Aphid fecundity and grassland invasion: Invader life history is the key

Abstract

Loss or gain of pathogens can determine the trajectory of biological invasions, and invasion by novel hosts also can alter pathogen dynamics to facilitate invasion. Recent empirical and theoretical work has implicated infection by barley and cereal yellow dwarf viruses (B/CYDV), a group of generalist pathogens of the Poaceae family (grasses), as a necessary precursor to the invasion of over 9 million hectares of California's perennial grasslands by exotic annual grasses. The mechanism underlying this pathogen-mediated invasion hypothesis is elevated vector fecundity on exotic annual grasses. While empirical evidence supports this hypothesis, the links between aphid fecundity, host identity, and host resource supply have not been thoroughly assessed. We performed field and laboratory experiments to examine the fecundity and preference responses of three of the most common aphid vectors of B/CYDV, Rhopalosiphum padi (L.), R. maidis (Fitch), and Sitobion avenae (Fab.), to a combination of host life history (annual and perennial), host provenance (native and exotic), and nutrient supply (mineral N and P fertilization), controlling for host phylogenetic lineage. Aphids consistently had higher fecundity on annual grasses than perennials, regardless of host provenance, age, or nutrient fertilization. In addition, aphids preferentially colonized annual hosts when offered a choice among host species. Multi-generation studies have found that nutrient addition affects both host quality and composition in natural communities; our experimental results indicate that the indirect effects of nutrient fertilization in determining host community composition are of more importance than are the direct effects on host quality to aphid population dynamics. To summarize the applications of our results, we demonstrate that, in contrast to the current focus on the qualitative differences between invaders and natives, the impact of invasive exotic grasses is not due to host provenance, per se, but arises because the annual invaders differ qualitatively from the native species in interactions with shared pathogen vectors. More generally, our work demonstrates the importance of isolating whether the fate and impacts of an invader are, at their root, due to the provenance of the invader, or due to other characteristics that determine its functional uniqueness in the context of the native community.

Non-random biodiversity loss underlies predictable increases in viral disease prevalence

“…However, B. hordeaceus was one of the two most efficient species to transmit virus infection, to attract aphid vectors and to support vector reproduction. Annual species were superior hosts compared with perennials for each of these parameters, which is consistent with previous findings [35,38], and the most ubiquitous annual hosts were also the most competent for aphid reproduction, preferential feeding and virus transmission. Interestingly, the ubiquity-competence relationship that underlies the disease dilution effect in this study is more related to annual host ability for transmission to other hosts than to susceptibility to virus inoculations.…”

“…We used data from two previously published experiments [38] to assess aphid (R. padi) fecundity and host preference for a subset of host species included in four different phylogenetic tribes (see electronic supplementary material, table S2). Although R. padi is one of many aphid vector species of B/CYDVs, it is an efficient agent in spreading BYDV-PAV [47].…”

“…Thus, compositional shifts favouring highly competent species in communities are expected to increase transmission rate leading to disease amplification [35,38], whereas an abundance of nonor poorly competent species would reduce disease incidence leading to dilution [23,32].…”

Relationship of Soybean Aphid (Hemiptera: Aphididae) to Soybean Plant Nutrients, Landscape Structure, and Natural Enemies

“…The growth and reproduction of aphids are affected by availability of essential nutrients in the phloem sap of host plants (Dixon 1998). Availability of limiting nutrients in plant tissues such as nitrogen is related to variability in aphid population growth (Nevo and Coll 2001, Awmack and Leather 2002, Borer et al 2009). For soybean aphid, lower concentrations of potassium in soybean leaves and soil have been shown to increase soybean aphid fecundity and population growth (Myers et al 2005, Myers and Gratton 2006, Walter and DiFonzo 2007.…”

Spatiotemporal Model of Barley and Cereal Yellow Dwarf Virus Transmission Dynamics with Seasonality and Plant Competition

“…We have amassed data on 20 different native and exotic, annual, and perennial grass US West Coast species (Cronin et al 2010;Borer et al 2009;Welsh, Borer, and Mitchell, unpubl. data).…”