Can leafhoppers help us trace the impact of climate change on agriculture?

Abstract

Climate change is reshaping agriculture and insect biodiversity worldwide. With rising temperatures, insect species with narrow thermal margins are expected to be pushed beyond their thermal limits, and losses related to herbivory and diseases transmitted by them will be experienced in new regions. Several previous studies have investigated this phenomenon in tropical and temperate regions, locally and globally; however, here, it is proposed that climate change impact on agriculture can be traced through the study of Nearctic migratory insects, specifically leafhoppers. To test this hypothesis, leafhoppers in strawberry fields located in the province of Québec, eastern Canada, were evaluated. The strawberry-leafhopper pathosystem offers a unique opportunity because leafhoppers can transmit, among other diseases, strawberry green petal disease (SbGP), which is associated with pathogenic phytoplasmas. Here, we found that in the last ten years, the number of leafhoppers has been increasing in correspondence with the number of SbGP cases detected in eastern Canada, reporting for the first time ten species new to eastern Canada and two to the country, although the leafhopper diversity has been seriously affected. Our model using more than 34 000 leafhoppers showed that their abundance is influenced by temperature, a factor that we found also influences the microbiome associated withMacrosteles quadrilineatus, which was one of the most abundant leafhoppers we observed. One of our most striking findings is that none of the insecticides used by strawberry growers can control leafhopper incidence, which could be linked to microbiome changes induced by changing temperatures. We suggest that Nearctic leafhoppers can be used as sentinels to trace the multilayered effects of climate change in agriculture.

Potential impact of climate change on Nearctic leafhopper distribution and richness in North America

“…During winter, some leafhopper species undergo temperature-related diapause in their egg, nymph, or adult stages 14,16,62 , while migratory species like Empoasca fabae overwinter in southern regions 20 . As temperatures rise in early spring, leafhopper populations start to increase from both diapausing stages and the arrival of migratory species due to continental-scale winds 21,22 , with populations peaking in warmer months 19,20,32 . Leafhopper populations in the Nearctic region exhibit shorter life cycles in warmer conditions 18 , resulting in more yearly generations than colder ones 20,62 .…”

“…These specimens spanned 54 genera and 110 species, with the genera Empoasca , Erythroneura , and Macrosteles being widespread. Plante et al 19 captured 33,007 leafhopper specimens from strawberry fields in Québec, which included 61 genera and 118 species, with Empoasca , Macrosteles , and Hebata as prevalent genera.…”

“…We obtained species occurrence records (latitude, longitude) for North America from openly available online repositories, including the Global Biodiversity Information Facility (GBIF, accessed on 9 June 2023; https://doi.org/10.15468/dl.h3x8mf), which also includes records from INaturalist platform. We also included recent literature on leafhoppers’ field surveys 19,32,34,35,45 . These records were collected after 1970 to ensure relevance to the environmental variables used in our models (1970-2000) while avoiding historical records that may not accurately reflect current species occurrence sites 46,47 .…”

“…Increasing temperatures favor Nearctic population growth, as higher temperatures decrease the species’ life cycle duration 18,19 . Additionally, continental winds facilitate their dispersal into northern regions during the spring and summer 20–22 .…”

“…However, recent findings indicate a tripling in the incidence of phytoplasma diseases in the Nearctic over the past decade 29 . This trend suggests several potential factors: ( i ) advancements in molecular diagnostic methods and novel detection technologies for phytoplasmas 30,31 ; ( ii ) a rise in the abundance of leafhopper vectors 32 ; ( iii ) the probable existence of yet-to-be-identified highly efficient vectors 19,33–35 ; and ( iv ) an expansion of the geographic range of leafhopper vectors 20 .…”