Sublethal Exposure to Phosphine Decreases Offspring Production in Strongly Phosphine Resistant Female Red Flour Beetles, Tribolium castaneum (Herbst)

Andrew W Ridley,Seymour Magabe,David I Schlipalius,Patrick J Collins,Michelle A Rafter,Mark F Feldlaufer

doi:10.1371/journal.pone.0053356

Andrew W Ridley, Seymour Magabe + Show 4 more

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https://doi.org/10.1371/journal.pone.0053356

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Abstract

The red flour beetle is a cosmopolitan pest of stored grain and stored grain products. The pest has developed resistance to phosphine, the primary chemical used for its control. The reproductive output of survivors from a phosphine treatment is an important element of resistance development but experimental data are lacking. We exposed mated resistant female beetles to 0.135 mg/L of phosphine for 48 h at 25°C. Following one week of recovery we provided two non-exposed males to half of the phosphine exposed females and to half of the non-exposed control females. Females that had been exposed produced significantly fewer offspring than non-exposed females. Females that remained isolated produced significantly fewer offspring than both exposed females with access to males and non-exposed controls (P<0.05). Some females were permanently damaged from exposure to phosphine and did not reproduce even when given access to males. We also examined the additional effects of starvation prior to phosphine exposure on offspring production. Non-exposed starved females experienced a small reduction in mean offspring production in the week following starvation, followed by a recovery in the second week. Females that were starved and exposed to phosphine demonstrated a very significant reduction in offspring production in the first week following exposure which remained significantly lower than that of starved non-exposed females (P<0.05). These results demonstrate a clear sublethal effect of phosphine acting on the female reproductive system and in some individuals this can lead to permanent reproductive damage. Pest population rebound after a fumigation may be slower than expected which may reduce the rate of phosphine resistance development. The results presented strongly suggest that phosphine resistance models should include sublethal effects.

Highlights

The red flour beetle, Tribolium castaneum (Herbst), is a cosmopolitan pest of stored grain, flour mills and grain products [1,2,3], and the fumigant phosphine is commonly used for its control
All females produced relatively high numbers of offspring prior to phosphine exposure, significantly fewer offspring were produced by females that would go on to be fumigated and have access to males compared to the other groups (Table 1)
Sublethal exposure to phosphine decreased the production of offspring of strongly resistant T. castaneum females

Summary

Introduction

The red flour beetle, Tribolium castaneum (Herbst), is a cosmopolitan pest of stored grain, flour mills and grain products [1,2,3], and the fumigant phosphine is commonly used for its control. High level resistance to phosphine has been reported in most countries where it has been surveyed [4,5,6,7,8,9] Adults of this pest are long lived and single mating pairs have been recorded to produce greater than 500 offspring over a three month period [10,11,12]. The development of heritable resistance to pesticides by insects is an evolutionary process that is wholly dependent on the survivors of a selection event (i.e. pesticide application) producing offspring This results in post-selection populations having a higher frequency of resistance alleles compared with pre-selection populations. In systems where resistance selection occurs on long-lived and fecund adults, sublethal effects on the ability of the adults to reproduce subsequent to a selection event may have a significant impact on the development of resistance

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