“Rising temperatures, molting phenology and epizootic shell disease in the American lobster”

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Maya L. Groner, Jeffrey D. Shields, Donald F. Landers Jr., John T. Swenarton, and John M. Hoenig (Nov 2018)

The DOI will be https://dx.doi.org/10.1086/699478

Rising temperatures cause phenological mismatch between molting and epizootic shell disease in the American lobster

American lobsters (Homarus americanus) caught in Long Island Sound. Pitting and erosion on the carapace of the lobster on the left is indicative of epizootic shell disease. The presence of white barnacles indicates that this lobster has not molted recently. An orange tag, used for mark-recapture, is visible on the lobster on the healthier lobster, on the right.
(Credit: John Swenarton)

Changing environmental conditions can alter the timing of key events during a species’ lifetime. In some cases this can cause a mismatch between an event and critical environmental or biological conditions. This ‘phenological mismatch’ has been investigated in a variety of scenarios such as the timing of breeding and migration with food availability and predation risk. However, it has not been well examined in the context of disease risk.

In this paper, the authors’ investigated how changing seawater temperature is altering responses to an emerging disease of the American lobster, epizootic shell disease (ESD). Using a 34-year mark-recapture dataset from Long Island Sound, CT, the authors investigated relationships between seawater temperature, molting phenology, and seasonal variation of epizootic shell disease (ESD). ESD is an emerging disease of lobsters caused by a suite of bacteria on the lobster cuticle that feed upon materials in the shell. Molting can be beneficial for diseased lobsters because it allows them to discard their diseased shell.

The authors’ analyses support the hypothesis that phenological mismatch is linked to seasonal variation in ESD. They found that warmer spring temperatures were associated with earlier spring molting. This increased the length of the intermolt period in the summer, when disease transmission is highest. For juvenile and adult male lobsters, earlier molting was associated with a greater proportion of diseased lobsters in September; however, in October, the proportion of diseased lobsters was most strongly associated with warmer summer seawater temperature. This suggests that spring temperatures affect the timing of the onset of disease by altering molting patterns, but, over time, this signal is swamped by the stronger signal of summer temperatures. October ESD prevalence was ~80% in years with hot summers, and ~30% in years with cooler summers. Population impacts of ESD are expected to increase with increasing seawater temperatures.


Abstract

Phenological mismatch, maladaptive changes in phenology resulting from altered timing of environmental cues, is an increasing concern in many ecological systems, yet its effects on disease are poorly characterized. American lobster (Homarus americanus) is declining at its southern geographic limit. Rising seawater temperatures are associated with seasonal outbreaks of epizootic shell disease (ESD), which peaks in prevalence in the fall. We used a 34-year mark-recapture dataset to investigate relationships between temperature, molting phenology, and ESD in Long Island Sound, where temperatures are increasing at 0.4 °C per decade. Our analyses support the hypothesis that phenological mismatch is linked to the epidemiology of ESD. Warming spring temperatures are correlated with earlier spring molting. Lobsters lose diseased cuticle by molting, and early molting increases the intermolt period in the summer, when disease prevalence is increasing to a fall peak. In juvenile and adult male lobsters, September ESD prevalence was correlated with early molting, while October ESD prevalence was correlated with summer seawater temperature. This suggests that temperature-induced molting phenology affects the timing of the onset of ESD, but, later in the summer, this signal is swamped by the stronger signal of summer temperatures, which we hypothesize are associated with an increased rate of new infections. October ESD prevalence was ~80% in years with hot summers, and ~30% in years with cooler summers. Yearly survival of diseased lobsters is <50% that of healthy lobsters. Thus, population impacts of ESD are expected to increase with increasing seawater temperatures.