Disease ecology of Hematodinium perezi in a high salinity estuary: investigating seasonal trends in environmental detection

Abstract

The blue crab Callinectes sapidus has seen a general decline in population levels. One factor influencing mortality is infections by Hematodinium perezi, a dinoflagellate parasite. A 2 yr study was conducted in 2014 and 2015 to monitor H. perezi DNA within the Maryland (USA) coastal bays, comparing seasonal cycles in the abundance of parasite DNA in environmental samples to parasite presence in host blue crabs. A late summer to early fall peak in H. perezi infections in blue crabs was observed, consistent with previous work. Infection intensities matched this trend, showing a slow progression of low intensity infections early in the year, with a peak in moderate and heavy infections occurring between July and September, for both years. It was hypo thesized that the peak in water column occurrence would coincide with those months when infection intensities were highest in blue crabs. As the peaks in water column occurrence were in July 2014 and August−September 2015, this is consistent with sporulation being the primary contributor to environmental detection in summer months. An additional peak in environmental detection occurred in both years during the early spring months, the cause of which is currently unknown but may be related to infections in overwintering crabs or alternate hosts. Several new crusta cean hosts were identified within this estuary, including grass shrimp Palaemonetes spp. and the sand shrimp Crangon septemspinosa, as well as the mud crab Dyspanopeus sayi. Improved knowledge of this disease system will allow for better management of this important fishery. KEY WORDS: Blue crab · Crustacean · Environment · DNA · quantitative PCR · qPCR Resale or republication not permitted without written consent of the publisherDis Aquat Org 124: [169][170][171][172][173][174][175][176][177][178][179] 2017 Epizootic events where infection prevalence reached 100% have been observed in the field, after which infections disappeared from the crab popu lation presumably due to high mortality (Messick 1994).Along the Maryland coastline, there are several oceanic bays where summer mortality events have been attributed to infections by H. perezi. For the purpose of this study, these bays are denoted as a unified system known as the Maryland coastal bays (MCB), which includes Isle of Wight, Assawoman, Sinepuxent, and Chincoteague bays, though a portion of Chincoteague Bay is in Virginia. Seasonal cycles of infection in this system suggest higher rates of infection when water temperatures are at their highest or beginning to cool from their summer peak (Messick 1994, Messick et al. 1999, Messick & Shields 2000.Although the exact mechanism of disease transmission is still unknown, there have been reports of sporulation events, where heavily infected hosts release dinospores into the water column (Shields & Squyars 2000). Despite this known connection to environmental release, limited work has investigated the hypothesis that sporulation in highly infected blue crabs leads to greater detection in the water ...

Differential host mortality explains the effect of high temperature on the prevalence of a marine pathogen

“…Prevalence is generally highest during the fall or early winter when water temperatures are relatively low, and may decline in late winter when temperatures are lowest [ 14 , 15 , 24 ]. Prevalence increases in spring as water temperatures rise, but later declines in summer when temperatures are highest [ 14 , 24 ], although this pattern is not always followed [ 27 ]. Prior to the results of that study [ 27 ], it has been suggested that extreme temperatures could inhibit either transmission or establishment of infection, with optimum temperatures for the pathogen in the moderate range of 15 to 18°C [ 14 , 24 ].…”

Parasitic dinoflagellate Hematodinium perezi prevalence in larval and juvenile blue crabs Callinectes sapidus from coastal bays of Virginia

“…In that study, active infections were observed in all months, and they rapidly developed into highintensity infections when held at 15°C. It is therefore likely that early benthic juveniles respond in a similar manner, and thus likely explains the bimodal peaks in prevalence observed in larger juveniles and adults, and the detection of H. perezi in environmental samples (Pitula et al 2012, Hanif et al 2013, Lycett & Pitula 2017.…”

The relationship of blue crab (Callinectes sapidus) size class and molt stage to disease acquisition and intensity of Hematodinium perezi infections

“…Blue crabs were collected in conjunction with the Maryland Department of Natural Resources Finfish Investigation Surveys. These surveys are performed at 20 sites throughout the Maryland Coastal Bays (MCBs) from April through October (2014–2016) using an otter trawl as discussed previously in detail [ 14 , 19 ]. Sampling typically began during the second week of the month and took place over the course of three non-consecutive days.…”

“…The mechanism for disease transmission is unknown, though a waterborne infective dinoflagellate stage is currently favored [ 7 – 10 ]. The peak of disease manifestation varies from host to host, and even between geographic locations within the same host species [ 1 , 11 – 19 ]. Infection prevalence by season is suggested to be related to various environmental factors such as the salinity, temperature, pH, dissolved oxygen, and chlorophyll a levels in water [ 19 – 23 ].…”

“…The peak of disease manifestation varies from host to host, and even between geographic locations within the same host species [ 1 , 11 – 19 ]. Infection prevalence by season is suggested to be related to various environmental factors such as the salinity, temperature, pH, dissolved oxygen, and chlorophyll a levels in water [ 19 – 23 ]. Physiological conditions, principally the molt cycle of host crustaceans, have also been implicated in disease cycles [ 14 , 15 , 24 ].…”