Estimating the magnitude and sensitivity of energy fluxes for stickleback hosts and Schistocephalus solidus parasites using the metabolic theory of ecology.

Parasites are ubiquitous, yet their effects on hosts are difficult to quantify and generalize across ecosystems. One promising metric of parasitic impact uses the metabolic theory of ecology (MTE) to calculate energy flux, an estimate of energy lost to parasites. We investigated the feasibility of using metabolic scaling rules to compare the energetic burden of parasitism among individuals. Specifically, we found substantial sensitivity of energy flux estimates to input parameters used in the MTE equation when using available data from a model host-parasite system (Gasterosteus aculeatus and Schistocephalus solidus). Using literature values, size data from parasitized wild fish, and a respirometry experiment, we estimate that a single S. solidus tapeworm may extract up to 32% of its stickleback host's baseline metabolic energy requirement, and that parasites in multiple infections may collectively extract up to 46%. The amount of energy siphoned from stickleback to tapeworms is large but did not instigate an increase in respiration rate in the current study. This emphasizes the importance of future work focusing on how parasites influence ecosystem energetics. The approach of using the MTE to calculate energy flux provides great promise as a quantitative foundation for such estimates and provides a more concrete metric of parasite impact on hosts than parasite abundance alone.

Long-term ecological research in freshwaters enabled by regional biodiversity collections, stable isotope analysis, and environmental informatics.

Biodiversity collections are experiencing a renaissance fueled by the intersection of informatics, emerging technologies, and the extended use and interpretation of specimens and archived databases. In this article, we explore the potential for transformative research in ecology integrating biodiversity collections, stable isotope analysis (SIA), and environmental informatics. Like genomic DNA, SIA provides a common currency interpreted in the context of biogeochemical principles. Integration of SIA data across collections allows for evaluation of long-term ecological change at local to continental scales. Challenges including the analysis of sparse samples, a lack of information about baseline isotopic composition, and the effects of preservation remain, but none of these challenges is insurmountable. The proposed research framework interfaces with existing databases and observatories to provide benchmarks for retrospective studies and ecological forecasting. Collections and SIA add historical context to fundamental questions in freshwater ecological research, reference points for ecosystem monitoring, and a means of quantitative assessment for ecosystem restoration.

A reconstruction of parasite burden reveals one century of climate-associated parasite decline.

Long-term data allow ecologists to assess trajectories of population abundance. Without this context, it is impossible to know whether a taxon is thriving or declining to extinction. For parasites of wildlife, there are few long-term data-a gap that creates an impediment to managing parasite biodiversity and infectious threats in a changing world. We produced a century-scale time series of metazoan parasite abundance and used it to test whether parasitism is changing in Puget Sound, United States, and, if so, why. We performed parasitological dissection of fluid-preserved specimens held in natural history collections for eight fish species collected between 1880 and 2019. We found that parasite taxa using three or more obligately required host species-a group that comprised 52% of the parasite taxa we detected-declined in abundance at a rate of 10.9% per decade, whereas no change in abundance was detected for parasites using one or two obligately required host species. We tested several potential mechanisms for the decline in 3+-host parasites and found that parasite abundance was negatively correlated with sea surface temperature, diminishing at a rate of 38% for every 1 °C increase. Although the temperature effect was strong, it did not explain all variability in parasite burden, suggesting that other factors may also have contributed to the long-term declines we observed. These data document one century of climate-associated parasite decline in Puget Sound-a massive loss of biodiversity, undetected until now.

STABLE ISOTOPE SIGNATURES OF AN ACANTHOCEPHALAN AND TREMATODE FROM THE HERBIVOROUS MARINE FISH KYPHOSUS BIGIBBUS (PERCIFORMES: KYPHOSIDAE).

Stable isotope analyses of carbon and nitrogen (δ13C and δ15N) are useful for elucidating consumer relationships of free-living organisms, as carbon isotopes indicate dietary carbon sources and incremental increases in nitrogen isotopic enrichment are correlated with increases in trophic position. However, host-parasite relationships are more difficult to interpret using isotopes, as data from different host-parasite systems rarely show any consistent pattern. This inconsistency of pattern reflects the complexity of host-parasite relationships, but also the scarcity of data from a diverse assemblage of host-parasite systems. We present stable isotope data from a host-parasite system including 2 ecologically contrasting helminths, an acanthocephalan (Filisoma filiformis) and a digenetic trematode (Enenterum sp.), which co-occur in the intestine of the same marine fish (Kyphosus bigibbus), the diet of which consists almost exclusively of macroalgae. We obtained δ13C and δ15N data from K. bigibbus muscle, stomach contents, and pooled infrapopulations of Enenterum sp. and F. filiformis. Consistent with other isotope studies including acanthocephalans, F. filiformis was depleted in δ13C and δ15N relative to K. bigibbus. Although Enenterum sp. exhibited values for δ13C similar to those for F. filiformis, they were enriched in δ15N relative to the acanthocephalan, with a signature similar to that of K. bigibbus. These findings are discussed within a host-ecosystem context, highlighting the importance of considering species-specific biology when interpreting host-parasite relationships using stable isotopes. Our study adds to the growing body of literature indicating that absorptive feeders, such as acanthocephalans, are typically depleted in δ13C and δ15N relative to their hosts, whereas trematodes, with a greater diversity of feeding opportunities, exhibit a wide variety of isotopic signatures across life stage and different host-parasite systems.

Fluid-preserved fishes are one solution for assessing historical change in fish trophic level.

There are few resources available for assessing historical change in fish trophic dynamics, but specimens held in natural history collections could serve as this resource. In contemporary trophic ecology studies, trophic and source information can be obtained from compound-specific stable isotope analysis of amino acids of nitrogen (CSIA-AA-N).We subjected whole Sebastes ruberrimus and Clupea pallasii to formalin fixation and 70% ethanol preservation. We extracted tissue samples from each fish pre-fixation, after each chemical change, and then in doubling time for 32-64 days once placed in the final preservative. All samples were subjected to CSIA-AA-N, and their glutamic acid and phenylalanine profiles and associated trophic position were examined for differences over time by species.Glutamic acid and phenylalanine values were inconsistent in direction and magnitude, particularly during formalin fixation, but stabilized similarly (in 70% ethanol) among conspecifics. In some cases, the amino acid values of our final samples were significantly different than our initial pre-preservation samples. Nonetheless, significant differences in glutamic acid, phenylalanine, and estimated trophic position were not detected among samples that were in 70% ethanol for >24 hr.Our results suggest that the relative trophic position of fluid-preserved specimens can be estimated using CSIA-AA-N, and CSIA-AA-N estimates for fluid-preserved specimens should only be reported as relative differences. Timelines of trophic position change can be developed by comparing specimens collected at different points in time, revealing trophic information of the past and cryptic ecosystem responses.

Hooked on you: shape of attachment structures in cymothoid isopods reflects parasitic strategy.

BACKGROUND: Parasite attachment structures are critical traits that influence effective host exploitation and survival. Morphology of attachment structures can reinforce host specificity and niche specialisation, or even enable host switching. Therefore, it is important to understand the determinants of variation in attachment structures. Cymothoid isopods are striking ectoparasites of fishes that include the infamous 'tongue-biters.' They are known to parasitise hosts in one of four qualitatively distinct anatomical regions. Here, we quantify variation in cymothoid attachment structures - hook-like appendages called dactyli - and test whether differences in dactylus shape are correlated with parasite mode (where they attach), allometry, or both, using multivariate ordinary least squares regression. We also assess the influence of shared ancestry on shape using a molecular phylogeny to weight our models using phylogenetic generalised least squares regression. RESULTS: We find clear differences in shape between externally-attaching and internally-attaching cymothoids but also between anterior and posterior dactyli across various species with the same attachment mode. Allometric effects are significant for anterior but not posterior dactyli. Mouth-attaching species show greater shape variability than gill- and mouth-attaching species. We find no evidence that there are clade-specific patterns of association between parasite mode and dactylus shape. CONCLUSIONS: Parasite mode appears to be the main driver of attachment morphology. This likely reflects several components of parasite ecology including feeding and functional demands of attachment in different microhabitats. Geometric morphometric approaches to the quantification of shape variation of simple structures is an effective tool that provides new insights into the evolvability of parasite attachment.

A new genus and species of fish parasitic cymothoid (Crustacea, Isopoda) from the Indian Ocean coast of South Africa, with a key to the externally attaching genera of Cymothoidae.

Bambalocra intwala gen. et sp. nov. is described from Sodwana Bay, north-eastern South Africa. The monotypic genus is characterised by the broadly truncate anterior margin of the head with a ventral rostrum, coxae 2-5 being ventral in position not forming part of the body outline and not or barely visible in dorsal view, and the posterolateral margins of pereonites 6 and 7 are posteriorly produced and broadly rounded. The antennulae bases are widely separated, with both antennula and antenna slender. The species is known only from the type locality and the known hosts are species of Pomacanthidae (Angelfish). A revised key to the externally attaching genera of Cymothoidae is provided.

Redescription and molecular characterisation of the fish ectoparasite Anilocra capensis Leach, 1818 (Isopoda: Cymothoidae), with description of six new species of Anilocra Leach, 1818 from Africa.

BACKGROUND: Anilocra capensis Leach, 1818 is the only named species of Anilocra Leach, 1818 from South Africa. Anilocra is a large genus (> 40 species) with high levels of diversity reported from the Caribbean and Indo-West Pacific. Considering it is highly unlikely that all records of Anilocra from South Africa can be of a single species, the aim of this study was to better understand the diversity of Anilocra from this region and continent. METHODS: To redescribe A. capensis, the syntypes of A. capensis and specimens recorded as A. capensis from Africa were borrowed from the Natural History Museum, London, UK, and The iZiko South African Museum, Cape Town. Newly collected fresh samples of A. capensis were collected from off Cape Town, South Africa. Morphological redescriptions of the syntypes, and other museum and fresh material were conducted. Fresh samples were used to characterise molecularly A. capensis using the mitochondrial cytochrome c oxidase subunit 1 gene (cox1). RESULTS: Morphological analyses demonstrated that apart from A. capensis there are six Anilocra species new to science from Africa: Anilocra ianhudsoni n. sp., Anilocra bunkleywilliamsae n. sp., Anilocra paulsikkeli n. sp., Anilocra jovanasi n. sp., Anilocra angeladaviesae n. sp. and Anilocra hadfieldae n. sp. Of the species under study, specimens of A. capensis appear to demonstrate the most individual variation, which occurs in pleonite width, pleotelson form and uropod length. We determined that African species of Anilocra can be primarily differentiated by the proportional shape and size of the full body in dorsal view and pereonites 1, 6 and 7. Other defining morphological traits include proportional shape and size of the pereopods, and the antenna and antennula peduncles. Lastly, the molecular characterisation of A. capensis is provided and the interspecific divergence with Mediterranean species is smaller than that with Caribbean species. CONCLUSIONS: The results of this study provide a detailed redescription of A. capensis and the first molecular barcode for this organism. Six new species of Anilocra from Africa are described, establishing that the diversity of Anilocra in this region is greater than previously known. With this new understanding of species differences, we can accurately conduct detailed molecular and ecological analyses of Anilocra from Africa with certainty of the organism under study.

Understanding growth relationships of African cymothoid fish parasitic isopods using specimens from museum and field collections.

Cymothoid isopods are a diverse group of ectoparasites of fish species, and are particularly conspicuous as they are large and attach to the body surface, mouth, and gill chamber of fish hosts. These parasites transition from juvenile to male to female, and how their size changes with ontogeny and correlates with host size is not well understood. To better understand these relationships, data from field and museum collected samples of South Africa were combined to test for the associations between host and parasite length for three mouth and one gill chamber-infesting genera (Ceratothoa, Cinusa, Cymothoa, and Mothocya respectively). Generally, the number of parasites collected from 90 h of museum surveying was similar to that of seven, one-week long field collections. For two of the three mouth-infesting parasites, parasite and host size were significantly and positively correlated for males and females, but not juveniles. For gill chamber-infesting parasites, female and male parasite sizes were weakly and not significantly correlated with host size. These results provide the first morphometric data and growth relationship data for African cymothoid species and their fish hosts, and demonstrate the value and efficiency of using museum collections in ecological research.

Apparent kleptoparasitism in fish-parasitic gnathiid isopods.

Gnathiid isopods are common external parasites/micropredators that feed on the blood of marine fishes. During the course of processing samples of gnathiid isopods collected from light traps in the central Philippines, we observed a gnathiid attached to and apparently feeding from the abdomen of another gnathiid. Because the abdomens of both gnathiids were enlarged, it was unclear whether one actually fed on the blood meal of the other. Introduction of unfed gnathiids with fed gnathiids revealed that one gnathiid could and did feed on the blood meal of another. This is the first observation of apparent conspecific kleptoparasitism reported for gnathiid isopods.

Molecular assessment of three species of Anilocra (Isopoda, Cymothoidae) ectoparasites from Caribbean coral reef fishes, with the description of Anilocra brillae sp. n.

A morphological review and molecular characterization of Anilocra haemuli Bunkley Williams & Williams, 1981, were completed using specimens collected from Haemulon flavolineatum Desmarest, 1823 (French grunt) and Epinephelus guttatus Linnaeus, 1758 (red hind). Molecular and morphological data suggest that the isopods parasitizing H. flavolineatum and E. guttatus are different species. The specimens collected from E. guttatus are recognized as a new species, Anilocra brillaesp. n. Differences between Anilocra brillaesp. n. and A. haemuli include but are not limited to the pleonites 1-3 of A. brillaesp. n. being wider than 4-5 and 4-5 subequal, whereas the pleonites 1-2 of A. haemuli are wider than 3-5, and 3-5 are subequal. The seventh pereopod of A. brillaesp. n. is proportionally larger, has more robust setae, and the setae are distributed more extensively over the articles when compared to A. haemuli. Additionally, this study provides the first genetic characterization of three Anilocra spp. from the Caribbean, and is based on mitochondrial cytochrome c oxidase subunit gene (COI) for A. haemuli from H. flavolineatum, A. brillaesp. n. from E. guttatus, and A. chromis Bunkley Williams & Williams, 1981 from Chromis multilineata Guichenot, 1853.

Drought-associated absence of alien invasive anchorworm, Lernaea cyprinacea (Copepoda: Lernaeidae), is related to changes in fish health.

Recently, Mozambique tilapia (Oreochromis mossambicus Peters, 1852) were listed on the IUCN Red List as near-threatened as their populations are at risk due to hybridization. Another factor that potentially contributes to their population decline is that they are regularly infected by the invasive parasitic copepod anchorworm, Lernaea cyprinacea Linnaeus, 1758. Considering anchorworm-infected Mozambique tilapia are common, understanding their condition with respect to infection is difficult as uninfected fish from the same localities have been unavailable for comparison. A severe drought in southern Africa has created hypersaline environments in the Phongolo River floodplain of north-eastern South Africa, such that freshwater parasites cannot survive and uninfected fish are now found. To determine how infection influences host health, infected and uninfected Mozambique tilapia were collected before and during drought conditions, from Nyamiti pan of the Phongolo River floodplain. Anchorworm-infected fish prevalence was recorded, and anchorworms were collected from hosts and identified to the species level using molecular data of the 18S rRNA gene. For each fish, intensity of anchorworm infection, total length, and weights of the gutted body, liver, spleen, and gonads were recorded. Gutted condition factor, hepato-, spleeno-, and gonado-somatic index values per fish, and prevalence of infection per collection were determined. A rapid health assessment was also conducted to determine a health score for each fish. Molecular analyses confirmed the anchorworm studied was L. cyprinacea. Prior to and during drought, prevalence of infection was 100%, and 0%, respectively. Before drought, fish had significantly reduced hepato-, spleeno-, and gonado-somatic index values, and higher health assessment scores, yet significantly higher gutted condition. Anchorworm intensity was indirectly correlated with fish liver and gonad condition. This study demonstrates that host condition and health varies greatly with respect to drought and infection, and provides the necessary data for follow-up studies in post-drought conditions.