Content uploaded by Arthur R. Bos
Author content
All content in this area was uploaded by Arthur R. Bos on Jan 18, 2018
Content may be subject to copyright.
2017 Environ Biol Fish 100(6): 745–748 DOI 10.1007/s10641-017-0600-7
745
The final publication is available at link.springer.com
Gymnothorax spp. (Muraenidae) as natural predators
of the lionfish Pterois miles in its native biogeographical range
Arthur R. Bos · Ashraf M. Sanad · Khamis Elsayed
1Department of Biology, American University in Cairo, P.O. Box 74, New Cairo 11835, Egypt
2Naturalis Biodiversity Center, P.O. Box 9517, 2300 RA Leiden, the Netherlands
3Dive Pro Academy, P.O. Box 94, Sahl Hasheesh, Hurghada, Egypt
E-mail: arbos@aucegypt.edu
Abstract Lionfish (Pterois miles) were observed avoiding
coral pinnacles inhabited by the moray eels Gymnothorax
flavimarginatus and G. javanicus in the northern Red Sea,
Egypt. Release of lionfish (Standard Length 93–104 mm) in
such coral pinnacles in November 2016 resulted in almost
immediate predation by large moray eels (Total Length > 1
m). Predation by moray eels may be the key control
mechanism of population growth in the native
biogeographical range of Pterois spp. and may indirectly
explain the success of the invasive populations. This is the
first videodocumented record of moray eels feeding on the
lionfish P. miles.
Keywords Moray eel · Predation · Pterois · Red Sea ·
Scorpaenidae
Introduction
Indo-Pacific lionfishes, Pterois miles (Bennett, 1828) and P.
volitans (Linneaus, 1758), have become invasive in the coral
reefs of theWestern Central Atlantic region, from Bermuda to
Brazil including the Mexican Gulf and the Caribbean Sea,
after being introduced accidentally in the late 1980s (e.g.,
Johnston and Purkis 2011; Côté et al. 2013; Luiz et al. 2013).
Success of the lionfish populations of the invaded regions has
been attributed to its unique biology and feeding strategy, as
well as the lack of natural predators (Cure et al. 2012). In
their native ranges, lionfish live relatively secretive in coral
crevices during the day (Fishelson 1997) and forage at night.
In contrast, lionfish of the invaded regions are mostly
diurnally active (Morris and Akins 2009). Lionfish defend
themselves with venomous spines in their anterior dorsal and
pectoral fins and are, for most predators, a challenging prey.
Incidental observations of large fish ingesting lionfish
have been reported from the invasive populations. For
example, two lionfish were found in the stomach of the
Nassau grouper Epinephelus striatus (Bloch, 1792)
(Maljković et al. 2008) and Jud et al. (2011) reported an
individual of the moray eel Gymnothorax funebris Ranzani,
1839 ingesting a wounded lionfish. Hackerott et al. (2013)
concluded that some predatory fish may occasionally
consume lionfish, but an Atlantic predator controlling the
invasive populations may not exist. Although the magnitude
of grouper predation has intensively been discussed (Bruno et
al. 2013; Mumby et al. 2013) there is a general consensus that
groupers cannot fully control the invasive populations.
Lionfish research has been initiated and intensified during
the last two decades to understand the ecological impacts of
the invasive populations. In the native habitats in the Indo-
Pacific region, few studies have been conducted on lionfish
populations because (1) densities are naturally low (Kulbicki
et al. 2012) and (2) the ecological role of lionfish in coral
reefs is poorly understood (Donaldson et al. 2010). As a
consequence, little is known about the lifecycles of these fish,
hence natural enemies have not been identified in the native
biogeographical range. Only one incidental observation was
reported from the Red Sea, where a lionfish was found in the
stomach of an individual of Fistularia commersonii (Rüppel,
1838) (Bernadsky and Goulet 1991). Throughout native
habitats however, there must be effective population control
mechanisms in place because lionfish abundance is much
lower there compared to theWestern Central Atlantic region
(McTee and Grubich 2014). During reef surveys in the
northern Red Sea (unpublished data), we noticed that coral
pinnacles, used as diurnal shelter by large moray eels of the
genus Gymnothorax spp., were rarely inhabited by lionfish.
These coral pinnacles usually had abundant prey for lionfish
(Morris and Akins 2009), suggesting that lionfish absence
was the consequence of moray eel presence. The goal of the
present study was to explore the possibility that moray eels of
the genus Gymnothorax spp. are natural predators of the
lionfish P. miles.
2017 Environ Biol Fish 100(6): 745–748 DOI 10.1007/s10641-017-0600-7
746
Material and methods
Observations were made while SCUBA diving on a coral reef
off Hurghada, Egypt in the northern Red Sea between 9:30
and 16:00 h on 25 November 2016. At the beginning of each
dive a lionfish of appropriate size (90–120 mm) was caught
with a handheld net. The standard length (SL) of the lionfish
was measured with a ruler at 1 mm accuracy. The behavior of
the lionfish and interactions with the moray eel were recorded
during the remaining dive time after releasing it near a coral
pinnacle occupied by a moray eel. The above procedure was
repeated with another lionfish during a second dive.
Moray eels were identified using Randall and Golani
(1995) and their total length (TL) was visually estimated to
the nearest 0.1 m. A Go-Pro camera in underwater housing
with red filter was used for documentation purposes. The
depth of the coral pinnacles was recorded to the nearest 1 m
using a depth gauge.
Results and discussion
A lionfish with a SL of 104 mm was released near a coral
pinnacle at 21 m depth inhabited by an individual of
Gymnothorax flavimarginatus (Rüppel, 1830) with an
estimated TL of 1.1 m. Initially the lionfish swam away from
the coral, but eventually settled within the pinnacle (Fig.
1).Within a couple of minutes, the moray eel noticed the
presence of the lionfish. Subsequently, the moray eel
positioned itself for attacking. Although the lionfish directed
its spines toward the predator, the moray eel swiftly attacked
the lionfish at the rear of its body (Online Resource 1). After
a short fight, the moray eel held the fish with the pectoral fins
and head protruding from its mouth, and pulled the fish
deeper into the crevice out of sight of the camera.
A second lionfish with a SL of 93 mm was released in a
coral pinnacle at 6 m depth inhabited by an individual of
Gymnothorax javanicus (Bleeker, 1859) with an estimated
TL of 1.7 m. Similarly as reported for the first release, the
lionfish initially swam away. While curiously being observed
by the moray eel, the lionfish was repeatedly returned to the
coral pinnacle by the divers. The moray eel seemed hesitant
to leave its shelter, most probably due to diver presence (e.g.,
Dickens et al. 2011). When the lionfish was presented right in
front of the protruding head of the moray eel, it struck as
soon as the lionfish swam out of the net (Online Resource 2).
At this occasion, the moray eel attacked the lionfish
frontally, which suggests that there may not be an optimal
strategy for approaching lionfish. However, the smaller
individual of the moray G. flavimarginatus seemed more
cautious, avoiding the spines by attacking at the rear end of
the prey. While holding the lionfish in its mouth, G.
javanicus pulled back into the crevice after striking and
briefly chewed on the lionfish. This is only partly visible on
the footage, because the camera housing did not fit into the
crevice (Online Resource 2). As soon as the lionfish was
swallowed, the moray eel returned to the net and curiously
investigated the camera.
Past studies have shown that moray eels tend to remain in
particular coral heads for one to several days up to seven
weeks depending of the species (Abrams et al. 1983; Abrams
and Schein 1986). We confirm, based on regular visits to
selected Red Sea coral pinnacles during the last 10 years, that
several moray eels of the genus Gymnothorax spp. have fixed
home bases (personal observation). Despite the abundance of
small fishes, such as representatives of the Anthiinae and
Apogonidae (Online Resources 1 and 2) that could serve well
as prey (Morris and Akins 2009; Green et al. 2012; McTee
and Grubich 2014), lionfish avoided coral pinnacles inhabited
by moray eels (unpublished data). The present observations
showed that lionfish released at such pinnacles initially swam
away. Whether the lionfish recognized the presence of moray
eels, or instinctively moved away from unfamiliar coral
heads, is unknown. Lionfish may avoid predation by not
frequenting pinnacles inhabited by moray eels, whereas those
who accidentally settle may be readily targeted. Our diurnal
Fig. 1 Individual of Pterois miles (SL = 104 mm) settling in
coral pinnacle at 21 m depth minutes before being preyed
upon by an individual of the moray eel Gymnothorax
flavimarginatus
2017 Environ Biol Fish 100(6): 745–748 DOI 10.1007/s10641-017-0600-7
747
observations of moray eels preying on lionfish may be
unique, because moray eels usually predate nocturnally
(Young and Winn 2003). However, the moray eels caught the
lionfish with minimal effort, possibly challenging their
normal feeding behavior.
Densities of moray eels have rarely been reported,
because it is difficult to get reliable numbers during the day
when they hide in crevices as well as during the night when
they are out hunting (Gilbert et al. 2005). As a result,
densities of hole-dwelling species, including moray eels, are
commonly underestimated (Willis 2001). In the Red Sea,
large moray eels (TL >1 m) are regularly encountered during
the day, either resting in crevices with their heads protruding
or, less frequently, free swimming (personal observation).
Moray eels may play a role in controlling the population size
of lionfishes in the Indo-Pacific region. Moreover, the role of
moray eels controlling the invasive populations may be
limited as a result of the much lower number of moray eel
species in the Western Central Atlantic region (Froese and
Pauly 2015).
Researchers have mainly concentrated on taxonomic
analyses of moray eels and the limited number of ecological
studies were mostly conducted in the Caribbean and tropical
Atlantic. Therefore, little is known about the ecology of Indo-
Pacific moray eels. Recently, lionfish were observed in
foraging association with individuals of the moray eel
Gymnothorax griseus (Lacepède, 1803) in the Red Sea
(Naumann and Wild 2013). Gymnothorax griseus grows to a
maximum TL of 0.65 m (Froese and Pauly 2015) and may
thus never pose a threat to lionfish. Only individuals of
Gymnothorax spp. growing well beyond 1 m in total length
may be able to prey on lionfish. Marine biodiversity is
exceptionally high in the tropical waters of the Indo-Pacific
region compared to any other sea on the planet (Carpenter
and Springer 2005; Hoeksema 2007). For example, in the
Western Central Pacific, the genus Gymnothorax is
represented by 63 species of which 16 have a maximum total
length of ≥1 m (Froese and Pauly 2015). In the Western
Indian Ocean, including the Red Sea, Gymnothorax is
represented by 51 species of which 14 grow larger than 1 m
(Froese and Pauly 2015). In contrast, in the Western Central
Atlantic region 12 species represent Gymnothorax of which
only five have a maximum total length of ≥1 m (Froese and
Pauly 2015). Considering the above, the potential predation
pressure on lionfish populations by Gymnothorax spp. is
much lower in the Western Central Atlantic region than in the
Indo-Pacific region and could have possibly contributed to
the success of the invasive populations. Nevertheless, one
individual of the moray eel G. funebris was reported feeding
on a wounded lionfish in Florida (Jud et al. 2011), confirming
that moray eels may potentially prey on lionfish in the
invasive range. Whether or not moray eels in the Western
Central Atlantic region actively prey on lionfish is presently
unknown. Although Hackerott et al. (2013) concluded that,
mainly referring to groupers, there may not be an effective
Atlantic predator, the quantification of the impact of moray
eels feeding on invasive lionfish may allow a different view
on the matter.
Acknowledgements All applicable international, national, and/or
institutional guidelines for the care and use of animals were followed.
Two anonymous reviewers provided valuable comments to improve the
manuscript.
References
Abrams RW, Abrams MD, Schein MW (1983) Diurnal observations on
the behavioural ecology of Gymnothorax moringa (Cuvier) and
Muraena miliaris (Kaup) on a Caribbean coral reef. Coral Reefs
1:185–192
Abrams RW, Schein MW (1986) Individual movements and population
density estimates for moray eels on a Caribbean coral reef. Coral
Reefs 5:161–163
Bernadsky G, Goulet D (1991) A natural predator of the lionfish,
Pterois miles. Copeia 1:230–231
Bruno JF, Valdivia A, Hackerott S, Cox CE, Green SJ, Côté IM, Akins
L, Layman CA, PrechtWF (2013) Testing the grouper biocontrol
hypothesis: a response to Mumby et al. 2013. PeerJ PrePrints
e139v1
Carpenter KE, Springer VG (2005) The center of the center of marine
shore fish biodiversity: the Philippine Islands. Environ Biol Fish
72:467–480
Côté IM, Green SJ, Hixon MA (2013) Predatory fish invaders: insight
from Indo-Pacific lionfish in the western Atlantic and Caribbean.
Biol Conserv 164:50–61
Cure K, Benkwitt CE, Kindinger TL, Pickering EA, Pusack TJ,
McIlwain JL, Hixon MA (2012) Comparative behavior of red
lionfish Pterois volitans on native Pacific versus invaded Atlantic
coral reefs. Mar Ecol Prog Ser 467:181–192
Dickens LC, Goatley CH, Tanner JK, Bellwood DR (2011) Quantifying
relative diver effects in underwater visual censuses. PLoS One
6:e18965
Donaldson TJ, Benavente D, Diaz R (2010) Why are lionfishes (Pterois,
Scorpaenidae) so rare in their native ranges? Proceedings of the
63rd gulf and Caribbean. Fisheries Institute 2011:352–359
Fishelson L (1997) Experiments and observations on food consumption,
growth and starvation in Dendrochirus brachypterus and Pterois
volitans (Pteroinae, Scorpaenidae). Environ Biol Fish 50:391–403
Froese R, Pauly D (2015) FishBase. World Wide Web Electronic
Publications. http://www.fishbase.org. Accessed on 28 Nov 2016
Gilbert M, Rasmussen JB, Kramer DL (2005) Estimating the density
and biomass of moray eels (Muraenidae) using a modified visual
census method for hole-dwelling reef fauna. Environ Biol Fish
73:415–426
Green SJ, Akins JL, Maljković A, Côté IM (2012) Invasive lionfish
drive Atlantic coral reef fish declines. PLoS One 7: e32596
Hackerott S, Valdivia A, Green SJ, Côté IM, Cox CE, Akins L, Layman
CA, Precht WF, Bruno JF (2013) Native predators do not influence
invasion success of Pacific lionfish on Caribbean reefs. PLoS One
8:e68259
Hoeksema BW (2007) Delineation of the Indo-Malayan centre of
maximum marine biodiversity: the coral triangle. In: Renema W(ed)
Biogeography, time, and place: distributions, barriers, and islands.
Springer, New York, pp 117–178
Johnston MW, Purkis SJ (2011) Spatial analysis of the invasion of
lionfish in the western Atlantic and Caribbean. Mar Poll Bull
62:1218–1226
Jud ZR, Layman CA, Lee JA, Arrington DA (2011) Recent invasion of
a Florida (USA) estuarine system by lionfish Pterois volitans / P.
miles. Aquat Biol 13(1):21–26
Kulbicki M, Beets J, Chabanet P, Cure K, Darling E, Floeter SR, Galzin
R, Green A, Harmelin-Vivien M, Hixon M, Letourneur Y (2012)
Distributions of Indo-Pacific lionfishes Pterois spp. in their native
ranges: implications for the Atlantic invasion. Mar Ecol Prog Ser
446:189–205
2017 Environ Biol Fish 100(6): 745–748 DOI 10.1007/s10641-017-0600-7
748
Luiz OJ, Floeter SR, Rocha LA, Ferreira CEL (2013) Perspectives for
the lionfish invasion in the South Atlantic: are Brazilian reefs
protected by the currents? Mar Ecol Prog Ser 485:1–7
Maljković A, van Leeuwen TE, Cove SN (2008) Predation on the
invasive red lionfish, Pterois volitans (Pisces: Scorpaenidae), by
native groupers in the Bahamas. Coral Reefs 27:501
McTee SA, Grubich JR (2014) Native densities, distribution, and diurnal
activity of Red Sea lionfishes (Scorpaenidae). Mar Ecol Prog Ser
508:223–232
Morris JA, Akins JL (2009) Feeding ecology of invasive lionfish
(Pterois volitans) in the Bahamian archipelago. Environ Biol Fish
86:389–398
Mumby PJ, Brumbaugh DR, Harborne AR, Roff G (2013) On the
relationship between native grouper and invasive lionfish in the
Caribbean. PeerJ PrePrints e45v1
NaumannMS,Wild C (2013) Foraging association of lionfish and moray
eels in a Red Sea seagrass meadow. Coral Reefs 32: 1111
Randall JE, Golani D (1995) Review of the moray eels (Anguilliformes:
Muraenidae) of the Red Sea. Bull Mar Sci 56(3):849–880
Willis TJ (2001) Visual census methods underestimate density and
diversity of cryptic reef fishes. J Fish Biol 59:1408–1411
Young RF,Winn HE (2003) Activity patterns, diet, and shelter site use
for two species of morays eels, Gymnothorax moringa and
Gymnothorax vicinus, in Belize. Copeia 2003:44–55