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Blood meal identification reveals extremely broad host range and host-bias in a temporary ectoparasite of coral reef fishes

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Appreciation for the role of cryptofauna in ecological systems has increased dramatically over the past decade. The impacts blood-feeding arthropods, such as ticks and mosquitos, have on terrestrial communities are the subject of hundreds of papers annually. However, blood-feeding arthropods have been largely ignored in marine environments. Gnathiid isopods, often referred to as “ticks of the sea”, are temporary external parasites of fishes. They are found in all marine environments and have many consequential impacts on host fitness. Because they are highly mobile and only associated with their hosts while obtaining a blood meal, their broader trophic connections are difficult to discern. Conventional methods rely heavily on detecting gnathiids on wild-caught fishes. However, this approach typically yields few gnathiids and does not account for hosts that avoid capture. To overcome this limitation, we sequenced blood meals of free-living gnathiids collected in light traps to assess the host range and community-dependent exploitation of Caribbean gnathiid isopods. Using fish-specific COI (cox1) primers, sequencing individual blood meals from 1060 gnathiids resulted in the identification of 70 host fish species from 27 families. Comparisons of fish assemblages to blood meal identification frequencies at four collection sites indicated that fishes within the families Haemulidae (grunts) and Lutjanidae (snappers) were exploited more frequently than expected based on their biomass, and Labrid parrotfishes were exploited less frequently than expected. The broad host range along with the biased exploitation of diel-migratory species has important implications for the role gnathiid isopods play in Caribbean coral reef communities.
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Oecologia (2023) 203:349–360
https://doi.org/10.1007/s00442-023-05468-w
ORIGINAL RESEARCH
Blood meal identification reveals extremely broad host range
andhost‑bias inatemporary ectoparasite ofcoral reef fishes
GinaC.Hendrick1· MatthewD.Nicholson1· J.AndresPagan2· JohnM.Artim3· MaureenC.Dolan3,4·
PaulC.Sikkel1,5
Received: 3 January 2023 / Accepted: 13 October 2023 / Published online: 11 November 2023
© The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature 2023
Abstract
Appreciation for the role of cryptofauna in ecological systems has increased dramatically over the past decade. The impacts
blood-feeding arthropods, such as ticks and mosquitos, have on terrestrial communities are the subject of hundreds of papers
annually. However, blood-feeding arthropods have been largely ignored in marine environments. Gnathiid isopods, often
referred to as “ticks of the sea”, are temporary external parasites of fishes. They are found in all marine environments and
have many consequential impacts on host fitness. Because they are highly mobile and only associated with their hosts while
obtaining a blood meal, their broader trophic connections are difficult to discern. Conventional methods rely heavily on
detecting gnathiids on wild-caught fishes. However, this approach typically yields few gnathiids and does not account for
hosts that avoid capture. To overcome this limitation, we sequenced blood meals of free-living gnathiids collected in light
traps to assess the host range and community-dependent exploitation of Caribbean gnathiid isopods. Using fish-specific
COI (cox1) primers, sequencing individual blood meals from 1060 gnathiids resulted in the identification of 70 host fish
species from 27 families. Comparisons of fish assemblages to blood meal identification frequencies at four collection sites
indicated that fishes within the families Haemulidae (grunts) and Lutjanidae (snappers) were exploited more frequently than
expected based on their biomass, and Labrid parrotfishes were exploited less frequently than expected. The broad host range
along with the biased exploitation of diel-migratory species has important implications for the role gnathiid isopods play
in Caribbean coral reef communities.
Keywords DNA barcoding· Parasite ecology· Resource selection· Blood feeding arthropods· Marine biology·
Community composition· Host selection
Introduction
The stability and function of ecosystems is dependent upon
the myriad trophic connections that control the transfer of
energy within the system (Saint-Béat etal. 2015). Thus,
identifying trophic dynamics as revealed by food webs
is essential to the understanding of any ecosystem. His-
torically, trophic ecology has excluded cryptic organisms,
especially parasites, resulting in limited knowledge of their
role in community processes (Lafferty etal. 2008; Johnson
etal. 2010). With the rise in interest in both cryptic ecology
(Brandl etal. 2017; Pearman etal. 2018) and parasite ecol-
ogy, the impact that these organisms have on trophic struc-
ture is being rapidly unveiled (Lafferty etal. 2006; Brandl
etal. 2018, 2019; Timi and Poulin 2020).
Incorporating parasites into food web studies can be chal-
lenging due in part to the cryptic nature of most parasites,
Communicated by Joel Trexler.
* Paul C. Sikkel
pcs75@earth.miami.edu
1 Department ofMarine Biology andEcology, Rosenstiel
School ofMarine, Atmospheric andEarth Science,
University ofMiami, Miami, FL, USA
2 Centro de Investigação em Biodiversidade e Recursos
Genéticos, CIBIO – Universidade doPorto, Vairão, Portugal
3 Department ofBiological Sciences, Arkansas State
University, Jonesboro, AR, USA
4 Arkansas Biosciences Institute, Arkansas State University,
Jonesboro, AR, USA
5 Water Research Group, Unit ofEnvironmental Sciences
andManagement, North-West University, Potchefstroom,
SouthAfrica
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