Age and growth of invasive lionfish - IngentaConnect

Bull Mar Sci. 90(4):953–966. 2014 http://dx.doi.org/10.5343/bms.2014.1022

research paper

Age and growth of invasive lionfish (Pterois spp.) in the Caribbean Sea, with implications for management School of Forest Resources and Conservation, University of Florida, 7922 NW 71st Street, Gainesville, Florida 32653. 1

2 School of Natural Resources and Environment, University of Florida, 103 Black Hall, Gainesville, Florida 32611.

Soil and Water Science Department, University of Florida, 7922 NW 71st Street, Gainesville, Florida 32653.

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Corresponding author email: , phone: 352–273–3648, facsimile: 352–392–3672.

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Date Submitted: 11 March, 2014. Date Accepted: 17 July, 2014. Available Online: 15 August, 2014.

Morgan A Edwards 1 * Thomas K Frazer 1, 2 Charles A Jacoby 2, 3 ABSTRACT.—Removal efforts designed to avoid or minimize impacts from introduced lionfish, Pterois volitans (Linnaeus, 1758) and Pterois miles (Bennett, 1828), in the western Atlantic Ocean, Caribbean Sea, and Gulf of Mexico will be improved by reliable life history information applicable to the invaded range. For example, length at age has been modeled for lionfish from temperate North Carolina, but parameters characterizing growth are likely to differ in the tropics. Using Pterois spp. from Little Cayman, we validated formation of annual increments and daily rings in sagittal otoliths; documented ages; and estimated parameters for a length-weight relationship, multiple von Bertalanffy growth models, and an asymptotic vulnerability schedule. Formation of annuli was confirmed with marginal increment analysis, and daily ring deposition in juveniles was confirmed using an oxytetracycline hydrochloride marker. Total weight (g) estimated from combined data for both sexes was equal to 0.000003 × total length (mm)3.24. Logistic regression indicated that 50% of lionfish were vulnerable to removal at 129 mm total length. Sagittal otoliths (n = 499) from lionfish collected weekly between January and December 2011 indicated that males were 0–5 yrs old and females were 0–3 yrs old. A maximum likelihood approach to fitting von Bertalanffy equations estimated K and L ∞ as 0.42 and 349 mm for the population, 0.38 and 382 mm for males, and 0.57 and 286 mm for females. An age-structured population model indicated that annual exploitation rates of 15%–35% may induce recruitment overfishing, with recovery to 90% of pre-removal biomass occurring 5–20 yrs after removals cease.

In the western Atlantic Ocean, Caribbean Sea, and Gulf of Mexico, the introduction, establishment, and spread of two species of lionfish, Pterois volitans (Linnaeus, 1758) and Pterois miles (Bennett, 1828), have added to concerns about pollution, disease, overfishing, and other threats confronting managers of the region’s marine resources. Lionfish were introduced to Florida’s waters in the 1980s (Morris and Whitfield 2009). They spread up the east coast of the United States, and by 2000, lionfish were found as far north as Cape Hatteras, North Carolina (Schofield 2010). Bulletin of Marine Science

© 2014 Rosenstiel School of Marine & Atmospheric Science of the University of Miami

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Since that time, lionfish have spread throughout the Caribbean Sea and Gulf of Mexico (Aguilar-Perera and Tuz-Sulub 2010), in part because they have broad environmental tolerances, the capacity for frequent reproduction (Morris 2009), a generalist diet (Green et al. 2011), and other traits that make them ideal invaders (Morris and Whitfield 2009). In addition to promoting the spread of lionfish, these traits have allowed lionfish to reach densities of 300–650 fish ha−1 in multiple locations (Green and Côté 2009, Frazer et al. 2012). Such densities have the potential to significantly reduce the numbers and biomass of native prey species. Albins and Hixon (2008), for example, found that lionfish on experimental patch reefs in The Bahamas reduced recruitment of native reef fish by approximately 80%. The significant concerns about lionfish have led to attempts to mitigate their impacts. Present management focuses on manual removal of lionfish at discrete locations (Albins and Hixon 2011). For example, Bermuda instituted a culling program in 2008 that provided training to those interested in removing lionfish (Morris 2009), and other countries are doing the same (López-Gómez et al. 2013). Even diligent application of these methods is unlikely to eradicate lionfish; however, reduced densities may yield benefits such as decreased predation pressure on native species (Frazer et al. 2012). The amount of effort necessary to generate tangible benefits depends on the population dynamics of lionfish. Key parameters determining population dynamics include vulnerability to removal and factors that vary among regions within the invaded range, such as compensatory survival, growth, and reproduction. Growth, for example, can be influenced by water temperature and food availability making information from different regions valuable (Rogers and Ruggerone 1993, Beamesderfer and North 1995). Thus far, estimates of growth coefficients have been published only for North Carolina waters (Potts et al. 2010, Barbour et al. 2011), the northernmost region in the invaded range where lionfish are expected to overwinter. Therefore, estimates of parameters characterizing population dynamics in the Caribbean Sea should benefit natural resource managers in the tropics. In an effort to provide such information, the present study was conducted at Little Cayman, where lionfish were first observed in 2008. Ages as determined from growth marks in sagittal otoliths, total lengths, total weights, and von Bertalanffy growth equations were used to estimate parameters characterizing the population dynamics of lionfish. The resulting information was used to evaluate the efficacy of removing lionfish. Thus, the objectives of our study were to: (1) validate the periodicity of annual and daily growth marks in otoliths; (2) model growth, morphometrics, and vulnerability to removal for lionfish from Little Cayman; (3) evaluate sex-specific growth rates; and (4) employ an age-structured population model (sensu Barbour et al. 2011) to assess the management implications associated with key life history parameters. Materials and Methods Little Cayman is approximately 17 km long and 2 km wide, with a population of fewer than 200 people (Manfrino et al. 2013). Members of the community organized weekly removals of lionfish between January and December 2011, and they donated the fish for the present study. Most lionfish were likely to be P. volitans, the dominant species in the Caribbean, but some specimens of P. miles may have been taken (Betancur-R et al. 2011). The majority (93%) of lionfish collected for our study were

Edwards et al.: Age and growth of lionfish

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removed from reef walls in Bloody Bay Marine Park, a focal point for tourist activity. Collections were made by scuba divers using either spears or nets in 15–30 m of water. After collection, fish were placed on ice and processed at Little Cayman Research Center. Total lengths to the nearest 1 mm and wet weights to the nearest 0.1 g were recorded for all fish. Lionfish were sexed via macroscopic examination of their gonads, and their sagittal otoliths were removed, rinsed in fresh water, dried, and stored in uniquely numbered plastic vials. Wet weights and total lengths were used to generate two relationships. The relationship between wet weights and total lengths was determined by fitting a power function to the relevant data. In addition, the length at which 50% of lionfish became vulnerable to capture was estimated by logistic regression using data from spearing and netting, which assumed the existence of an asymptotic vulnerability schedule. Ages were determined from sagittal otoliths. Whole sagittae were submersed in fresh water on a black background, and examined under reflected light using a dissecting microscope at 40–60× magnification. An age in years was assigned according to the number of opaque zones present. To ascertain within-reader consistency, one reader analyzed all otoliths twice, with the two readings separated by several months. If the two readings did not agree, those otoliths were excluded from future analyses. A second experienced reader examined otoliths with matching independent readings to assess consistency between readers. The opinion of a third experienced reader settled disagreements between the first and second readers. Indistinct zones in otoliths may be due to impaired physiological condition; therefore, relative condition factors (Kn) were computed as:

Kn =

W o (Eq. 1) aLb

where Wo is the observed weight, L is the total length, a is the coefficient from the allometric relationship between weight and length, and b is the exponent in that relationship. A two-sample t-test that did not assume equal variances was used to compare relative condition factors between fish that were aged and those with unreadable otoliths. Marginal increment analysis was employed to validate production of annuli and to determine the timing of increment formation for lionfish from Little Cayman. These analyses were based on an index of completion (C):

W C = W n (Eq. 2) n-1 where Wn represents the width of the marginal increment, and Wn−1 represents the width of the preceding, complete annulus (Tanaka et al. 1981). Measurements of Wn and Wn−1 were made on photographs of whole otoliths using ImageJ software (http:// imagej.nih.gov/ij/). Means were calculated from values for fish that were at least 1-yr old, and a distribution of mean indices of completion exhibiting higher values in consecutive months was interpreted as evidence that visible increments represented annuli (Murie and Parkyn 2005). Daily rings in otoliths of age-0 fish were counted to improve modeling of growth by assigning ages based on partial years to fish with fewer than one annulus, determine an approximate date of spawning, and calculate a daily growth rate for juvenile

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lionfish. Otoliths were fixed to glass slides using Histamount® and then wet-ground and polished until the plane passing through the nucleus was reached and daily rings became visible. Otoliths were viewed through a compound microscope at 100–200× magnification. Daily rings were counted twice by a single reader, with the counts separated by 4 wks. If an otolith had more than 110 rings, that otolith was excluded due to a documented decrease in the accuracy of counts for large numbers of rings (Sweatman and Kohler 1991). The date of hatching was calculated by subtracting the daily ring count from the date when the fish was collected, and an age, as a fraction of a year, was assigned to the fish by dividing the number of daily rings by 365. In addition, average daily growth rates (mm of growth d−1) were calculated by dividing total lengths by the daily ring count. Daily ring formation was validated by immersing five, age-0 lionfish in a solution of 500 mg L−1 oxytetracycline hydrochloride (OTC) for 24 hrs. Lionfish were removed from the OTC treatment and held for 10 d in an aquarium before otoliths were prepared as described for reading of daily rings. The fluorescent band produced by OTC exposure and the number of daily rings produced subsequently were identified at 400× magnification using a compound microscope equipped with a blue filter. Age and length data were used to model growth by estimating parameters in von Bertalanffy growth equations (von Bertalanffy 1957):

L t = L 3 Q1 - e -K!t - t $V (Eq. 3) 0

where Lt = length at age (t), L∞ = asymptotic maximum length, K = the Brody growth coefficient or rate of growth toward L∞ (Newman et al. 1996), and t0 = the theoretical age at which a fish would be 0 mm in length. A maximum likelihood framework was used to estimate L∞, K, and t0 for the population. Models also were created using data for males only and for females only, with data for one half of the juvenile, unsexed lionfish randomly allocated to each sex. In both cases, the estimate of t0 derived for the population was used because independent estimates did not yield realistic values. Thus, four different models were compared: (1) L∞ and K estimated independently for males and females; (2) the estimate of K derived from data for the population assigned to both sexes and L∞ allowed to vary independently; (3) the estimate of L∞ derived for the population assigned to both sexes and K allowed to vary independently; and (4) estimates of L∞ and K for the whole population assigned to males and females. Akaike information criteria (AIC) were used to identify the most appropriate model, with t0 excluded because it was constrained. Models with AIC values that differed by 10 indicated no support for the alternative model (Burnham and Anderson 2004). Given the relatively recent arrival of lionfish at Little Cayman, the potential for biased estimates of growth due to the absence of older fish was investigated with two models applied to data from North Carolina, where lionfish were reported 8 yrs earlier (Barbour et al. 2011). The length-at-age data from North Carolina were truncated to include only fish that were 0–5 yrs old, and estimates of L∞ and K generated by a von Bertalanffy model were compared to those generated for data from fish 0–8 yrs old (Barbour et al. 2011).


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Figure 1. Length-weight relationship for lionfish (n = 1887) collected off Little Cayman in 2011.

In addition, parameters generated in our study were substituted into a model that predicted the efficacy of removals (Barbour et al. 2011). The results of this modeling were compared to those generated for data from the North Carolina population of invasive lionfish (Barbour et al. 2011). Results Over the 12-mo period, 1991 lionfish were collected from the waters surrounding Little Cayman. Of the 1991 lionfish collected, 1096 could be sexed yielding 563 males and 533 females. Fish ranged from 27 to 391 mm in total length (TL) and 0.2 to 973.0 g in weight, with 50% of lionfish becoming vulnerable to removal by spearing and netting at 129 mm TL. For combined data from juveniles, males and females, wet weights were related to total lengths (r 2 = 0.97; Fig. 1) according to:

Wet weight = 0.000003 # TL3.24 (Eq. 4) In total, 1188 pairs of otoliths were undamaged by spearing and suitable for reading. Lack of within-reader agreement resulted in 689 otoliths being eliminated (58%). Lack of agreement between readers (56% of the remaining otoliths) was resolved by a third reader resulting in 499 otoliths being used in further analyses. No significant difference (t1033 = 1.11, P = 0.267) was found between condition factors for aged fish [mean = 1.15 (SD 0.16)] and condition factors for fish that were not aged [(1.16 (SD 0.17)]. Of the fish yielding readable otoliths, 238 could be sexed, with 110 being males and 128 being females. This ratio, approximately 1:1, was consistent with that observed for all sexed lionfish collected off Little Cayman in 2011 (i.e., 563 males and 533 females). Formation of annuli and daily rings in otoliths was confirmed. Higher mean monthly indices of completion indicated the formation of one annulus per 12-mo period, with annuli being completed across multiple months as expected for a tropical fish (Fig. 2; Sparre and Venema 1998). In fish treated with OTC and held for 10 d,

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Figure 2. Mean indices of completion (SE) for 1–5 yr old lionfish (n = 288). Numbers indicate the number of otoliths examined in each month.

the presence of 10–11 rings beyond the fluorescent OTC mark confirmed formation of daily rings. Otoliths extracted from 29 fish that had total lengths of 27–199 mm contained 23–110 daily rings. Growth rates ranged from 1.10 to 2.55 mm TL d−1 and averaged 1.55 mm TL d−1, which translated to 0.80–1.86 mm d−1 increases in standard length (SL) with an average of 1.13 mm d−1 (SL = 0.73 × TL) (D Huge, University of Florida, unpubl data). Back-calculations indicated multiple recruitment events by fish that hatched in January, February, March, June, and November of 2011. Two-yr old fish represented the largest age class for both sexes (Fig. 3). Males were 0–5 yrs old and 27–391 mm TL, whereas females were 0–3 yrs old and 40–333 mm TL (Table 1). The three growth curves fit to length-at-age data for all fish, males, and females differed (Fig. 4; Table 2). The AIC values supported the use of a model where all parameters varied independently (Table 2). Males were predicted to grow larger (L∞ = 382 mm, Table 1) and reach their asymptotic maximum length more slowly (K

Figure 3. Age frequency distribution for lionfish (n = 499) collected off Little Cayman in 2011.


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Table 1. Parameters of von Bertalanffy growth equations estimated for all lionfish, males and females. L∞ = asymptotic maximum length; K = rate of growth toward L∞; t0 = theoretical age when total length is 0. Group All lionfish Males Females

L∞ (mm) 349 382 286

K 0.42 0.38 0.57

t0 −1.01 −1.01 −1.01

n 499 110 128

Range of ages 0–5 0–5 0–3

Figure 4. Growth curves fit to length (Lt) at age (t) data for (A) all lionfish (n = 499), (B) males (n = 110), and (C) females (n = 128).

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Table 2. Akaike Information Criteria (AIC) for model comparisons. L∞ = asymptotic maximum length; K = rate of growth toward L∞; sig = variance around the mean size at age; (h) = a separate parameter for males and females; (●) = parameter shared by both sexes; Total LL = total log likelihood for the model; ΔAIC = change in Akaike Information Criterion. Models L∞(h)K(h)sig(h) L∞(h)K(●)sig(h) L∞(●)K(h)sig(h) L∞(●)K(●)sig(●)

Parameters 6 5 5 3

Total LL −1,560.86 −1,566.60 −1,572.98 −1,586.93

AIC 3,133.72 3,143.20 3,155.97 3,179.87

ΔAIC 0.00 9.48 22.25 46.15

= 0.38, Table 1) than females (L∞ = 286 mm, K = 0.57, Table 1). The model based on data from all lionfish yielded intermediate values (L∞ = 349 mm, K = 0.42, Table 1). Modeling of intentionally truncated length-at-age data from North Carolina resulted in minor differences in L∞ and K. With t0 set at −0.05, the 0–8-yr old age range yielded an L∞ of 483 mm TL and a K of 0.30 (Barbour et al. 2011) and the 0–5-yr old age range yielded an L∞ of 495 mm TL and a K of 0.29. These differences would generate a 9 mm or 2% difference in TL for 10-yr old lionfish, with the similarity of estimates potentially due to only nine lionfish being over 5 yrs old. The potential success of removals was explored using a model previously applied by Barbour et al. (2011) to data for lionfish from North Carolina. In this approach, values of L∞, K, a (the coefficient from the power function relating wet weight to total length), b (the exponent from the power function relating wet weight to total length), and Lvul (the length at which 50% of lionfish became vulnerable to removal) used by Barbour et al. (2011) were replaced with values generated for Little Cayman (Table 3). As reported by Barbour et al. (2011), changes in Lvul generated differences in effort needed to achieve success through removals and the persistence of reductions in biomass. When values for Lvul were similar, the effort required to induce recruitment overfishing also was similar, i.e., 15%–35% (Table 3). In contrast, the model based on values generated for lionfish from Little Cayman indicated that recovery to 90% of initial, unfished biomass would take an additional 4 yrs when natural mortality and the Goodyear compensation ratio were set at their lower values (Table 3). Discussion Here we provide the first insights into the age structure of the invasive lionfish population established off Little Cayman, the first successful validation of daily ring deposition in otoliths of lionfish, and the first estimates of key parameters needed to model growth of lionfish in the Caribbean Sea. Such information can be used to improve management of this invasion in an effort to reduce detrimental impacts on Caribbean coral reefs. Although annuli in otoliths from tropical fish can be difficult to interpret due, in large part, to less pronounced seasonality (Caldow and Wellington 2003, Marriott and Mapstone 2006, Green et al. 2009), readings of whole otoliths provided useful estimates of age for lionfish from Little Cayman, and marginal increment analysis validated annual deposition of increments. The visibility of annual increments in otoliths varied among fish, but sufficiently distinct opaque and hyaline bands allowed ages to be determined for approximately 50% of the fish sampled. As found by Vilizzi and Walker (1999) for common carp, sectioning did not increase interpretability.


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Table 3. Results of Barbour et al. (2011) compared to outputs using parameters generated for Little Cayman. All models used 10% of the length at 50% vulnerability as its standard deviation, and 0.07 kg as the weight at which 50% of female lionfish were mature. L∞ = asymptotic maximum length, K = Brody growth coefficient, a = coefficient from the power equation relating wet weight to total length, b = exponent from the power equation relating wet weight to total length, Lvul = length at 50% vulnerability to removal, M = natural mortality, CR = Goodyear compensation ratio, USPR < 0.35 = the finite annual exploitation rate (U) required to reduce the spawning potential ratio (SPR) below 0.35 thereby causing recruitment overfishing, Rec = years required for the population to recover to 90% of its initial biomass after removals cease. North Carolina

Little Cayman

L∞ K a b Lvul M CR USPR < 0.35 Rec L∞ K a b Lvul M CR USPR < 0.35 Rec 425 0.47 2.89 × 10−5 2.89 159 0.5 15 0.35 6 349 0.42 3.00 × 10−6 3.24 129 0.5 15 0.30 5 5 0.30 10 5 0.25 9 0.2 15 0.20 12 0.2 15 0.20 12 5 0.15 16 5 0.15 20 259 0.5 15 0.65 6 5 0.50 9 0.2 15 0.25 11 5 0.20 16

It is possible that the inability to age approximately half of the lionfish otoliths collected in our study may have been a consequence of differential growth. Hoyer et al. (1985), for example, suggested that slower growing fish produced crowded annuli that were difficult to discern. Condition factors calculated for the two groups of fish in our study (i.e., fish that could be aged and those that could not be aged) provided no evidence for differential growth; therefore, the growth equations provided here should not be biased. Annuli in sagittal otoliths indicated that the population of lionfish off Little Cayman comprised 0–5-yr old males and 0–3-yr old females. In general, these results matched the reported timeline of the invasion, with lionfish initially reported off Little Cayman in 2008 (Schofield 2009). The single 5-yr old male provided evidence that undetected lionfish arrived before 2008. Introduced species often remain undetected until their densities increase, creating a lag between actual introduction and discovery (Crooks 2005). Daily ageing validated by incorporation of OTC improved estimates of growth. These results also provided evidence of multiple periods of recruitment consistent with the potential for multiple periods of spawning (Morris and Whitfield 2009, Gardner 2012). In addition, combining ages in days with sizes yielded a mean growth rate of 1.55 mm TL d−1 or 1.13 mm SL d−1. This estimate exceeded the mean daily growth rate of 0.46 SL mm d−1 reported by Jud and Layman (2012) for lionfish from the lower Loxahatchee River in Florida. The two estimates were generated from fish of similar sizes (21–156 mm SL here and 45–185 mm SL for Jud and Layman 2012), but Jud and Layman (2012) used a mark-recapture technique to estimate growth. Beyond this methodological difference, other factors (e.g., temperature, salinity, and/ or diet) likely played important roles in generating different growth rates for juvenile lionfish from the two locations (Moyle and Light 1996, Baltz et al. 1998). Lionfish from Little Cayman appeared to reach their maximum length as fast or slightly faster than fish from North Carolina, with K values for fish from Little Cayman equal to 0.42 for the population, 0.38 for males, and 0.57 for females (Table 1), and K values for lionfish from North Carolina equal to 0.32 or 0.47 (Potts et al.

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2010, Barbour et al. 2011). Lionfish from Little Cayman may not, however, have reached the same maximum size, with L∞ values for fish from Little Cayman equal to 349 mm for the population, 382 mm for males, and 286 mm for females (Table 1) and L∞ values for lionfish from North Carolina equal to 455 mm or 425 mm (Potts et al. 2010, Barbour et al. 2011). Faster growth for a tropical population was not unexpected given the warmer water temperatures, with Beamesderfer and North (1995), for example, reporting faster growth rates for largemouth bass in southern waters as compared to northern populations. Furthermore, Murie and Parkyn (2005) suggested that species exhibiting high site fidelity may be especially susceptible to developing regional differences in growth rates, and Jud and Layman (2012) provided evidence that most lionfish do remain within 10 m of a site in south Florida. In comparison to several other native, medium-bodied predators in the Caribbean, lionfish appeared to reach their asymptotic maximum length faster, with growth coefficients being 2–4× greater (Table 4). Eventually, the relatively rapid growth exhibited by lionfish may be moderated by abiotic or biotic factors, such as water temperature or food availability (Rogers and Ruggerone 1993, Rose 2000). The Potts et al. (2010) and Barbour et al. (2011) studies did not produce separate growth coefficients for the sexes. However, estimates of growth coefficients for males and females were provided in our study. The lionfish population off Little Cayman exhibited sexually dimorphic growth, when t0 was constrained to the value estimated for the population. As found by Vilizzi and Walker (1999), if t0 was not constrained, curve fitting led to unreasonable values for L∞ and K. Given this constraint, female lionfish from Little Cayman reached their asymptotic maximum length 1.5× faster than males, but they only achieved a maximum length that was 0.75× that of males. Sexually dimorphic growth is a relatively common phenomenon for fish, and it has been reported for a number of taxa including snappers and white grunt (Newman et al. 1996, Murie and Parkyn 2005). Data from larger numbers of 0 to 1-yr old fish from Little Cayman should have increased the accuracy of estimates for growth parameters. According to logistic regression, 50% of lionfish became vulnerable to removal at 129 mm TL. As a consequence, smaller size classes may have been underrepresented, which typically leads to a more negative estimate of t0 and a lower estimate of K (Gwinn et al. 2010). Estimates of L∞ and K also may have been affected by the fact that the relatively recently-established population of lionfish off Little Cayman lacks older and larger fish, which results in a truncated growth curve. Potts et al. (2010) found that the maximum size of lionfish taken from a 10-yr old population of lionfish off North Carolina was 464 mm TL and the maximum age was 8 yrs old, with these fish representing larger and older fish than the 391 mm TL and 5-yr old fish from Little Cayman. Nevertheless, growth appeared to be asymptotic from age 5 onward in the North Carolina population (Barbour et al. 2011), which was the oldest age class found off Little Cayman. For this reason, we suggest that the most critical portion of the curve is represented in our data, and we can infer that key parameters describing growth reflect the current state of the population. Using parameters generated for lionfish from Little Cayman, output from the model constructed by Barbour et al. (2011) indicated that similar effort would be necessary to induce recruitment overfishing in the Caribbean; however, our estimate of Lvul led to a 4-yr delay in recovery to 90% of pre-removal biomass when natural mortality and compensation were low. Improvements in the effectiveness of


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Table 4. Growth coefficients for lionfish and native, medium-bodied predators from the Caribbean Sea [values from http://www.fishbase.org (Froese and Pauly 2009), accessed February 28, 2014]. K = rate of growth toward L∞ the asymptotic maximum length. Scientific name Pterois spp. Haemulon flavolineatum (Desmarest, 1823) Lutjanus analis (Cuvier, 1828) Ocyurus chrysurus (Bloch, 1791) Epinephelus striatus (Bloch, 1792) Epinephelus guttatus (Linnaeus, 1758) Mycteroperca tigris (Valenciennes, 1833)

Common name Lionfish French grunt Mutton snapper Yellowtail snapper Nassau grouper Red hind Tiger grouper

K 0.42 0.20 0.20 0.10 0.10 0.20 0.10

Source Present study Fishbase Fishbase Fishbase Fishbase Fishbase Fishbase

removals when smaller lionfish were vulnerable confirmed the results of Morris et al. (2011) whose model also showed that inflicting mortality on juveniles improved the results of removals. Here we provide important information for those working to ameliorate detrimental effects from the lionfish invasion in the form of the first estimates of growth coefficients, sex ratios, and age structure for the Caribbean region. The relatively fast and sexually dimorphic growth of lionfish combined with evidence of multiple recruitment events from analysis of daily rings in otoliths generates several implications for managers. For example, repeated recruitment may force managers to increase the frequency of removals to keep pace with the supply of lionfish. In addition, the relatively fast growth exhibited by lionfish is likely to translate into earlier onset of reproduction, which exacerbates concerns about the supply of recruits (Hutchings 1993). Further management implications may be related to sexually dimorphic growth. Typically, concerns arise if females reach larger sizes than males and fishing differentially removes larger individuals to the extent that sex ratios become skewed, spawning stock biomass is reduced, overall fecundity is decreased, and the fishery collapses (Marshall et al. 2005). For lionfish, the pattern of sexually-dimorphic growth could lead to removal of more males because current methods have been shown to remove larger lionfish first (Frazer et al. 2012). If removals do not eliminate a sufficient number of females, then the success of removals may be compromised by sustained reproductive output. The sex ratio of lionfish removed in the present study was approximately 1:1; however, managers should remain vigilant to ensure that this ratio does not change. In the future, our understanding of the level of harvest necessary to reduce detrimental impacts of invasive lionfish would benefit from accurate estimates of natural mortality as well as documentation of any compensatory survival, growth, or reproduction. Acknowledgments We thank the resorts and dive staff on Little Cayman for donating the fish they removed; M Allen for comments and suggestions that improved the manuscript; A Dutterer and C Barrientos for assistance with otolith processing; A Barbour for assistance with modeling; D Murie and D Parkyn for assistance with marginal increment analysis; S Heppell for laboratory assistance and helpful input; J Morris and J Potts for training in reading otoliths from lionfish; the Central Caribbean Marine Institute for providing room, board, and the use of their facilities; and the Disney Worldwide Conservation Fund for providing financial support.

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