009; coral cover continues to decline (Bell et al. 2013). Szczebak et al. 2013; McCammon and Brooks 2014). While In shallow tropical seas worldwide, sea anemones the underlying ecology of most actiniarian-associate relation- (Actiniaria) (herein, anemones) are common, often conspicuous ships is poorly understood, especially with regard to facultative components of benthic communities (Fautin et al. 2013). interactions, it is clear that anemones provide an important mi- Generally consisting of a solitary , the individuals of most crohabitat, and so variations in anemone abundance or diversity species of anemone are highly site attached, affixing themselves could have strong effects on community structure. to the substrate via their pedal disc and extending into the water While tropical anemones can support complex faunal as- column. From this position, the anemone uses its tentacles to semblages, increasing biodiversity and facilitating ecosystem feed, either autotrophically via Symbiodiniaceae and/or hetero- processes such as cleaning interactions (Huebner and trophically using specialized nematocyst cells to capture passing Chadwick 2012; Titus et al. 2015; Colombara et al. 2017), organic material. Anemones range from under 1 mm to over 1 m few studies have examined how broader habitat characteristics in diameter, with some species forming dense aggregations and and anemone morphology affect associate richness and abun- patterns of high local abundance (Colombara et al. 2017;Dixon dance, particularly with regard to facultative associates et al. 2017; Titus et al. 2017a). As such, they can represent an (Huebner et al. 2012). With this in mind, we quantified the important driver of habitat complexity. diversity and abundance of two major groups of anemone- Despite the nematocysts of many actiniarians being highly associated taxa, decapod crustaceans and teleost fishes, across toxic, capable of quickly incapacitating prey, anemones support two adjacent habitat types, coral reef and seagrass meadow, in a variety of associated , including numerous fishes and Belize. These sites were chosen as, while they are largely decapod crustaceans (Chadwick et al. 2008; Briones-Fourzán subject to the same environmental and hydrodynamic condi- et al. 2012; Colombara et al. 2017;Feeneyetal.2019). tions, they contrast with regard to habitat characteristics, with Anemone populations can be somewhat ephemeral in nature, the topographically complex, highly heterogeneous reef hab- exhibiting rapid recruitment, growth, and turnover of individuals itat markedly different to the structurally simple, largely ho- (Dixon et al. 2017;O’Reilly and Chadwick 2017;O’Reilly et al. mogeneous seagrass meadow. Specifically, we examined (a) if Mar Biodiv (2019) 49:2609–2620 2611 anemone species composition differed between habitat types was conducted. For both reef and seagrass habitats, 100 indi- and (b) if anemone-associated fish or decapod vidual anemones were surveyed. All surveys took place dur- abundance or richness differed between reef- and seagrass- ing daylight hours, between 0900 and 1600. Anemones were dwelling anemones. Finally, we examined (c) whether associ- haphazardly selected by the observer swimming over an area ates displayed consistent patterns of distribution between and of habitat on SCUBA in a grid pattern and recording the first within their host species. anemones encountered, ensuring no selective bias and that they were not sampled repeatedly. For each individual survey, anemone species, anemone size, attachment substrate, and Materials and methods water depth were recorded. Anemone size was estimated by measuring the maximum length and width across the tentacle Study site and species crown and using this to calculate area (Dixon et al. 2017; O’Reilly et al. 2018). All associated decapod crustaceans This study was conducted on the shallow coral reef and adja- and teleost fishes observed on each anemone were then re- cent seagrass habitats surrounding the Smithsonian Carrie corded, with these faunal groups selected as they occur in both Bow Cay Research Station, Belize (16° 48′ 9.8316″ N, 88° habitat types, commonly associate with anemones, and can be 4′ 54.8148″ W) in January–February 2018. These habitats are generally be distinguished to or species in the field home to a wide range of anemones, fishes, and decapod crus- based on visual assessment. Where identification was uncer- taceans, many of which occur throughout the Central tain, photographs were taken for subsequent examination. Caribbean (Harborne 2000; Briones-Fourzán et al. 2012). Each associated individual was identified to the lowest taxo- Taxonomic information and genus or species authorities for nomic rank possible (species, species complex, or superfami- all referenced organisms are outlined in Table 1. ly) and its location on the host when first observed noted. Status of relationship with anemones (obligate or facultative) was determined from published records (i.e. Briones-Fourzán Surveys of anemone distribution, species et al. 2012; Bos and Hoeksema 2015; Colombara et al. 2017; composition, and habitat characteristics Feeney et al. 2019). Taxonomic validity was confirmed using the World Register of Marine Species (WoRMS Editorial To determine whether the abundance or composition of anem- Board 2019). Locations were classed as either in contact with one species differed between coral reef and seagrass habitats, the tentacles on or around the oral disc (T—tentacle), not in we conducted a series of transect surveys. Thirty 25-m tran- contact with the tentacles but on the column beneath the ten- sects were run in each habitat type, in water between 1 and 3 m tacles (C—column), or underneath the anemone on the sub- depth perpendicular to the shoreline. Care was taken to ensure strate immediately surrounding the pedal disc (B—base). transects did not overlap, with a minimum of 5-m distance To compare the overall assemblage of anemone-associates between transects. For each transect, all anemones within in each habitat, assemblage compositional data was investi- 1 m of either side of the transect tape were recorded to species gated with a non-metric multidimensional scaling (nMDS). level (Humann et al. 2013), along with the substrate type that Records of anemones with no associates were removed from it was directly attached to. Substrates were classified as sand, the analyses, leaving 164 individuals (of 200 total) with com- bare rubble, dead coral, live coral, or seagrass. In addition, the bined fish and decapod abundance data. Associated species overall benthic composition along each transect was quanti- that were only observed once (singletons) were removed from fied by recording the habitat type at each meter mark using the the analysis (two fish species, Tigrigobius bifasciatum and same habitat categories as above. Differences in the propor- Stegastes leucostictus), leaving 20 distinct taxonomic groups tion of substrate categories between coral reef and seagrass consisting of 16 decapods and four fishes. In addition to dis- habitats were analyzed using a MANOVA on arcsine- tinct species, this included two decapod species complexes transformed proportional data. A second MANOVA test was ( armatus complex and Petrolisthes galathinus com- used to determine if the total number of anemones differed plex) and a grouped “hermit ” category consisting of all among substrate categories. All statistics were performed paguroid individuals observed. Due to the highly variable using R (version 3.5). abundance of associates, data was 4th-root transformed and scaled with a Wisconsin double standardization with a Surveys of anemone-associated fishes and decapod Hellinger distance transformation (function decostand, pack- crustaceans age Vegan). This standardization adjusted for rarity and horse- shoe effects where there may be many shared absences among To determine if the distribution, abundance, and diversity of samples. nMDS were performed based on Bray-Curtis dissim- anemone-associated fishes and decapod crustaceans differed ilarity (function metaMDS) with sites divided among the two between habitats or anemone species, a survey of anemones habitat types (“reef” and “seagrass”) and individual associate 2612 Mar Biodiv (2019) 49:2609–2620

Table 1 Taxonomic information and genus or species authorities Class Order Species Authority for all organisms referred to in this manuscript. Authorities were Actiniaria Actinoporus elegans Duchassaing, 1850 taken from the Word Register of (Le Sueur, 1817) Marine Species (WoRMS; www. gigantea (Weinland, 1860) marinespecies.org) Laviactis lucida (Duchassaing de Fombressin & Michelotti, 1860) Lebrunia neglecta Duchassaing & Michelotti, 1860 (Ellis, 1768) florida Duchassaing & Michelotti, 1860 Alpheus armatus Rathbun, 1901 Alpheus immaculatus Knowlton & Keller, 1983 Alpheus polystictus Knowlton & Keller, 1985 pedersoni (Chace, 1958) Amphithrax pilosus (Rathbun, 1892) Clibanarius tricolor (Gibbes, 1850) Gnathophyllum americanum Guérin-Méneville, 1855 (in Guérin-Méneville, 1855–1856) Lysmata ankeri Rhyne & Lin, 2006 Mithraculus cinctimanus Stimpson, 1860 Mithraculus forceps A. Milne-Edwards, 1875 (Lamarck, 1818) rathbunae Schmitt, 1924 Periclimenes yucatanicus (Ives, 1891) Petrolisthes caribensis Werding, 1983 Petrolisthes galathinus (Bosc, 1802) scutellatus Rankin, 1898 seticornis (Herbst, 1788) amboinensis (De Man, 1888) Thor manningi Chace, 1972 Perciformes Halichoeres poeyi (Steindachner, 1867) nuchipinnis (Quoy & Gaimard, 1824) macropus (Poey, 1868) Stegastes leucostictus (Müller & Troschel, 1848) Thalassoma bifasciatum (Bloch, 1791) Tigrigobius gemmatus (Ginsburg, 1939) Scorpaeniformes Scorpaena plumieri Bloch, 1789 Littorinimorpha Lobatus gigas (Linnaeus, 1758) Magnoliopsida Alismatales Syringodium filiforme Kützing, 1860 K.D.Koenig, 1805

scores labeled. To test the relationship between habitat vari- among fish and decapod crustacean abundance or richness. ables and anemone-associated assemblages, transformed hab- However, decapod crustacean abundance was over-dispersed, itat variables were fitted on to the nMDS ordination (function while decapod crustacean richness and both fish metrics were envfit, permutations = 1000, p <0.05). under-dispersed. For evaluating decapod crustacean richness, Data on associate richness and abundance on individual fish species richness, and fish abundance, glm used a Poisson anemones in each habitat was analyzed with generalized linear regression. A negative binomial model, which can be used models (glm). Due to highly variable count data, initial steps with over-dispersed count data, was used for decapod crusta- compared multiple glm to confirm the type of glm best suited cean abundance data. Models compared varying levels of to this analysis and that data conformed to the assumptions of complexity, from the simplest including just the factor that glm type. There was little evidence of zero inflation Habitat (reef or seagrass) to models with Habitat and the other Mar Biodiv (2019) 49:2609–2620 2613 factors (anemone species, anemone size, depth, and attach- (Table 2). In addition, a seventh fish species, Labrisomus ment substrate). Models were then compared with Akaike nuchipinnis, was also seen within the tentacles of an individual information criterion (AIC) and log-likelihood values. of C. gigantea within the seagrass outside of these surveys. While the Alpheus individuals could not be identified to species from field observations, they belonged to the Alpheus armatus Results complex, with three known species occurring in the region: A. armatus, A. immaculatus,andA. polystictus (Hurt et al. Surveys of anemone distribution, species 2013). Similarly, the Petrolisthes individuals observed were a composition, and habitat characteristics member of the Petrolisthes galathinus complex, most likely ei- ther P. galathinus or P. caribensis (Hiller et al. 2006). Of the Anemones were widely distributed across both coral reef and associate species observed, was only seagrass habitats, although mean abundance was higher on the observed on the reef, while Gnathophyllum americanum, reef, with an average of 4.97 ± 0.97 SE anemones per 50 m2 Halichoeres poeyi, Petrolisthes galathinus complex, Scorpaena reef transect versus 1.87 ± 0.35 SE anemones per 50 m2 plumieri, S. leucostictus, Stenopus scutellatus, Thor manningi, seagrass transect. A total of five actiniarian species were ob- and T. gemmatus were only recorded within the seagrass. served: Stichodactyla helianthus, Bartholomea annulata, However, overall associate diversity did not significantly differ Lebrunia neglecta, , and Actinoporus between habitat types, as seagrass anemone assemblages fell elegans.However,oftheseL. neglecta and A. elegans were within the multidimensional space of the reef anemone assem- only recorded within the reef and C. gigantea only within the blages (nMDS R2 = 0.992, stress = 0.10) (Fig. 1). While overall seagrass. Stichodactyla helianthus was by far the most com- associate diversity did not differ, and no significant difference mon actiniarian observed on transects in both habitats ac- was found in size (area) of anemones between habitats (lm, counting for 94.6% (141 of 149) of all reef anemones and p = 0.47), associate richness was significantly higher on seagrass 85.7% (48 of 56) of all seagrass anemones, frequently with anemones than on reef anemones, for both decapod crustaceans clustered distributions. Underlying habitat characteristics var- (Poisson glm p < 0.001) and fishes (Poisson glm p < 0.05) ied substantially between reef and seagrass (MANOVA), with (Fig. 2). A similar trend was seen for abundance, with a higher differing proportions of seagrass, rock, coral, rubble, sand, abundance of associates on seagrass anemones for both decapod and among the two habitat types (Pillai = 0.99, F crustaceans (2.7 more decapods, NB glm p < 0.001) and fishes

6,53 =1062.8,p < 0.001). The reef was highly heterogeneous (1.9 more fish, Poisson glm p <0.05)(Fig. 2). Differences in with transects consisting of large sand patches (41.79 ± decapod crustacean abundance were primarily driven by the 4.30%), bare rubble (26.50 ± 3.91%), dead coral (21.49 ± multi-species assemblage of hermit which formed large 3.22%), live coral (10.05 ± 2.41%), and sponges (0.18 ± aggregations, of up to 400 individuals, on and immediately sur- 0.12%). In contrast, the seagrass habitat was homogeneous, rounding the base of seagrass anemones, primarily S. helianthus consisting almost entirely of Thalassia testudinum and (Fig. 2). While the diversity of paguroid species that contributed Syringodium filiforme sea grass growing on rubble (99.00 ± to these assemblages was not determined, they did include 0.74%) interspersed with small patches of bare sand (1.00 ± Clibanarius tricolor as reported by Colombara et al. (2017). 0.74%). While scarce enough that they were not recorded While these hermit crabs were present on the reef, they did not during transects, several small patch reefs under 1 m in diam- reach aggregations of more than 10 individuals per host eter were scattered within the seagrass meadow areas. (Table 2). However, even when hermit crabs are excluded, deca- Likewise, the number of total anemones differed between pod abundance remained higher on the seagrass anemones substrate types (Pillai = 0.25, F 6,53 =2.9,p < 0.01), with indi- (p < 0.01). Many associates displayed consistent patterns of dis- viduals seldom found on sand or other loose substrate. tribution on anemones, being either associated with the tentacles and oral disc, base, or the substrate directly next to the anemone Surveys of anemone-associated fishes and decapod (Table 3). In addition to decapod crustaceans and fishes, brittle crustaceans stars (Ophiuroidea) were also occasionally associated with anem- ones, although these were not quantified or identified to species. Haphazard selection of anemones for associate surveys indicated a greater abundance of rarer anemone species than suggested by transects alone with one additional anemone, Laviactis lucida, Discussion recorded on the reef during observations (Table 2). This is likely due to the frequently clustered distribution of S. helianthus,es- This study demonstrates the importance of anemones as habitat pecially within the reef. Anemones represented an important within both coral reef and seagrass communities, providing a source of microhabitat in both reef and seagrass, with a total of source of structure and shelter for a range of small decapods and 16 groups of decapod crustaceans and six species of fish recorded fishes. While the general patterns seen at Carrie Bow Cay are 2614

Table 2 Diversity of anemone-associated decapod crustaceans and fishes from surveys in seagrass and reef habitat in Belize. Anemone species are listed across the horizontal axis, with each anemone split into two categories: reef and seagrass. “Relationship” indicates type of interaction (obligate or facultative) with anemones. Number in brackets is the total of each species surveyed in each habitat out of 100. Within each box, the first number is the number of sampled anemones on which that associate was observed. The following number in brackets is the range of group sizes observed

Anemone species

Stichodactyla helianthus Condylactis gigantea Bartholomea annulata Laviactis lucida Lebrunia neglecta Actinoporus elegans

Type Species Relationship Reef (35) Grass (86) Reef (2) Grass (8) Reef (25) Grass (6) Reef (11) Grass (0) Reef (25) Grass (0) Reef (2) Grass (0)

Decapod spp. O17(1–4) 77 (1–6) – 3(1–2) ––3(1–2) – 1(1) ––– Periclimenes yucatanicus O –––1(1) ––1(1) – 1(1) ––– Ancylomenes pedersoni O ––––13 (1–5) – 1(1) – –––– Alpheus armatus complex O ––––8(2) 5(1–2) –– –– – – F17(1–8) 21 (1–4) 2 (1–2) – 2(1–2) – 4(1–2) – 3(1) ––– Thor manningi F – 9(1–4) – 1(1) – – –– –– – – Lysmata ankeri F1(2)3(1–7) – – – – –– –– – – Stenopus scutellatus F – 1(2) – – – – –– –– – – Gnathophyllum americanum F – 1(2) – – – – –– –– – – Mithraculus cinctimanus O 4 (1) 1 (1) – 1(1) ––1(1) – –––– Mithraculus sculptus F2(1)41(1–8) – 3(1–2) – – –– –– – – Mithraculus forceps F1(1)2(1–2) – 1(1) – – –– –– – – Amphithrax pilosus F8(1–3) 7 (1–3) ––––1(1) – –––– F – 11 (1–2) ––4(1–2) 1 (1) –– 4(1) ––– Petrolisthes galathinus complex F – 5(1–2) – – – – –– –– – – Hermit crab spp. F 7 (1–10) 71 (1–400) – 4(3–30) – 3(8–15) –– 1(1) ––– Fish spp. Malacoctenus macropus F – 2(1) – 3(1–2) –––– 1(1) ––– Thalassoma bifasciatum F –––1(1) –––– 1(1) ––– Halichoeres poeyi F –––2(1) – – –– –– – – a idv(09 49:2609 (2019) Biodiv Mar Tigrigobius gemmatus F – 1(1) – – – – –– –– – – Stegastes leucostictus F – 1(1) – – – – –– –– – – Scorpaena plumieri F – 1(1) – 1(1) – – –– –– – – – 2620 Mar Biodiv (2019) 49:2609–2620 2615

Habitat Reef Seagrass

Anemone Sp. 4 Bartholomea annulata Condylactis gigantea Lebrunia neglecta 1 Laviactis lucida Stichodactyla helianthus

2 NMDS1 2 3 4 5

6 7 8 9 10 11 0 12 14 13 15 16 17

18 20 19

-4 -2 0 NMDS2 Fig. 1 Species compositions of anemone-associated assemblages on reef bifasciatum,(4)Halichoeres poeyi,(5)Malacoctenus macropus,(6) and seagrass habitats in Belize (non-metric multidimensional scaling of Gnathophyllum americanum,(7)Thor mannigi,(8)Scorpaena plumieri, fourth-root transformed abundance data of decapod crustaceans and fish- (9) Mithraculus sculptus, (10) hermit crab spp., (11) Periclimenes es). Points represent where anemone-associated assemblages are posi- rathbunae,(12)Stenorhynchus seticornis, (13) Petrolisthes galathinus tioned in the multidimensional space based on what species they do or complex, (14) Alpheus armatus complex, (15) Lysmata ankeri,(16) do not share. Numbers correspond to position of associate species: (1) Stenopus scutellatus, (17) Mithraculus cinctimanus, (18) Amphithrax Periclimenes yucatanicus,(2)Mithraculus forceps,(3)Thalassoma pilosus, (19) Thor amboinensis, (20) Ancylomenes pedersoni broadly comparable to what has been reported elsewhere in the reef substrate, with structural complexity facilitating the estab- Caribbean, with most anemones and associates observed widely lishment of S. helianthus aggregations and providing the numer- distributed throughout this area (Harborne 2000; Silbiger and ous crevices, holes, and overhangs where the reef-only anem- Childress 2008; Briones-Fourzán et al. 2012; González-Muñoz ones were found. While Bartholomea annulata is also a crevice- et al. 2012; Colombara et al. 2017), these results highlight the dwelling anemone similar to L. lucida, this species frequently diversity of obligate and, in particular, facultative species that occupied empty queen conch (Lobatus gigas) shells scattered associate with anemones within this system. While a total of six within the seagrass site, permitting its spread into this habitat. anemone species were recorded (five of which possessed asso- Despite the differences in habitat structure, analysis of overall ciates), anemone assemblages in both the reef and seagrass hab- associate richness indicated that this was not significantly differ- itats were dominated by the sun anemone, Stichodactyla ent between habitats, with the seagrass assemblage nested within helianthus, with high localized densities that likely result from the reef assemblage. Nonetheless, several associates were only clonal replication (Colombara et al. 2017). The high abundance observed in one of the two habitats; while it is possible that these of S. helianthus may also reflect the shallow nature of the study differences reflect variations in the spatial distribution of associ- sites, with this anemone generally found at depths between 0.5 ate species, the low rate at which they were observed means this and 1.5 m (Briones-Fourzán et al. 2012). Although anemones pattern may simply be due to scarcity. While comparatively rare, were common benthic components within both habitats, overall other non-scleractinian anthozoans also provide a source of hab- abundance was higher on the reef, with this habitat also home to itat, with a single Periclimenes rathbunae observed within the three species only observed there: Laviactis lucida, Lebrunia oral disc of the corallimorpharian, Ricordea florida, on the reef. neglecta,andActinoporus elegans. Greater abundance and di- This unusual interaction has currently only been reported from versity are likely due to the rugosity and heterogeneity of the Belize (Ritson-Williams and Paul 2007). 2616 Mar Biodiv (2019) 49:2609–2620

40 a Decapod crustaceans Coral reef greater relative microhabitat value, leading facultative deca- 35 Seagrass pod crustaceans and fishes to associate with them at greater frequency. 30 Decapod crustaceans were the most frequent and abundant 25 group of associates and were generally consistent in where they were located on their host, which may allow a greater 20 number of individuals to occupy an individual anemone by 15 limiting inter- or intraspecific competition for space and re- sources (Chesson 2000; Hayes and Trimm 2008). The space 10 partitioning of individuals appeared to reflect the degree of 5 specialization towards anemones as microhabitat, with obli- gate anemone symbionts such as the palaemonid , 0 P. rathbunae, alpheid , Alpheus armatus complex, Abundance Abundance Richness (hermit crabs) (other) (total) and majid crab, Mithraculus cinctimanus, almost always found in direct contact with the tentacles. Position also 0.20 b Fishes reflected the presence of specialized behaviors such as 0.18 cleaning. For instance, the two other symbiotic palaemonids 0.16 encountered, Ancylomenes pedersoni and Periclimenes yucatanicus, are both considered dedicated (obligate) 0.14 cleaners, regulating the abundance or size of ectoparasites on 0.12 fishes (McCammon et al. 2010; Titus et al. 2015, 2017b; Associates per anemone (mean ± SE) 0.10 Vaughan et al. 2016). The ability to provide cleaning services 0.08 is thought to reduce predation risk (Grutter 2004; Chapuis and 0.06 Bshary 2010; Grutter and Feeney 2016), with reef fishes using anemones to locate shrimp cleaning stations (Huebner and 0.04 Chadwick 2012). As such, these species were generally found 0.02 in conspicuous positions on the tentacles or in front of the 0 host, often engaging in signaling behaviors aimed at mediat- Abundance Richness (total) (total) ing cleaning interactions (Caves et al. 2018). While the anem- one surveys were conducted during daylight hours, some Fig. 2 Abundance and species richness of decapod crustacean and fish associates on anemones within coral reef and seagrass habitats. a From L anemone symbionts exhibit dial patterns of migration between to R, total abundance of hermit crabs per anemone, total abundance of all areas of their host, moving from the tentacles to the base at other decapod crustacean groups per anemone, and total decapod night when the anemone contracts (Khan et al. 2004; b associate richness per anemone. From L to R, total abundance of fish Chadwick et al. 2008). The majority of decapod crustaceans associates per anemone and species richness of fish associates per anemone. Abundance is defined as the total number of associates per observed can be considered facultative associates, opportunis- anemone while species richness is defined as the total number of tically interacting with anemones. These opportunistic species associate taxonomic groups per anemone. Total number of anemones were commonly located on the column or near the pedal base per habitat n = 100. Data are shown as means + SE well away from the stinging nematocysts. However, while presumably less specialized, some facultative associates still While overall associate richness was similar between hab- possessed the ability to maintain contact with the tentacles, itats, individual anemones within the seagrass had a greater although the mechanisms by which this ability is acquired, diversity and abundance of associates than reef anemones. how this prevents identification by the anemone, and if this This could reflect a higher abundance of potential associates is transferable between anemones remain uncertain within the seagrass or result from differences in structural (Colombara et al. 2017). Of these facultative associates, complexity between the two habitats. As mentioned, the study Gnathophyllum americanum and the Petrolisthes galathinus site reef was highly heterogeneous and rugose, representing a complex have not, to our knowledge, been previously report- complex matrix of microhabitats, and so facultative anemone ed. By far the most abundant anemone-associated decapod associates in this habitat are likely to have access to a range of crustaceans were the multi-species assemblage of small hermit alternative microhabitats of equal value. In contrast, the crabs which generally aggregated on the column and around seagrass meadow was largely homogeneous, with three- the base of anemones. While this anemone-hermit crab asso- dimensional structure primarily provided by the seagrass rhi- ciation was almost ubiquitous in the seagrass habitat, it has zomes and small pieces of rubble. In these habitats, structur- only recently been described, and only for Clibanarius ally complex, chemically defended anemones likely have tricolor (Colombara et al. 2017). Therefore, further work is Mar Biodiv (2019) 49:2609–2620 2617

Table 3 Location of anemone-associated decapod crustaceans and fish- facultative) with anemones. Each anemone is split into three categories es surveyed across reef and seagrass habitats in Belize. Anemone species each representing a location: T: in contact with the tentacles and around are listed across the horizontal axis, with the bracketed number oral disc, C: on the column but not in contact with the tentacles, and B: representing the number of anemones from both habitats that had associ- around the base of the anemones directly next to the pedal disc. The ates and the total samples (i.e. anemone sp. (total with associates/total number within each box represents the total number of individuals re- sampled)). “Relationship” indicates type of interaction (obligate or corded on that species in that location

Anemone species

Stichodactyla Condylactis Bartholomea Laviactis Lebrunia helianthus gigantea annulata lucida neglecta (113/121) (10/10) (23/31) (10/11) (9/25)

Type Species Relationship T C B T C B T C B T C B T C B

Decapod spp. Periclimenes rathbunae O1411714––––11––100 Periclimenes yucatanicus O –– –1 –––––––1 ––1 Ancylomenes pedersoni O –– ––––10 – 20 1 ––– – – Alpheus armatus complex O –– ––––16 –––––––– Thor amboinensis F2058134– 431––312 1 – Thor manningi F21221––––––––––– Lysmata ankeri F2– 7 ––– – – ––––––– Stenopus scutellatus F –– 2 ––– – – ––––––– Gnathophyllum americanum F – 2 ––––––––––––– Mithraculus cinctimanus O43– 1 ––––––2 ––– – Mithraculus sculptus F – 74 7 – 4 –––––––––– Mithraculus forceps F – 4 ––1 –––––––––– Amphithrax pilosus F – 22 3 ––– – – –1 ––– – – Stenorhynchus seticornis F159––– 213–––3 – 1 Petrolisthes galathinus complex F – 6 ––––––––––––– Hermit crab spp. F 3 339 2430 – 663–––––––1 – Fish spp. Malacoctenus macropus F11– 31–––––––1 –– Thalassoma bifasciatum F –– –1 ––––––––1 –– Halichoeres poeyi F –– –2 ––––––––––– Tigrigobius gemmatus F1–––––––––––––– Stegastes leucostictus F – 1 ––––––––––––– Scorpaena plumieri F – 1 ––1 ––––––––––

required to understand this relationship, the diversity of highly specialized species such as the Amphiprioninae paguroid species involved, and their relative abundance. (Hanlon and Hixon 1983; Randall and Fautin 2002; A surprising number of fishes were found associating Feeney et al. 2019). While taxonomically diverse, all asso- with anemones, with a total of six species recorded during ciated individuals were either small-bodied adults observations and one additional species observed outside of (M. macropus, T. gemmatus) or small juveniles of larger formal surveys. As with the decapod crustaceans, neither growing species (T. bifasciatum, H. poeyi, L. nuchipinnis, Halichoeres poeyi nor Tigrigobius gemmatus have been pre- S. plumieri,andS. leucostictus). This is consistent with the viously reported as anemone-associates to our knowledge trends seen in other fishes facultative associated with anem- (Feeney et al. 2019). While all were in physical contact with ones and other anemone-like invertebrates (Bos and the anemone, only Malacoctenus macropus, Thalassoma Hoeksema 2015; Feeney et al. 2019) where size-dependent bifasciatum, H. poeyi,andLabrisomus nuchipinnis were re- predation risk drives the ontogenetic stage of association. By corded interacting with the stinging tentacles with the rest far the most common anemone-associated fish recorded was found on the column or underside of the oral disc. These M. macropus. Informal monitoring of several individuals fishes all appear to be facultative anemone-associates, and so over multiple months suggests that these fishes have small it is unknown if they possess specialized mechanisms for home ranges that center around individual anemones, using avoiding recognition by the anemone such as is found in it as the primary source of shelter. 2618 Mar Biodiv (2019) 49:2609–2620

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In: Por FD (ed) The improbable gulf: habitat and to conserve this often overlooked resource. history, biodiversity, and protection of the Gulf of Aqaba (Eilat). Magnes Press, Jerusalem, pp 209–223 Acknowledgments We would like to thank the editor and three anonymous Chapuis L, Bshary R (2010) Signalling by the cleaner shrimp reviewers for their comments and suggestions on this manuscript. Thanks to Periclimenes longicarpus. Anim Behav 79:645–647 the Smithsonian Institution and the Carrie Bow Cay Field Station, Z. Foltz, S Chesson P (2000) Mechanisms of maintenance of species diversity. Annu & J Alanko, Z-L Cowan, and D Dixson for assistance and logistical support. Rev Ecol Syst 31:343–366 Permission to conduct this study was granted under Marine Science Research Coker DJ, Wilson SK, Pratchett MS (2014) Importance of live coral Permit 0009-18, issued by the Belize Fisheries Department. This manuscript habitat for reef fishes. Rev Fish Biol Fish 24:89–126 represents CCRE contribution 1025. Colombara AM, Quinn D, Chadwick NE (2017) Habitat segregation and population structure of Caribbean sea anemones and associated Funding This work was supported by National Geographic Explorer crustaceans on coral reefs at Akumal Bay, Mexico. Bull Mar Sci Grant to RMB (9860-16). 93:1025–1047 Crawford JA (1992) Acclimation of the shrimp, Periclimenes Compliance with ethical standards anthophilus,tothegiantseaanemone,Condylactis gigantea.Bull Mar Sci 50:331–341 Dixon AK, McVay MJ, Chadwick NE (2017) Demographic modelling of Conflict of interest The authors declare that they have no conflict of giant sea anemones: population stability and effects of mutualistic interest. anemonefish in the Jordanian Red Sea. 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