A novel marine bioinvasion vector: Ichthyochory, live passage through fish

Many species of Indo‐Pacific holobenthic foraminifera have been introduced and successfully established sustainable populations in the Mediterranean Sea over the past few decades. However, known natural and anthropogenic vectors do not explain how these species were introduced long distances from their origin. We present evidence for a novel marine bioinvasion vector explaining this long‐distance transport and introduction using both contemporary field and historical analyses. In 2015–2016, we found living specimens of 29 foraminiferal species in the fecal pellets of two Red Sea herbivorous rabbitfish—Siganus rivulatus and Siganus luridus in the Mediterranean. In our historical analysis, we found 34 foraminiferal species in preserved Red Sea rabbitfish specimens, dating between 1967 and 1975. In addition, we found congruent propagation patterns of the non‐indigenous rabbitfish and foraminifera, lagging 4–11 yrs between discoveries, respectively. Predation of marine benthos by non‐indigenous fish, followed by incomplete digestion and defecation of viable individuals, comprise the main introduction vector of these organisms into novel environments.

• Publication year

  2017

• Venue

  Limnology and Oceanography Letters

• Publication date

  2017-05-15

• Fields of study

  Biology, Environmental Science

• Identifiers
  DOI 10.1002/lol2.10039
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar

• No claims are published for this paper.

• No concepts are published for this paper.

• On the origin of species by means of natural selection: Or the preservation of the favoured races in the struggle for life.

  2019cited by this paper
• Did Amphistegina lobifera Larsen reach the Mediterranean via the Suez Canal

  2016cited by this paper
• ‘Double trouble’: the expansion of the Suez Canal and marine bioinvasions in the Mediterranean Sea

  2015cited by this paper
• Plastic debris in the open ocean

  2014cited by this paper
• The tropicalization of temperate marine ecosystems: climate-mediated changes in herbivory and community phase shifts

  2014cited by this paper
• Characteristics of benthic foraminifera inhabiting rocky reefs in northern Israeli Mediterranean shelf

  2014cited by this paper
• Traveling through time: The past, present and future biogeographic range of the invasive foraminifera Amphistegina spp. in the Mediterranean Sea

  2013cited by this paper
• Biological invasions: a field synopsis, systematic review, and database of the literature

  2013cited by this paper
• Elemental and Isotopic Proxies of Past Ocean Temperatures

  2013cited by this paper
• Invasive zebra mussels (Driessena polymorpha) and Asian clams (Corbicula fluminea) survive gut passage of migratory fish species: implications for dispersal

  2013cited by this paper
• Dispersal in marine organisms without a pelagic larval phase.

  2012cited by this paper
• “STRANGERS” IN PARADISE: MODELING THE BIOGEOGRAPHIC RANGE EXPANSION OF THE FORAMINIFERA AMPHISTEGINA IN THE MEDITERRANEAN SEA

  2012cited by this paper
• Alien species in the Mediterranean Sea by 2012. A contribution to the application of European Union’s Marine Strategy Framework Directive (MSFD). Part 2. Introduction trends and pathways

  2012cited by this paper
• Foraminifera in the diet of coral reef fish from the lagoon of New Caledonia: Predation, digestion, dispersion

  2011cited by this paper
• The experimental study of seed dispersal by fish (ichthyochory)

  2011cited by this paper
• Dispersal, survival and delayed growth of benthic foraminiferal propagules

  2010cited by this paper
• Invasive Species: Detection, Impact and Control

  2009cited by this paper
• Contribution of Fish to the Marine Inorganic Carbon Cycle

  2009cited by this paper
• Benthic foraminifera assemblage change along the southeastern Mediterranean inner shelf due to fall-off of Nile-derived siliciclastics

  2008cited by this paper
• Spread dynamics of invasive species.

  2006cited by this paper
• Ecology and Applications of Benthic Foraminifera: Taxonomic Index

  2006cited by this paper
• Ecology and applications of benthic foraminifera

  2006cited by this paper
• A novel trophic relationship between cassid gastropods and mysticete whale carcasses

  2005cited by this paper
• Long-distance movements of coral reef fishes

  2004cited by this paper
• The most complete global overview of invasive species in natural areas

  2004cited by this paper
• 6.14 – Elemental and Isotopic Proxies of Past Ocean Temperatures

  2003cited by this paper
• Invasive species: vectors and management strategies.

  2003cited by this paper
• Community disassembly by an invasive species

  2003cited by this paper
• The Importance of Ship Hull Fouling as a Vector of Species Introductions into the North Sea

  2002cited by this paper
• Biological invasions—How are they affecting us, and what can we do about them?

  2001cited by this paper
• Distinguishing live from dead Foraminifera; methods review and proper applications

  2000cited by this paper
• Invasion by a Japanese marine microorganism in western North America

  2000cited by this paper
• Positive Interactions of Nonindigenous Species: Invasional Meltdown?

  1999cited by this paper
• Colonization of new habitats by benthic foraminifera : A review

  1999cited by this paper
• Protist transport via ballast water — biological classification of ballast tanks by food web interactions

  1997cited by this paper
• General Circulation of the Eastern Mediterranean

  1992cited by this paper
• Locomotion of some benthic foraminifera in and on sediments

  1988influential reference
• Trophic biology of herbivorous reef fishes: alimentary pH and digestive capabilities

  1981influential reference
• Lessepsian migration. The influx of Red Sea biota into the Mediterranean by way of the Suez Canal: By Francis D. Por. Pp. 228. Springer, Berlin. 1978. DM 64 ($32.00)

  1979cited by this paper
• Lessepsian Migration: The Influx of Red Sea Biota into the Mediterranean by Way of the Suez Canal

  1978cited by this paper
• Evolution and distribution of the genus Mya, and Tertiary migrations of Mollusca

  1965cited by this paper
• Sedimentary Belts in Lagoon of Kapingamarangi Atoll

  1959cited by this paper
• The Origin of Species by means of Natural Selection; or the Preservation of Favoured Races in the Struggle for Life

  1872cited by this paper

• Analysis of a human-mediated microbioinvasion: the global spread of the benthic foraminifer Trochammina hadai Uchio, 1962

  2025cites this paper
• The influence of biogenic habitat created by the non-indigenous bryozoan, Amathia verticillata, on the resident marine invertebrate community in San Diego, California

  2025cites this paper
• Virgulinella fragilis in the North Adriatic Coastal Sediments: A New Non-Indigenous Benthic Foraminiferal Taxon?

  2025cites this paper
• How Did It Get Here? First Record of Trochamminita ⁠irregularis, a Cosmopolitan Estuarine Organic-Cemented Agglutinated Foraminifer, in South-West Western Australia

  2025cites this paper
• The spread of non-native species.

  2025cites this paper
• Palaeontological signatures of the Anthropocene are distinct from those of previous epochs

  2024cites this paper
• From ctenophores to scyphozoans: parasitic spillover of a burrowing sea anemone

  2024cites this paper
• Why Amphistegina lobifera, a tropical benthic foraminiferal species, is thriving at temperate latitudes in the Mediterranean Sea

  2024cites this paper
• Eocene sediments and a fresh to brackish water biota from the early rifting stage of the Upper Rhine Graben (west of oil field Landau, southwest Germany): implications for biostratigraphy, palaeoecology and source rock potential

  2023cites this paper
• Tracing the introduction of Dictyota acutiloba (Dictyotales, Phaeophyceae) in the Mediterranean Sea, with a reassessment of its geographic distribution

  2023cites this paper
• A synthesis of biological invasion hypotheses associated with the introduction–naturalisation–invasion continuum

  2023cites this paper
• The invasive Asian benthic foraminifera Trochammina hadai Uchio, 1962: identification of a new local in Normandy (France) and a discussion on its putative introduction pathways

  2023cites this paper
• Invasion success of a Lessepsian symbiont-bearing foraminifera linked to high dispersal ability, preadaptation and suppression of sexual reproduction

  2023cites this paper
• Ecological impacts of invasive ecosystem engineers: A global perspective across terrestrial and aquatic systems

  2023cites this paper
• Recent shallow water foraminifera from the Selvagens Islands (Northeast Atlantic) – Assemblage composition and biogeographic significance

  2022cites this paper
• Siganus luridus (dusky spinefoot)

  2022cites this paper
• Shift and homogenization of gut microbiome during invasion in marine fishes

  2022cites this paper
• Siganus rivulatus (marbled spinefoot)

  2022cites this paper
• Alleged Lessepsian foraminifera prove native and suggest Pleistocene range expansions into the Mediterranean Sea

  2022cites this paper
• Living and dead foraminiferal assemblage from the supratidal sand Japsand, North Frisian Wadden Sea: distributional patterns and controlling factors

  2021cites this paper
• Numerous new records of tropical non-indigenous species in the Eastern Mediterranean highlight the challenges of their recognition and identification

  2021cites this paper
• Benthic foraminifera from the Southeastern Mediterranean shelf: Dead assemblages and living-dead comparisons recording consequences of Nile River damming

  2021cites this paper
• Reconstructing Bioinvasion Dynamics Through Micropaleontologic Analysis Highlights the Role of Temperature Change as a Driver of Alien Foraminifera Invasion

  2021cites this paper
• Going with the flow: Experimental simulation of sediment transport from a foraminifera perspective

  2021cites this paper
• Checklist, assemblage composition, and biogeographic assessment of Recent benthic foraminifera (Protista, Rhizaria) from São Vincente, Cape Verdes.

  2020cites this paper
• Ocean warming and tropical invaders erode the performance of a key herbivore.

  2020cites this paper
• Alien and cryptogenic Foraminifera in the Mediterranean Sea: A revision of taxa as part of the EU 2020 Marine Strategy Framework Directive

  2020cites this paper
• High productivity of Peneroplis (Foraminifera) including aberrant morphotypes, in an inland thalassic salt pond at Lake Macleod, Western Australia

  2020cites this paper
• Modeling the effects of brine outflow from desalination plants on coastal food-webs of the Levantine basin (eastern Mediterranean Sea)

  2020cites this paper
• Endozoochory by parrotfish replenishes reefs with coral-associated microbiome

  2020cites this paper
• Effect of different derivatization protocols on the calculation of trophic position using amino acids compound-specific stable isotopes

  2020cites this paper
• Review Toxicological risks on the human health of populations living around the Mediterranean Sea linked to the invasion of non-indigenous marine species from the Red Sea.

  2020cites this paper
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  2019cites this paper
• Primera presencia y distribución de las especies exóticas Parasorites orbitoloides (Hofker, 1930) y Euthymonacha polita (Chapman, 1900): efectos sobre la comunidad de macroforaminíferos bentónicos del Mediterráneo Occidental

  2019cites this paper
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  2019cites this paper
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  2019cites this paper
• Effects of sampling site, season, and substrate on foraminiferal assemblages grown from propagule banks from lagoon sediments of Corfu Island (Greece, Ionian Sea)

  2019cites this paper
• “Hidden invaders” conquer the Sicily Channel and knock on the door of the Western Mediterranean sea

  2019cites this paper
• Recent saltmarsh foraminiferal assemblages from Iceland

  2018cites this paper
• Deep cleaning of alien and cryptogenic species records in the Greek Seas (2018 update)

  2018cites this paper
• Patterns of species richness and the center of diversity in modern Indo-Pacific larger foraminifera

  2018cites this paper
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  2017cites this paper