Reduced disease in black abalone following mass mortality: phage therapy and natural selection

Carolyn S. Friedman,Lisa M. Crosson,Glenn R. VanBlaricom,Kevin D. Lafferty,Nathan Wight

doi:10.3389/fmicb.2014.00078

Abstract

Black abalone, Haliotis cracherodii, populations along the NE Pacific ocean have declined due to the rickettsial disease withering syndrome (WS). Natural recovery on San Nicolas Island (SNI) of Southern California suggested the development of resistance in island populations. Experimental challenges in one treatment demonstrated that progeny of disease-selected black abalone from SNI survived better than did those from naïve black abalone from Carmel Point in mainland coastal central California. Unexpectedly, the presence of a newly observed bacteriophage infecting the WS rickettsia (WS-RLO) had strong effects on the survival of infected abalone. Specifically, presence of phage-infected RLO (RLOv) reduced the host response to infection, RLO infection loads, and associated mortality. These data suggest that the black abalone: WS-RLO relationship is evolving through dual host mechanisms of resistance to RLO infection in the digestive gland via tolerance to infection in the primary target tissue (the post-esophagus) coupled with reduced pathogenicity of the WS-RLO by phage infection, which effectively reduces the infection load in the primary target tissue by half. Sea surface temperature patterns off southern California, associated with a recent hiatus in global-scale ocean warming, do not appear to be a sufficient explanation for survival patterns in SNI black abalone. These data highlight the potential for natural recovery of abalone populations over time and that further understanding of mechanisms governing host–parasite relationships will better enable us to manage declining populations.

Highlights

The black abalone, Haliotis cracherodii, was once abundant along rocky shores of the NE Pacific (Haaker et al, 1986; Geiger, 1999)
Our findings suggest that the increased survivorship seen at San Nicolas Island (SNI) was due to reduced metaplasia and withering syndrome (WS)-RLO loads in the digestive gland (DG)
While we found some evidence for our hypothesis of the evolution of resistance in black abalone following mass mortality, the significance of these results varied among trials

Summary

Introduction

The black abalone, Haliotis cracherodii, was once abundant along rocky shores of the NE Pacific (Haaker et al, 1986; Geiger, 1999). In some locations, such as the California islands, black abalone were often stacked 4–5 deep (Douros, 1987). Black abalone populations supported indigenous subsistence fisheries for at least nine millennia (e.g., Erlandson et al, 1996) and, more recently, supported a relatively stable commercial harvest (Karpov et al, 2000) until 1982 when a strong El Niño Southern Oscillation (ENSO) preceded catastrophic population declines (Dayton and Tegner, 1984). Concern over the ability of depleted populations of black abalone to recover following mass mortality was heightened by the fact that recruits have been shown to largely originate from local stocks (Hamm and Burton, 2000; Chambers et al, 2005, 2006)

Methods

Results

Discussion

Conclusion