Blood Meal Identification Reveals Extremely Broad Host Range and Host Bias in a Temporary Ectoparasite of Coral Reef Fishes

doi:10.21203/rs.3.rs-2440357/v1

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Blood Meal Identification Reveals Extremely Broad Host Range and Host Bias in a Temporary Ectoparasite of Coral Reef Fishes

https://doi.org/10.21203/rs.3.rs-2440357/v1

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published 11 Nov, 2023

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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 1,060 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.

DNA barcoding

Parasite ecology

Resource selection

Blood feeding arthropods

Marine biology

Community composition

Host selection

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. Historically, 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 ecology, the impact that these organisms have on trophic structure is being rapidly unveiled (Lafferty et al. 2006; Brandl et al. 2018, 2019; Timi and Poulin 2020).

Parasites can have direct and indirect effects on trophic dynamics through their effects on hosts. Directly, parasites increase energetic demands of their hosts which can lead to reduced host fitness (Holmstad et al. 2005; Hudson et al. 2006; Hatcher et al. 2012; Wood and Johnson 2015). This is partly due to the high metabolic cost associated with physiological responses to parasitism, such as mounting an immune response, replacing materials removed by the parasite, and wound repair (Zhou et al. 2020). Additionally, antiparasitic behaviors among hosts, such as avoiding certain habitats, reduced foraging, and excessive grooming, are especially costly where resources are limited (Giorgi et al. 2001; Luong et al. 2017). Indirectly, parasites can affect trophic interactions by increasing the susceptibility of hosts to predation (Ebert 2005; Johnson et al. 2010), as well as facilitating the transmission of diseases (Pingen et al. 2016).

Terrestrial hematophagous, or blood-feeding, arthropods (e.g., mosquitoes, ixodid ticks and fleas) are well-studied vectors of pathogens (McHugh 1994; Pingen et al. 2016). Mosquitoes alone are responsible for over 400,000 human deaths from malaria and dengue each year (World Health Organization 2020). Ixodid ticks transmit a variety of pathogens, including pathogenic fungi, protozoa, viruses, and bacteria (Brites-Neto et al. 2015), which are responsible for more than 15 infectious diseases (Brites-Neto et al. 2015; Esser et al. 2016; Fatmi et al. 2017; Vandegrift and Kapoor 2019). Bubonic plague, which caused more than 25 million human deaths in Medieval Europe, is perhaps the most well-known vector-borne disease (VBD) transmitted by fleas (Glatter and Finkelman 2021). Factors contributing to the emergence of VBDs include environmental conditions and the competence of both arthropod vectors and their hosts (Esser et al. 2019). Blood-feeding arthropods with low host specificity and wide host range (generalists) can have major impacts on the spread of diseases within and among communities (Wodecka and Skotarczak 2016).

Incorporating parasites into food web studies can be challenging due in part to the cryptic nature of most parasites, especially those that have complex life cycles (Lafferty et al. 2008). While many externally attaching parasites (ectoparasites) can be easily found on hosts, some are primarily free-living and feed briefly on multiple hosts (often called “micropredators” (Penfold et al. 2008)) making their trophic connections particularly difficult to interpret (Lafferty and Kuris 2002; Lafferty et al. 2008). Host range estimations often do not accurately represent natural systems due to biases in sampling methods, varying host assemblages, and differing infection probabilities among hosts (Dallas et al. 2017). Even with extensive sampling efforts, rare, cryptic and transient hosts, or hosts that are otherwise difficult to catch can be completely missed (Kent 2009). Further difficulties arise when hosts undergo ontogenetic or diel niche shifts, such as permanent habitat and dietary changes commonly seen in fishes (Kimirei et al. 2013).

Among the many parasitic arthropods infecting marine fishes, gnathiid isopods (“gnathiids”) are the only ones that specialize in feeding on blood (Smit and Davies 2004). They are among the most common ectoparasites of teleost and elasmobranch fishes and are ubiquitous in marine environments (Grutter 1994; Ferreira et al. 2009; Coile and Sikkel 2013). As such, their biomass likely exceeds that of terrestrial blood-feeding arthropods (Smit and Davies 2004; Tanaka 2007; Kirkim et al. 2011; Quattrini and Demopoulos 2016). Considering the profound effects blood-feeding arthropods have on terrestrial communities, investigating the dynamics of gnathiid-host interactions is essential to our understanding of ecological processes in marine environments.

Gnathiids can cause behavioral changes, increased mortality, and even potential infection by blood-borne pathogens among hosts (Davies 1995; Smit and Davies 2004; Raffel et al. 2008; Hayes et al. 2011; Curtis et al. 2013; Sikkel and Welicky 2019). Other, sublethal effects of gnathiid infection can include anemia (Jones and Grutter 2005), decreased cognitive function (Sellers et al. 2019), impaired movement (Allan et al. 2020), and the release of stress hormones (Triki et al. 2016; Allan et al. 2020). The severity of impact on their hosts depends on several factors, including the size of the blood meal acquired, the size of the host fish, and the intensity of infection. For example, a single gnathiid can cause mortality in small, larval fishes, whereas mortality in large hosts requires heavy infestation (Grutter et al. 2011a; Artim et al. 2015; Green et al. 2015; Sellers et al. 2019). The extent to which these effects impact host populations, and ultimately communities, depends on both the host range and selection bias of gnathiid isopods.

In ticks, the degree of host specificity can be influenced by life history stage, host phylogeny and availability, as well as geographic location (Esser et al. 2016). Host specificity in fleas generally decreases as the ecological similarities among hosts increases (Bitam et al. 2010). In mosquitoes, even species with strong host preferences exhibit plasticity in their foraging behavior in areas where preventative measures are more widely applied and preferred hosts are less accessible (Chaves et al. 2010; Takken and Verhulst 2013). In addition to behavioral defenses, hosts can develop resistance to blood feeding by arthropods, thereby reducing both future infestation (Wikel 1999) and the risk of infection by vector-borne pathogens (Wikel 2013). Whether fishes similarly develop resistance to gnathiid infection is unknown.

While gnathiids are regarded as “generalists”, susceptibility to gnathiid infection has been shown to vary among fishes in the Caribbean (Coile and Sikkel 2013; Sikkel et al. 2014; Jenkins et al. 2018), and host preferences have been suggested for some gnathiids found on the Great Barrier Reef (Jones et al. 2007; Nagel and Grutter 2007). Much of what is known about the range of hosts exploited by gnathiid isopods has resulted from examining wild-caught fish (Sikkel et al. 2006, 2009; Nagel and Grutter 2007; Farquharson et al. 2012; Coile and Sikkel 2013; Coile et al. 2014). However, these methods likely misrepresent natural patterns of host exploitation, as they rely on the opportunistic capture of potential hosts, which gnathiids can abandon when the fish is captured (Grutter 1995, 1996; Sikkel et al. 2004). Because most of the gnathiid life cycle is spent free living, this limitation can be overcome by sequencing host DNA within blood meals of wild-caught gnathiids (Nagel, L., & Lougheed 2006; Jones et al. 2007; Hendrick et al. 2019).

DNA barcoding is a valuable tool in the study of host-parasite interactions, allowing for host identification from free-living stages of hematophagous arthropods (Alcaide et al. 2009; Lassen et al. 2012; Brugman et al. 2015; Reeves et al. 2016). These methods involve the amplification of targeted genes that are highly conserved among taxa, yet are distinguishable among species (Nagel, L., & Lougheed 2006; Jones et al. 2007; Borland and Kading 2021). Blood meal sequencing has identified the hosts of many blood-feeding arthropods, including some gnathiid species found on the Great Barrier Reef (Nagel, L., & Lougheed 2006; Jones et al. 2007) and in the Caribbean (Hendrick et al. 2019; Sikkel et al. 2020). However, to our knowledge, no study has compared these data to assemblages of available host fish.

In this study, we employed a large-scale sampling effort to collect recently-fed, free-living gnathiid isopods across five sites in the eastern Caribbean. We sequenced 1,060 individual gnathiid blood meals, resulting in the most comprehensive host range assessment among marine blood-feeding arthropods to date. Our main objective was to assess the community-dependent variation in host exploitation by Caribbean gnathiid isopods. Because gnathiids are considered host generalists, we hypothesized that fishes that are both highly available and highly susceptible to infection are exploited most frequently. To test this, we calculated selection ratios of gnathiid host use to relative biomass of fishes (host availability) at collection sites.

Study species

Gnathiid isopods

Gnathiids employ feeding strategies similar to those of ticks and mosquitoes, attaching externally to a host to obtain a blood meal (Fig. 1) (Smit and Davies 2004). During each of three parasitic juvenile stages (instars), an unfed gnathiid, or zuphea (Z1 – Z3), will emerge from the benthos to feed on a single host fish. Once engorged, fed gnathiids, or pranizae (P1 – P3), detach from their host and return to the benthos. Each subsequent stage is larger than the previous, thus requiring a larger blood meal volume and more time to feed. Third stage pranizae (P3) metamorphose into free-living adults that do not feed. In tropical species, feeding typically lasts from minutes to hours and depends on the stage of the gnathiid.

The gnathiid isopod, Gnathia marleyi, is extremely abundant throughout the north-eastern Caribbean (Farquharson et al. 2012). G. marleyi is primarily active at night and exhibits a diel ontogenetic niche shift, with each juvenile stage showing marked differences in peak activity periods (Sikkel et al. 2006, 2009). While previous sampling efforts suggest that G. marleyi is the predominant species at our study sites (Farquharson et al. 2012), conventional identification methods rely heavily on morphology of adult males (Smit and Davies 2004). Recent COI (cox1) barcoding of gnathiids collected in the region suggest the possibility of additional, but rare, Gnathia species (Sikkel et al. 2020; Pagán et al. 2020).

Fishes

The majority of fishes commonly occurring at our study sites are species typically associated with coral reefs in this region (Bellwood 1996; Cowman 2014; Floeter et al. 2018) and all fishes were considered as potential hosts for gnathiids in this study. Nineteen species were identified as hosts of Gnathia marleyi through their detection on wild-caught fishes (Online Resource 1) (Sikkel et al. 2006; Farquharson et al. 2012; Coile and Sikkel 2013; Coile et al. 2014; Nicholson et al. 2020). Previously, the use of blood meal sequencing aided in the identification of an additional 17 host species, bringing the total known hosts of G. marleyi to 36 species from 14 families (Hendrick et al. 2019).

Study sites and sample collection

To assess the host range of Caribbean gnathiids, we collected free-living gnathiids from shallow reefs (depth < 10 m) and adjacent seagrass beds at five sites in the US Virgin Islands and Puerto Rico. Gnathiids used in our statistical analyses were collected from 10 plots at four sites (sites 1–4) (Online Resource 1, Fig. S1). Plots (10 m by 20 m) were divided into 66 evenly spaced grid points. Grid point numbers were randomly selected and sampled once. The number of traps deployed per night ranged from 10–20, with a total of 40–50 traps per plot deployed within 7 days. Specimens and survey data were collected between May and August of 2015 and 2016.

Gnathiids were collected using lighted plankton traps following the protocol of Artim and Sikkel (2016). Briefly, light traps were deployed before dusk and retrieved at dawn the following morning. Each trap was filtered immediately upon retrieval. Plankton samples were sorted under a stereomicroscope to remove the visibly fed (pranizae) juveniles. These gnathiids were immediately preserved in 100% molecular grade ethanol and stored at ≤ -20°C. All samples were shipped to the Arkansas Biosciences Institute (Arkansas State University, Jonesboro, AR), where they were kept at -80°C.

Within-plot host abundance and biomass

Prior to deploying plankton traps within plots, daytime point surveys were conducted at each trap location. Nighttime point surveys were conducted within 24 h of plankton trap retrieval and never occurred while traps were deployed. For all point surveys, all fishes within a 1.5 m radius of each trap location were recorded. Fish biomass was estimated for each species at sites 1–4 following methods outlined by Artim et al. (2020).

Because genetic distances of the COI gene can be as high as 19% within families of coral reef fishes (Shan et al. 2021), comparisons between host biomass and sequencing results were made at the family level. This was also done to avoid discrepancies between field- and molecular-based identification of hybrid fishes (Bhattacharya et al. 2016), such as those commonly seen in the genus Hypoplectrus (Serranidae).

Fishes within Labridae, Pomacentridae, and Serranidae were grouped as follows: Pomacentridae was split into groups of shoaling (e.g., Abudefduf spp. and Chromis spp.) versus territorial species (e.g., Microspathodon sp. and Stegastes spp.); the genus Hypoplectrus was considered separately from all other fishes within Serranidae; and parrotfishes (formerly Scaridae) were considered separately from all other species within Labridae.

DNA extraction and sequencing

DNA was extracted from 1,060 individual, fed gnathiids using the PureLink® Genomic DNA extraction kit (Invitrogen, Carlsbad, CA), following the manufacturer’s ‘Mammalian Tissue and Mouse/Rat Tail Lysate’ protocol. Prior to DNA extraction, whole gnathiids were quickly rinsed with dH₂O and blotted dry with a Kimwipe™ (Kimberly-Clark, Roswell, GA) then immediately transferred to a sterile 1.5 mL tube containing extraction buffer. Purified DNA was eluted using 50 µL dH₂O. Purified DNA was concentrated from 50 µL to 15 µL using the ThermoSavant ISS110 SpeedVac® System (Thermo Fisher Scientific, Wilmington, DE).

PCR reactions were carried out following the protocol outlined by Hendrick et al. (2019). Briefly, host DNA was amplified using diagnostic primers of the mitochondrial gene cytochrome c oxidase subunit 1 (cox1, COI, or MT-CO1) (5’-TCAACYAATCAYAAAGATATYGGCAC-3’; 5’ACTTCYGGGTGRCCRAARAATCA-3’). PCR reactions (20 µL) included 10 µL of concentrated template DNA and 10 µL of master mix solution containing forward and reverse COI primers, 1.25 units GoTaq Hot Start Polymerase, 1x buffer with 1.5 mM MgCl2 (Promega, Madison, WI), and 0.2 mM dNTP Mix (Thermo Fisher Scientific, Wilmington, DE). A Veriti 96 Well Thermal Cycler (Applied Biosystem, Foster City, CA) was used to carry out PCR reactions with the following thermocycling conditions: initial denaturation step of 94°C for 2 min, 30 cycles of 96°C for 20 s, 55°C for 20 s, and 72°C for 45 s, and a final extension step of 72°C for 7 min.

ExoSAP-IT (Applied Biosystem, Foster City, CA) was used for enzymatic digestion of excess PCR reagents prior to Sanger sequencing.

All samples were sent to the University of Chicago Comprehensive Cancer Center, DNA Sequencing & Genotyping Facility for sequencing. DNA from the tissue of a previously confirmed species was used as a positive control for both PCR and DNA sequencing. For samples that did not result in successful host identification after one PCR reaction, a second PCR was performed using 10 µL of PCR product from the initial PCR reaction as template DNA. PCR products of select samples were visualized on a 1.5% agarose 1X TBE (89 mM Tris, 89 mM boric acid, 2 mM EDTA, pH 8.6) gel, using a DNA low mass ladder (Invitrogen, Cat no. 10068-013) and visualized using ethidium bromide staining to confirm target COI amplicons of expected size (540–600 bp).

Host identification

DNA sequences and chromatograms for each gnathiid blood meal were edited as necessary using Geneious R10 (Biomatters Limited, Auckland, New Zealand). DNA sequences were identified using the Basic Local Alignment Search Tool (BLAST) on the National Center for Biotechnology Information (NCBI) website and further confirmed using the Barcode of Life Data Systems (BOLD) website. Sequence similarity of ≥ 98% was considered species-level identification. For sequence similarity < 98%, host families were identified using neighbor joining trees of the BLAST results as outlined by Jones et al. (2007).

Comparison of host assemblages

All statistical analyses were conducted using RStudio 2022.07.1 + 554 (R Core Team, 2022) and the vegan (Oksanen et al. 2022), ade4 (Dray and Dufour 2007), and adehabitatHS (Calenge 2006) packages. At sites 1–4, we compared three types of host assemblages: 1) host families identified by blood meal sequencing (“ID”); 2) fish families recorded during day surveys (“Day”); and 3) fish families recorded during night surveys (“Night”). The dissimilarity of host assemblage composition among sites was evaluated using non-metric multidimensional scaling (NMDS) based on Bray-Curtis distances. NMDS was also used to compare within-site dissimilarities among the three host assemblage types (ID, Day, Night). The stress-value and Shepard stress plot were used to assess the goodness of fit of the NMDS analysis. A permutational multivariate analysis of variance (PERMANOVA) was used to validate the significance of NMDS-calculated variation in the composition of host groups. An ANOVA was performed to test whether variation among host group composition was due to significant beta-dispersion.

Gnathiid host selection

Resource selection ratios (w) were used to measure host selection by gnathiids collected within surveyed plots at sites 1–4 (n = 358). Manly selectivity measures were calculated using the function “widesI” for design I data, based on the formula:

$${w}_{i}=\frac{relative use for host family i}{relative availability for host family i}=\frac{{o}_{i}}{{\pi }_{i}}$$

For the purposes of this study, “use" by gnathiids was defined as the frequency of blood meal identifications for each host family. For each host family, “relative use” equals the ratio of use to the total number of hosts identified at each site. Biomass was used as an index for host “availability” to account for variations in size and rarity among host families (e.g., larger transient fishes versus smaller resident fishes) to avoid false indications of selectivity (Kent 2009). Fish families frequently seen in areas adjacent to our plots (e.g., sand patches and seagrass beds), rare fishes not present at the time of surveys, and highly abundant, cryptic fishes were excluded from selectivity analyses to avoid errors resulting from underrepresented availability. Data were grouped by site to account for potential gnathiid transport between plots by hosts with larger home ranges. Selection ratios were calculated separately for day and night availability. Hosts families with significant selectivity measures were then compared to levels of host susceptibility previously reported by Coile and Sikkel (2013).

DNA sequencing and host identification

Of the 1,060 blood meals processed, 75% (n = 796) were used to find sequence homologies using the Basic Local Alignment Search Tool (BLAST). Species-level identification was achieved for 452 sequences resulting in the identification of 70 fish-host species (Table 1). When combined with results from neighbor joining trees for sequence similarity of < 98%, family-level identification was achieved for 653 sequences with results from 27 fish families. Of the fish families present at all sites, only two lacked representation by our sequencing results: Aulostomidae and Chaetodontidae. Among the sequences indicating invertebrate homologies (n = 111), gnathiid isopods were the closest match to 100 of these. The remaining 11 invertebrate homologies had a percent identity ranging from 79–86%. Two of these samples likely originated from polychaete worms in the family Syllidae (Annelida, Polychaeta), but the remaining 9 samples most closely matched to terrestrial organisms not likely to serve as hosts for gnathiids. Another 31 samples matched bacteria, which may be indicative of sample decomposition. The remaining 25% of samples resulted in failed or low-quality sequencing reactions.

Due to the combination of rarity and low sequencing success for both first- and second stage gnathiids, we did not separate sequencing results by larval stage during our statistical analyses. Therefore, we were unable to assess whether ontogenetic dietary shifts occur during the life cycle of Gnathia marleyi. The results presented here are thus predominantly from third stage juveniles. Similarly, we have previously shown that G. marleyi can successfully feed on soft-bodied invertebrates (Shodipo et al. 2019; Nicholson et al. 2019), and although sequencing results for two blood meals suggest polychaete worm origin, their use was likely an artifact of co-occurrence with unfed gnathiids in light traps. Thus, invertebrate homologies were excluded from our statistical analyses.

Host assemblage comparisons

Non-metric multidimensional scaling (NMDS) analysis in k = 3 dimensions resulted in a stress value of 0.048, indicating an excellent representation of the observed dissimilarity among all host assemblages across sites 1–4 (n = 499), based on reference levels outline by Clarke (Clarke 1993). The relationship between calculated ordination distances and observed dissimilarity among host groups was visualized using a Shepard stress plot (stress value = 0.059) (Fig. 2).

Host assemblage dissimilarities were visualized using an ordination plot grouped by both site and host group type (Fig. 3). A PERMANOVA of the NMDS centroid distances revealed no significant variation in the overall composition of hosts across sites (P = 0.65), as shown by the overlapping polygons in Fig. 3a. A PERMANOVA of the centroid distances among host group types (Fig. 3b) revealed significant differences across all sites (P = 0.001). Beta-dispersion among sites and host group types did not contribute to the significant differences among centroid distances (P = 0.103 and P = 0.437, respectively).

Host selection ratios

Hosts with significant Manly selectivity measures are listed in Table 2. At all sites, fishes from either Haemulidae or Lutjanidae were exploited disproportionately more often than expected based on their availability (relative biomass). Labrid parrotfishes were consistently exploited less than their relative availability at all sites, except when compared to night availability at Culebra. Labrid wrasses and Sphyraenidae were “avoided” at site 3 (Culebra). When compared to night availability only, Holocentridae use was low at sites 1–3, and Serranidae use was low at sites 3 and 4. Calculating separate selectivity measures for diurnal and nocturnal fishes had little influence on the results indicating high use by gnathiids. However, more families were identified as “low-use” when compared to night availability than when compared to day availability.

Theory on niche breadth evolution suggest that diverse host populations lead to broad host ranges in parasites (Gibson et al. 2020). Accordingly, and given that coral reefs are biodiversity hotspots (Reaka-Kudla 1997; Knowlton et al. 2010), our results reveal an unprecedented host range for gnathiid isopods.. In total, we identified 70 species from 27 families, bringing the host range of Caribbean gnathiid isopods to at least 83 species from 31 families. This includes several cryptic (e.g., Gobiidae and Labrisomidae) and uncommon (e.g., Albulidae, Centropomidae and Echeneidae) species that were not recorded in our surveys. No cartilaginous fishes were identified in this study, which is surprising as some Pacific gnathiids are known to feed on elasmobranchs (sharks, skates, and rays) (Heupel and Bennett 1999; McKiernan et al. 2005). Given the extremely broad host range reported here and the impact of gnathiids on hosts, especially those in early life history stages, our findings have several major ecological implications: 1) gnathiids at our study sites are less sensitive to biodiversity loss; 2) the ecological connectivity of hosts can further contribute to variations in gnathiid abundance within and among neighboring habitats; and 3) gnathiids may have a significant role in disease transmission cycles.

Habitat degradation typically selects for a generalist lifestyle (Stuart-Smith et al. 2021). Accordingly, our previous studies in the Caribbean and elsewhere have shown an inverse relationship between gnathiid abundance and live coral cover (Santos and Sikkel 2019; Artim et al. 2020; Paula et al. 2021). Because the gnathiids at our study sites temporarily associate with hosts and can infect such a wide range of taxa, they likely resist negative impacts from losses in host biodiversity such as secondary extinctions, and thus may increase food web robustness (Lafferty and Kuris 2009; Chen et al. 2011). Numerous host traits (e.g. behavioral and physiological defense mechanisms, physical condition (Fenton et al. 2015), home range, and seasonal availability) contribute to variation in host associations among, and even within, potential host species (Kent 2009; Bakhoum et al. 2016). Several studies by our team have shown the ability of each juvenile stage to successfully feed from multiple host families with varying degrees of susceptibility, all of which are present in our sequencing results. These include Acanthuridae, Haemulidae, Holocentridae, Labridae, Lutjanidae, Pomacentridae, and Serranidae (Sikkel et al. 2006, 2009). Thus, each juvenile stage likely has similar responses to fluctuations in host biodiversity.

The similarity in host assemblages across our study sites allowed us to detect broad patterns of host utilization. Most of the observed hosts were exploited by gnathiids at levels proportional to their availability. However, selectivity measures revealed consistent high use of haemulid grunts and lutjanid snappers, which have been shown to have the highest susceptibility to infection by Gnathia marleyi (Coile and Sikkel 2013). In contrast, another nocturnal group, holocentrid squirrelfishes, are both less susceptible and less exploited than expected. While these fish remain on the reef at night where gnathiids are most abundant, they also eat gnathiids (Artim et al. 2017), which may contribute to their relatively low level of exploitation. Lower than expected exploitation was also seen for fishes within Labridae. Despite having higher availability than even some high-use hosts (e.g., lutjanid snappers), parrotfishes remained low-use at all sites. Some parrotfishes envelop themselves in a mucous cocoon at night, which has been shown experimentally to deter gnathiids (Grutter et al. 2011b). Thus, our findings support the hypothesis that at least one function of these cocoons is prevention of gnathiid infestation (Grutter et al. 2011b). Similarly, labrid wrasses are known to bury themselves in the sand at night, which, in addition to reducing exposure to predators (Nemtzov 1994; Tatom-Naecker and Westneat 2018), may provide protection from gnathiid infection.

While some hosts employ behaviors that effectively prevent gnathiid infection, in doing so they may facilitate infection among other host populations. A significant proportion of the fishes migrating from mangrove and reef to seagrass habitats at night consists of haemulid grunts and lutjanid snappers (Clark et al. 2009). By leaving the reef at night to feed (Nagelkerken et al. 2000; Clark et al. 2009), these fishes not only avoid areas where gnathiid density is highest, but they also avoid peak activity periods of gnathiids (Sikkel et al. 2006). While their exposure to gnathiids is reduced (Sikkel et al. 2017), our findings here indicate that it is not eliminated, and that the most susceptible species are also the most exploited. Areas where aggregations of grunts and snappers reside during the day may become gnathiid "hotspots", such that when they are absent during nightly migrations, gnathiids that fed on them previously will emerge from the benthos to feed on the next available hosts. Alternatively, grunts and snappers may transport gnathiids to neighboring habitats. Non-resident, transient fishes are also major contributors to trophic flow through habitats within their home ranges (Clark et al. 2009). Multiple sequences from gnathiids collected in areas surrounding our reef plots matched to fishes with high connectivity, such as jacks (Carangidae). A recent study measuring the connectivity of permit, Trachinotus falcatus, found the average distance between mark and recapture sites to be 16.8 km, with some individuals traveling over 30 km (Boucek et al. 2022). Although gene flow among populations of Gnathia marleyi is estimated to occur within 40 km, this distance increased to over 250 km following a major hurricane (Pagán et al. 2020). A possible explanation for this is passive transport by transient host fishes escaping storms (Pagán et al. 2022).

Transport of terrestrial arthropod parasites by their hosts is known to facilitate the transmission of diseases among host populations (Hasle 2013; Kilpatrick et al. 2014). For example, the prevalence of Lyme disease in humans is positively correlated with the density of local deer populations (Kilpatrick et al. 2014). The poleward migration of hosts due to climate change has even led to the introduction of vector-borne diseases into naïve habitats (Caminade et al. 2019; Esser et al. 2019). Gnathiids have been implicated as vectors of haemogregarine-like parasites, and the majority of families infected by Caribbean gnathiids have at least one species known to carry blood parasites (Cook et al. 2015). However, gnathiids are limited in the number of hosts they can exploit by the number of feeding juvenile stages during their life cycle (Smit and Davies 2004), which may impact their ability to transmit pathogens. If gnathiids are preferentially selecting for competent hosts, disease transmission may be amplified. Earlier studies revealed high infection rates of an undescribed blood parasite within populations of yellowtail snapper, Ocyurus chrysurus (Lutjanidae), in the eastern Caribbean (Cook et al. 2015). This is interesting considering they are both highly susceptible and highly exploited hosts of gnathiid isopods.

Trophic selectivity for high quality resources is predicted to increase in environments with high abundance of heterogeneous resources (Francois et al. 2020). Although what constitutes a high-quality host for gnathiids is largely unknown, we have shown trophic selectivity for grunts and snappers, female gnathiids produce larger offspring than those that fed on hosts with lower susceptibility (Coile et al. 2014). In future studies, host traits that affect both the feeding success by gnathiids and the establishment of subsequent infections by pathogens must be investigated. The high diversity of blood parasites infecting numerous Caribbean coral reef fishes (Cook et al. 2015; Sikkel et al. 2020), the variety of fish pathogens previously detected within larval stages of gnathiid isopods, and the host breadth reported here suggest potential major implications for epidemiological cycles in coral reef ecosystems. Due to the ecological and socio-economic importance of many reef fishes, including lutjanid snappers, elucidating the role of gnathiids as vectors of disease requires further attention.

Acknowledgements We thank E. Brill, K. Driskill, A. McCammon, S. Robles, A. Savage, T. Santos, J. Sellers, B. Velez, and O. Rullan, and A. Hook for their assistance during field work. We also thank E. Babcock for insightful discussions regarding statistical analyses. We thank the staff of the MacLean Marine Science Center of University of the Virgin Islands, Arkansas State University, Arkansas Biosciences Institute, and the University of Puerto Rico. Funding was generously provided by U.S. National Science Foundation grant OCE-1536794 (PC Sikkel, PI).

Funding Funding was provided by U.S. National Science Foundation grant OCE-1536794 (PC Sikkel, PI).

Conflict of interest The authors declare that they have no conflict of interest.

Ethics approval All applicable institutional and/or national guidelines for the care and use of animals were followed.

Consent to participate Not applicable

Consent for publication Not applicable

Data availability These data were contributed to the Biological & Chemical Oceanography Data Management Office (BCO-DMO) database under the project title “Beyond Cleaning Symbiosis: Ecology of ‘Ticks of the Sea’ on Coral Reefs” (https://www.bco-dmo.org/project/562115).

Code availability Not applicable

Authors’ contributions GCH, JDA, MCD, and PCS conceived and designed the idea. GCH, MDN, JDA, and PCS developed field methodologies. GCH and MCD developed molecular methods. GCH, MDN, JAP, and JDA conducted fieldwork. GCH performed laboratory work, data analysis, and wrote the manuscript. MDN, JAP, JDA, MCD, and PSC provided editorial advice.

Alcaide M, Rico C, Ruiz S, Soriguer R, Muñoz J, Figuerola J (2009) Disentangling Vector-Borne Transmission Networks: A Universal DNA Barcoding Method to Identify Vertebrate Hosts from Arthropod Bloodmeals. PLoS One 4:e7092 doi: 10.1371/journal.pone.0007092
Allan BJM, Illing B, Fakan EP, Narvaez P, Grutter AS, Sikkel PC, McClure EC, Rummer JL, McCormick MI (2020) Parasite infection directly impacts escape response and stress levels in fish. J Exp Biol 223:doi: 10.1242/jeb.230904
Artim JM, Hook A, Grippo RS, Sikkel PC (2017) Predation on parasitic gnathiid isopods on coral reefs: a comparison of Caribbean cleaning gobies with non-cleaning microcarnivores. Coral Reefs 36:1213–1223 doi: 10.1007/s00338-017-1613-6
Artim JM, Nicholson MD, Hendrick GC, Brandt M, Smith TB, Sikkel PC (2020) Abundance of a cryptic generalist parasite reflects degradation of an ecosystem. Ecosphere 11:1–8 doi: 10.1002/ecs2.3268
Artim JM, Sellers JC, Sikkel PC (2015) Micropredation by gnathiid isopods on settlement-stage reef fish in the eastern Caribbean Sea. Bull Mar Sci 91:479–487 doi: 10.5343/bms.2015.1023
Artim JM, Sikkel PC (2016) Comparison of sampling methodologies and estimation of population parameters for a temporary fish ectoparasite. Int J Parasitol Parasites Wildl 5:145–157 doi: 10.1016/j.ijppaw.2016.05.003
Bakhoum MT, Fall M, Seck MT, Gardès L, Fall AG, Diop M, Mall I, Balenghien T, Baldet T, Gimonneau G, Garros C, Bouyer J (2016) Foraging range of arthropods with veterinary interest: New insights for Afrotropical Culicoides biting midges (Diptera: Ceratopogonidae) using the ring method. Acta Trop 157:59–67 doi: 10.1016/j.actatropica.2016.01.023
Bellwood DR (1996) The Eocene fishes of Monte Bolca: the earliest coral reef fish assemblage. Coral Reefs 15:11–19 doi: 10.1007/s003380050025
Bhattacharya M, Sharma AR, Patra BC, Sharma G, Seo EM, Nam JS, Chakraborty C, Lee SS (2016) DNA barcoding to fishes: Current status and future directions. Mitochondrial DNA 27:2744–2752 doi: 10.3109/19401736.2015.1046175
Bitam I, Dittmar K, Parola P, Whiting MF, Raoult D (2010) Fleas and flea-borne diseases. Int J Infect Dis 14:e667–e676 doi: 10.1016/j.ijid.2009.11.011
Borland EM, Kading RC (2021) Modernizing the Toolkit for Arthropod Bloodmeal Identification. Insects 12:37 doi: 10.3390/insects12010037
Boucek RE, Ellis RD, Forauer AR, Adams AJ (2022) A decade-long connectivity study of Permit (Trachinotus falcatus) in Florida supports a spatial management approach. Environ Biol Fishes. doi: 10.1007/s10641-022-01302-z
Brandl SJ, Casey JM, Knowlton N, Duffy JE (2017) Marine dock pilings foster diverse, native cryptobenthic fish assemblages across bioregions. Ecol Evol 7:7069–7079 doi: 10.1002/ece3.3288
Brandl SJ, Goatley CHR, Bellwood DR, Tornabene L (2018) The hidden half: ecology and evolution of cryptobenthic fishes on coral reefs. Biol Rev 93:1846–1873 doi: 10.1111/brv.12423
Brandl SJ, Tornabene L, Goatley CHR, Casey JM, Morais RA, Côté IM, Baldwin CC, Parravicini V, Schiettekatte NMD, Bellwood DR (2019) Demographic dynamics of the smallest marine vertebrates fuel coral reef ecosystem functioning. Science 364:1189–1192 doi: 10.1126/science.aav3384
Brites-Neto J, Duarte KMR, Martins TF (2015) Tick-borne infections in human and animal population worldwide. Vet World 8:301–315 doi: 10.14202/vetworld.2015.301-315
Brugman VA, Hernández-Triana LM, Prosser SWJ, Weland C, Westcott DG, Fooks AR, Johnson N (2015) Molecular species identification, host preference and detection of myxoma virus in the Anopheles maculipennis complex (Diptera: Culicidae) in southern England, UK. Parasit Vectors 8:421 doi: 10.1186/s13071-015-1034-8
Calenge C (2006) The package “adehabitat” for the R software: A tool for the analysis of space and habitat use by animals. Ecol Modell 197:516–519 doi: 10.1016/j.ecolmodel.2006.03.017
Caminade C, McIntyre KM, Jones AE (2019) Impact of recent and future climate change on vector-borne diseases. Ann N Y Acad Sci 1436:157–173 doi: 10.1111/nyas.13950
Chaves LF, Harrington LC, Keogh CL, Nguyen AM, Kitron UD (2010) Blood feeding patterns of mosquitoes: random or structured? Front Zool 7:3 doi: 10.1186/1742-9994-7-3
Chen HW, Shao KT, Liu CWJ, Lin WH, Liu WC (2011) The reduction of food web robustness by parasitism: Fact and artefact. Int J Parasitol 41:627–634 doi: 10.1016/j.ijpara.2010.12.013
Clark RD, Pittman S, Caldow C, Christensen J, Roque B, Appeldoorn RS, Monaco ME (2009) Nocturnal fish movement and trophic flow across habitat boundaries in a coral reef ecosystem (SW Puerto Rico). Caribb J Sci 45:282–303 doi: 10.18475/cjos.v45i2.a15
Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Austral Ecol 18:117–143 doi: 10.1111/j.1442-9993.1993.tb00438.x
Coile AM, Sikkel PC (2013) An experimental field test of susceptibility to ectoparasitic gnathiid isopods among Caribbean reef fishes. Parasitology 140:888–896 doi: 10.1017/S0031182013000097
Coile AM, Welicky RL, Sikkel PC (2014) Female Gnathia marleyi (Isopoda: Gnathiidae) feeding on more susceptible fish hosts produce larger but not more offspring. Parasitol Res 113:3875–3880 doi: 10.1007/s00436-014-4090-7
Cook CA, Sikkel PC, Renoux LP, Smit NJ (2015) Blood parasite biodiversity of reef-associated fishes of the eastern Caribbean. Mar Ecol Prog Ser 533:1–13 doi: 10.3354/meps11430
Cowman PF (2014) Historical factors that have shaped the evolution of tropical reef fishes: A review of phylogenies, biogeography, and remaining questions. Front Genet 5:1–15 doi: 10.3389/fgene.2014.00394
Curtis LM, Grutter AS, Smit NJ, Davies AJ (2013) Gnathia aureamaculosa, a likely definitive host of Haemogregarina balistapi and potential vector for Haemogregarina bigemina between fishes of the Great Barrier Reef, Australia. Int J Parasitol 43:361–370 doi: 10.1016/j.ijpara.2012.11.012
Dallas T, Huang S, Nunn C, Park AW, Drake JM (2017) Estimating parasite host range. Proc R Soc B Biol Sci 284:20171250 doi: 10.1098/rspb.2017.1250
Davies AJ (1995) The biology of fish haemogregarines. Adv Parasitol 36:191–201 doi: 10.1016/S0065-308X(08)60491-1
Dray S, Dufour A-B (2007) The ade4 Package: Implementing the Duality Diagram for Ecologists. J Stat Softw 22:516–519 doi: 10.18637/jss.v022.i04
Ebert D (2005) Introduction to Daphnia Biology
Esser HJ, Herre EA, Blüthgen N, Loaiza JR, Bermúdez SE, Jansen PA (2016) Host specificity in a diverse Neotropical tick community: An assessment using quantitative network analysis and host phylogeny. Parasites and Vectors 9:1–14 doi: 10.1186/s13071-016-1655-6
Esser HJ, Mögling R, Cleton NB, Van Der Jeugd H, Sprong H, Stroo A, Koopmans MPG, De Boer WF, Reusken CBEM (2019) Risk factors associated with sustained circulation of six zoonotic arboviruses: A systematic review for selection of surveillance sites in non-endemic areas. Parasites and Vectors 12:1–17 doi: 10.1186/s13071-019-3515-7
Farquharson C, Smit NJ, Sikkel PC (2012) Gnathia marleyi sp. nov. (Crustacea, Isopoda, Gnathiidae) from the Eastern Caribbean. Zootaxa 3381:47 doi: 10.11646/zootaxa.3381.1.3
Fatmi SS, Zehra R, Carpenter DO (2017) Powassan Virus—A New Reemerging Tick-Borne Disease. Front Public Heal 5:doi: 10.3389/fpubh.2017.00342
Fenton A, Streicker DG, Petchey OL, Pedersen AB (2015) Are all hosts created equal? Partitioning host species contributions to parasite persistence in multihost communities. Am Nat 186:610–622 doi: 10.1086/683173
Ferreira ML, Smit NJ, Grutter AS, Davies AJ (2009) A New Species of Gnathiid (Crustacea: Isopoda) Parasitizing Teleosts from Lizard Island, Great Barrier Reef, Australia. J Parasitol 95:1066–1075 doi: 10.1645/GE-1920.1
Floeter SR, Bender MG, Siqueira AC, Cowman PF (2018) Phylogenetic perspectives on reef fish functional traits. Biol Rev 93:131–151 doi: 10.1111/brv.12336
Francois CM, Simon L, Malard F, Lefébure T, Douady CJ, Mermillod-Blondin F (2020) Trophic selectivity in aquatic isopods increases with the availability of resources. Funct Ecol 34:1078–1090 doi: 10.1111/1365-2435.13530
Gibson AK, Baffoe-Bonnie H, Penley MJ, Lin J, Owens R, Khalid A, Morran LT, Baffoe‐Bonnie H, Penley MJ, Lin J, Owens R, Khalid A, Morran LT (2020) The evolution of parasite host range in heterogeneous host populations. J Evol Biol 33:773–782 doi: 10.1111/jeb.13608
Giorgi MS, Arlettaz R, Christe P, Vogel P (2001) The energetic grooming costs imposed by a parasitic mite (Spinturnix myoti) upon its bat host (Myotis myotis). Proc R Soc London Ser B Biol Sci 268:2071–2075 doi: 10.1098/rspb.2001.1686
Glatter KA, Finkelman P (2021) History of the Plague: An Ancient Pandemic for the Age of COVID-19. Am J Med 134:176–181 doi: 10.1016/j.amjmed.2020.08.019
Green AL, Maypa AP, Almany GR, Rhodes KL, Weeks R, Abesamis RA, Gleason MG, Mumby PJ, White AT (2015) Larval dispersal and movement patterns of coral reef fishes, and implications for marine reserve network design. Biol Rev 90:1215–1247 doi: 10.1111/brv.12155
Grutter A (1996) Parasite removal rates by the cleaner wrasse Labroides dimidiatus. Mar Ecol Prog Ser 130:61–70 doi: 10.3354/meps130061
Grutter AS (1994) Spatial and temporal variations of the ectoparasites of seven reef fish species from Lizard Island and Heron Island, Australia. Mar Ecol Prog Ser 115:21–30 doi: 10.3354/meps115021
Grutter AS (1995) Relationship between cleaning rates and ectoparasite loads in coral reef fishes. Mar Ecol Prog Ser 118:51–58 doi: 10.3354/meps118051
Grutter AS, Crean AJ, Curtis LM, Kuris AM, Warner RR, Mccormick MI (2011a) Indirect effects of an ectoparasite reduce successful establishment of a damselfish at settlement. Funct Ecol 25:586–594 doi: 10.1111/j.1365-2435.2010.01798.x
Grutter AS, Rumney JG, Sinclair-Taylor T, Waldie P, Franklin CE (2011b) Fish mucous cocoons: The “mosquito nets” of the sea. Biol Lett 7:292–294 doi: 10.1098/rsbl.2010.0916
Hasle G (2013) Transport of ixodid ticks and tick-borne pathogens by migratory birds. Front Cell Infect Microbiol 4:1–6 doi: 10.3389/fcimb.2013.00048
Hatcher MJ, Dick JT, Dunn AM (2012) Diverse effects of parasites in ecosystems: linking interdependent processes. Front Ecol Environ 10:186–194 doi: 10.1890/110016
Hayes PM, Smit NJ, Grutter AS, Davies AJ (2011) Unexpected response of a captive blackeye thicklip, Hemigymnus melapterus (Bloch), from Lizard Island, Australia, exposed to juvenile isopods Gnathia aureamaculosa Ferreira & Smit. J Fish Dis 34:563–566 doi: 10.1111/j.1365-2761.2011.01261.x
Hendrick GC, Dolan MC, McKay T, Sikkel PC (2019) Host DNA integrity within blood meals of hematophagous larval gnathiid isopods (Crustacea, Isopoda, Gnathiidae). Parasit Vectors 12:316 doi: 10.1186/s13071-019-3567-8
Heupel MR, Bennett MB (1999) The occurrence, distribution and pathology associated with gnathiid isopod larvae infecting the epaulette shark, Hemiscyllium ocellatum. Int J Parasitol 29:321–330 doi: 10.1016/S0020-7519(98)00218-5
Holmstad PR, Hudson PJ, Skorping A (2005) The Influence of a Parasite Community on the Dynamics of a Host Population: A Longitudinal Study on Willow Ptarmigan and Their Parasites. Oikos 111:377–391
Hudson PJ, Dobson AP, Lafferty KD (2006) Is a healthy ecosystem one that is rich in parasites? Trends Ecol Evol 21:381–385 doi: 10.1016/j.tree.2006.04.007
Jenkins WG, Demopoulos AWJ, Sikkel PC (2018) Effects of host injury on susceptibility of marine reef fishes to ectoparasitic gnathiid isopods. Symbiosis 75:113–121 doi: 10.1007/s13199-017-0518-z
Johnson PTJ, Dobson A, Lafferty KD, Marcogliese DJ, Memmott J, Orlofske SA, Poulin R, Thieltges DW (2010) When parasites become prey: Ecological and epidemiological significance of eating parasites. Trends Ecol Evol 25:362–371 doi: 10.1016/j.tree.2010.01.005
Jones CM, Grutter AS (2005) Parasitic isopods (Gnathia sp.) reduce haematocrit in captive blackeye thicklip (Labridae) on the Great Barrier Reef. J Fish Biol 66:860–864 doi: 10.1111/j.0022-1112.2005.00640.x
Jones CM, Nagel L, Hughes GL, Cribb TH, Grutter AS (2007) Host specificity of two species of Gnathia (Isopoda) determined by DNA sequencing blood meals. Int J Parasitol 37:927–935 doi: 10.1016/j.ijpara.2007.01.011
Kent RJ (2009) Molecular methods for arthropod bloodmeal identification and applications to ecological and vector-borne disease studies. Mol Ecol Resour 9:4–18 doi: 10.1111/j.1755-0998.2008.02469.x
Kilpatrick HJ, Labonte AM, Stafford KC (2014) The relationship between deer density, tick abundance, and human cases of lyme disease in a residential community. J Med Entomol 51:777–784 doi: 10.1603/ME13232
Kimirei IA, Nagelkerken I, Trommelen M, Blankers P, van Hoytema N, Hoeijmakers D, Huijbers CM, Mgaya YD, Rypel AL (2013) What Drives Ontogenetic Niche Shifts of Fishes in Coral Reef Ecosystems? Ecosystems 16:783–796 doi: 10.1007/s10021-013-9645-4
Kirkim F, Gozler AM, Kopuz U, Agirbas E (2011) New Records of Two Species of Gnathiid Isopods,Paragnathia Formica (Hesse, 1864) and Gnathia Maxillaris (Montagu, 1804) (Isopoda, Gnathiidae) from the Black Sea. Crustaceana 84:1719–1725 doi: 10.1163/156854011X607088
Knowlton N, Brainard RE, Fisher R, Moews M, Plaisance L, Caley MJ (2010) Coral Reef Biodiversity. Life World’s Ocean Divers Distrib Abundance 65–77
Lafferty KD, Allesina S, Arim M, Briggs CJ, De Leo G, Dobson AP, Dunne JA, Johnson PTJ, Kuris AM, Marcogliese DJ, Martinez ND, Memmott J, Marquet PA, McLaughlin JP, Mordecai EA, Pascual M, Poulin R, Thieltges DW (2008) Parasites in food webs: The ultimate missing links. Ecol Lett 11:533–546 doi: 10.1111/j.1461-0248.2008.01174.x
Lafferty KD, Dobson AP, Kuris AM (2006) Parasites dominate food web links. Proc Natl Acad Sci U S A 103:11211–11216 doi: 10.1073/pnas.0604755103
Lafferty KD, Kuris AM (2002) Trophic strategies, animal diversity and body size. Trends Ecol Evol 17:507–513 doi: 10.1016/S0169-5347(02)02615-0
Lafferty KD, Kuris AM (2009) Parasites reduce food web robustness because they are sensitive to secondary extinction as illustrated by an invasive estuarine snail. Philos Trans R Soc B Biol Sci 364:1659–1663 doi: 10.1098/rstb.2008.0220
Lassen SB, Nielsen SA, Kristensen M (2012) Identity and diversity of blood meal hosts of biting midges (Diptera: Ceratopogonidae: Culicoides Latreille) in Denmark. Parasites and Vectors 5:1–10 doi: 10.1186/1756-3305-5-143
Luong LT, Horn CJ, Brophy T (2017) Mitey costly: Energetic costs of parasite avoidance and infection. Physiol Biochem Zool 90:471–477 doi: 10.1086/691704
McHugh CP (1994) Arthropods: Vectors of disease agents. Lab Med 25:429–437 doi: 10.1093/labmed/25.7.429
McKiernan JP, Grutter AS, Davies AJ (2005) Reproductive and feeding ecology of parasitic gnathiid isopods of epaulette sharks (Hemiscyllium ocellatum) with consideration of their role in the transmission of a haemogregarine. Int J Parasitol 35:19–27 doi: 10.1016/j.ijpara.2004.10.016
Nagel, L, & Lougheed SC (2006) A Simple Molecular Technique for Identifying Marine Host Fish by Sequencing Blood- Feeding Parasites. J Parasitol 92:665–668
Nagel L, Grutter AS (2007) Host preference and specialization in Gnathia sp., a common parasitic isopod of coral reef fishes. J Fish Biol 70:497–508 doi: 10.1111/j.1095-8649.2007.01320.x
Nagelkerken I, Dorenbosch M, Verberk W, Cocheret de la Morinière E, van der Velde G (2000) Day-night shifts of fishes between shallow-water biotopes of a Caribbean bay, with emphasis on the nocturnal feeding of Haemulidae and Lutjanidae. Mar Ecol Prog Ser 194:55–64 doi: 10.3354/meps194055
Nemtzov SC (1994) Intraspecific variation in sand-diving and predator avoidance behavior of green razorfish,Xyrichtys splendens (Pisces, Labridae): effect on courtship and mating success. Environ Biol Fishes 41:403–414 doi: 10.1007/BF02197856
Nicholson MD, Artim JD, Hendrick GC, Packard AJ, Sikkel PC (2019) Fish-Parasitic Gnathiid Isopods Metamorphose Following Invertebrate-Derived Meal. J Parasitol 105:793 doi: 10.1645/19-59
Nicholson MD, Hendrick GC, Packard AJ, Strobel DL, Vondriska C, Sikkel PC (2020) Vertical limits of host infestation by gnathiid isopods (Isopoda: Gnathiidae) parasitic on Caribbean coral reef fishes. J Crustac Biol 40:866–871 doi: 10.1093/jcbiol/ruaa067
Oksanen J, Simpson G, Blanchet F, Kindt R, Legendre P, Minchin P, O’Hara R, Solymos P, Stevens M, Szoecs E, Wagner H, Barbour M, Bedward M, Bolker B, Borcard D, Carvalho G, Chirico M, De Caceres M, Durand S, Evangelista H, FitzJohn R, Friendly M, Furneaux B, Hannigan G, Hill M, Lahti L, McGlinn D, Ouellette M, Ribeiro Cunha E, Smith T, Stier A, Ter Braak C, Weedon J (2022) Vegan: Community Ecology Package. R package version 2.6-2. https://CRAN.R-project.org/package=vegan
Pagán JA, Veríssimo A, Sikkel PC, Xavier R (2020) Hurricane-induced disturbance increases genetic diversity and population admixture of the direct-brooding isopod, Gnathia marleyi. Sci Rep 10:8649 doi: 10.1038/s41598-020-64779-7
Pagán JA, Xavier R, Sikkel PC, Veríssimo A (2022) Host-mediated dispersal shapes spatial distribution of genetic variability in marine symbionts. Bull Mar Sci 98:317–330 doi: 10.5343/bms.2021.0046
Paula JR, Sun D, Pissarra V, Narvaez P, Rosa R, Grutter AS, Sikkel PC (2021) The role of corals on the abundance of a fish ectoparasite in the Great Barrier Reef. Coral Reefs 40:535–542 doi: 10.1007/s00338-021-02051-8
Pearman JK, Leray M, Villalobos R, Machida RJ, Berumen ML, Knowlton N, Carvalho S (2018) Cross-shelf investigation of coral reef cryptic benthic organisms reveals diversity patterns of the hidden majority. Sci Rep 8:1–18 doi: 10.1038/s41598-018-26332-5
Penfold R, Grutter A, Kuris A, McCormick M, Jones C (2008) Interactions between juvenile marine fish and gnathiid isopods: predation versus micropredation. Mar Ecol Prog Ser 357:111–119 doi: 10.3354/meps07312
Pingen M, Bryden SR, Pondeville E, Schnettler E, Kohl A, Merits A, Fazakerley JK, Graham GJ, McKimmie CS (2016) Host Inflammatory Response to Mosquito Bites Enhances the Severity of Arbovirus Infection. Immunity 44:1455–1469 doi: 10.1016/j.immuni.2016.06.002
Quattrini AM, Demopoulos AWJ (2016) Ectoparasitism on deep-sea fishes in the western North Atlantic: In situ observations from ROV surveys. Int J Parasitol Parasites Wildl 5:217–228 doi: 10.1016/j.ijppaw.2016.07.004
Raffel TR, Martin LB, Rohr JR (2008) Parasites as predators: unifying natural enemy ecology. Trends Ecol Evol 23:610–618 doi: 10.1016/j.tree.2008.06.015
Reaka-Kudla ML (1997) The global biodiversity of coral reefs: a comparison with rain forests. In: Reaka-Kudla ML, Wilson DE, Wilson EO (eds) Biodiversity II: Understanding and Protecting Our Biological Resources. Joseph Henry Press, Washington, DC, pp 83 – 108
Reeves LE, Holderman CJ, Gillett-Kaufman JL, Kawahara AY, Kaufman PE (2016) Maintenance of host DNA integrity in field-preserved mosquito (Diptera: Culicidae) blood meals for identification by DNA barcoding. Parasites and Vectors 9:1–11 doi: 10.1186/s13071-016-1791-z
Saint-Béat B, Baird D, Asmus H, Asmus R, Bacher C, Pacella SR, Johnson GA, David V, Vézina AF, Niquil N (2015) Trophic networks: How do theories link ecosystem structure and functioning to stability properties? A review. Ecol Indic 52:458–471 doi: 10.1016/j.ecolind.2014.12.017
Santos TRN, Sikkel PC (2019) Habitat associations of fish-parasitic gnathiid isopods in a shallow reef system in the central Philippines. Mar Biodivers 49:83–96 doi: 10.1007/s12526-017-0756-6
Sellers JC, Holstein DM, Botha TL, Sikkel PC (2019) Lethal and sublethal impacts of a micropredator on post-settlement Caribbean reef fishes. Oecologia 189:293–305 doi: 10.1007/s00442-018-4262-8
Shan B, Liu Y, Yang C, Zhao Y, Zhang G, Wu Q, Sun D (2021) DNA Barcoding of Fish in Mischief Reef—Fish Diversity of a Reef Fish Community From Nansha Islands. Front Mar Sci 7:1–10 doi: 10.3389/fmars.2020.618954
Shodipo MO, Gomez RDC, Welicky RL, Sikkel PC (2019) Apparent kleptoparasitism in fish—parasitic gnathiid isopods. Parasitol Res 118:653–655 doi: 10.1007/s00436-018-6152-8
Sikkel PC, Cheney KL, Côté IM (2004) In situ evidence for ectoparasites as a proximate cause of cleaning interactions in reef fish. Anim Behav 68:241–247 doi: 10.1016/j.anbehav.2003.10.023
Sikkel PC, Pagan JA, Santos JL, Hendrick GC, Nicholson MD, Xavier R (2020) Molecular detection of apicomplexan blood parasites of coral reef fishes from free-living stages of ectoparasitic gnathiid isopods. Parasitol Res 119:1975–1980 doi: 10.1007/s00436-020-06676-6
Sikkel PC, Schaumburg CS, Mathenia JK (2006) Diel infestation dynamics of gnathiid isopod larvae parasitic on Caribbean reef fish. Coral Reefs 25:683–689 doi: 10.1007/s00338-006-0154-1
Sikkel PC, Tuttle LJ, Cure K, Coile AM, Hixon MA (2014) Low susceptibility of invasive red lionfish (Pterois volitans) to a generalist ectoparasite in both its introduced and native ranges. PLoS One 9:1–8 doi: 10.1371/journal.pone.0095854
Sikkel PC, Welicky RL (2019) The Ecological Significance of Parasitic Crustaceans. pp 421–477
Sikkel PC, Welicky RL, Artim JM, McCammon AM, Sellers JC, Coile AM, Jenkins WG (2017) Nocturnal migration reduces exposure to micropredation in a coral reef fsh. Bull Mar Sci 93:475–489 doi: 10.5343/bms.2016.1021
Sikkel PC, Ziemba RE, Sears WT, Wheeler JC (2009) Diel ontogenetic shift in parasitic activity in a gnathiid isopod on Caribbean coral reefs. Coral Reefs 28:489–495 doi: 10.1007/s00338-009-0474-z
Smit NJ, Davies AJ (2004) The curious life-style of the parasitic stages of gnathiid isopods. Adv Parasitol 58:289–391 doi: 10.1016/S0065-308X(04)58005-3
Stuart-Smith RD, Mellin C, Bates AE, Edgar GJ (2021) Habitat loss and range shifts contribute to ecological generalization among reef fishes. Nat Ecol Evol 5:656–662 doi: 10.1038/s41559-020-01342-7
Takken W, Verhulst NO (2013) Host Preferences of Blood-Feeding Mosquitoes. Annu Rev Entomol 58:433–453 doi: 10.1146/annurev-ento-120811-153618
Tanaka K (2007) Life history of gnathiid isopods-current knowledge and future directions. Plankt Benthos Res 2:1–11 doi: 10.3800/pbr.2.1
Tatom-Naecker TAM, Westneat MW (2018) Burrowing fishes: Kinematics, morphology and phylogeny of sand-diving wrasses (Labridae). J Fish Biol 93:860–873 doi: 10.1111/jfb.13789
Timi JT, Poulin R (2020) Why ignoring parasites in fish ecology is a mistake. Int J Parasitol 50:755–761 doi: 10.1016/j.ijpara.2020.04.007
Triki Z, Grutter AS, Bshary R, Ros AFH (2016) Effects of short-term exposure to ectoparasites on fish cortisol and hematocrit levels. Mar Biol 163:187 doi: 10.1007/s00227-016-2959-y
Vandegrift KJ, Kapoor A (2019) The ecology of new constituents of the tick virome and their relevance to public health. Viruses 11:1–13 doi: 10.3390/v11060529
Wikel S (2013) Ticks and tick-borne pathogens at the cutaneous interface: Host defenses, tick countermeasures, and a suitable environment for pathogen establishment. Front Microbiol 4:1–10 doi: 10.3389/fmicb.2013.00337
Wikel SK (1999) Tick modulation of host immunity: An important factor in pathogen transmission. Int J Parasitol 29:851–859 doi: 10.1016/S0020-7519(99)00042-9
Wodecka B, Skotarczak B (2016) Identification of host blood-meal sources and Borrelia in field-collected Ixodes ricinus ticks in north-western Poland. Ann Agric Environ Med 23:59–63 doi: 10.5604/12321966.1196853
Wood CL, Johnson PTJ (2015) A world without parasites: exploring the hidden ecology of infection. Front Ecol Environ 13:425–434 doi: 10.1890/140368
World Health Organization (2020) Vector-borne diseases. https://www.who.int/news-room/fact-sheets/detail/vector-borne-diseases
Zhou W, Tahir F, Wang JCY, Woodson M, Sherman MB, Karim S, Neelakanta G, Sultana H (2020) Discovery of Exosomes From Tick Saliva and Salivary Glands Reveals Therapeutic Roles for CXCL12 and IL-8 in Wound Healing at the Tick–Human Skin Interface. Front Cell Dev Biol 8:1–22 doi: 10.3389/fcell.2020.00554

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03 Jan, 2023

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Blood Meal Identification Reveals Extremely Broad Host Range and Host Bias in a Temporary Ectoparasite of Coral Reef Fishes

Status:

Journal Publication

Version 1

Abstract

Figures

Introduction

Methods

Study species

Gnathiid isopods

Fishes

Study sites and sample collection

Within-plot host abundance and biomass

DNA extraction and sequencing

Host identification

Comparison of host assemblages

Gnathiid host selection

Results

DNA sequencing and host identification

Host assemblage comparisons

Host selection ratios

Discussion

Declarations

References

Tables

Supplementary Files

Status:

Journal Publication

Version 1