Review Article |
Corresponding author: Davide Bottacini ( davide.bottacini@wur.nl ) Academic editor: Cascade Sorte
© 2024 Davide Bottacini, Bart J. A. Pollux, Reindert Nijland, Patrick A. Jansen, Marc Naguib, Alexander Kotrschal.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Bottacini D, Pollux BJA, Nijland R, Jansen PA, Naguib M, Kotrschal A (2024) Lionfish (Pterois miles) in the Mediterranean Sea: a review of the available knowledge with an update on the invasion front. NeoBiota 92: 233-257. https://doi.org/10.3897/neobiota.92.110442
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Invasive species often severely impact ecosystems and human activities in the areas that they invade. The lionfishes Pterois miles and P. volitans are regarded as the most successful invasive fishes in marine ecosystems. In the last 40 years, these Indo-Pacific predators have established in the tropical western Atlantic Ocean, with well-documented detrimental effects on the local fish communities. Around 10 years ago, a second invasion began in the Mediterranean Sea, which is being colonised by P. miles. Given the invasive potential of P. miles and the fact that the ecology and biodiversity of the temperate/sub-tropical Mediterranean Sea offer a different setting from the tropical western Atlantic, specific knowledge on this second invasion is needed. Here, we: (i) review the scientific knowledge available on the ecology of invasive lionfishes, (ii) discuss such knowledge in the context of invasion ecology and (iii) suggest future research avenues on the P. miles invasion in the Mediterranean Sea. In addition, we offer an update on the spread of P. miles in the Mediterranean Sea. While the history and development of the Mediterranean invasion are resolved and some mitigation plans have been implemented locally, the study of the interactions of P. miles with Mediterranean species and their impact on the local biodiversity is in its infancy. Closing this gap will lead to important fundamental insights in invasion ecology and will result in predictions on the impact of P. miles on the ecology and ecosystem services of the Mediterranean Sea. Such information will have practical implications for policy-makers aiming to devise sound and efficient mitigation plans.
Citizen science, exotic predators, invasion ecology, marine ecology, predation ecology
Invasive species are species that establish and spread in a new range at a high rate (
The lionfishes Pterois miles and P. volitans (hereafter, referred together as ‘lionfish’) are virtually undistinguishable and show almost identical morphological traits (
The Mediterranean is a unique ecosystem: it is the largest enclosed sea on Earth and a highly biodiverse basin, home to more than 11000 animal species, some of which are found nowhere else in the world (
There are important differences between the Mediterranean and the tropical western Atlantic. The Mediterranean is a temperate/sub-tropical sea dominated by rocky reefs, seagrass meadows and sandy patches (
The first lionfish ever reported in the Mediterranean was caught by a trawler off the coast of Israel in 1991 and identified as P. miles (
Genetic studies revealed that lionfish found in the Mediterranean originate from the Red Sea and that they most likely entered their new range during multiple invasion events through the Suez Canal (
The northern Red Sea is inhabited by another lionfish species that is biologically and ecologically similar to P. miles; Pterois radiata. P. miles and P. radiata often occur together on the coral reefs of the northern Red Sea and in comparable abundances (
P. miles entered the Mediterranean from one of its easternmost locations and continue to expand westwards and northwards (
As a follow-up to
Contacting 996 dive centres yielded 326 responses (Fig.
Maps of respondents and lionfish sightings. Panel A shows the respondents to our survey in 2023. Each dot represents a dive centre that we contacted, with orange dots representing dive centres that responded and black dots representing dive centres that did not. Panel B shows the responses to our survey in 2023. Each dot represents a dive centre that responded to our survey in 2023 with orange dots representing dive centres that reported lionfish sightings and black dots representing dive centres that reported no sightings. Panel C shows the responses to the survey in 2021 (
The years and locations where lionfish were first seen (Fig.
Map of years of first sighting. Each dot represents a dive centre that reported lionfish sightings, either in 2021 or 2023 and included in their response the year when lionfish were first sighted. The darkness of dots shows the year range when lionfish were first sighted.
Our results show that the invasive range of P. miles continues to expand rapidly in the Mediterranean. Similar to most coral reef fishes, lionfish eggs hatch into pelagic larvae (
Many Lessepsian species remain confined to the eastern Mediterranean and are rarely found in high numbers elsewhere (
Remarkably, several P. miles sightings were reported in areas that were considered to have winter surface temperatures that are too cold for this species (< 15 °C) such as the northern Aegean and southern Adriatic (
Our study shows that citizen science is a fruitful approach to monitor lionfish populations at the large scale in the Mediterranean, where the dive industry is strong and awareness towards lionfish is high. Different approaches are needed to monitor the state of the invasion on the southern coasts of the Mediterranean, where data are lacking and the number of dive centres is extremely low (Fig.
Lionfish have 18 venomous spines; one on each of the first 13 rays of their dorsal fin, one on each of their pelvic fins and three on their anal fin (Aktaş and Mirasoğlu 2017). They show high site fidelity and often return to the same hiding place over the course of several weeks (
Fishes make up most of the lionfish diet (
The high predation effectiveness in their invaded range has been attributed, at least in part, to prey naïveté (
Experiments on prey naïveté in the context of lionfish invasions raise the question of whether the selection pressure posed by this new predator will result in adaptations in local prey. It follows from the definition of prey naïveté that it can be counteracted by evolutionary adaptation: after several generations of co-existence with a novel predator, prey should evolve innate responses (
Prey naïveté interferes with innate predator recognition in animals (
Predator recognition allows prey to mount an appropriate behavioural response to a predator. Therefore, invasive lionfish are predicted to select on traits that make prey better able to recognise them, either innately or through learning. However, predators can also select on prey behavioural traits that make them less likely to be preyed on due to processes that are not related to predator recognition (
The ‘enemy release hypothesis’ posits that exotic organisms benefit from reduced top-down control due to a paucity of natural enemies in their newly-invaded ranges (
There are other factors than reduced predation on adults that could explain the large population sizes that lionfish reach in their invaded ranges. First, parasites, rather than predators, could be limiting the fitness of adults in their native range (
The high effectiveness of lionfish as predators implies that they are a potential threat to the native fish community of the areas that they are invading. P. volitans are, indeed, having a profound impact on the fish community of the western Atlantic, where they prey heavily on numerous species of very high conservation value (
The high predation rates shown by lionfish raised concerns on their potential effects on economically valuable species and the fishing industry of the Mediterranean (
Lionfish are venomous and reach large population sizes in their invaded ranges (
Lionfish are highly sedentary and easy to identify by divers due to their conspicuous appearance. This resulted in the involvement of lay people in initiatives aimed at curbing lionfish populations through spearfishing. In so-called ‘culling tournaments’ (or ‘derbies’), divers are encouraged to hunt for lionfish by means of spear-guns (often simpler Hawaiian slings) while free or SCUBA diving (
Culling tournaments were organised in the Mediterranean soon after the start of the invasion (
The history and development of the lionfish invasion in the Mediterranean are well-resolved and can be updated promptly through citizen-science initiatives involving the aware and collaborative local dive centres (
Studies on the predation ecology of P. miles in the Mediterranean remain scant, especially in comparison with the large body of literature available on the Atlantic invasion (
Prey naïveté is a contributor to the success of lionfish in the Atlantic and Mediterranean, where native prey show virtually no response to this new predator (
Individual prey fishes have the potential to learn that lionfish are dangerous through associative learning, even in the absence of co-evolutionary history (
Another major question on the ecology of lionfish, both in their native and invaded ranges, is what their main source of mortality is (
While the history and development of the P. miles invasion in the Mediterranean are well-resolved and can be easily updated through citizen-science initiatives, the study of the predation ecology of invasive P. miles is its infancy, especially at high ecological levels. In addition, the ongoing lionfish invasion in the Mediterranean offers the opportunity to test for major fundamental questions on prey naïveté and learned predator responses. We outlined approaches that could be used to answer these major questions by taking advantage of the ongoing and more recent lionfish invasion in the Mediterranean. Tackling questions such as the community-level impact of lionfish in the Mediterranean and the evolutionary and learned responses in prey will add to the body of knowledge on the best documented invasion in marine ecosystems. This will result in insights into fundamental questions in invasion and predation ecology, but will also be important for policy-makers to estimate the impact of invasive lionfish on human activities.
We thank Elizabeth Phillips for providing us with the list of dive centres and the data collected in 2021. We thank the native speakers who helped with the translations of our emails: Antoine Parsekian, Elisa Vallejo Marquez, Fotini Kokou, Patricija Gran, Tomer First and Utku Urhan. We also thank the numerous dive centres that kindly responded to our survey.
The authors have declared that no competing interests exist.
No ethical statement was reported.
This study was supported by a WIAS (Wageningen Institute of Animal Sciences) Graduate Programme fellowship awarded to D.B.
D.B. and A.K. conceived the study. D.B. collected the data. D.B. analysed the data and wrote the first version of the manuscript. All authors (D.B., B.A.J.P., R.N., P.A.J., M.N. and A.K.) provided feedback on earlier versions of the manuscript and contributed to its final version.
Davide Bottacini https://orcid.org/0009-0003-2902-1067
Bart J. A. Pollux https://orcid.org/0000-0001-7242-2630
Reindert Nijland https://orcid.org/0000-0003-0049-3768
Patrick A. Jansen https://orcid.org/0000-0002-4660-0314
Marc Naguib https://orcid.org/0000-0003-0494-4888
Alexander Kotrschal https://orcid.org/0000-0003-3473-1402
All of the data that support the findings of this study are available in the main text.