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Journal of Fish Biology - 2018 - C T - The Lionfish Pterois SP Invasion Has The Worst Case Scenario Come To Pass
Journal of Fish Biology - 2018 - C T - The Lionfish Pterois SP Invasion Has The Worst Case Scenario Come To Pass
This review revisits the traits thought to have contributed to the success of Indo-Pacific lionfish Pterois
sp. as an invader in the western Atlantic Ocean and the worst-case scenario about their potential
ecological effects in light of the more than 150 studies conducted in the past 5 years. Fast somatic
growth, resistance to parasites, effective anti-predator defences and an ability to circumvent predator
recognition mechanisms by prey have probably contributed to rapid population increases of lionfish
in the invaded range. However, evidence that lionfish are strong competitors is still ambiguous, in part
because demonstrating competition is challenging. Geographic spread has likely been facilitated by the
remarkable capacity of lionfish for prolonged fasting in combination with other broad physiological
tolerances. Lionfish have had a large detrimental effect on native reef-fish populations in the north-
ern part of the invaded range, but similar effects have yet to be seen in the southern Caribbean. Most
other envisaged direct and indirect consequences of lionfish predation and competition, even those that
might have been expected to occur rapidly, such as shifts in benthic composition, have yet to be real-
ized. Lionfish populations in some of the first areas invaded have started to decline, perhaps as a result
of resource depletion or ongoing fishing and culling, so there is hope that these areas have already
experienced the worst of the invasion. In closing, we place lionfish in a broader context and argue that
it can serve as a new model to test some fundamental questions in invasion ecology.
© 2018 The Fisheries Society of the British Isles
Key words: biotic invasion; biotic resistance; coral reefs; environmental management; invasive species
control; Scorpaenidae.
INTRODUCTION
The invasion of the western Atlantic Ocean by Indo-Pacific lionfish Pterois sp. is
undoubtedly the best documented marine invasion to date. Predatory lionfish were first
reported off the coast of Florida, U.S.A., in 1985 (Schofield, 2009), their introduction
most likely the result of aquarium releases (Whitfield et al., 2002; Semmens et al.,
2004). By 2000, lionfish were a common sight off the coast of North Carolina, U.S.A.,
(Whitfield et al., 2002), where their abundance soon rivalled that of the commonest
native grouper species, Mycteroperca phenax Jordan & Swain 1884 (Whitfield et al.,
2007). In 2004, lionfish reached Bahamian coral reefs (Schofield, 2009) and by 2010,
they had become established around every island and along most of the Central and
South American coasts of the Caribbean Sea, as well as in the eastern portion of the
Gulf of Mexico (Schofield, 2010). In 2014, the first lionfish was recorded south of the
660
© 2018 The Fisheries Society of the British Isles
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R E- E VA L U AT I N G T H E L I O N F I S H I N VA S I O N 661
N E W K N O W L E D G E A B O U T C O R R E L AT E S O F P O P U L AT I O N
INCREASE
The last few years have seen a rapid rise in the number of studies documenting
aspects of lionfish life-history that have a bearing on their capacity for rapid popu-
lation increase. The early contention that lionfish show high individual growth rates
(Albins & Hixon, 2013) is now well supported (Table II). Lionfish can grow up to
2·5 mm (total length, LT ) per day, depending on their initial length and geographic
© 2018 The Fisheries Society of the British Isles, Journal of Fish Biology 2018, 92, 660–689
662
(a) (b)
40
35
30
25
20
15
Number of publications
10
1995 1960 1965 1970 1975 1980 1985 1990 1995 2000 2005 2010 2015 1985 1990 1995 2000 2005 2010 2015
Year Year
Ecology, genetic or physiology Social science Venon & ciguatera Indo Pacific Mediterranean Sea Western Atlantic Ocean
I . M . CÔ TÉ A N D N . S . S M I T H
Fig. 1. Annual numbers of peer-reviewed publications on lionfish Pterois sp. by (a) research topic and (b) geographic region, based on a search of ISI Web of Science database
1900 to 7 October 2017, using the terms ‘Pterois and (volitans OR miles)’. Studies on lionfish venom and ciguatera were excluded from the regional numbers.
© 2018 The Fisheries Society of the British Isles, Journal of Fish Biology 2018, 92, 660–689
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R E- E VA L U AT I N G T H E L I O N F I S H I N VA S I O N 663
Table I. List of life-history and ecological traits of lionfish Pterois sp. and of fish in recipient
communities that might have contributed to the successful establishment and rapid spread of
invasive lionfish in the northwest Atlantic, according to three reviews of this invasion.
Establishment/population increase
√
Early maturation –
√ –
√ √
High individual growth rates √
High population growth rates –
√ √ –
√
Predatory habit √ √ √
Generalist diet √ √
Native prey naïveté – √
Masquerade mimicry – √ –
√
Effective competitor – √ √
Lack of predators – √ √
Resistant to ectoparasites –
√
Long lifespan √ – –
Large body size – –
Geographic spread
√
Long-range larval dispersal –
√ –
√ √
High reproductive rates √ √
Generalized habitat use –
√ √
High physical tolerance –
location (Table II). They grow faster than ecologically similar native predatory fishes
under the same conditions (Albins, 2013). The growth parameter K, which describes
how quickly a fish reaches the theoretical asymptotic length where growth essentially
stops (i.e. L∞ ), is variable for lionfish (0·32–1·48 in the invaded range; Table II), but
much higher than matching estimates for ecologically similar Atlantic mesopredators.
For species of Caribbean groupers (Cephalopholis spp., Epinephelus spp. and Myc-
teroperca spp.) and snappers (Lutjanus spp.), for example, K usually ranges from 0·1
to 0·2 (reviewed in Côté et al., 2013a; Edwards et al., 2014). Fast growth rates, espe-
cially for females (Edwards et al., 2014), translate into early ages at maturity (<1 year;
Morris, 2009) and scope for rapid rates of population increase.
A large part of the success of lionfish as an invasive predator is thought to be its broad
diet (Morris & Whitfield, 2009; Albins & Hixon, 2013; Côté et al., 2013a). Invading
species that are ecological generalists, in terms of either food or habitat, are often more
successful at establishing new populations because they are better equipped to deal
with environmental stochasticity in the recipient region (García-Berthou, 2007). The
large number of prey species consumed by lionfish led to the early conclusion that
they were generalists (Morris & Akins, 2009). The number of lionfish diet studies and
lists of known prey has grown considerably over the past few years (Table III), with
taxonomic resolution of diet being greatly enhanced by the use of DNA barcoding
(Valdez-Moreno et al., 2012; Côté et al., 2013b; Harms-Tuohy et al., 2016). Lionfish
© 2018 The Fisheries Society of the British Isles, Journal of Fish Biology 2018, 92, 660–689
664
Table II. Mean daily growth rates of lionfish Pterois sp. from locations across the invaded Atlantic Ocean range
Native range
Pusack et al., 2016 – – – – 1·62 Tagging Philippines–Guam
Invaded range
Potts et al., 2010 – – – – 0·32 Otoliths North Carolina
Barbour et al., – – – – 0·47 Otoliths North Carolina
2011
Jud & Layman, 0·46 0·18–0·78 – – – Tagging Florida (estuary)
2012
Johnson & – – – – 0·47 Length-based + otoliths Florida
Swenarton,
2016
Albins, 2013 – – 0·8 – – Visual Bahamas
Benkwitt, 2013 – – – 0·85–1·10 – Tagging Bahamas
I . M . CÔ TÉ A N D N . S . S M I T H
© 2018 The Fisheries Society of the British Isles, Journal of Fish Biology 2018, 92, 660–689
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R E- E VA L U AT I N G T H E L I O N F I S H I N VA S I O N 665
do consume a broad diversity of prey species (Table III). A generalist diet at the popu-
lation level, however, sometimes belies individual specialization (Layman & Allgeier,
2012) as well as ontogenetic shifts from invertivory to piscivory (Morris & Akins,
2009; Dahl & Patterson III, 2014; Arredondo-Chávez et al., 2016; Dahl et al., 2017).
Moreover, a generalist habit does not preclude specific preferences. Lionfish consume
some fish species and families more than expected based on their relative abundance
(Green & Côté, 2014; Chappell & Smith, 2016). Over-consumed prey species tend
to have specific characteristics: small, shallow-bodied, solitary fishes that live on or
just above reefs, that do not remove ectoparasites and that are nocturnally active are at
greatest risk of lionfish predation (Green & Côté, 2014). Although our general under-
standing of prey selection by lionfish is now deeper, some distinct prey preferences
remain puzzling, such as the propensity to attack fairy basslet Gramma loreto Poey
1868 when the ecologically and morphologically similar congener blackcap basslet
Gramma melacara Böhlke & Randall 1963 is also available (Kindinger & Anderson,
2016), which suggests that additional prey characteristics enhance vulnerability to lion-
fish predation.
Lionfish have been described as effective competitors (Albins & Hixon, 2013), but
evidence for this contention is still ambiguous. This is at least in part because com-
petition is so difficult to demonstrate convincingly. Nevertheless, to our knowledge,
there is no indication of territoriality by lionfish or overt interference competition with
native fish in the introduced range. Instead, by virtue of their high predation rates
(Côté & Maljković, 2010; Green et al., 2011; Albins, 2013) and extensive overlap
of prey use with native predatory fishes (Layman & Allgeier, 2012; O’Farrell et al.,
2014; Curtis et al., 2017), lionfish have the potential to deplete resources shared by
native mesopredators and perhaps exercise more subtle interference competition via
fear effects. But do they? A negative relationship between the density or biomass of
lionfish and potential native competitors would be expected under strong competition
(Hardin, 1960; Bøhn et al., 2008), but such a relationship has so far been largely elu-
sive (Hackerott et al., 2013; Anton et al., 2014; Valdivia et al., 2014; Bejarano et al.,
2015; Curtis et al., 2017; but see Mumby et al., 2011). Such a purely demographic mea-
sure would, of course, overlook shifts in microhabitat or in diet that could result from
exploitation competition. Either or both shifts are suggested by the narrower isotopic
niche of graysby grouper Cephalopholis cruentata (Lacépède 1802) and the smaller
overlap with the lionfish niche at sites with abundant lionfish compared with sites with
lower lionfish biomass in Florida; the isotopic niche of lionfish, in contrast, does not
change with their abundance (Curtis et al., 2017). To date, however, no physiologi-
cal costs in terms of reduced growth rates (Albins, 2013) or body condition (Curtis
et al., 2017) of native predators have been detected to confirm that competition is
actually occurring. This conclusion could change in more resource-limited habitats.
Competition for other resources, such as shelter, could also occur and at least in meso-
cosms, Nassau grouper Epinephelus striatus (Bloch 1792) change their shelter use in
the presence of lionfish, while shelter use by lionfish remains constant (Raymond et al.,
2015).
The apparent invulnerability of lionfish to predation is another factor that might
have contributed to their invasion success (Albins & Hixon, 2013). Indeed, it seems
that few predators in any ocean basin should be equipped to contend with the physical
(e.g. venomous dorsal, anal and pelvic spines; Vetrano et al., 2002) and behavioural
defences (e.g. head-down pose with dorsal spines directed towards a perceived threat;
© 2018 The Fisheries Society of the British Isles, Journal of Fish Biology 2018, 92, 660–689
Table III. Diet of lionfish Pterois sp. across the invaded Atlantic range
666
Dahl et al., 2017 Northern Gulf of Mexico Natural & artificial reefs Visual + barcoding 770 41 N/A
Valdez-Moreno et al. 2012 Mexico Coral reefs Visual + barcoding 144 34 1
Arredondo-Chávez et al., Mexico Coral reefs, seagrass Visual 962 48 29
2016 meadows, gorgonian
fields, hard pavement
Rocha et al., 2015 Belize Coral reefs Visual + barcoding 44 15 N/A
Sandel et al., 2015 Costa Rica Coral reefs Visual 298 11 1
The number of lionfish examined (n) includes only stomachs containing prey. Numbers of prey species refer only to prey identified to species. Visual method refers to
identification of prey in stomachs of lionfish; in situ method refers to direct observations of lionfish successfully hunting prey.
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R E- E VA L U AT I N G T H E L I O N F I S H I N VA S I O N 667
Whitfield et al., 2007; Green et al., 2011) of lionfish. Yet, they do sometimes get eaten.
There were early anecdotal reports that Atlantic predators [E. striatus, tiger grouper
Mycteroperca tigris (Valenciennes 1833)] occasionally consume small lionfish in the
wild (Maljković et al., 2008) and a single report of predation by Pacific cornetfish
Fistularia commersonii Rüpell 1838 in the native range (Bernadsky & Goulet, 1991).
There are now more observations of predation on lionfish. Yellow-edged moray Gym-
nothorax flavimarginatus (Rüppel 1830) and giant moray Gymnothorax javanicus
(Bleeker 1859) in the native range were observed preying on lionfish (Bos et al.,
2017), as were green moray Gymnothorax funebris Ranzani 1839 and spotted moray
Gymnothorax moringa (Cuvier 1829) in the invaded range (Barbour et al., 2011; Jud
et al., 2011; Pimiento et al., 2013; Muñoz, 2017). Moreover, native predators (e.g.
nurse shark Ginglymostoma cirratum (Bonnaterre 1788), E. striatus) will consume
small, tethered lionfish (Diller et al., 2014) and lionfish are sometimes cannibalistic
in the invaded range (Valdez-Moreno et al., 2012; Côté et al., 2013b; Dahl et al.,
2017). It seems, however, that these events are highly infrequent. For example, no
lionfish was found in the stomach contents of a large sample of multiple species of
Atlantic groupers (henceforth including Cephalopholis spp., Epinephelus spp. and
Mycteroperca spp.) (N. S. Smith & I. M. Côté, unpubl. data). Cannibalism, as revealed
by DNA barcoding, is also quite rare (c. 4–11% of stomachs; Valdez-Moreno et al.,
2012; Côté et al., 2013b; Dahl et al., 2017). Meanwhile, a vigorous debate about
whether healthy populations of large-bodied Atlantic groupers can control lionfish
populations through direct predation or fear effects continues, with most studies
reporting no relationship between lionfish and grouper biomass (Hackerott et al.,
2013; Anton et al., 2014, Valdivia et al., 2014, Bejarano et al., 2015; Curtis et al.,
2017; but see Mumby et al., 2011). In Florida, the presence of large red groupers
Epinephelus morio (Valenciennes 1828) mitigates the negative effect of lionfish on
reef-fish recruitment and induces a shift in lionfish diet from mostly fish, when they
are on their own, to mostly invertebrates (Ellis & Faletti, 2016). In this case, however,
the effect is triggered by grouper territorial aggression rather than fear of predation.
The bottom line is that lionfish are not invulnerable to predation, especially when
small, but their natural mortality rate is likely to be lower than that of ecologically
equivalent, but less well-defended species.
Resistance to parasites might also contribute to the performance of invasive lionfish
(Albins & Hixon, 2013). In the invaded range, lionfish have acquired a variety of
generalist macroparasites that commonly infect Atlantic fishes (Bullard et al., 2011;
Sikkel et al., 2014; Ramos-Ascherl et al., 2015; Sellers et al., 2015; Fogg et al., 2016;
Tuttle et al., 2017; Supporting Information Table S1). Although the susceptibility of
introduced species to parasites in the recipient environment can change as the invasion
progresses (Llewellyn et al., 2012; Brown et al., 2015), current evidence suggests that
lionfish have fewer and less diverse macroparasites than many native Atlantic fishes
inhabiting the same environment (Sikkel et al., 2014; Loerch et al., 2015; Sellers
et al., 2015; Tuttle et al., 2017). Interestingly and perhaps related, bacteria in lionfish
mucus exhibit anti-bacterial activity, which might confer disease resistance (Stevens
et al., 2016). A key question is whether reduced parasite loads translate to a fitness
advantage for lionfish, such as growing faster than native groupers that exploit the
same resources (Albins, 2013). The only pertinent evidence so far is that native C.
cruentata lose body condition with increasing parasite abundance, but lionfish do
not (Sellers et al., 2015). It is not clear, however, whether this difference is because
© 2018 The Fisheries Society of the British Isles, Journal of Fish Biology 2018, 92, 660–689
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668 I . M . CÔ TÉ A N D N . S . S M I T H
lionfish are better able to bear the cost of parasitism or because they never experience
the high parasite intensities of native fishes.
Beyond invader traits, characteristics of species in the recipient communities can
facilitate population increases of invaders. One such feature invoked to explain the suc-
cess of lionfish as predators is prey naïveté, i.e. the lack of adaptive responses by prey
exposed to a novel predator (Sih et al., 2010). A number of methods have been used to
assess the naïveté of Atlantic prey fishes to lionfish, from observations of fish on natu-
ral and artificial reefs (Albins & Hixon, 2008; Côté & Maljković, 2010; Anton et al.,
2016; Benkwitt, 2017), to field presentations to prey of predators and non-predators in
cages and bottles (Black et al., 2014; Kindinger, 2015; Anton et al., 2016) and various
laboratory experiments that confront prey with visual or chemical cues of predators
and non-predators (Marsh-Hunkin et al., 2013; Eaton et al., 2016). The prey responses
measured are equally varied and range from behaviours expected to change under risk
of predation (e.g. hiding time, approach distance, group size, aggression, courtship
and foraging rates) to whole-reef recruitment rates. Taken together, these studies paint
an unclear picture of prey naïveté. Native prey fish display no more fear or aggression
towards lionfish than they do towards native non-predators or empty, control containers
(Black et al., 2014; Kindinger, 2015; Anton et al., 2016). They also readily recruit onto
reefs with lionfish while avoiding reefs inhabited by native predators (Benkwitt, 2017).
Native prey fish, however, also sometimes show responses that are consistent with the
perception of risk, such as foraging less (Eaton et al., 2016; Kindinger & Albins, 2017),
spending more time under cover (Marsh-Hunkin et al., 2013), forming larger groups
(Eaton et al., 2016) and moving less (Marsh-Hunkin et al., 2013), but these responses
are inconsistent across studies. The confusion is heightened by the recent finding that
prey fish in the native range do not recognize P. volitans as a potential threat (Lönnstedt
& McCormick, 2013; McCormick & Allen, 2016). Lionfish in the native range some-
how circumvent the mechanisms by which prey usually identify predators. How they
do this remains a mystery, but it seems unlikely that they would have lost this ability
upon introduction into the Atlantic. The predatory success of lionfish may therefore
not be premised solely on prey naïveté but also on this unique feature of the species.
N E W K N OW L E D G E A B O U T D E T E R M I NA N T S O F G E O G R A P H I C
SPREAD
The spatial spread of invasive species can be enhanced by high reproductive rates,
efficient dispersal capacity, high physical tolerance and the ability to survive in many
habitats (Table I). Little new information has emerged about the reproductive rates
of lionfish. Individuals from the Gulf of Mexico (Fogg et al., 2017) and Little Cay-
man (Gardner et al., 2015), like those from North Carolina and The Bahamas (Morris,
2009), have the potential to spawn every 2–4 days year round. Although the batch
fecundity of lionfish is low compared with native Caribbean mesopredators (Côté et al.,
2013a), their high rate of batch production translates into a high annual fecundity of c.
2 million eggs (Morris, 2009; Fogg et al., 2017). Amazingly, no one has yet witnessed
lionfish spawning in the wild.
There is also limited new information about lionfish larval dispersal. Ahrenholz &
Morris (2010) established that the pelagic larval duration of lionfish in the invaded
range is 20 to 35 days (mean 26 days). This is not especially long for a coral-reef fish
(Lester & Ruttenberg, 2005), but it still provides ample time for long-distance dispersal.
© 2018 The Fisheries Society of the British Isles, Journal of Fish Biology 2018, 92, 660–689
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R E- E VA L U AT I N G T H E L I O N F I S H I N VA S I O N 669
Only a handful of lionfish larvae have been collected so far (Vásquez-Yeomans et al.,
2011; Kitchens et al., 2017), but a biophysical model suggests that some of these
14–17 day old larvae might have dispersed up to c. 900 km on local currents from
where they were spawned (Kitchens et al., 2017). However, currents alone do not
account for the speed of lionfish spread. Through increased larval transport, hurri-
canes appear to have greatly hastened the expansion of lionfish across the Bahamian
archipelago and northern Greater Antilles (Johnston & Purkis, 2015a).
Lionfish tolerate a broad range of abiotic conditions, but not inordinately more than
other reef fishes in most aspects. In Florida, their preferred temperature is 28–30∘ C
(Barker et al., 2018), which is c. 5∘ warmer than in the native range (Dabruzzi et al.,
2017). Their minimum (9·5–16.5∘ C) and maximum critical temperatures (30–40∘
C), i.e. the temperatures beyond which they lose function, vary with acclimation tem-
perature and define a habitable thermal range of c. 25∘ , which is similar to that of
co-occurring native mesopredators (Barker et al., 2018). Lionfish can live in low salin-
ities: they behave and grow in long-term (i.e. > 1 month) exposures to salinities of
7–10‰ (Jud et al., 2015; Schofield et al., 2015) and they survive brief exposures to
1‰ as well as daily fluctuations of 28‰ in tidal estuaries (Jud et al., 2011; Jud et al.,
2015). But again, this tolerance for a wide range of salinity conditions is seen in other
reef fishes (Wu & Woo, 1983; Woo & Chung, 1995). Lionfish, however, might be
exceptional in their capacity for prolonged fasting. Individuals starved for 3 months lost
<20% of their body weight and survived (Fishelson, 1997). To our knowledge, there
are no other similar studies of coral-reef fishes for comparison. Surviving long-term
food deprivation might be linked to the ability of lionfish to eat extremely large meals,
which make their stomach swell to 30 times its original size (Fishelson, 1997) and to
accumulate large amounts of visceral fat (Morris & Whitfield, 2009; pers. obs.). Taken
together, these environmental tolerances, combined with their broad diet, mean that
lionfish can occupy a wide range of depths and habitats (Claydon et al., 2012; Nut-
tall et al., 2014; Switzer et al., 2015) and therefore largely overcome environmental
stochasticity, which is typically a significant barrier to non-native species establishment
and spread.
D I R E C T E F F E C T S O N F I S H P O P U L AT I O N S
Lionfish have caused marked changes in many native Atlantic fish populations
(Table I). In some places, rates of prey consumption by lionfish far exceed prey
production rates (Green et al., 2014) and the majority of native fish biomass is being
converted to lionfish biomass, as envisioned by Albins & Hixon (2013). A couple
of trends, however, are emerging from the many observational and experimental
© 2018 The Fisheries Society of the British Isles, Journal of Fish Biology 2018, 92, 660–689
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670 I . M . CÔ TÉ A N D N . S . S M I T H
Table IV. The current status of elements of the worst-case scenario envisaged by Albins &
Hixon (2013) about the invasion of the western Atlantic by lionfish Pterois spp.
© 2018 The Fisheries Society of the British Isles, Journal of Fish Biology 2018, 92, 660–689
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R E- E VA L U AT I N G T H E L I O N F I S H I N VA S I O N 671
studies that have examined lionfish predation. First, lionfish have so far not driven the
same large declines in prey abundance everywhere. The few studies conducted in the
southern Caribbean have so far reported no declines in prey populations (Table V).
Although these studies tend to have been carried out soon after the local arrival of
lionfish (< 5 years), marked effects were already evident at that stage of the invasion
further north. Second, of those studies that report an effect, those conducted on very
small experimental patches (i.e. translocated corals and artificial concrete-block reefs
of <4 m2 ) report far larger losses (mean ± 1 S.E. = 90% ± 6%, n = 3) than studies from
natural habitats (50% ± 7%, n = 8; t9 = 3·82, P < 0·01). This difference is not simply
due to an experimental versus observational dichotomy, since the habitat difference
still holds within experimental studies (experimental patches: 90% ± 6%, natural
habitats: 49% ± 9%; t6 = 3·19, P < 0·05). Even if studies of experimental patches
inflate the apparent effect of lionfish, losing half of the abundance of prey fishes, as
seen in natural habitats in a matter of weeks, remains an extraordinary concern.
The envisioned declines in species of commercial importance have not yet been
reported, although lionfish do consume these species (Dahl et al., 2017). The losses
observed so far have affected prey-sized fishes (usually <10 cm LT ), as Albins & Hixon
(2013) had speculated, but even within longer studies, these losses have not translated
into similar deficits in larger prey size classes (Green et al., 2014; Albins, 2015). The
one possible exception is the regional decline of adult tomtate grunt Haemulon auro-
lineatum Cuvier 1830 off the south-eastern U.S.A. (Table V), which has been attributed
to lionfish predation on juveniles (Ballew et al., 2016). It might ultimately be difficult
to ascribe part or all of downward trends in commercially important species to lionfish
predation because of the coarseness of most fisheries data and the multiple stressors
(including fishing) affecting these species.
Lionfish were expected to cause other significant shifts in fish community structure,
marked especially by declines in abundance of mesopredators (owing to competition
and predation) and increases in species not susceptible to lionfish predation (Albins
& Hixon, 2013). There is mixed evidence for the former (Table V). Ballew et al.
(2016) found no changes in predatory fish numbers while lionfish density increased
and H. aurolineatum abundance tumbled on the south-east coast of the U.S.A. On one
Bahamian mesophotic reef, however, there appears to have been a wholesale replace-
ment of native mesopredators by the same density of lionfish (Lesser & Slattery, 2011),
although the mechanism by which this substitution occurred is unclear. Other declines
of mesopredators occurring concurrently with a build-up of lionfish numbers cannot
be clearly ascribed to predation or competition (Green et al., 2012; Tuttle, 2017). In
one case, transient predators stopped visiting the reefs where lionfish had eaten most
of the prey fish and some of the Elacatinus Jordan 1904 cleanerfishes (Tuttle, 2017).
Whether unpalatable species such as puffers [e.g. Canthigaster rostrata (Bloch, 1786)]
and their relatives have increased in relative abundance in fish communities exposed
to lionfish predation (Albins & Hixon, 2013) is eminently testable, but has not been
examined so far.
Finally, although not considered by Albins & Hixon (2013), the ultimate worst-case
effect is that lionfish might drive native fish species to extinction. To our knowledge,
this irreversible outcome has not occurred yet, but some evidence now points to this
idea as a realistic possibility. In several experiments, the presence of lionfish caused
a loss of prey richness that was not observed in their absence or in the presence of
native predators (Albins, 2013, 2015; Benkwitt, 2015; Ellis & Faletti, 2016; Table V).
© 2018 The Fisheries Society of the British Isles, Journal of Fish Biology 2018, 92, 660–689
Table V. Studies of direct (consumptive) effects of invasive lionfish Pterois sp. on Atlantic fish populations and species
672
Source Location Habitat Study type Study length Time since invasion Effects observed
Ballew et al., 2016 South-east U.S.A. Variety Survey 17 years c. 5 years pre to c. Haemulon aurolineatum
12 years post abundance ↓45%
Albins & Hixon, Bahamas Experimental Manipulative 5 weeks 2 years Abundance ↓79%
2008 patch reefs
Lesser & Slattery, Bahamas Mesophotic reefs Survey 7 years 6 years pre to 1 year Most trophic groups abundance ↓;
2011 (60–90 m) post replacement of native
Epinephelus groupers by
lionfish
Green et al., 2012 Bahamas Natural reefs Survey 2 years 4–6 years Biomass ↓ 65%
(crest)
Albins, 2013 Bahamas Experimental Manipulative 8 weeks 3 years Abundance ↓ 94%; richness ↓ by
patch reefs 4–5 spp.; evenness ↑
Benkwitt, 2015 Bahamas Experimental Manipulative 7 weeks 6 years Abundance ↓ 97% at highest
patch reefs lionfish density; richness ↓; no
effect on evenness
Benkwitt, 2016 Bahamas Natural reefs Manipulative 7 weeks 8 years Abundance ↓ in coral habitats with
(patches & lionfish; no effect on fish on
small coral sand or in seagrass
heads), seagrass
I . M . CÔ TÉ A N D N . S . S M I T H
& sand
Green et al., 2014 Bahamas Natural reefs Manipulative 24 months 4–6 years Abundance ↓ 40–60%; no effect
(patches) on larger fishes
Albins, 2015 Bahamas Natural reefs Manipulative 14 months 4–5 years Abundance ↓ 38–46%; biomass ↓
patches) 32%; richness ↓ by 5 spp.; no
effect on evenness; no effect on
larger fishes
Ingeman & Bahamas Natural reefs Survey 8 years 2 year pre and Gramma loreto abundance ↓ 52%
Webster, 2015 (ledges) 6 years post
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Table V. Continued
Source Location Habitat Study type Study length Time since invasion Effects observed
Ingeman & Webster, 2015 Bahamas Natural reefs Manipulative 8 weeks 6 years Gramma loreto per capita loss ↑
(ledges)
Ingeman, 2016 Bahamas Natural reefs Manipulative 4 weeks Unreported Gramma loreto abundance ↓ 34%;
(patches) local extinction of 2–14
populations
Kindinger & Albins, 2017 Bahamas Natural reefs Manipulative 24 months 4–6 years Small herbivore abundance ↓; no
(patches) effect on large herbivores
Tuttle, 2017 Bahamas Natural reefs Manipulative 9 weeks 9 years Thalassoma bifasciatum abundance ↓
(patches) 33%; large non–resident reef fish
abundance ↓ 78%; no effect on
Elacatinus gobies or large resident
reef fishes
Ellis & Faletti, 2016 Florida Karst solution Manipulative 6 weeks 4 years Recruitment ↓ 84%; richness ↓ by 4·5
holes spp.; evenness ↑
Hackerott et al., 2017 Belize Natural reefs(spur Field surveys 4 years 1 year pre to 3 years No effect on density, richness or
& groove) post community structure
Elise et al., 2015 Venezuela Natural reefs Field surveys 2 years 1–3 years No effect on density, richness or
(crest & slope) community structure
R E- E VA L U AT I N G T H E L I O N F I S H I N VA S I O N
Palmer et al., 2017 Panama Natural reefs Manipulative 12 months 4 years Stegastes partitus and Halichoeres
© 2018 The Fisheries Society of the British Isles, Journal of Fish Biology 2018, 92, 660–689
garnoti recruit abundance ↓, adult
abundance ↓; no effect on
Thalassoma bifasciatum; no effect
on genetic diversity
Results pertain to all fishes that are potential prey of lionfish (i.e. total length < 10–15 cm) unless otherwise specified. Studies are ordered chronologically by location
(north to south). Study length for field surveys represents the length of time series. The magnitude of observed changes is given when reported in the sources.
673
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674 I . M . CÔ TÉ A N D N . S . S M I T H
Moreover, the added mortality imposed by lionfish, over and above that of native preda-
tors, led to the extirpation of two of 14 experimental populations of G. loreto (Inge-
man, 2016). Lionfish appear to prey on G. loreto in a density-independent fashion:
unlike native predators, lionfish continue to hunt them even when their populations are
small, which increases the risk of population loss through demographic stochasticity
(Ingeman & Webster, 2015; Ingeman, 2016). While G. loreto is not at risk of global
extinction because of their broad distribution across the Caribbean, the same cannot be
said of restricted-range endemic species. For example, the critically endangered social
wrasse Halichoeres socialis Randall & Lobel 2003, which is found only around the
Pelican Cayes in Belize, appears to be a common prey of lionfish in that area (Rocha
et al., 2015). Similarly, the arrival of lionfish in Brazil is causing concern for the many
small-range endemic fishes of the region (Ferreira et al., 2015). Lionfish are also prey-
ing on fish species that have yet to be described (Tornabene & Baldwin, 2017) and for
which we have no life-history or distribution information that could help assess the
threat posed by lionfish.
D I S T R I B U T I O N E X PA N D I N G T O T H E R M A L L I M I T S I N
A B S E N C E O F B I O T I C R E S I S TA N C E
In the absence of biotic resistance, i.e. a high diversity or abundance of native preda-
tors, competitors or parasites that can constrain invader numbers (Stachowicz et al.,
1999; Levine et al., 2004), the distribution of lionfish might eventually expand and be
limited only by thermal tolerance (Albins & Hixon, 2013). Based on a 10∘ C lower
thermal limit (Kimball et al., 2004), the geographic range of lionfish in the Atlantic
Ocean is expected to span from Cape Hatteras in the north to Uruguay in the south
(Morris & Whitfield, 2009). Lionfish reached the predicted northern edge in 2000,
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R E- E VA L U AT I N G T H E L I O N F I S H I N VA S I O N 675
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676 I . M . CÔ TÉ A N D N . S . S M I T H
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R E- E VA L U AT I N G T H E L I O N F I S H I N VA S I O N 677
2013) or tethered (Diller et al., 2014) lionfish. Low predation on lionfish is therefore
more likely a result of lionfish being well defended against predators in general than
of Atlantic predator naïveté. Even if predator training were possible, scaling up from
learning by individual fish to the regional scale needed for effective biocontrol seems
unachievable.
Finally, implementing fishing restrictions and networks of MPAs could increase the
abundance and body size of species that could prey on, compete with, or scare lionfish
(Albins & Hixon, 2013). Both measures have a track record of success at rebuilding
depleted fish populations (Lester et al., 2009; Hilborn & Ovando, 2014). There is cur-
rently limited evidence, however, for biotic resistance of Atlantic marine communities
(see above). Moreover, marine reserves are sometimes havens for non-native species
(Simberloff, 2000; Byers, 2005; Klinger et al., 2006; Burfeind et al., 2013). It is not
clear whether this is the case for lionfish. The only comparison of lionfish abundance
in and out of an MPA (Mumby et al., 2011) might have been confounded by culling
(Hackerott et al., 2013; Valdivia et al., 2014). There are many good reasons to establish
marine reserves, but controlling lionfish is probably not one of them.
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678 I . M . CÔ TÉ A N D N . S . S M I T H
Côté et al., 2013a; Andradi-Brown et al., 2017a, 2017b), relatively easy to catch, tag
and release (Akins, 2012; Akins et al., 2014) and many aspects of their ecology and
behaviour are now well understood (Fig. 1). Their large body sizes (Darling et al.,
2011), however, and sometimes extensive movement between habitat patches (Tam-
burello & Côté, 2014), make them less tractable to experimental manipulation than
other taxa like terrestrial plants, which have fuelled the development of invasion the-
ory (Lockwood et al., 2005; Fridley et al., 2007; Catford et al., 2009; Jeschke, 2014).
These drawbacks, however, are surmountable (Green et al., 2014; Smith et al., 2017).
Lionfish can be used as a model system for testing prominent invasion hypotheses.
For example, the importance of biotic resistance (Elton, 1958) in predation- rather than
competition-driven systems could be tested by introducing lionfish into experimen-
tally assembled reef communities or examining their establishment and effect along
geographic gradients of species richness. Similarly, investigations of lionfish parasites
in both the native and invaded ranges are empirically relevant to the ‘enemy release’
hypothesis (Keane & Crawley, 2002) and can be used to test the ‘evolution of increased
competitive ability’ hypothesis, whereby escape from parasites can lead to invaders
reallocating resources from defences towards reproduction or growth (Blossey & Nöt-
zold, 1995). Other key hypotheses, however, cannot be easily tested with lionfish. For
example, propagule pressure (i.e. the size and frequency of release events as well as the
composition of propagules) is arguably the most important determinant of establish-
ment success (Lockwood et al., 2005; Simberloff, 2009). Information on this crucial
aspect of the invasion process, however, is scarce for lionfish and must be largely
inferred from genetic studies. Lionfish might therefore serve as a useful model system
to address at least a few general ideas in invasion ecology.
CONCLUSION
This overview of the lionfish invasion focused on recent information pertaining to the
traits that have made lionfish effective invaders, their realized and predicted effects and
how to manage them. This is a small fraction of the knowledge gained about lionfish
over the past few years. Great strides have been made in understanding their ecology
in the native range [Darling et al., 2011; Cure et al., 2012, 2014; Kulbicki et al., 2012;
Sikkel et al., 2014; Stevens & Olson, 2015; Pusack et al., 2016; Tuttle et al., 2017;
Fig. 1(b)], how best to survey them (Green et al., 2013; Tilley et al., 2016; Bacheler
et al., 2017), their movement patterns (Tamburello & Côté, 2014; Bacheler et al., 2015;
Benkwitt, 2016) and their genetic structure (Hamner et al., 2007; Freshwater et al.,
2009; Betancur-R et al., 2011; Toledo-Hernández et al., 2014; Butterfield et al., 2015;
Johnson et al., 2016). There is also recent molecular evidence that P. volitans in the
native range might in fact be a hybrid between two sister lineages (Indian Ocean P.
miles x Pacific Ocean Pterois russelii Bennett 1831; Wilcox et al., 2018). This could
partly explain both the extraordinary performance of lionfish in the invaded range (i.e. a
result of heterosis) and why P. miles, a pure species, has not invaded the Mediterranean
Sea with the same swiftness as a Lessepsian migrant (Johnston & Purkis, 2014).
There is no doubt that lionfish have had a tremendous detrimental effect on some
native reef-fish populations in the northern part of the invaded range. Similar large
effects, however, have yet to be seen in the southern Caribbean. Most of the other
envisaged direct and indirect consequences of lionfish predation and competition, even
© 2018 The Fisheries Society of the British Isles, Journal of Fish Biology 2018, 92, 660–689
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R E- E VA L U AT I N G T H E L I O N F I S H I N VA S I O N 679
70 1·8
Fig. 2. Mean ± S.E. changes in lionfish Pterois sp. (a) sighting frequency and (b) density since it was first reported
in The Bahamas in 2004. Data are from the Reef Environmental Education Foundation (www.REEF.org)
volunteer survey project database for natural and artificial reefs in the central Bahamas (n = 3 island groups;
the Exumas, New Providence and San Salvador). Sighting frequency refers to the percentage of all surveys
in which lionfish were reported; density index is a measure of how many lionfish were observed during a
survey, and ranges from one (a single individual) to four (over 100 individuals). A score of 2 (the 2008
maximum) represents 2–10 individuals.
those that might have been expected to occur rapidly (e.g. shifts in benthic composi-
tion as a result of lower herbivory), have yet to pass (Table IV). This is not to say that
they will not, given more time and better data. For example, the continued expansion
of lionfish to its thermal limit in the southern hemisphere is almost a certainty. Lionfish
populations in some of the first areas invaded, however, have started to decline (Fig. 2;
Benkwitt et al., 2017), perhaps as a result of resource depletion, fishing and culling,
so there might be hope that these areas have already experienced the worst of the
invasion.
Many key questions remain as the lionfish invasion continues to unfold in the west-
ern Atlantic Ocean; we highlight four. First, is there an ontogenetic shift from shal-
low to deep water? Such a shift is assumed to occur (Johnson & Swenarton, 2016;
Andradi-Brown et al., 2017a, 2017b) and it has large implications for strategies to
control lionfish, which currently focus on scuba-diveable depths (i.e. < 30 m). Sec-
ond, what are the effects of lionfish on invertebrates? The vast majority of research to
date has focused on prey fish, but lionfish consume a variety of invertebrates (Table III).
There is evidence that the proportion of invertebrates in their diet has increased over
time (Green et al., 2014) and that lionfish can reduce invertebrate populations drasti-
cally (Layman et al., 2014; Ellis & Faletti, 2016). Third, how do lionfish circumvent
predator recognition mechanisms in prey fish? Figuring out how lionfish manage to
cloak themselves and how to disable this mechanism could provide a new tool to
mitigate their effect on other fish. Finally, what factors limit and regulate lionfish in
the native range? Benkwitt (2013) showed density-dependent growth but no density
dependence in recruitment, immigration or loss (i.e. emigration + mortality) in inva-
sive lionfish, which may or may not reflect population processes in the native range.
The rarity of lionfish in the Indian and Pacific Oceans has made this question difficult
to address but it remains one of the most important questions to answer.
© 2018 The Fisheries Society of the British Isles, Journal of Fish Biology 2018, 92, 660–689
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680 I . M . CÔ TÉ A N D N . S . S M I T H
We thank the organizers of the 50th Anniversary Symposium of The Fisheries Society of the
British Isles, S. Simpson and I. Barber, for the invitation to give a plenary presentation on the
lionfish invasion and for the opportunity to contribute this paper.
Supporting Information
Supporting Information may be found in the online version of this paper:
Table S1. List of parasite taxa found on lionfish Pterois sp.
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