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Home , Bartholomea annulata, Fungiidae, Sea anemone, Tentacle

Journal of Experimental Marine and Ecology 509 (2018) 44–53

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Journal of Experimental and Ecology

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Giant ephemeral ? Rapid growth and high mortality of corkscrew anemones annulata (Le Sueur, 1817) under variable T conditions ⁎ O'Reilly E.a,1, Titus B.M.a,b,1, Nelsen M.W.a, Ratchford S.c, Chadwick N.E.a, a Department of Biological Sciences, 101 Rouse Life Sciences Building, Auburn University, Auburn, AL 36849, United States b Division of , American Museum of Natural History, New York, NY 10024, United States c College of Science and Math, University of the Virgin Islands, St. Thomas, USVI 00802, United States

ARTICLE INFO ABSTRACT

Keywords: In shelter symbioses, the recruitment, growth, and lifespan of host organisms influence the life history char- reef acteristics of symbiotic guests. Corkscrew sea anemones (Le Sueur, 1817) host diverse Life history ectosymbionts in the Tropical Western Atlantic, some of which are cleaner that attract and Senescence clean Caribbean reef fishes. These sea anemones potentially function as short-lived cleaning stations due to their Cleaning high mortality and short lifespans relative to that of many reef fishes. A combination of methods (field mon- Population dynamics itoring, population modeling, manipulative field experiments) was applied to quantify variation in rates of re- Sea cruitment, growth, shrinkage, and mortality of this anemone. Population projections at reef sites on St. Thomas, U. S. Virgin Islands, indicated that the most important contributors to population growth were the recruitment and fate of the smallest individuals. Field experiments revealed that recruitment and growth varied significantly with reef site, but that lifespan did not. Population modeling demonstrated effects of body size and habitat on life history traits, with smaller anemones growing faster than large ones, and both very large and small individuals dying more frequently than medium-sized ones. The combined data reveal that B. annulata is among the shortest- lived sea anemones, with most individuals surviving < 12 months, and maximum lifespan of only ~1.5–2 years at all examined sites. Together, these suggest that this anemone exhibits characteristics of a weedy ; individuals grow and reach adult body size rapidly and populations have rapid turnover. Life history and recruitment data for crustacean symbionts of B. annulata indicate that this host may be long-lived enough to mediate multiple generations of crustacean associates, fulfilling the expectations of an evolutionarily stable host. The short lifespan of these anemones relative to those of many reef fishes may cause fishes to search frequently for new cleaning stations on Caribbean coral reefs.

1. Introduction (Hernández et al., 2012). Therefore, in most sessile marine symbioses, hosts should be longer-lived than guests so that each individual can host Symbioses cause ecologically and evolutionarily important adapta- at least one full generation of guest symbionts. However, this prediction tions that impact all aspects of a symbiont's life history (Herre et al., remains largely untested because the lifespans and survival rates of 1999; Hoeksema and Bruna, 2000; Thrall et al., 2007). Typically, most sessile marine organisms remain unknown. symbioses involve relatively small guest symbionts living with com- On tropical coral reefs, giant sea anemones are conspicuous and paratively large hosts (Hernández et al., 2012). The degree of mobility often engage in charismatic and ecologically-important symbioses with and host specificity of the guest, in conjunction with the size, lifespan, fishes and (Chadwick et al., 2008; Colombara et al., 2017). and population dynamics of the host, greatly affect the degree to which While some guest symbionts may be highly mobile (e.g., anemone- symbiotic partners co-evolve (Thompson, 1994; Thrall et al., 2007). fishes) and transition easily from one host species to another (Huebner Host size and lifespan may regulate the intraspecific group size, re- et al., 2012), smaller invertebrate guests may be functionally sessile productive opportunities, parental care, and lifespan of the guest post-recruitment. Thus, it is expected that the population dynamics of

⁎ Corresponding author. E-mail address: [email protected] (N.E. Chadwick). 1 Denotes equal contribution and shared first authorship. https://doi.org/10.1016/j.jembe.2018.08.013 Received 2 March 2018; Received in revised form 23 August 2018; Accepted 31 August 2018 0022-0981/ Published by Elsevier B.V. E. O'Reilly et al. Journal of Experimental Marine Biology and Ecology 509 (2018) 44–53 the anemones (i.e., recruitment, growth, maximum size and longevity) abundance, inter- and intraspecific group sizes, mobility, reproductive will be critically important for mediating intraspecific group size, re- opportunities, and lifespan. productive opportunity, fecundity, and generation time for macro-in- An initial field study indicated that populations of B. annulata may vertebrate guest species such as crustaceans (Baeza and Thiel, 2007; exhibit high turnover (O'Reilly and Chadwick, 2017), but was con- McKeon and O'Donnell, 2015). ducted in Florida Bay where seasonal sea surface temperatures can vary Population dynamics of some temperate sea anemones are known, by 10 °C, representing atypical conditions compared with more stable especially for spp. in the northeastern Pacific(Sebens, environments in the Greater Caribbean (Bramanti and Edmunds, 2016; 1983), indicating that they may live for > 100 yrs. and have high re- Briones-Fourzán et al., 2012), so may not be directly generalizable − – cruitment rates of 3–25 individuals m 2 yr 1 (Sebens, 1982). However, across the entire species range. Here, the findings of O'Reilly and recruitment rates are poorly characterized for many tropical genera, Chadwick (2017) are compared with those obtained at other and may be highly variable and species-specific(Dixon et al., 2017; locations, to test the hypothesis that large sea anemones are long-lived O'Reilly and Chadwick, 2017), with members of some taxa able to with stable population structure as a prerequisite for supporting as- produce both sexual and asexual recruits (Fautin, 2002; Jennison, 1981; semblages of ectosymbionts. Findings are presented from monitoring Scott et al., 2014). On coral reefs, the limited available substrate space and modeling of B. annulata populations at two Caribbean reef sites and and potentially intense for space with reef-building from experimental field manipulations, to determine the extent to (Chadwick and Arvedlund, 2005; Chadwick and Morrow, 2011) may which these sea anemones adapt to specific sites. Conclusions then are severely limit anemone recruitment. Sea anemones in general have made about the impacts of anemone life history patterns on the dy- been described as potentially long-lived (> 50 yrs., Ottaway, 1980; namics of crustacean symbionts and cleaning stations, as a conceptual Sebens, 1983; Shick, 1991), and those that produce asexual clones framework for understanding the ecology and evolution of this sym- could further prolong the lifespan of the genet, even if the ramet is biotic system. short-lived (Jackson and Coates, 1986; Bythell et al., 2018). Thus, sea anemones as symbiotic hosts may provide long-term stability, and fit 2. Methods the general expectations of large symbiotic host species. Large sea anemones in the tropical Indo-Pacific, all of which host 2.1. Field population monitoring clownfishes in the Amphiprion, have received the most attention in terms of characterizing their patterns of recruitment, growth, sur- To explore patterns of recruitment, growth, and mortality in situ for vival, and effects of hosting symbionts on their life history character- B. annulata, two sites were established at St. Thomas, US Virgin Islands istics (Dixon et al., 2017; Scott et al., 2011; Szczebak et al., 2013). They (USVI), and monitored every 3 mo for 1 yr (March 2007–March 2008): are expected to have stable population sizes and extended lifespans, Brewers Bay (BB: 18° 20′ 27.95“N, 64° 58' 42.41"W) and Flat Cay (FC: given that associated fishes may live for multiple decades (Buston and 18°19′ N, 64°59′ W). BB was a small inshore (200 m from shore) patch García, 2007). However, recent evidence indicates that some Indo-Pa- reef in a partially-enclosed bay (described in Huebner and Chadwick, cific anemones may live only 3–9 years, and exhibit high turnover of 2012a, 2012b), while FC was an offshore (2.2 km from shore) fringing individuals even if they are stable in terms of population size (Dixon reef. The sites were near each other (~2 km distant) at similar depth et al., 2017; McVay, 2015). In contrast, Caribbean anemones host di- below sea surface (6–10 m). At each site, the following five major ha- verse, shorter-lived crustaceans (> 15 species, Briones-Fourzán et al., bitat characteristics were quantified to determine how they varied be- 2012; Colombara et al., 2017; Herrnkind et al., 1976), and extended tween the sites: % cover of live stony corals, downwelling intensity of − − host lifespan may not be required for symbiotic stability because the photosynthetically active radiation (PAR, μEm 2 s 1), sedimentation crustaceans can be either highly mobile (Chadwick et al., 2008; rate (after Gilmour, 2002), and two relative measures of water motion Huebner et al., 2012) or short-lived (only 1–2 yrs., Bauer, 2004; Gilpin level (sediment grain size and clod card dissolution rate, Jokiel and and Chadwick, 2017). Morrissey, 1993; for details on measurement of physical parameters, Corkscrew sea anemones Bartholomea annulata (Le Sueur, 1817) fill see Nelsen, 2008). Percent coral cover was determined using photo- an important ecological niche in that they harbor obligate cleaner quadrats (N = 20) placed at random intervals (via random number shrimps that remove parasites from reef fishes (Huebner and Chadwick, generator) along a 50-m transect tape located haphazardly on the coral 2012a, 2012b; Limbaugh et al., 1961; McCammon et al., 2010). The reef in each site, and quantified using a grid of 25 randomly-generated cleaner shrimps receive protection from living among the anemone points superimposed over each photograph, following Walker et al. , and may benefit the anemone by attracting fishes for (2007). Significant differences in habitat characteristics between the 2 cleaning, which in turn excrete dissolved nutrients absorbed by the host sites were assessed using independent two-sample t-tests in SAS v. 9.1 (Cantrell et al., 2015). snapping shrimps also form mutualisms (SAS Institute Corp., 2005). with these anemones, in which both partners benefit by receiving The sites were established along coral reef margins, because B. an- mutual shelter from (McCammon and Brooks, 2014). In- nulata abundance peaked in these areas of intermixed coral patches, dividuals of B. annulata are the most common large sea anemones in the rubble, and (Briones-Fourzán et al., 2012; Mahnken, 1972). An Tropical Western Atlantic, and are habitat generalists that occur in area of 47 × 6 m was monitored at BB (282 m2), and 70 × 11 m plus small pockets at the rock-sand interface along the margins of coral 73 × 5 m at FC (1135 m2, details in Nelsen, 2008), both with long axis reefs, as well as in sea grass beds and mangrove habitats (Briones- parallel to the reef edge. A larger reef area was examined at FC than BB Fourzán et al., 2012; Jennison, 1981; Sebens, 1976). Food is acquired to include enough individuals for population dynamic monitoring at through both heterotrophy, and autotrophy in which B. annulata as- both sites (after Hattori, 2002; Hirose, 1985; Dixon et al., 2017), be- sociates with several species of microalgae (Grajales cause the anemones occurred in lower abundance at FC (N = 53) than et al., 2016), similar to most other coral reef anemones (Baker, 2003; at BB (N = 107, assessed in March 2007). The body size of each B. Rowan, 1998). Individuals reproduce sexually twice each year through annulata was measured as the length (L) and width (W) of the fully broadcast spawning (Jennison, 1981) and clonally year-round via pedal extended crown, to calculate tentacle crown surface area laceration (Cary, 1911), occurring as single individuals or small ag- (TCSA = [L/2] * [W/2] * π, Briones-Fourzán et al., 2012; Hattori, gregations that may or may not comprise asexual clones (Titus et al., 2002; O'Reilly and Chadwick, 2017). Contracted anemones were re- 2017). This is a model system to test expectations about the stability of turned to later in the survey to obtain measurements. The few ane- hosts and the maintenance of crustacean symbioses, be- mones that remained contracted for the entire 1-wk survey during each cause the population dynamics and life history of B. annulata likely 3-mo period (0–1.4% of individuals depending on the period, see exert a major influence over many crustaceans in terms of their below) were removed from population analyses for that period, leading

45 E. O'Reilly et al. Journal of Experimental Marine Biology and Ecology 509 (2018) 44–53 to slight variation in sample sizes between periods. TCSA was used contribution. Elasticity analyses estimated the effect of a proportional because it is the only major body dimension measurable in these ane- change in the vital rates on population change (λ), and revealed life mones that extend their tentacle crowns out of reef holes, and because it stages or sizes classes that were particularly influential to a specific correlates significantly with other size parameters (pedal and oral disk parameter in the model, such as λ. These values were calculated for diameter, wet and dry mass, Cantrell et al., 2015; Dixon et al., 2017; each element in the matrix, to determine the vital rates that were most O'Reilly, 2015). Each individual was mapped and tagged with an alu- important for population growth. Transition probabilities were boot- minum oval tag engraved with an ID number, attached to adjacent reef strapped 1000 times to obtain confidence intervals for λ and damping substrate using a stainless steel nail. This tagging method is reliable ratios ρ (after Bierzychudek, 1999; Edmunds, 2010). because most coral reef anemones, including B. annulata, attach their bases deep within reef holes and crevices, and do not locomote sub- 2.3. Field experiments stantially across the substratum (Dixon et al., 2017; Hattori, 2006; O'Reilly and Chadwick, 2017). Sand often surrounds these crevices, so Two 4.5 mo reciprocal transplant experiments were conducted B. annulata are unlikely to locomote among them as they are not known during March–July and July–November 2009, in which anemones were to move across sand. transplanted between the inshore (BB) vs. offshore (FC) sites to examine Field data were collected during a 1-wk period at the start of each 3- the impacts of coral reef habitat type on anemone phenotypic plasticity, mo sampling period (first week of the month in March 2007, June 2007, in terms of recruitment, growth, and mortality. Two experiments were Sept 2007, Dec 2007, March 2008). During the five sequential popu- performed to increase the experimental sample size, because time lation surveys, rates of recruitment, growth, and mortality were de- constraints limited the number of anemones that could be manipulated termined based on the presence and body size of individuals. All new during each field experimental period. Prior to initial transplantation in anemones were recorded and tagged when they recruited to the reef March 2009, anemones were selected that each occurred on a piece of (newly appeared in sites), to determine recruitment rate as well as small movable substrate (conch shell, coral rubble; 24 at BB and 22 at potential lifespan. Most sea anemones and corals have planktonic FC) near to but outside of the mapped areas described in section 2.1), durations of only a few days to weeks before they settle on the and then tagged, measured, and mapped. Ten tagged anemones were (Strathmann, 1987) therefore the age (within a few weeks) of each assigned randomly at each site to a control group of no transplantation anemone that was followed post-recruitment is known. Anemones that between sites, and the remainder (14 at BB and 12 at FC) to a treatment disappeared between sample periods were considered to have been lost group of reciprocal transplantation between the sites. To control for to the population and were recorded as a mortality event (after Dixon effects of manipulation disturbance, all anemones were collected and et al., 2017; O'Reilly and Chadwick, 2017). then either reciprocally transplanted or returned to their original site. Anemones from BB and FC were not genotyped prior to the present All anemones on the experimental substrates were surrounded entirely study, because suitable population-level markers did not exist at the by sand, ensuring that any missing anemones were the result of mor- time. However, more recent genetic data for B. annulata show only tality rather than locomotion across hard substrate (see section 2.1). weak population genetic structure across the entire Caribbean, and do They were monitored after 1 mo and 4.5 mos for recruitment of ad- not show any population genetic differentiation between BB and FC jacent new individuals to the same experimental substrate (conch shell (Titus, 2017). Thus, we can largely reject the hypothesis that locally or coral rubble), changes in body size, and mortality. Tagged substrates adapted genotypes drive any observed differences between sites. that could not be re-located after 1 or 4.5 mos were excluded from We used Chi-squared tests to test the null hypothesis of no differ- analyses due to the uncertainty of anemone survival. ence in sea anemone population size structure between the 2 sites This field experiment was repeated during July–November 2009 during each sample period. Two-sample t-tests were employed to test using an additional 24 anemones at BB and 22 at FC. Rates of anemone the null hypotheses that anemone body sizes and recruitment rates did recruitment, growth, and mortality did not differ significantly between not differ between the sites throughout the study, performed in SAS/ the two experiments, so the data were pooled for statistical analyses STAT v. 9.1 (SAS Institute Inc., 2004). (total N = 48 at BB and 44 at FC). The null hypothesis of no significant difference in initial body size between the treatment and control groups 2.2. Stage-based population dynamic modeling within each site was analyzed using Mann-Whitney U tests. Growth rate data were log-transformed to meet assumptions of normality, and the Population dynamics were analyzed using a stage-based model, null hypothesis of no difference in growth rate between BB and FC was because this type of modeling can elucidate the extent to which po- analyzed using 2-way Analysis of Variance (ANOVA). Significant dif- pulations maintain demographic stability (after Hughes, 1984; Lirman, ferences in anemone mortality between treatments and sites were 2003; O'Reilly and Chadwick, 2017). Transition matrices were created analyzed using chi-squared tests of independence in SYSTAT v13.0 based on three body size classes (TCSA, 0.1–25.0 cm2 [I], (2010). All results are presented as means ± one standard deviation 25.1–50.0 cm2 [II], and > 50.0 cm2 [III]) and showed the proportion of unless otherwise indicated. each population that exhibited growth or shrinkage (after Dixon et al., 2017; Edmunds, 2010; Hughes and Jackson, 1985). Size class limits 3. Results were chosen so that each size class contained at least 10 individuals during the initial survey in March 2007 at BB; however, FC exhibited 3.1. Field population monitoring lower abundance and significantly smaller individuals, so did not contain as many individuals in size classes II and III (see section 3.1). The offshore site at FC exhibited significantly higher levels of live Each matrix showed the proportion of individuals that exhibited growth stony coral cover, irradiance (a measure of water clarity), and sediment into a larger size class (I-II, I-III, II-III), stasis in the same size class (I-I, grain size and clod card mass (both measures of water motion level), II-II, III-III), or shrinkage into a smaller size class (II-I, III-II, III-I) be- than did the inshore site at BB; the two sites did not differ significantly tween surveys. For each transition matrix, the dominant eigenvalue (λ), in sedimentation rate (Table 1). damping ratio (ρ), and elasticity were determined (Caswell, 2001). All At the beginning of the study in March 2007, B. annulata abundance − population parameters were calculated using the Microsoft Excel add- was almost 10-fold greater at BB (0.38 individuals m 2; N = 107 in − on PopTools 3.2 (www.poptools.org). The transition matrices did not 282 m2 area) than at FC (0.05 m 2; N = 53 in 1135 m2). By March − include the effects of on population growth, due to un- 2008, anemone abundance had increased by ~15% at BB (to 0.44 m 2; − determined fecundity rates. Therefore, rates of population change (λ) N = 122) and ~45% at FC (0.07 m 2; N = 77). Initial population size reported here represent rates calculated without reproductive structure differed significantly between the two sites (Chi-squared test,

46 E. O'Reilly et al. Journal of Experimental Marine Biology and Ecology 509 (2018) 44–53

Table 1 Variation in habitat characteristics between two coral reef sites: Brewers Bay (BB) and Flat Cay (FC), at St. Thomas, US Virgin Islands. Data are presented as means ± SD, numbers of replicates examined at each site are shown as sample sizes (df = degrees of freedom), and statistical results of 2-tailed t-tests are indicated as t- and p-values. PAR = photosynthetically-active radiation at the sea floor (6–10 m depth). Sediment grain size refers to the grain sizes (mm diameter) of bottom sediments collected from the reef-sand interface at each site, and sedimentation rate refers to the dry mass (g) of suspended sediments that settled per unit area per day into sediment traps; both plus clod card dissolution rate are measures of water motion level. See Nelsen (2008) for methods details.

Coral reef site % cover of stony corals PAR at midday (μE Sedimentation rate (g 125 cm2 Bottom sediment grain size Clod card dissolution rate (% loss of − − − − m 2 s 1) d 1) (mm) clod card mass, g d 1)

Brewers bay 15.2 ± 15.3 59.2 ± 3.3 0.06 ± 0.02 0.53 ± 0.04 19.1 ± 0.9 Flat cay 31.0 ± 19.3 194.6 ± 8.8 0.06 ± 0.06 0.75 ± 0.04 20.8 ± 1.1 Sample size (df) 20 (19) 40 (39) 3 (2) 3 (2) 10 (9) t-value 3.04 14.53 0.07 5.40 4.07 p-value < 0.01 < 0.0001 0.95 < 0.05 < 0.001

widely within each site (11–59% at BB and 0–43% at FC) but generally were higher at BB than at FC, especially for the largest size class (di- agonal proportions within each period in Table 2; I-I, II-II, III-III). The percent of individuals in each size class that shrank (transitioned to a smaller size class) also ranged widely both at BB (4–26%) and FC (0–60%) during each 3-mo period (upper right proportions within each period in Table 2; II-I, III-II, III-I). For all individuals combined, rates of shrinkage were low (BB 9–11% through the year, FC 5–24%) compared to rates of stasis or growth. Shrinkage rates were identical at both sites in spring (Mar-Jun; 9% at both BB and FC), then became higher at BB (10%) than at FC (5%) in summer (Jun-Sep). They peaked in the fall (Sep-Dec) when the percent of individuals that shrank more than quadrupled at FC to 24% (compared to only 11% at BB), then returned to lower levels in winter at both sites (Dec-Mar BB: 11%, FC 7%). Rates of growth, stasis, and shrinkage overall were highly variable, with most Fig. 1. Population size structure of corkscrew sea anemones Bartholomea polyps remaining static during each 3-mo period at both sites (Table 2). annulata. Size structure of B. annulata coral reefs at Brewers Bay (BB; N = 107) The percent of individuals in each size class that died ranged widely and Flat Cay (FC; N = 53) St. Thomas, US Virgin Islands, at the beginning of the from 14 to 42% at BB and 12–60% at FC during each 3-mo period study year in March 2007. TCSA = tentacle crown surface area; significantly (mortality rates; row qx in Table 2). During spring (Mar-Jun), total larger at BB than FC (see section 3.1). mortality for all size classes combined was lower at BB (28%) than at FC (41%), then in summer (Jun-Sep) it remained constant at BB (31%) but 2 rose to a peak at FC of 64%, and returned to lower levels at both sites Mar 07, χ3 = 31.14, p < 0.001, Fig. 1) and remained significantly 2 during fall (Sep-Dec; BB: 34%, FC: 43%) and spring (Dec-Mar (BB: 40%, different throughout the study (Jun 07, χ3 = 38.25; Sep 07, 2 2 2 FC: 42%). Overall mortality was higher at FC than BB during all 4 χ3 = 31.15; Dec 07, χ3 = 51.22; Mar 08, χ3 = 48.32, p < 0.001). At BB, individuals ranged 0.8–451.6 TCSA cm2, while at FC they ranged census periods. During most periods at both sites, individuals in the only 1.6–98.9 cm2. At BB, ~50% of the anemones occupied the smallest smallest size class (I) exhibited the highest mortality (Table 2). Dy- size class, while at FC almost 70% were in the smallest size class, and no namic survival curves for both populations showed that < 25% of the individuals at FC reached 100 cm2 TCSA during the study. Conse- original anemones remained after 12 mos (Fig. 2). quently, individuals were significantly larger at BB than at FC, both at the beginning of the study in March 2007 (2-tailed t-test, t160 = 2.88, 3.2. Stage-based population dynamic modeling p < 0.01) and at the end of the study (March 2008: t197 = 4.07, p < 0.0001). Matrix models reflected the temporally variable nature of B. annu- fi Recruitment was signi cantly more frequent at BB than at FC, in lata populations at both sites, as evidenced by reliance on a steady terms of the number of new individuals observed per unit area − supply of recruits to maintain population size, rapid rates of transition (BB = 0.17 ± 0.03 recruits m 2 per 3 mos; FC = 0.04 ± 0.01 recruits −2 among size classes, and high mortality (Table 2). The population at BB m per 3 mos; N = 4 3-mo periods examined; t6 = 7.13, p < 0.001). showed greater decline during winter (Sep-Mar) than summer (Jun- Recruitment was high during both spring and summer at BB compared Sep), while FC exhibited the opposite . Elasticity analyses at BB to fall and winter, while at FC it was relatively high only during spring indicated that stasis in the smallest and largest size classes exerted the (row Rn in Table 2). largest effect on population growth rate; in 2 of the 4 censuses, these The percent of individuals within each size class that grew (transi- matrix elements possessed the two highest elasticity values (Table 3). – tioned into larger size classes) ranged from 11 to 35% at BB and 3 33% Results were less consistent at FC, but revealed that the stasis of small at FC during each 3-mo period (lower left proportions within each anemones was the most influential contributor toward population period in Table 2; transitions I-II, I-III, II-III). For all size classes com- growth during fall and winter. bined, during spring (Mar-Jun) about the same percentage of in- Rates of intrinsic population change (dominant eigenvalues, λ)at dividuals grew at both sites (BB: 18%, N = 107; FC: 19%, N = 53). BB and FC were < 1 when input from reproduction was not included, Then during summer (Jun-Sep) the percent of individuals that grew indicating a decrease in population size during each period (Table 4). peaked at BB (22%, N = 127) while it decreased at FC (to only 10%, During all periods, λ values were within the 95% confidence intervals N = 86), and remained higher at BB than at FC for the rest of the year of values obtained through bootstrap resampling. The damping ratio (ρ) (Sep-Dec BB: 9%, N = 147; FC: 3%, N = 72; Dec-Mar BB: 14%, varied among sample periods (Table 4), indicating a variable rate of N = 136; FC: 10%, N = 71, Table 2). Stasis rates of individuals in each convergence to a stable size distribution. Flat Cay showed lower λ and ρ size class (percent remaining in the same size class) similarly ranged in summer and fall than during winter to spring, while Brewer's Bay

47 E. O'Reilly et al. Journal of Experimental Marine Biology and Ecology 509 (2018) 44–53

Table 2 Transition matrices of Bartholomea annulata over 12 mos at two coral reef sites on St. Thomas, U. S. Virgin Islands (Brewers Bay and Flat Cay), based on three size classes: I (0.1–25 cm2 tentacle crown surface area), II (25.1–50.0 cm2), and III (> 50 cm2). Columns refer to the proportion of individuals in each size class that transitioned to other size classes (rows) during each transition period. Bold cells represent parameters with highest elasticity for each year (see Table S1). qx = mortality rate (proportion of individuals that died during each transition period), qx N = number of individuals that died, Rn = number of recruits (those in the largest size class were excluded from recruitment analyses, see Methods), N = number of individuals present at the beginning of each transition period (two individuals that remained contracted during the Sep 2007 survey at FC and the Dec 2007 survey at BB were excluded from analysis, leading to variation in sample sizes among periods). Survey data were collected during the first week of the month in each of 5 mos: Mar 2007, Jun 2007, Sep 2007, Dec 2007, and Mar 2008. The initial 3-mo transition period thus extended from ~1 Mar – 1 Jun 2007, the second period extended ~ 1 Jun – 1 Sep 2007, etc. Note that these data are from 3-mo censuses, in contrast to Table 1 in O'Reilly and Chadwick (2017) that reports data in similar format, from 2-mo censuses in Florida for this species.

Mar – Jun 2007 Jun – Sep 2007 Sep – Dec 2007 Dec 2007 – Mar 2008

I II III I II III I II III I II III

A. Brewers Bay I 0.50 0.13 0.04 0.40 0.13 0.07 0.52 0.20 0.14 0.39 0.26 0.13 II 0.11 0.26 0.23 0.21 0.20 0.24 0.11 0.28 0.05 0.10 0.11 0.08 III 0.04 0.35 0.59 0.07 0.30 0.48 0.00 0.17 0.52 0.09 0.22 0.45

qx 0.35 0.26 0.14 0.32 0.37 0.21 0.37 0.35 0.29 0.42 0.41 0.34

qx N 19 8 3 22 11 6 24 14 12 30 11 13

Rn 36 11 3 32 13 14 23 7 10 22 5 13 N5431 2268302965404271 27 38

B. Flat Cay I 0.33 0.22 0.00 0.22 0.17 0.00 0.42 0.42 0.40 0.43 0.25 0.33 II 0.15 0.33 0.60 0.06 0.17 0.20 0.03 0.19 0.20 0.05 0.42 0.34 III 0.03 0.33 0.00 0.02 0.22 0.20 0.00 0.04 0.20 0.05 0.08 0.00

qx 0.49 0.12 0.40 0.70 0.44 0.60 0.55 0.35 0.20 0.47 0.25 0.33

qx N19124483209226 3 1

Rn 48 6 1 19 18 4 26 4 0 30 4 2 N 39 9 5 63 18 5 36 26 10 56 12 3

showed relatively low λ during fall and winter.

3.3. Field experiments

In the field experiments, seven recruits appeared on experimental substrates at BB after 1 mo, while only one recruit appeared at FC. By 4.5 mos, this number had grown to a total of 12 recruits at BB, but remained only one at FC. Newly-recruited anemones formed small ag- gregations of 2–4 individuals together with the original anemone on each tagged substrate. Recruits were small, ranging only 7.85–61.26 TCSA cm2 (26.31 ± 14.55 cm2, N = 13). The initial TCSA of anemones did not differ significantly between the control and treatment groups at either BB or FC (Mann-Whitney U Tests, U = 101, p = 0.20 at BB; U = 76.5, p = 0.14 at FC). However, anemones at BB initially were significantly larger than those at FC, because individuals in the source population at BB were larger on average than those at FC (Section 3.1; Fig. 1). The growth rate of small anemones was highly variable, with individuals ranging from 90% shrinkage to > 100% growth after only 1 mo. Although growth varied considerably within site, across all size classes the anemones at BB grew significantly more and shrank less than did those at FC, regardless of the site of origin (Fig. 3). After 1 mo, the percent change in anemone body size varied significantly with the site of destination (two-way ANOVA,

F1,90 = 14.94, p < 0.001; Fig. 3a), but not site of origin (F1,90 = 0.22, ff Fig. 2. Dynamic survival curves for corkscrew sea anemones Bartholomea p = 0.64), and there was no interaction e ect (F1,90 = 0.28, p = 0.60). annulata. Survival curves for corkscrew sea anemones at (A) Brewers Bay (BB; In terms of positive versus negative changes in body size (growth versus N = 107) and (B) Flat Cay (FC; N = 53), St. Thomas, U. S. Virgin Islands. shrinkage), after 1 mo, 11 of 24 surviving anemones (46%) exhibited Survival was determined as the proportion of initially-tagged anemones that positive growth at BB while significantly fewer anemones (only 3 of 25 remained at each site during each 3-mo census over 1 yr (March 2007 to March surviving individuals, 12%) exhibited positive growth at FC (test of 2008). Disappeared anemones were considered to have died (see text for de- 2 independence, χ1 = 6.86, p < 0.01). The impact of destination site on tails). Based on the survival curves, these anemones were projected to survive anemone size change did not persist after 4.5 mos (F1,90 = 0.72, for ~ 1.5 yr at BB and ~ 1 yr at FC. p = 0.40; Fig. 3b), nor did the effect of site of origin (F1,90 = 0.24, p = 0.63; no interaction effect, F1,90 = 0.48, p = 0.49), possibly due to low anemone survival after 4.5 mos (see below). Between-site differ- ences in positive versus negative growth were not significant at 4.5 mos 2 (χ1 = 2.73, p = 0.09). Rates of anemone mortality were high, and did not differ

48 E. O'Reilly et al. Journal of Experimental Marine Biology and Ecology 509 (2018) 44–53

Table 3 Elasticity values for population transitions of Bartholomea annulata at 2 coral reef sites (Brewers Bay and Flat Cay) on St. Thomas, U. S. Virgin Islands, each 3 mos during March 2007 – March 2008. Elasticity matrices were calculated using the equation eij = aij/λ × ∂λ/∂aij, where eij = elasticity of the (i,j) entry of the size-based matrix, aij =(i,j) transition probability in the matrix, and λ = population growth. Values in bold indicate the transitions with the highest elasticity values during each time step, corresponding to the transitions that had the greatest effect on intrinsic rates of population change (λ), shown as bolded cells in Table 2.

Mar – Jun 2007 Jun – Sep 2007 Sep – Dec 2007 Dec 2007 – Mar 2008

I II III I II III I II III I II III

A. Brewers Bay I 0.06 0.02 0.01 0.11 0.05 0.04 0.38 0.05 0.05 0.26 0.06 0.08 II 0.03 0.08 0.15 0.06 0.08 0.14 0.10 0.09 0.02 0.07 0.03 0.05 III 0.01 0.15 0.49 0.03 0.15 0.36 0.00 0.06 0.26 0.07 0.06 0.32

B. Flat Cay I 0.08 0.09 0.00 0.07 0.07 0.00 0.69 0.08 0.01 0.31 0.09 0.04 II 0.08 0.28 0.24 0.05 0.18 0.22 0.09 0.07 0.01 0.07 0.31 0.07 III 0.01 0.23 0.00 0.01 0.21 0.19 0.00 0.02 0.02 0.06 0.05 0.00

Table 4 Demographic characteristics of Bartholomea annulata at 2 coral reef sites (Brewers Bay and Flat Cay) on St. Thomas, U. S. Virgin Islands, each 3 mos during March 2007 – March 2008. Size-based transition matrices were used to calculate λ, the intrinsic rate of population change and ρ, the damping ratio. Transition matrices and therefore λ analysis did not include effects of recruit- ment, thus λ values < 1 indicated declining populations without recruitment. Transition probabilities were bootstrapped 1000 times to create confidence intervals for λ and ρ. λ1000 and ρ1000 show mean values based on the boot- strapped transition matrices (95% CI); λsample and ρsample show values from the transition matrices based on the population data.

Site and Period λρ

λ1000 λsample ρ1000 ρsample

A. Brewers Bay Mar – Jun 2007 0.76 (0.40–1.16) 0.78 0.47 (0.02–2.23) 0.08 Jun – Sep 2007 0.80 (0.50–1.11) 0.72 0.51 (0.08–1.75) 0.12 Sep – Dec 2007 0.67 (0.32–1.06) 0.66 0.28 (0.00–1.27) 0.08 Dec 2007 – Mar 2008 0.61 (0.37–0.90) 0.61 0.20 (0.04–0.69) 0.10

B. Flat Cay Mar – Jun 2007 0.65 (0.33–1.03) 0.71 0.31 (0.01–1.84) 0.12 Jun – Sep 2007 0.42 (0.23–0.56) 0.43 0.05 (0.00–0.15) 0.02 Sep – Dec 2007 0.65 (0.31–0.99) 0.48 0.22 (0.00–0.87) 0.03 Dec 2007 – Mar 2008 0.64 (0.32–0.99) 0.61 0.22 (0.01–0.85) 0.09

2 significantly between BB and FC after either 1 mo (χ1 = 0.39, p = 0.53) 2 or 4.5 mos (χ1 = 0.72, p = 0.40). Of the 48 anemones tagged at BB, after 1 mo 20 had disappeared (42% mortality), while at FC, of the 44 anemones tagged 15 had disappeared (34% mortality). A total of 13 tagged substrates could not be relocated and were omitted from sta- tistical analyses. A final total of 42 substrates at BB and 37 substrates at FC were present throughout each transplant experiment, and were used for statistical analysis. Mortality rates did not differ significantly be- tween the FC control anemones and those transplanted from FC to BB 2 2 after 1 mo (χ1 = 2.64, p = 0.10) or 4.5 mos (χ1 = 3.80, p = 0.054), nor between BB control anemones and those transplanted from BB to FC 2 2 after 1 mo (χ1 = 0.32, p = 0.57) or 4.5 mos (χ1 = 0.87, p = 0.35). As such, neither site of origin nor destination affected anemone mortality Fig. 3. Variation in percent change in Bartholomea annulata body size, rates at the time scales examined here. comparing transplanted and non-transplanted individuals. Change in body size (TCSA = tentacle crown surface area in cm2, x ± SD) of corkscrew sea anemones Bartholomea annulata with site of origin versus site of destination, at 4. Discussion (A) 1 mo and (B) 4.5 mo after reciprocal transplantation between 2 coral reef sites on St. Thomas, U.S. Virgin Islands: BB = Brewers Bay and FC = Flat Cay. 4.1. General comments Sample sizes are shown in parentheses. Note that all anemones showed net shrinkage at FC, regardless of timescale or site of origin. This study demonstrates that individuals of Bartholomea annulata exhibit high levels of turnover under both experimental and natural tropical sea anemones specifically, are necessarily long-lived with static conditions. Rapid recruitment and growth, high mortality, and short populations. These data place B. annulata among the fastest-growing lifespan are shown to be inherent life history characteristics of this and shortest-lived tropical sea anemones on record, as observed species, contravening expectations that symbiotic hosts in general, and

49 E. O'Reilly et al. Journal of Experimental Marine Biology and Ecology 509 (2018) 44–53 recently for this species in the Florida Keys (O'Reilly and Chadwick, studies thus far. Anemones may grow more slowly in the field vs. la- 2017). These findings have important implications for symbionts of B. boratory due to a range of environmental stressors that are present on annulata, both microalgae and crustaceans, as well as for reef fishes that coral reefs (e.g., partial predation, pollution, sedimentation, extreme use these anemones as cleaning stations (reviewed in Cantrell et al., temperatures) but absent in laboratory tanks. The degree to which in- 2015, Huebner and Chadwick, 2012a, 2012b). Three major implica- dividuals of B. annulata rely on their endosymbiotic for nutrition tions are: (1) Crustacean symbionts of B. annulata, especially obligate remains unknown. However, high rates of water flow in the field po- associates, are likely to have short lifespans and to mature quickly. The tentially damage the soft tissues of delicate-bodied sea anemones such degree to which these small crustaceans are mobile also will determine as B. annulata and limit both their heterotrophic feeding ability and the extent to which B. annulata influences symbiotic crustacean life exposure of their microalgae to sunlight, by changing the size of the histories. (2) Cleaning stations centered around B. annulata function as tentacle crown and reducing tentacle expansion (Koehl, 1977; Shick, short-lived features of Caribbean coral reefs; reef fishes thus must fre- 1991). This process could contribute to the low abundance of B. an- quently search for new cleaning stations that they locate using visual nulata at reef sites with relatively high water motion (Colombara et al., cues transmitted by the anemones (Huebner and Chadwick, 2012a). (3) 2017). Exposure to more rapid rates of water flow on coral reefs than in Any process that disrupts recruitment likely leads to rapid population laboratory tanks thus may cause these anemones to redirect energy decline of B. annulata, and subsequently affects the demography of from growth into tissue regeneration, or into the relatively high en- crustacean symbionts and the ability of reef fish assemblages to engage ergetic costs of remaining expanded in rapidly-moving water (O'Reilly in symbiotic interactions with cleaner . Conversely, because and Chadwick, 2017). Water flow and food availability may work in these anemones exhibit rapid recruitment, their populations potentially concert to partially drive patterns of local abundance and recruitment, could recover quickly from disturbance events at some reef sites. as both were higher at the inshore site (BB) that exhibited lower water motion and higher suspended particulate matter (Table 1) than did the 4.2. Recruitment, growth, and mortality offshore site (FC). Comparison of anemone transition rates in all five types of studies conducted to date for this species indicate that they Rates of recruitment, growth, and mortality varied somewhat be- vary, in terms of positive or neutral transitions (growth/stasis) versus tween the sites examined here, but overall trends suggest that these negative ones (shrinkage/death), between studies conducted at traits are largely dependent on anemone body size and age. These northern vs. southern sites, at inshore vs. offshore sites, and under la- findings demonstrate that populations are heavily reliant on regular boratory vs. field conditions (Fig. 4). Individuals exhibit a higher pro- recruitment to maintain population size, and can experience 100% portion of positive transitions at calm-water, high-nutrient, cooler sites, turnover of individuals within 12–24 mos. than at rough-water, low-nutrient, relatively warm sites. Additionally, Recruitment rates vary widely for these anemones between sites the growth and survival rates of these anemones vary temporally, and within region (two sites each within the USVI and Florida) that are only are higher in the field during winter periods with relatively cool tem- ~ 2 km apart, and between regions (USVI vs. Florida, ~1800 km apart, peratures, than during summer when temperatures are warmer O'Reilly and Chadwick, 2017, present study). A combination of ane- (O'Reilly and Chadwick, 2017; present study). Recent experimental mone body size, abundance, and local environmental conditions may laboratory data indicate that the optimal temperature for this species is contribute to this variation. In particular, small anemones under la- ~24o C (similar to temperatures in the laboratory and in the northern boratory conditions produce recruits via pedal laceration, but only Florida Keys during winter), with body shrinkage occurring when when starved, suggesting that nutritional limitation may trigger clonal temperatures are substantially higher (as in the USVI or in the southern replication in this species (Titus, 2011). Local abundance also could enhance recruitment (O'Reilly and Chadwick, 2017), with populations that contain the highest abundance receiving the most recruits. Recruits likely are produced by both sexual and asexual processes, although a genetic study by Titus et al. (2017) indicated that populations in both the USVI and Florida rely primarily on . Long-lived genets or ramets of some cnidarians may occupy the same locations on coral reefs over long time spans (Bythell et al., 2018), but this likely is rare for B. annulata and other sea anemones (Dixon et al., 2017; O'Reilly and Chadwick, 2017; present study). Dispersal ability and the degree to which B. annulata larvae self- recruit to their home reefs remain unknown, but recent evidence sug- gests weak genetic structure and moderate gene flow across large spa- tial scales (Titus, 2017). This species may rely primarily on sexual re- production via broadcast spawning (Titus et al., 2017), and the subsequent recruits may be attracted to parent populations, similar to scleractinian corals in which the planktonic larvae are attracted to Fig 4. Variation in matrix transition rates among populations of conspecifics (Bramanti and Edmunds, 2016) and often self-recruit to Bartholomea annulate at various Caribbean sites. Variation in transition parent populations (Figueiredo et al., 2013; Swearer et al., 2002). The rates among populations of corkscrew sea anemones Bartholomea annulata,in pattern of significantly higher recruitment observed here per unit reef terms of the proportion of individuals in each population that exhibited growth, stasis, shrinkage, or mortality. Rates are shown for 2 sites at St. Thomas, U.S. area at a site that contained relatively more abundant anemones, in Virgin Islands: Flat Cay, an offshore site (USVI FC), and Brewers Bay, an inshore addition to similar patterns observed between sites examined in Florida site (USVI BB; present study); 2 sites in the lower Florida Keys: Cudjoe, a (O'Reilly and Chadwick, 2017) support the hypothesis that these larvae southern site (FL Keys C), and Quarry, a northern site (FL Keys Q; O'Reilly and may self-recruit to parental reef areas. Chadwick, 2017); and for individuals cultured under laboratory conditions at Individual growth rates in this species are inversely proportional to Auburn University (Lab; O'Reilly, 2015). Data are expressed as mean values body size, with small anemones growing 2-3× faster than large ones. from 4 census periods extending 3 mo each (USVI sites), or 6 census periods The growth rate of B. annulata under laboratory conditions (Titus, extending 2 mo each (Florida sites and laboratory tanks). See text for details. 2011; O'Reilly, 2015) generally outpaces that under field conditions, as Note that growth plus stasis were highest, and mortality lowest, in the la- measured in both the USVI (present study) and Florida (O'Reilly and boratory populations; Florida values were intermediate; and that the offshore Chadwick, 2017), but the smallest individuals grow the fastest in all USVI site exhibited the lowest growth

50 E. O'Reilly et al. Journal of Experimental Marine Biology and Ecology 509 (2018) 44–53

Florida Keys during summer) or lower (as during low-temperature la- several decades, members of this species might have extensive enough boratory experiments, A. Colombara and N. Chadwick, unpublished lifespans to serve as effective hosts for many types of associated dec- data). apod crustaceans. Anemone shrimps reach sexual maturity within a few The patterns observed here of decreasing growth rate with body size months (Knowlton, 1980) and live < 2 yrs. (Gilpin and Chadwick, parallel those known for other coral reef cnidarians with indeterminate 2017; Spotte and Bubucis, 1997). Thus, juvenile crustaceans that recruit body size, including sea anemones (Chomsky et al., 2004; Dixon et al., to newly-settled sea anemones may acquire hosts that live the 6+ mos 2017; Sebens, 1980), mushroom corals (Chadwick-Furman et al., needed for the crustaceans to produce several generations of offspring. 2000), cup corals (Goffredo et al., 2004), and zooanthids (Karlson, Early sexual maturity and short lifespan thus could be a universal fea- 1988). The upper limit of body size for many marine may ture of tropical anemone-associated crustaceans (Chace Jr. and Bruce, be set by current environmental conditions rather than by pre-de- 1993). Although the abundance of associated crustaceans may increase termined limits imposed by genotype (Sebens, 1980). Further, large with anemone body size (Briones-Fourzán et al., 2012), there is no individuals require less energy per unit mass to meet metabolic re- evidence that B. annulata needs to meet a certain size threshold before quirements than do small individuals, and can allocate more energy hosting symbionts. Crustaceans recruit to B. annulata when the hosts toward reproduction (Sebens, 1982). Organisms must thus invest more are still quite small (Gilpin and Chadwick, 2017; S. Ratchford and N. energy into growth and metabolic requirements than into reproduction, Chadwick, unpublished data). As such, relative to the apparent biology when relatively small. The interplay of these factors may partially ex- of their symbionts, these anemones appear to be static enough to plain the patterns observed for B. annulata at FC, where relatively high mediate multiple generations of crustaceans. water flow may act to limit body size well below biomechanical or Shrimp migration among anemones could limit the impact of B. genetic restrictions, whereas calmer and higher nutrient conditions at annulata on crustacean lifespans. Sexually mature A. armatus move up BB may allow individuals to reach body sizes closer to their physical to 4 m from their anemones at night, to forage and colonize new, pos- maxima. However, the present study did not include replicate analyses sibly younger hosts (Knowlton, 1980). Likewise, the anemone shrimps at the site level, so definite conclusions about effects of physical or A. pedersoni and P. yucatanicus are host generalists and can reside on a biological variables on anemone demography in the field cannot yet be variety of large tropical anemone species (Briones-Fourzán et al., 2012; made. Titus and Daly, 2017), although their rates of among-host migration The inverse relationship observed here between body size and remain unknown. The closely-related cleaner shrimp long- mortality rate is similar to that recorded for field populations in Florida icarpus on Indo-Pacific reefs migrates frequently among anemones (O'Reilly and Chadwick, 2017), as well as for other sea anemones and nocturnally (Chadwick et al., 2008). Because some of these associated corals that die over decadal time scales (Goffredo and Chadwick- crustaceans provide behavioral and physiological benefits to anemones Furman, 2000; Hughes and Tanner, 2000; Dixon et al., 2017). Small (Cantrell et al., 2015; McCammon and Brooks, 2014), future studies are anemones likely face high rates of predation and impacts from other warranted to examine how crustacean symbionts impact the hosts at types of biological interactions, as well as enhanced sensitivity to the level of population dynamics. changes in physical factors such as temperature and water flow com- It is concluded that B. annulata displays far more rapid turnover of pared to large individuals, as known for other reef cnidarians (Shick, individuals than would be expected for a symbiotic host species. For the 1991). large assemblage of fishes that relies on this symbiosis for ectoparasite Turnover rates were high at both sites examined here, indicating removal services, these anemone-based cleaning stations thus are that population abundances may fluctuate rapidly and rely heavily on transient, short-lived features of coral reefs. The reef fishes in > 20 frequent recruitment. The similar turnover rates at all sites examined common families that regularly visit A. pedersoni cleaning stations thus far, with < 25% of populations surviving 12 mos, and complete (Huebner and Chadwick, 2012a) must frequently search for recently- population turnover in < 24 mos (O'Reilly and Chadwick, 2017; pre- recruited anemones, as the older ones senesce and die. In Florida and sent study), together indicate that short lifespan likely is an inherent Puerto Rico, these anemones and symbiotic crustaceans are harvested feature of this species. Some large, old laboratory individuals have been for the ornamental aquarium trade, and are listed as a species of con- observed to senesce (shrink) prior death (O'Reilly, 2015), as also ob- servation concern (Legore et al., 2005; Rhyne et al., 2009). The short served at field sites in Florida (O'Reilly and Chadwick, 2017). While lifespans (compared to that of some other cnidarians) of these cnidarians have been thought not to age or senesce (Comfort, 1979; and their reliance on frequent reproduction (Titus et al., 2017) suggest Finch, 1991; Kirkland, 1989), senescence and limited lifespan that, while this symbiotic system may be stable where populations are (< 10 yrs) have been documented for large Indo-Pacific sea anemones abundant, overharvesting could lead to an almost immediate popula- (Dixon et al., 2017; McVay, 2015). Individuals of the short-lived tion crash of both anemones and crustaceans. Given the ecological branching coral Stylophora pistillata cease sexual reproduction and stop importance of these symbioses as cleaning stations for reef fishes, there growing, and their exosymbiotic fish and symbionts desert them, could be immediate, radiating effects of either anemone or cleaner over several months prior to death (Rinkevich and Loya, 1986; shrimp removal from coral reef ecosystems. Wolodarsky, 1979). Senescence likewise has been reported for hydro- medusae Gonionemus vertens, in which old individuals exhibit a higher Declarations of interest frequency of infection and deterioration than do young ones (Mills, 1993). Genetically-programmed senescence could be a common feature None. of old age in some cnidarians, but may be detected rarely due to a lack of frequent monitoring near the end of individual lifespans. Estimates Acknowledgements for B. annulata reveal that this species is the shortest-lived sea anemone on record, with lifespans much shorter than those quantified for the few We thank members of the Chadwick laboratory who assisted with other tropical (Dixon et al., 2017) and temperate sea anemones this study, especially Stanton Belford, Channing Cantrell, Lindsay (Ottaway, 1980; Sebens, 1983) that have been examined to date. Huebner, Ashley Isbell, Kathy Morrow, Joey Szczebak, Jessica Gilpin, Mark Stuart, and Jill Titus. We also thank the students at the University 4.3. Conceptual framework for the symbiosis of the Virgin Islands (UVI) who assisted with the field work, and the staff of the MacLean Marine Science Center at UVI for logistical support, These findings have important implications for population dynamics especially Steve Prosterman. This work was supported by NOAA Puerto of the crustaceans that form exosymbiotic associations with B. annulata. Rico Sea Grant [R-101-1-08] to NEC, and an NSF EPSCoR mini-grant While our data contravene expectations that tropical anemones live for from the University of the Virgins Islands to NEC and SR. Portions of the

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53 Erratum for:

O'Reilly, E., Titus, B.M., Nelsen, M.W., Ratchford, S., Chadwick, N.E. 2018. Giant ephemeral anemones? Rapid growth and high mortality of corkscrew sea anemones Bartholomea annulata (Lesueur, 1817) under variable conditions. J. Exp. Mar. Biol. Ecol. 509: 44-53.

Additional Acknowledgements

This material is based upon work supported by the National Science Foundation under Grant No. 0346483, as part of an NSF EPSCoR mini-grant from the University of the Virgins Islands (UVI) to NEC and SR. This is contribution number 200 from the Center for Marine and Environmental Studies at UVI.