Wednesday, June 7, 2017

Lessons from Lionfish, by Don Orth

Invasions are scary and often lead to a simple logic. Invasive species are bad.  The Lionfish is an invasive species. Therefore, we should kill and remove all lionfish.  While some people support categorization of species as invasive based solely on its origin, others seek for evidence of economic or environmental harm or harm to human health. There is much in the news about the Lionfish invasion, and here I highlight some of the latest findings on the lionfish, how we can discuss the controversy with students, and speculate on what comes next.  
Red Lionfish Pterois volitans   Photo by D.J. Orth
Lionfish (Pterois) are a fish in the Scorpaenidae family. They are are native to the Indo-Pacific ocean.  There are many species characterized by large, venomous spiky fin rays and warning coloration and banding patterns.  Two species are recent invaders in the western Atlantic, Gulf of Mexico, and Caribbean Sea, the Devil Firefish (Pterois miles) and the Red Lionfish (P. volitans).  Lionfish were first introduced to south Florida in the mid-1980’s and became established and common within ten years (Schofield 2009).  This was the first non-native marine fish to become established in the western Atlantic.  Invasion and spread were imminent, but there were no plans in place to deal with potential effects.  The combination of generalist feeding stratey, cryptic coloration, and undetectable chemical cues made the lionfish particularly successful in colonizing reefs where large predators were overfished.  Lionfish quickly rose to high densities and ate many small fish and invertebrate species (Côté et al. 2013).   

While considering these characteristics and early studies in small patch reefs in the Bahamas, scientists proposed a “worst case scenario in which most reef-fish biomass was converted to lionfish biomass, leaving invaded reefs depauperate of native fishes” (Albins & Hixon 2011; Albins 2015).  Emergence of the lionfish stimulated coordinated and long-term study by numerous investigators. The lionfish appeared in The Bahamas in 2004 and Green et al. (2012) observed a decline in 42 prey fishes during a rapid increase in lionfish abundance. Lionfish  reduced the abundance of many fishes, such as the Tomtate (a native forage fish Haemulon aurolireatum), as much as 45% since the invasion began in the hard-bottom reef habitat in Atlantic waters from North Carolina to Florida (Bellew et al. 2016).

Tomtate Haemulon aurolireatum is one of many prey species of the lionfish.   Illustration: © Diane Rome Peebles    

(Left) Standardized Tomtate abundance per trap at different stages of the lionfish invasion for areas not invaded by lionfish (gray points) and areas invaded by lionfish (red points). (right) Lionfish-attributed change in tomtit abundance.  Bellew et al. (2016).
But among the reefs along the coast of Belize, lionfish had no apparent effect on native prey communities four years post-invasion.  Oops!  Unexpected finding not concordant with prevailing storyline!   Serena Hackerott and her colleagues quantified lionfish and the density, richness, and composition of native prey fishes at sixteen reefs along of the Belize Barrier Reef from 2009 to 2013. Using a powerful, before-after-control-impact study design with reefs that spanned approximately 250 kilometers, they detected no evidence that lionfish measurably influenced the density, richness, or composition of prey fishes.  Similar findings were reported by Elise et al. (2015) from the Archipelago Los Roques National Park, Venezuela.
Why?  habitat complexity had up to five times greater effect on the density and richness of some families of small reef fishes than lionfish densities.  Of course, the lionfish did eat many small reef fishes. Disparate findings are largely dependent on the spatial and temporal scale of experiments.  In experiments that demonstrated a significant effect on reef fish recruits, lionfish comprised 50–100% of the predator biomass (Albins & Hixon 2011; Albins, 2015), whereas in the Belize reef study lionfish were only 10% of the total potential predator biomass.  Perhaps a longer study is needed? Perhaps lionfish are less likely to have apparent impacts in more intact protected reef ecosystems, such as the Belizean Barrier Reef. 

What are the options besides doing nothing? First, there is the invasivorism solution, where we “Eat our way out” of the lionfish problem and create a market-based solution for this dangerous and delicious fish (Chapman et al. 2016).  Second, manage large top predators, such as groupers, to eat the lionfish.  Third, annihilate all the lionfish with robots.  Fourth, discover some novel lionfish control methods.  The "Eat our way out" solution was hindered when the FDA announced a significant risk from ciguatera poisoning and  recommended that lionfish from certain areas not be eaten (Robertson et al. 2013). 

Plot of lion fish biomass versus grouper biomass at 71 reef sites (Valdivia et al. 2014). Black dots=protected sites, grey dots=non-protected sites, and red squares=sites from Mumby et al. (2011). 
The Bahamas is home to the oldest MPA in the world, the Exuma Cays Land and Sea Park, created in the 1950s, and a 20-year fishing ban here enabled grouper populations to recover from overfishing. Mumby et al. (2011) discovered a negative correlation (see red line and data in figure) between lionfish and grouper biomass,  suggesting that large grouper may serve as a natural biocontrol in no-fishing areas. However, in a follow-up study, Valdivia et al. (2014) concluded that we cannot rely on current native grouper populations to control the lionfish.  Manual removals appear to be effective at least at short timeframes in small areas (Bellew et al. 2016).  However, because the lionfish are more abundant in deeper, edge-of-sea locations, complete control is unlikely at larger spatial scales. How will the lionfish respond to robot predators? Côté et al. (2014) learned that the lion fish responded to culling by lowering their activity levels and hiding more. 
Robotic lionfish zapper.  Photo by J-P ROUJA/LOOKBERMUDA
Is the worst-case scenario happening? Studies by numerous investigators support no effect to varying degrees of negative effect.  It appears that negative effects are more typical in small scale, isolated reefs while effects on large open systems is less certain.   The scientific consensus is far from settled and most research has focused on effects on the reef fish with far less attention paid trying to understand stakeholders’ views on this species and its management.   

Caballo-Cárdenas (2017) claims that the dominant discourse labels the lionfish as “ultimate predators” that are a threat and characterize control efforts as a war.  Lionfish hunting and consumption by humans are deemed a necessary part of the war effort.  In presenting this case to students, it is important to first compare the criteria for invasive species.  Should invasive species be categorized based simply on their origin?  Or should we define "invasive species" as a species that is: (1) non-native (or alien) to the ecosystem under consideration, and (2) whose introduction causes or is likely to cause economic or environmental harm or harm to human health.   Next, we may discuss what Moore (2012) means when she says that the lionfish and fishermen are malleable?   What roles do social scientists play in the management of introduced fishes, such as the lionfish?   How do fisheries emerge and become sustainable?  What evidence support the position that the lionfish is a 'keystone species' ?  After discussion of these issues, students may explore other examples of invasive species, the problems they caused and proposed solutions.

Many unanswered questions remain concerning this new addition to our marine reef ecosystem.  Will they learn to be more wary ?   What is the role of marine protected areas and should be remove lionfish from MPAs? (Cox et al. 2017).  What would happen if we restore populations of apex predators in reef environments? (Valdivia et al. 2014).   There are many more questions than answers.   No matter what new discoveries may occur,  the lionfish has changed the way that marine fish managers view invasive fish forever.
For more information click here. 
Albins, MA. 2015. Invasive Pacific lionfish Pterois volitans reduce abundance and species richness of native Bahamian coral-reef fishes. Marine Ecology Progress Series 522:231-243
Albins MA, and MA Hixon. 2011. Worst case scenario: potential long-term effects of invasive predatory lionfish (Pterois volitans) on Atlantic and Caribbean coral-reef communities. Environmental Biology of Fishes 96:1151-1157
Bellew, N.G., N.M. Bacheler, G.T. Kellison, and A.M. Schueller. 2016.  Invasive lionfish reduce native fish abundance on a regional scale. Scientific Reports 6: 32169   doi: 10.1038/srep32169.  
Caballo-Cárdenas, E.C. 2016. Controversies and consensus on the lionfish invasion in the Western Atlantic Ocean. Ecology and Society 20(3); 24.
Chapman, J.K., L.G. Anderson, C.L.A. Gough, and A.R. Harris. 2016. Working up an appetite for lionfish: a market-based approach to manage the invasion of Pterois volitans in Belize. Marine Policy 73:256-262
​​Côté, I.M., S.J. Green, J.A. Morris, Jr., J.L. Akins, and D. Steinke D. 2013. Diet richness of invasive Indo-Pacific lionfish revealed by DNA barcoding. Marine Ecology Progress Series 472:249-256.
Côte, I.M. et al.  2014. What doesn’t kill you makes you wary? Effect of repeated culling on the behaviour of an invasive predator. PLOS One 9(4):    doi: 10.1371/journal.pone.0094248.
Cox, C.E., A. Valdivia, M.D. McField, K.D. Castillo, and J.F. Bruno. 2017. Establishment of marine protected areas alone does not restore coral reef communities in Belize. Marine Ecology Progress Series 563:65-79.
Elise, S., I. Urbina-Barreto, H. Boadas-Gil, M. Galindo-Vivas, and M. Kulbicki.   2015. No detectable effect of lionfish (Pterois volitans and P. miles) invasion on a healthy reef fish assemblage in Archipelago Los Roques National Park, Venezuela. Marine Biology 162(2): 319-330.
Green, S.J., J.L. Akins, A. Maljković, and I.M. Côté. 2012. Invasive lionfish drive Atlantic coral reef fish declines. PLOS One 7: e32596
Hackerott S, A. Valdivia, C.E. Cox, N.J. Silbiger, and J.F. Bruno. 2017. Invasive lionfish had no measurable effect on prey fish community structure across the Belizean Barrier Reef. PeerJ 5:e3270
Moore, A. 2012.  The aquatic invader: Marine management figuring fishermen, fisheries, and lionfish in The Bahamas. Cultural Anthropology 27(4): 667–688.

Mumby, P.J., A.R. Harborne, and D.R. Brumbaugh. 2011. Grouper as a natural biocontrol of invasive lionfish. PLoS ONE 6(6): e21510.
Robertson, A. 2013. Invasive lionfish (Pterois volitans): a potential human health threat for ciguatera fish poisoning in tropical waters.  Marine Drugs 12(1): 88-97. 

Schofield, P. 2010. Update on geographic spread of invasive lionfishes (Pterois volitans [Linnaeus, 1758] and P. miles [Bennett, 1828]) in the Western North Atlantic Ocean, Caribbean Sea and Gulf of Mexico. Aquatic Invasions 5: S117-S122

Valdivia, A., J.F. Bruno, C.E. Cox, S. Hackerott, and S.J. Green. 2014. Re-examining the relationship between invasive lionfish and native grouper in the Caribbean. PeerJ 2:e348