The Role of Phytopathogenicity in Bark Beetle–Fungus Symbioses: A Challenge to the Classic Paradigm

Abstract

The idea that phytopathogenic fungi associated with tree-killing bark beetles are critical for overwhelming tree defenses and incurring host tree mortality, herein called the classic paradigm (CP), has driven research on bark beetle-fungus symbiosis for decades. It has also strongly influenced our views of bark beetle ecology. We discuss fundamental flaws in the CP, including the lack of consistency of virulent fungal associates with tree-killing bark beetles, the lack of correspondence between fungal growth in the host tree and the development of symptoms associated with a successful attack, and the ubiquity of similar associations of fungi with bark beetles that do not kill trees. We suggest that, rather than playing a supporting role for the host beetle (tree killing), phytopathogenicity performs an important role for the fungi. In particular, phytopathogenicity may mediate competitive interactions among fungi and support survival and efficient resource capture in living, defensive trees.

Bark and ambrosia beetles (Curculionidae: Scolytinae), their phoretic mites (Acari) and associated Geosmithia species (Ascomycota: Hypocreales) from Virgilia trees in South Africa

“…Bark and ambrosia beetles (Curculionidae, Scolytinae) are economically and ecologically important pests of trees in urban, forest, plantation and agricultural settings (Avtzis et al 2012;Harrington 2005;Kirisits 2004;Paine et al 1997;Six & Wingfield 2011), with about 225 genera and more than 6 000 described species globally (Avtzis et al 2012;Linnakoski et al 2012). Some, like the southern pine bark beetle (SPB), Dendroctonus frontalis Zimmermann, are capable of killing healthy trees, and causes substantial financial losses (Price et al 1992).…”

“…and other members of the Lauraceae . However, many scolytine beetles attack only trees that are weakened and/or stressed, or dead (Avtzis et al 2012;Paine et al 1997;Raffa et al 1993;Six & Wingfield 2011). Despite their ecological importance in, for example, initiating nutrient cycling (Christiansen et al 1987;Stark 1982), they have not attracted much research interest, as they seldom cause economic losses, except for those few that vector detrimental fungi (Lieutier et al 2009).…”

“…Scolytine beetles usually have complex associations with various organisms, including fungi (Linnakoski et al 2012;Six & Paine 1998;Six & Wingfield 2011;Whitney 1982), bacteria (Bridges 1984), mites (Cardoza et al 2008;Klepzig et al 2001;Moser et al 1995Moser et al , 2005 and nematodes (Cardoza et al 2008;Moser et al 2005). Those associated with ophiostomatoid fungi (e.g., species of Ceratocystis, Ophiostoma and Raffaelea) are of particular interest, as these fungi include important tree pathogens (Klepzig et al 2001;Moser et al 1995;Wood 1982).…”

“…Those associated with ophiostomatoid fungi (e.g., species of Ceratocystis, Ophiostoma and Raffaelea) are of particular interest, as these fungi include important tree pathogens (Klepzig et al 2001;Moser et al 1995;Wood 1982). Microbial and scolytine relationships may be incidental or obligatory, mutualistic, commensal or antagonistic (Kolařík et al 2008;Six 2003;Six & Wingfield 2011). The fungi benefit by being vectored to new plant hosts (Paine et al 1997;Six 2003;Six & Wingfield Harrington 2005;Klepzig et al 2001;Moser et al 1995;Six 2003;Six & Wingfield 2011).…”

“…Various other fungi in this system may, in turn, be antagonistic to the beetles (Barras 1970;Harrington & Zambino 1990;Hofstetter et al 2006;Klepzig et al 2001;Six & Wingfield 2011). In addition to fungivorous mites, other phoretic taxa can be parasitic, predatory and/or omnivorous (Klepzig et al 2001).…”