Information adapted from Harrington, 2005 (Insect-fungal associations: ecology and evolution, p. 264)—Nine species of bark beetles associated with well-defined mycangial, and their associated fungi.
Insects share complex interactions with mites and fungi that range from obligate mutualisms to antagonistic relationships. These multitrophic interactions often result in changes to the host environment and population dynamics of the insect. Here, we review Scolytidae and Platypodidae beetles (bark beetles and ambrosia beetles, Coleoptera: Curculionidae) and their micro-organismal interactions with mites and fungi. Many bark beetles and ambrosia beetles are closely associated with mutualistic fungi used as a food source. These fungi are carried by the beetles in specialized pockets called “mycangia.” In addition to beetle-specific fungi, secondary fungi are often vectored by mite populations phoretic on the beetles. These secondary introductions create a complex fungal micro-biome within the host tree of the associated Scolytid beetles, with a myriad of consequences to beetle success and tree mortality. In this chapter, we provide a detailed review of specific beetle-fungal and mite-fungal associations, mutualistic and antagonistic effects of these fungal relations, and ecological and evolutionary consequences of beetle-fungal-mite relationships within the host complex.
A wide diversity of symbionts has contributed to the success of bark and ambrosia beetles (Curculionidae: Scolytinae) . All ambrosia beetles and most bark beetles have mutualistic fungi that serve as a nutrition source for young and adult beetles. However, some fungal (and other) symbiotic associations may be detrimental to beetles. Other beetle symbionts include mites that are frequently found traveling on adult beetles and live under the bark of beetle-infested trees . Similar to fungi, the impacts of mites on beetles vary widely. Mites too can be beneficial or detrimental to beetles. Some mite species can contribute to the fungal diversity in beetle galleries by transporting spores within and between trees [3, 4] impacting the behavior, development, and population dynamics of beetles [5, 6]. Such complex systems are evolutionary unique and can be considered principal factors in the success of Scolytid beetles.
Ambrosia beetles possess symbiotic mutualistic relationships with fungi (
Mites (Subphylum: Chelicerata, Class: Arachnida, Subclass: Acari) share a common, but important relationship termed “phoresy” with insects and other organisms . Phoresy refers to an interspecific relationship between two species where one acts as a host and the other acts as a “phoront,” attaching itself to the host for the purpose of dispersal or migration. Consequently, Farish  explicitly defines “phoresy” as follows: a phenomenon in which one animal actively seeks out and attaches to the outer surface of another animal for a limited time during which the attached animal (the “phoretic” animal or “phoront”) ceases both feeding and ontogenesis, presumably resulting in dispersal from areas unsuited for further development, either of the individual or its progeny. This sort of commensalism is common in species that live in rapidly changing environments, and/or in species that have limited mobility . Mites are small-minute organisms ranging from 50 μm to 3 mm in body length [21, 22] and thus have limited dispersal ability, other than being blown by the wind or carried by other animals or objects. They generally feed on other small arthropods or larvae and eggs of other arthropods, nematodes, fungi, bacteria, or dead organic matter . Due to their small size and limited mobility, mites are likely to be phoretic on insects that are able to transport them quickly and efficiently, i.e., flying insects such as bees (Hymenoptera), beetles (Coleoptera), and flies (Diptera). For instance, mites associated with ants tend to prefer alate queens (i.e., flying queens) over workers or any other type of ant , presumably because they are able to travel longer distances over a short span of time and can be introduced into future ant nests. Mites are usually found attached to setae (i.e., external hairs), to grooves in the tarsi, under the wings, under the elytra (hardened exoskeleton of beetles), or attached to any part of an insect’s body that provides a firm holdfast (Figure 1).
Phoretic mites may have either advantageous, disadvantageous, or no effect on their insect host. During the act of phoresy itself, even though mites cease to feed, their mere presence may be antagonistic/parasitic as insects can be weighed down by the presence of numerous mites (e.g., southern pine beetles being weighed down by masses of Uropodine mites ) slowing down flight speed and increasing energy expenditure (Figure 2). The risk of antagonistic effects increase when mites are deposited at the insect’s final destination. For example, varroa mites (
2. Bark and ambrosia beetle-fungal interactions
Ambrosia beetles and bark beetles (Coleoptera: Curculionidae, Scolytinae) are known to share intimate relationships with fungi. The subfamily Scolytinae consists of bark beetles (~7000 species), ambrosia beetles (~3400 species), and other various seed and pith-feeding beetles [8, 30]. A prominent characteristic of Scolytinae is a widespread association with fungal species, particularly the bark beetles and ambrosia beetles. These fungal associations are mutualistic or commensal (i.e., benefiting the fungi via dispersal by beetles) with beetles and are primarily Ascomycetes in the genera
2.1. Bark beetle-fungal associations
Bark beetles can be distinguished from ambrosia beetles and other Scolytinae by the fact that they exclusively invade the bark and phloem of trees, and not the woody tissue. Fungi associated with bark beetles are carried/introduced to the host in one of two ways—mycangially or nonmycangially—which indicate the specificity of the relationship between the fungus and the beetle. Some bark beetles such as the southern pine beetle (
|Bark Beetle||Tribe||Principal plant hosts||Mycangial type||Ascomycete associates||Basidiomycete associates|
2.2. Ambrosia beetle-fungal associations
Ambrosia beetles (Family: Curculionidae; subfamily: Scolytinae) occur worldwide and share close novel symbioses with fungi, such as
Ambrosia beetles are not typically associated with significantly damaging tree diseases in the way bark beetles are, as they often attack trees that are already dead or severely stressed [41, 51, 54, 55]. Coevolution theory suggests that the ambrosia beetle-fungal association is adaptable to a given host environment. However, problems arise when atypical beetle-host relationships form, i.e., exotic ambrosia beetles attack foreign hosts [50, 51, 54]. A recent concern in North America is an increase in exotic species of ambrosia beetles attacking living trees with. In most cases, these beetles are inoculating trees with non-native ambrosia fungi, for which native North American trees have little resistance . For example, the redbay ambrosia beetle (
The full ecological potential of ambrosia beetle-fungal relationships for exotic invasives is still unknown . There is little available detail on phoretic mite populations of ambrosia beetles as there is for bark beetles. Therefore, we are unaware of specific mite-fungal interactions for a given species of ambrosia beetle. There is a potential for similar complex mite-fungal interactions in ambrosia beetles as there are in bark beetles, particularly in situations with multiple beetle species attacking one host tree(s).
2.3. Factors affecting beetle-fungal associations
Both mutualistic and antagonistic fungal associations are context-dependent and highly affected on a combination of biotic and abiotic factors such as temperature, moisture, host tree defenses, presence of other microbes (i.e., bacteria, yeast, etc.), and other arthropods. Depending upon the beetle complex in question, such context-dependent conditions suggest that some fungi benefit from multipartite relationships in bark beetles more than others, and that the beetle’s ecological niche is determined by the external factors that govern it [57, 58].
Host tree type and conditions (moisture, phytochemical composition/concentrations, etc.) have a significant influence on bark beetle-fungal associations. For instance, changes in the chemistry and nutritional content of the host tree have the ability to alter the distribution and relative prevalence of fungal associates within the tree [8, 59–62]. A conifer tree’s primary defenses are resins and other induced secondary chemical compounds, which vary between tree species [57, 60, 63, 64]. In their study of the effect of tree defenses against fungi associated with the southern pine beetle, Hofstetter et al.  found that in general the phytochemistry of
Variations in temperature are one of the most vital factors affecting the relative abundance and diversity of fungal species, in turn affecting the ecological associations of the fungus’ host bark beetle [3, 67–69]. The mountain pine beetle,
For bark beetles associated with multiple mycangial symbionts, the prevalence of a specific mycangial fungal associate depends upon the beetle’s environmental temperature and consequently determines the beetle’s ability to survive in a given geographic location. Often, the presence of multiple beetle-associated fungi results in competition between the different fungal species with one species dominating the other. Changes in external factors (such as host tree chemistry and temperature) can determine the competitive advantage of a resource between multiple fungal symbionts, and also determine the success of antagonistic tree-killing pathogens such as species of blue-stain (
3. Mite-fungal-beetle interactions
Mites are a prominent phoront of bark beetles and some ambrosia beetles [2, 58]. Mites (Arachnida: Acari) are subdivided into two main super orders: Parasitiformes and Acariformes . The Parasitiformes are further divided into four orders—Ixodidae, Holothyrida, Opilioacaridae, and Mesostigmata, and the Acariformes are divided into two orders—Sarcoptiformes and Trombidiformes . Mites phoretic on bark beetles are predominantly species of the order Mesostigmata and Trombidiformes [62, 72, 73] and range from 80 μm (e.g.,
The fungal symbionts of bark beetles often provide a food source for the mites, and the fungal associations of the mites provide a food source for the beetle.
3.1. Role of mites in altering population dynamics of bark beetles
We know little of the potential impact of mites on beetle population dynamics. A few studies indicate that mites may influence factors affecting beetle life history such as reproductive success, development, and mortality, for example,
The effect of mite-vectored fungi varies between mycangial and nonmycangial bark beetles. The presence of symbiont specific mycangia (e.g.,
3.2. Role of mites in spreading fungal pathogens
Bark and ambrosia beetles have been pinpointed as one of the primary vectors of tree disease-causing pathogens such as
Bark beetles are associated with an array of mites. The southern pine beetle alone is associated with 96 different species of mites . The mountain pine beetle is associated with 57 different phoretic mite species , and the spruce beetle (
Dutch elm disease, a vascular wilt disease that affects elm trees, is caused by the introduction of the Ascomycete species (such as
Complex interactions, particularly mutualisms like that of bark and ambrosia beetles and mycangial fungi have vast implications on the ability to exploit marginal resources and determining habitat range, which in turn affect the host tree environment, spread of fungal pathogens, changes in fungal community structure, etc. Mite-beetle-fungal interactions are likely to alter these ecological implications and effects. Phoretic mites (e.g.,
Scolytid beetles, mites, and fungi share a unique tripartite relationship that has the potential to affect entire ecosystems. Bark beetle-fungal relations are a primary cause for pine tree mortality, and mite-induced fungal complexity may potentially alter the effects/progress of such pathogenic fungi by either enhancing or diminishing them. For example, mites associated with the southern pine beetle cause blue-stain by vectoring
While bark and ambrosia beetle populations are typically monitored, their mite and fungal associations are not. We believe that geographic expansion, reproductive fitness, and other factors of beetle population dynamics rely on a thorough understanding of the mite and fungal diversity associated with beetles. The mite-beetle-fungal tripartite relationship is a relatively new realm of study in the field of multipartite symbioses, with a vast scope for new discoveries that expand or knowledge and understanding of ambrosia and bark beetle ecology.
We would like to acknowledge and thank Derek Uhey, PhD Student, Northern Arizona University, Flagstaff AZ 86011, USA, for his assistance with initial editing and formatting of the information presented.
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