Ontogenetic and spatial variability in parasite communities of white shrimp Penaeus setiferus (Decapoda: Penaeidae)

Abstract

Understanding the combined effects of multi-parasite infections on their hosts is necessary for documenting parasite impacts and is particularly important for developing effective management strategies for economically important organisms. The white shrimp Penaeus setiferus supports important recreational and commercial fisheries along the southeastern and Gulf coasts of the United States and occupies an important ecological niche in estuarine and offshore habitats throughout these regions. The goal of this study was to identify and assess ontogenetic and spatial variation in white shrimp parasite communities and their relation to shrimp health. We used a series of trawl surveys in tidal creek and open water habitats of an estuary in the southeastern USA to collect and identify parasites of white shrimp using morphological and DNA sequencing techniques. Parasite communities in white shrimp were composed of organisms belonging to 6 classes: Conoidasida (gregarines), Oligohymenophorea (apostome and sessilid ciliates), Microsporea (meiodihaplophasids), Chromadorea (rhabditids), Cestoda (cyclophyllideans, lecanocephalideans and trypanorhynchs) and Trematoda (plagiorchiids). Parasite communities differed significantly among white shrimp life stages and localities. Furthermore, the health condition known as black gill occurred in some shrimp and was significantly related to parasite community structure. Infection metrics for the apostome ciliate Hyalophysa lynni, the trypanorhynch larvae Prochristianella sp. and the rhabditid larvae Hysterothylacium sp. were significantly different between shrimp exhibiting and not exhibiting black gill. These results highlight the importance of understanding parasite communities and the potential interactive effects of multiple parasite infections on shrimp health.

Keywords: Apostomatida; Rhabditida; Trypanorhyncha; parasite interactions; shrimp health; shrimp life history.

Graphical abstract

Fig. 1.

Map of sampling localities in the greater Charleston Harbor, South Carolina, USA: Wando River, Ashley River and Charleston Harbor. Credit: Gary Sundin, South Carolina Department of Natural Resources (SCDNR).

Fig. 2.

Parasites of the white shrimp, Penaeus setiferus observed in the Charleston Harbor watershed, South Carolina, USA. (A) Excysted metacercaria of the plagiorchiid Opecoeloides fimbriatus, scale bar 150 μm. (B) Juvenile of the rhabditid Hysterothylacium reliquens, scale bar 200 μm. (C) Microsporidian meiodihaplophasid Agmasoma penaei, scale bar 25 μm. (D) Sessilid Zoothamnium sp., scale bar 75 μm. (E) Cyclophyllidean Parorchites zederi, scale bar 85 μm. (F) Lecanicephalidean Polypocephalus sp., scale bar 75 μm. (G) Scolex of plerocercus of the trypanorhynch Prochristianella sp., scale bar 100 μm. (H) Gregarine gametocysts, scale bar 100 μm. (I) Apostome Hyalophysa lynni, scale bar 40 μm.

Fig. 3.

Non-metric multi-dimensional scaling (NMDS) plot of white shrimp infected with parasites in the greater Charleston Harbor watershed, South Carolina, USA (stress = 0.11). Data are presented by collection localities: Ashley River (filled black circles), Wando River (open circles) and Charleston Harbor (filled grey circles). Vectors represent significant (P ⩽ 0.01) factors related to community structure; taxa names (e.g. Sessilid) highlight locations in ordinal space most associated with those taxa. Dashed ovals represent data ellipses for parasite communities from each locality.

Fig. 4.

Black gill score related to apostome ciliate Hyalophysa lynni abundance for individual white shrimp (filled grey circles) and mean abundances (filled black circles ± s.e.; n = 306). Segmented regression showed a significant relationship between black gill score (when ⩾6) and apostome abundance on individual shrimp.

Fig. 5.

Infection metrics of parasites in white shrimp with black gill (black) and without black gill (white). Prevalence presented as (A) the percentage of shrimp infected and (B) mean intensity (±s.e.) and mean relative abundance (±s.e.) (for the apostome). Asterisks indicate significant differences between groups for prevalence (logistic regression, Table 5) and mean intensity or mean relative abundance (general linear mixed-effects model, Table 5).