Grouper as a Natural Biocontrol of Invasive Lionfish

Peter J. Mumby

1,2*, Alastair R. Harborne1,2, Daniel R. Brumbaugh3,41

and Environmental Sciences, University of Exeter, Exeter, Devon, United Kingdom,

York, New York, United States of America,

Marine Spatial Ecology Lab, School of Biological Sciences, University of Queensland, St. Lucia, Queensland, Australia, 2 Biosciences, Hatherly Laboratory, College of Life3 Center for Biodiversity and Conservation, American Museum of Natural History, New4 Institute of Marine Sciences, University of California Santa Cruz, Santa Cruz, California, United States of AmericaAbstract

Lionfish (

of native fishes with a broad habitat distribution, lionfish are poised to cause an unprecedented disruption to coral reef

diversity and function. Controls of lionfish densities within its native range are poorly understood, but they have been

recorded in the stomachs of large-bodied Caribbean groupers. Whether grouper predation of lionfish is sufficient to act as a

biocontrol of the invasive species is unknown, but pest biocontrol by predatory fishes has been reported in other

ecosystems. Groupers were surveyed along a chain of Bahamian reefs, including one of the region’s most successful marine

reserves which supports the top one percentile of Caribbean grouper biomass. Lionfish biomass exhibited a 7-fold and nonlinear

reduction in relation to the biomass of grouper. While Caribbean grouper appear to be a biocontrol of invasive

lionfish, the overexploitation of their populations by fishers, means that their median biomass on Caribbean reefs is an order

of magnitude less than in our study. Thus, chronic overfishing will probably prevent natural biocontrol of lionfishes in the

Caribbean.

Pterois volitans/miles) have invaded the majority of the Caribbean region within five years. As voracious predatorsCitation:

journal.pone.0021510

Mumby PJ, Harborne AR, Brumbaugh DR (2011) Grouper as a Natural Biocontrol of Invasive Lionfish. PLoS ONE 6(6): e21510. doi:10.1371/Editor:

Brian Gratwicke, Smithsonian’s National Zoological Park, United States of AmericaReceived

April 14, 2011; Accepted May 30, 2011; Published June 23, 2011Copyright:

unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

2011 Mumby et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permitsFunding:

Fellowship (www.pewenvironment.org) to PJM and a NERC Fellowship (NE/F015704/1) to ARH. The funders had no role in study design, data collection and

analysis, decision to publish, or preparation of the manuscript.

This project was funded by an ARC (http://www.arc.gov.au/) Laureate Fellowship, NERC (http://www.nerc.ac.uk/) grant, EU FORCE project, and PewCompeting Interests:

* E-mail: p.j.mumby@uq.edu.au

The authors have declared that no competing interests exist.Introduction

Over the last five years, one of the world’s most ornate fishes,

the lionfish (

Caribbean, spanning an area exceeding 5,000 km

generally believed that

miles

What makes the invasion of these species so important is their

voracious appetite for small fishes [3,4,5], combined with their

ability to invade multiple habitats, ranging from the outer margins

of reefs to sheltered mangrove lagoons [6,7]. Thus, small-bodied

and juvenile reef fish are now subjected to greatly elevated

predation and the usual strategies employed to avoid predation,

such as the usage of mangrove nurseries [8,9], may confer limited

benefit as lionfish occupy most habitats. The long-term consequences

of such predation on reef biodiversity and function are not

yet clear, but are a matter of grave concern.

The success of lionfish is partly attributable to its resistance to

predation, largely because of its elaborate portfolio of venomous

spines. In its native range of the Indo-Pacific, identification of

the predators of lionfish has proven elusive, although reports of

predation by the cornetfish,

for

[11] and the only confirmed indication of predation has been

the observation of lionfishes in the stomachs of two large-bodied

species of grouper,

Here, we ask whether grouper, one of the most heavily targeted

fisheries species in the world [13], could serve as a natural form

of biocontrol for invasive lionfishes. The use of predatory fishes

for controlling invasive species has been used in other

ecosystems [14], but has not previously been described for coral

reefs.

While grouper may have the capacity to consume lionfish, this

does not necessarily imply that they act as a biocontrol. Effective

biocontrol would require that grouper predation exerted a

significant net impact on the density of their prey, which might

not be the case if predation rates are low and/or lionfish

recruitment rates high. To establish whether grouper represent a

natural form of biocontrol for lionfish, we took advantage of a

natural fishing experiment in the Bahamas. A 20 year ban on

fishing within the Exuma Cays Land and Sea Park (ECLSP) has

enabled grouper populations to exceed those in fished areas [15].

Some five years after the invasion began, we ask whether these

increased densities of groupers are reducing lionfish densities and,

if so, consider whether this biocontrol mechanism is likely to be

feasible elsewhere in the Caribbean region.

Pterios volitans/miles), has invaded much of the2 [1]. It isP. volitans, together with a sister species, P., escaped from aquaria in Florida within the last decade [2].Fistularia commersoni, have been madeP. miles [10]. Fistularids are uncommon in the CaribbeanEpinephelus striatus and Myceteroperca tigris [12].Results and Discussion

A 20 year ban on fishing in the Exuma Cays Land and Sea Park

(ECLSP) has allowed predatory groupers to attain some of the

highest biomasses reported anywhere in the Caribbean. Taking

the region-wide dataset from the Atlantic Gulf Rapid Reef

Assessment Program [16], we show that the mean biomass of

grouper in the Park,

Caribbean sites (Fig. 1). Thus the ECLSP and it’s surrounding

areas provide an unusual opportunity to examine the potential of

groupers to act as a natural biocontrol of non-native lionfish.

,2000 g 100 m22, falls in the top 1% of allPLoS ONE | www.plosone.org 1 June 2011 | Volume 6 | Issue 6 | e21510

The biomass of lionfish was significantly negatively correlated

with the biomass of grouper, with predator biomass explaining

56% of the variance of prey biomass (linear regression p = 0.005,

Fig. 2, Table 1). Unlike large-bodied groupers (mean total length

55 cm, range 30–110 cm), other smaller predatory fishes such as

Cephalopholis

significant bearing on lionfish biomass (p =0.17, Table 1), which

might imply that large-bodied fish are the primary predators of

lionfish. The relationship of grouper on lionfish was strongly nonlinear

such that an 18-fold variation in predator biomass among

sites (

lionfish density (

lionfish biomass (Fig. 2). A 50% reduction in lionfish biomass was

achieved with a grouper biomass of 800 g 100 m

lionfish density to 30% its highest value required a further

doubling of grouper biomass to approximately 1516 g 100 m

spp., lutjanids, carangids and aulostomids had no,170–3000 g 100 m22) was related to a tenfold difference in,0.3–0.03 fish 100 m22) and 7-fold difference in22. Reducing22(Fig. 2). The mean body length of lionfish was 24.5 cm (SD 4.1,

range 15–34 cm).

Biocontrol is defined as the use of living organisms to suppress

the population density or impact of a specific pest organism,

making it less abundant or less damaging than it would otherwise

be [17]. Thus, at high levels, grouper appear to be a natural

biocontrol of lionfish, and likely caused the 7-fold difference in

lionfish biomass within a 30 km stretch of reef. Although we have

no data on whether this biocontrol is driven by grouper predation

or competitive pressure, three lines of evidence suggest that

predation is the most likely mechanism. First, lionfish have been

found in grouper stomachs [12] so there is direct evidence

supporting the mechanism. Second, large-bodied species of

grouper, such as

food resources as lionfish. A study comparing predation by small

individuals of

prey to lionfish [4,5],

grouper species targeted larger food items [18] such as fish

[19]. Given that the large-bodied grouper in our study were mostly

adults and larger than those studied by Stallings [18], it seems even

more unlikely that the two groups compete for food. Third, studies

of interactions between adult grouper and smaller, reef mesopredators

have discovered predation-based behavioural responses

of the prey rather than evidence of direct competition [20].

There remains much to learn about the scope for biocontrol of

lionfish. Laboratory and field trials are needed to understand the

size-dependency of the predator-prey relationship and the role that

small-bodied grouper and other piscivores may play, particularly

in preying upon juvenile lionfish. We also observed that lionfish

appeared to remain closer to refugia at sites with high grouper

densities suggesting that grouper may both reduce lionfish

densities and reduce the predation rates of lionfish in the area,

as they do for functionally similar small-bodied grouper [20].

Given that lionfish were absent in 2006 and only began to appear

throughout the Exumas in 2007, our results suggest the ability of

groupers to constrain the invasion over a 3 year period. It is

feasible that the absolute density of lionfish may change as the

invasion continues and repeated monitoring will study any change

in the relationship with grouper biomass. Further, it is not clear

whether continued recruitment of lionfish in non-reefal habitats,

that lack large predatory grouper [6], might increase the future

settlement of lionfish on reefs and challenge the efficacy of

biocontrol in grouper habitats. Finally, it is unclear whether sharks

play an active role in lionfish predation. The entire Exuma Cays

possess relatively high densities of reef sharks, with at least one

individual encountered per hour at each site. However, while

sharks are unlikely to have contributed to the gradients of lionfish

density observed here – because they were found throughout the

Epinephelus striatus, are unlikely to share the sameE. striatus and a meso-predator that feeds on similarsizedCephalopholis fulva, found that the largebodiedFigure 1. Frequency distribution of the number of sites supporting the current range of grouper biomasses recorded in the

Caribbean.

doi:10.1371/journal.pone.0021510.g001

Grouper Deplete Invasive Lionfish

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Data derived from the Atlantic Gulf Rapid Reef Assessment database. ECLSP = Exuma Cays Land and Sea Park.study region and are protected from fishing throughout the

bahamas – it is possible that they depress the overall density of

lionfish in The Bahamas [3].

Although the impacts of the lionfish invasion on biodiversity and

ecosystem function are not yet clear, our study provides insights

into the feasibility of natural biocontrol. It is sobering that

overfishing of large-bodied grouper [21,22] has left the median

biomass at only 178 g 100 m

results suggest that such a low biomass, which is more than an

order of magnitude less than that in the ECLSP, would have only

a minor impact on lionfish biomass because it is barely detectable

using our regression relationship. Thus, while grouper appear to

have the capacity to serve as a natural biocontrol, this is only likely

to be feasible in protected marine reserves [23] or if fishing

practices change to allow the maintenance of large individuals in

the population. One potential option would be the usage of slot

fisheries, that target intermediate-sized fishes and leave the largest

individuals to maintain reproduction and ecosystem processes

[24]. However, if the historical trend of poor management

continues [25] then direct capture and eradication may be the only

practicable form of lionfish control for much of the Caribbean.

Economic incentives, such as the development of a commercial

market for lionfish – which is beginning to happen in some parts of

the Caribbean – might help make direct interventions a costeffective

option.

22 in the Caribbean (Figure 1). OurMaterials and Methods

In May 2010, 12 sites were selected along a stretch of reef

spanning 30 km of the Exuma Cays, central Bahamas (Table S1).

Five sites were located in the ECLSP and seven sites were located

in fished areas to the north of the Park. Eight of the sites had been

visited before the invasion [26] and were therefore revisited.

Additional sites were selected near mooring buoys that provided

the same

lionfish were seen at any site in 2004 or 2006. In May 2007, a

survey of nine sites (six of the sites chosen in 2010, plus three to the

south of the Park) recorded the presence of lionfish both to the

north and south of the Park, though densities were too low for

effective fish censuses. Dive boats had not collected lionfish at dive

sites in the Exuma Cays for at least 2 years prior to surveys.

Indeed, the highest and lowest densities of lionfish were both

observed at dive sites that receive occasional visitation (once per

week).

The same habitat (complex

15 m) was surveyed at each site. This is the preferred habitat of

adult large-bodied grouper [27]. Previous studies along the Exuma

Cays found no systematic variation across reserve boundaries in

habitat complexity or predicted fish larval supply [28]. Lionfish

and all large-bodied species of grouper (

Montastraea reef habitat at a suitable depth of 7–15 m. NoMontastraea forereef at a depth of 7–Epinephelus striatus,Mycteroperca tigris

subsequently ‘grouper’) were visually censused simultaneously

using eight replicate timed swims per site. Timed swims represent

a more appropriate and efficient technique for censusing relatively

, M. bonaci, M. venenosa, and M. interstitialis;Figure 2. Relationship between grouper biomass and lionfish density.

filled squares are sites within the Park. Errors bars represent standard error.

doi:10.1371/journal.pone.0021510.g002

Open squares are sites outside the Exuma Cays Land and Sea Park,Table 1.

the biomass of grouper (g 100 m

(g 100 m

Linear regression of lionfish biomass (g 100 m22) on22) and other predator fishes22).Predictor Coefficient Std. Dev. T p

Constant 224.34 45.41 4.94 0.001

Grouper biomass (log)

Other predator biomass 0.008 0.005 1.46 0.179

R

doi:10.1371/journal.pone.0021510.t001

259.54 15.30 23.89 0.0042 = 0.56. Std. Dev. denotes standard deviation.Grouper Deplete Invasive Lionfish

PLoS ONE | www.plosone.org 3 June 2011 | Volume 6 | Issue 6 | e21510

rare and patchy species than more traditional transect approaches.

Each timed swim lasted 5 minutes, covered approximately

300 m

was taken to examine cryptic habitats and the count, size and

species of individuals was recorded. Additional predatory fishes in

the families Sphryaenidae, Serranidae, Lutjanidae, Aulostomidae,

and Muraenidae were sampled using eight 30

site (Muraenidae have been observed to consume a wounded

lionfish [7]). Given that biomass is a better proxy for trophic

impact than density, grouper data were converted to mass using

allometric scaling relationships with body length [29]. Allometric

scaling relationships for lionfish were obtained elsewhere [30].

To assess patterns of grouper biomass around the Caribbean

and place the Exuma Cays data in context, we extracted data from

443 forereef sites in the Atlantic Gulf Rapid Reef Assessment

(AGRRA) database [16]. Sites spanned 15 countries including the

British Virgin Islands, US Virgin Islands, Florida, Venezuela,

Puerto Rico, Panama, Bonaire, Curac¸ao, Mexico, Cayman

Islands, Cuba, Costa Rica, Belize, Jamaica and The Bahamas.

These data were collected using visual fish census along 30

transects. In order to compare grouper biomass from our Exumas

sites to the AGRRA data, we also measured grouper biomass

along nine 30

50

quantified the total fish community structure for non-cryptic

species.

2, and was undertaken by the same surveyor (PJM). Care64 m transects per64 m64 m transects at nine of our sites in 2010 and five64 m transects in 2004. Surveys in 2007 and 2004 alsoSupporting Information

Table S1

denotes whether the site was within the Exuma Cays Land and

Sea Park.

(DOC)

Survey locations in the Exuma Cays. Reserve statusAcknowledgments

We thank Bruce Purdy and his crew for providing such excellent field

support. We also thank all the contributors to the AGRRA program for

creating such a valuable dataset.

Author Contributions

Conceived and designed the experiments: PJM. Performed the experiments:

PJM ARH DRB. Analyzed the data: PJM. Contributed reagents/

materials/analysis tools: PJM. Wrote the paper: PJM ARH.

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