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, 10 (6), e0128674
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Assessing the Effects of Trematode Infection on Invasive Green Crabs in Eastern North America

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Assessing the Effects of Trematode Infection on Invasive Green Crabs in Eastern North America

April M H Blakeslee et al. PLoS One.

Abstract

A common signature of marine invasions worldwide is a significant loss of parasites (= parasite escape) in non-native host populations, which may confer a release from some of the harmful effects of parasitism (e.g., castration, energy extraction, immune activation, behavioral manipulation) and possibly enhance the success of non-indigenous species. In eastern North America, the notorious invader Carcinus maenas (European green crab) has escaped more than two-thirds its native parasite load. However, one of its parasites, a trematode (Microphallus similis), can be highly prevalent in the non-native region; yet little is known about its potential impacts. We employed a series of laboratory experiments to determine whether and how M. similis infection intensity influences C. maenas, focusing on physiological assays of body mass index, energy storage, and immune activation, as well as behavioral analyses of foraging, shelter utilization, and conspicuousness. We found little evidence for enduring physiological or behavioral impacts four weeks after experimental infection, with the exception of mussel handling time which positively correlated with cyst intensity. However, we did find evidence for a short-term effect of M. similis infection during early stages of infection (soon after cercarial penetration) via a significant drop in circulating immune cells, and a significant increase in the crabs' righting response time. Considering M. similis is the only common parasite infecting C. maenas in eastern North America, our results for minimal lasting effects of the trematode on the crab's physiology and behavior may help explain the crab's continued prominence as a strong predator and competitor in the region.

Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1. Life cycle of Microphallus similis in eastern North America with Carcinus maenas as second-intermediate host.
Microphallus similis infects multiple hosts to complete its life cycle, starting with (A) two species of Littorina snails (L. saxatilis and L. obtusata), where the trematode asexually reproduces, producing numerous cercariae. (B) These cercariae are shed from the snail into the water column, where they seek out and encyst as a metacercariae within a second-intermediate host, primarily the green crab, Carcinus maenas. To sexually reproduce, (C) the trematode’s crab host must be ingested by a definitive host, often a Larus gull species, where (D) the trematode’s eggs, containing miracidia, are then deposited into the marine environment with the birds’ feces. Grazing snails accidentally ingest these eggs, and the cycle continues.
Fig 2
Fig 2. Average (± SE) infection intensity of metacercarial cysts in hepatopancreas, gonad, and thoracic ganglion tissues in each treatment and naturally at Appledore Island, ME and metacercarial cyst intensity per gram hepatopancreas tissue by crab carapace width (mm).
(a) Differences in capitalized letters above the bars indicate a significant difference in infection intensity (p<0.05) of counted cysts. Numbers above the control bars indicate the average infection intensities per control (all less than 1). LOW (24) and CONT (24) refer to the 24 hour infection treatment and its associated control; MED (72) and CONT (72) refer to the 72 hour infection treatment and its associated control; HIGH (120) and CONT (120) refer to the 120 hour infection treatment and its associated control; ‘LARUS’ refers to naturally infected crabs collected at Larus Ledge in 2007 and 2012 on Appledore Island, Isles of Shoals, ME. (b) There is a significant exponential relationship between crab size (CW) and cyst intensity per gram hepatopancreas.
Fig 3
Fig 3. Average (± SE) righting response time (seconds) for uninfected and infected crabs from the 72h (medium) treatment.
This demonstrates the average time it took for crabs to right themselves after being placed on their dorsal side. These trials took place two hours after the 72h induction experiment ended, shortly after cercarial penetration of crab tissues.
Fig 4
Fig 4. Regression of mussel handling time by metacercarial cyst intensity.
Metacercarial infection intensity represents actual counts. The regression remains significant with (R2 = 0.238; p<0.001) or without (R2 = 0.123; p = 0.005) the crab with 6500 cysts.
Fig 5
Fig 5. Hepatosomatic index (HSI) and gonadosomatic index (GSI) analyses by cyst intensity (estimated metacercarial abundance).
Panel ‘a’ represents HSI for all crabs combined; ‘b’ represents GSI for all crabs combined; ‘c’ represents GSI for females only; ‘d’ represents GSI for males only. Cyst intensity for HSI is lower bound estimated hepatopancreas metacercarial cyst abundance, and cyst intensity for GSI is lower bound estimated gonad metacercarial cyst abundance.
Fig 6
Fig 6. Average (± SE) hemocyte counts in crabs 72 hours after exposure and after the four week incubation period.
The grey bar is the control and the black bar is the experimental treatment showing circulating hemocytes per μL hemolymph from blood drawn for exposed and control crabs for two exposure periods. *refers to a significant difference (p<0.05) between the treatments.

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Grant support

This work was supported by a Research Opportunity Award to AMHB and BDG as a supplemental to BDG’s National Science Foundation award (NSF #OCE-1129166). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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