Review: Behavioral cues in the colonization cycle of Dendroctonus Erichson species

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1 Review: Behavioral cues in the colonization cycle of Dendroctonus Erichson species Javier E. Mercado Department of Bioagricultural Sciences and Pest Management Colorado State University, Fort Collins, Colorado Abstract In any given ecosystem there exist a dynamic and complex mixture of volatile chemicals which together with visual and auditory signals that affect the behavior of the different insects living in their vicinity. Particular combinations and concentrations of these signals have been found to function as cues to different behavior responses of bark beetles (Coleoptera: Curculionidae) species. The understanding of these factors as they occur in nature is utilized to help predict models of spread and colonization and to help understand and manage these important pests. In this review I will present some of the research involving the study of these signals in the understanding of the response behavior by bark beetles of the genus Dendroctonus Erichson in North America north of Mexico. I will review the important role of olfaction in the response and behavior of these species and how environmental stress conditions mediate their release into their ecosystem. The role of attractants of mycological origin has also been mentioned by researchers and will also be mentioned. Semiochemicals synthesized by the beetles will be mentioned including: sex and aggregations as well as anti-aggregation pheromones, and the behavioral effects on the genus will be presented. Introduction At endemic population levels, bark beetles (Coleoptera: Curculionidae) are an essential part of many ecosystem s natural balance as they attack injured or dying trees advancing their integration into the soil and providing niches to many other organisms. Nevertheless, populations of trees can become very large and particularly homogeneous, is in these occasions when an

2 endemic population of these insects can become epidemic, with substantial detrimental effects such as the recent of the Mountain Pine Beetle in the Rocky Mountains and British Columbia. After emergence, between late spring and early fall, pioneer beetles take flight in search of a suitable host in which to ensure their progeny. They use different strategies to get to a suitable host; some fly under the canopy where they could theoretically disperse over four kilometers calculated as function of their speed and capacity of flight as suggested by flight mill experiments (Williams, et al., 2009), while others can be pushed by thermals over the canopy and are often transported by the wind to distances of over 30 kilometers per day as estimated by studies using Doppler radar in British Columbia (Straussfogel, et al., 2008). Bark beetles are not blind, and they can see and detect different light intensities and perhaps all colors in the visible light spectrum. The bark beetles efficacy in finding their host when using visual cues should not be discarded given the success of these beetles which have constructed their galleries in conifers since the late Mesozoic (Falder, et al.,1998). As suggested by studies in Florida and Louisiana on the southern pine beetle, Dendroctonus frontalis Zimmermann, which measured the visual orientation on capture rates on different structures, including tree trunks painted with black or white paint (Strom, et al., 1999), it was found that the beetle are significantly more attracted by the black colored surfaces. Once on suitable habitat they keep orienting themselves with the integration of olfactory cues, randomly landing at trees were they sense for the plant s secondary compounds which act as kairomones and perhaps other olfactory cues which act as primary attractants to the pioneer beetles. These attractants are dispersed by the wind in a particular plume array of any given size and concentration (Byers, 2008). After landing in a particular tree Dendroctonus beetles sense the suitability, often digging through the cortex into the phloem and then they either take flight again or accept the suitable host and start to build an entrance into the tree s phloem. Once the host tree is accepted aggregation pheromones are released to attack more females and mass 2

3 attack the host to overcome its defenses. These hormones travel and mix with the wind-carried monoterpenes and together work as secondary attractants to more females which help arrest the host tree defenses. Once the females have overcome the tree s defenses males are attracted with the release of sex pheromones which also become part of the preexisting odorous plume. Pioneer beetle emergence In general, bark beetles of the genus Dendroctonus can overwinter as both larvae and adults and are considered to be univoltine; although, species living in the cooler northern or higher areas are considered to be facultative semivoltine as is the case of D. rufipennis Kirby which can take up to four years to complete a generation (Wood, 1982) or as species living in southern and warmer areas such as D. frontalis can be multivoltine having more than three generations each year. On the species of colder regions such as those on the Rocky Mountains environmental temperature has to reach a certain threshold for both adult and larval forms breaking diapause and begin to feed. Emergence occurs when environmental conditions permit their survival; a raise in temperature is the cue that triggers this behavior. In a study to develop a model to predict mountain pine beetle development temperatures Bentz (Bentz, et al., 1985) determined the optimal temperature to be from 23 and 25 C for the different developmental stages. Pioneer beetles of the genus Dendroctonus are all females and they have the task of flying and orienting themselves in the direction of its suitable host s habitat and more difficult to find a host tree and test its suitability for colonization. It has been noticed by several authors that not always the bark beetles land on the right host or if it does, not always accepts it for colonization. These tasks definitely require a little more effort, thus energy, from the pioneering beetle than for her emerging mate. Experimentally it has been demonstrated that flight capacity in beetles is proportional to fat body size (Atkins, 1969, 1975). Callow adults of Dendroctonus feed in the phloem of their brooding tree before 3

4 emergence and studies of their digestive tracts content has showed that the pioneering females had higher amount of food than the males in the same tree (McNee, et al., 2000). Flight behavior After emergence the first behavior performed by bark beetles is to disperse in the search of a suitable host; dispersal in Dendroctonus has only been documented to be by means of flying but perhaps it could occur in certain instances by gliding or walking to an adjacent three as hypothesized for the European species D. micans Kugelann (Gilbert, et al., 2001); this could explain, in part, the clumped patterns of dying conifers seen on the peripheries of an outbreak area. Flight takes energy and the capacity of flight of Dendroctonus beetles have been studied in terms of their fat content. In the late sixties experiments showed a positive correlation between fat reserves and the beetle s inclination to fly (Atkins, 1969); more recently, in laboratory experiments using flight mills (Williams, et al., 2009), 143 D. pseudostugae Hopkins were sampled and found to contain 14.3 ± 1.0% of their body weight as fat. They tested such fat could sustain flight on the beetles for 2.87 hours on average meaning a theoretically flight dispersal 4.67 kilometers per day. Mark-recapture experiments have showed that 99.7% of D. ponderosae Hopkins beetles fly under 250 meters during dispersal (Trzcinski, et al., 2008 citing Safranyik et al., 1992). However, there are other rather extreme ways these beetles can move; studies in British Columbia (Jackson, et al., 2008) found that D. ponderosae was being transported by the wind at heights of up to 800 meters over the canopy, possibly carried there by the power of thermal currents. They calculated these beetles could be flying pushed with help of the wind currents distances from 30 to 110 kilometers, but they used maximum sustained flight hypothetical values of 4 ± 2 hours; the longest flight time has been showed to be rare, thus the suggested longer ranges perhaps will need to be tested experimentally. 4

5 Orientation behavior The use of more than one receptor to respond to their host-tree different cues has enable these beetles to be highly successful in finding their way to the trees since perhaps the middle Eocene (some 45 million years ago, (Labandeira, et al., 2001) from where galleries corresponding to the genera have been identified in the wood of a fossilized Larch tree on the Heiberg Island, on the high Canadian Arctic. During an endemic or epidemic attack the bark beetles behavioral response to semiochemicals is an indispensable and major part of their life history. The use of olfactory reception in Dendroctonus beetles has been well established for several decades (Byers 1989; Dickens, et al., 1985; Moeck, et al., 1981; Payne, et al., 1973; Payne, 1975; Tommeras, et al., 1984). The primary olfactory sensors in this genus and all the other bark beetles are located in the antennae and its morphology was first compared by Payne (Payne, et al., 1973), he studied the structures of the antennae of the species D. adjunctus Blandford, D. brevicomis LeConte, D. frontalis, D. ponderosae and D. tenebrans Olivier and found the most important sensorial elements to be concentrated in their antennal club. Among these species the only morphological difference found was that D. frontalis lacked a partial third sensorial band on the apical portion of the club but instead had pores on the sensila basiconica short type, this modification was related with chemoreceptors on cockroaches. Orientation behavior during primary attraction When the first beetles emerge in spring or summer they perhaps find a less intense chemical mix of volatiles than that which will be encountered by their mates following their colonization. This primary attraction to compounds other than pheromones occurs in about half the species in the genus which are primordially primary pests and requires more integration of other cues such as visual from the female pioneering beetles and unlike many other species in the sub families Scolytinae half the member species in Dendroctonus are considered to be primary colonizers or species that attack healthy, living trees, but most of the rest are facultative primary, 5

6 for instance, responding like this in a epidemic situation. Tree s secondary compounds such as kairomones (Pureswaran & Borden, 2005), allomones and other compounds such as those produce by fungi have been exploited by these invaders of trees. For instance alcohols and esters released as metabolites from fungi related to Dendroctonus frontalis was found to elicit an enhanced attraction by the beetles when tested synergistically with other attractants (Brand, et al., 1977). The burning by fire or a lightning attracts several species of secondary Dendroctonus. But the attraction to aggregation pheromones which are often produced de novo after the ingestion of the oleoresin like frontalin, exo-brevicomin and other pheromones are released by females on some of the species such as D. frontalis and D. brevicomis definitely elicits the strongest effect on the second part of the primary attraction process. It is widely accepted that chemical cues are main attractants in these insects but it has been difficult to test how effective these signals are perceived in different situations, for instance, in long versus short range situations and perhaps visual cues are a stronger cue when the olfactory cues are too far to be sensed. Like all scolytids, Dendroctonus beetles have functional compound eyes, capable of detecting light from the visible spectrum. In a walking bioassay (Groberman,et al., 1981), were two light wavelength choices covering the whole visible spectrum were presented to D. pseudostugae, the beetle had a stronger response to those corresponding to the violet-blue and green colors. During a host-habitat search flight both positive and negative wavelengthdependent phototaxis has been showed in experiments subjecting host- searching D. frontalis to adjacent contrasting black and white vertical silhouettes (Strom, et al., 1999; Strom, et al., 2001; Goyer, et al., 2004) it was showed that attraction is reduced towards the white surfaces and vice versa (See fig1). The study was replicated and tested on D. ponderosae and D. pseudostugae. 6

7 Figure 1. Visual orientation towards the darker green conifers in Dendroctonus Colonization and gallery formation After a series of trial landings and the acceptance of suitability of a host conifer the beetles start the colonization process. Aggregation pheromones are released at this time by the different species with the purpose of aggregating enough burrowing females to overcome the trees defenses which are the chemical composition and the mechanical actions of the resin flow. The beetles have evolved resistance to the chemical compounds of their various hosts resins but high flow intensity can serve as a deadly trap and it has to be arrested by the synchronized mass attack of many pioneer females. When do the females decide to stop the aggregation, is not fully understood, but suggestions point to vibration associated with the gallery construction (Wallin, et al., 2002) or perhaps by that of their stridulating organ (Rudinsky, et al., 1973). A strong and healthy tree would likely overcome an attack by secreting copious amounts of resin trapping and killing the attacking beetles, however a susceptible tree resin flow will progressively decrease its resin flow has as a result of an increasing attack mass attack by females. This perhaps can be sensed by the burrowing female and could constitute a strong cue for the release of the anti aggregation pheromones. 7

8 During colonization the females continue burrowing into the phloem forming the galleries, they pack them with frass that gets inoculated by spores which reside in specialized structures called mycangium. This helps to kill the tree blocking further the phloem. In laboratory studies the length of the gallery was affected by the number of arriving females to a small and contiguous area but up to certain threshold (Wallin, et al., 2002). Galleries in the previous instance were longer the more females there were and this could be a strategy to reduce competition by growing larva which occurs scattered lengthwise on the gallery. Other cue which could control gallery spacing was suggested by Rudinsky (et al. 1973) as a function of the females stridulating organ. Orientation behavior during secondary attraction The decrease of the resin flow is the cue female pioneer beetles perceive probably triggers the release of the strongest attractant in the life history of these interesting pests, the sex pheromones. After colonization has been achieved sex pheromones pheromones are released by females on some of the species such as D. frontalis and D. brevicomis; the males antennal receptors are strongly tuned to these, their antennal response has been determined to respond the strongest to these chemicals. The anti-aggregation behavior After the defeat of its host oleoresin s chemical and mechanical defenses by the mass aggregation and attack they have evolved behaviors to which ensure them a well balanced proportion of individuals per host which will ensure reproductive successes. Dendroctonus have evolved the capacity of sensing inter as well as intra-specific competition within a single tree. It will be advantageous for these insects to be able to detect and respond as quickly as possible to any cue that could signal that a particular host has met its carrying capacity; and perhaps this can be accomplished before landing by the olfaction of a pheromome (Byers, 1989). 8

9 Verbenone is an anti-aggregation pheromone of a number of pine-infesting bark beetles including D. brevicomis (Tilden, et al., 1988; Bertram, et al., 1994). Other anti-aggregation pheromones have been identified such as 1-Octen-3-ol on studies with the species D. ponderosae, D. pseudostugae and D. rufipennis (Pureswaran, et al., 2004) and found to reduce the activity of both of the sexes of D. ponderosae and D. pseudostugae but curiously in their study different responses were recorded on the males of populations of costal and interior samples of D. pseudostugae and possibly requires more study. Discussion The great success of these bark beetles should not be determined by any single method of guidance to their host but to the integration of visual orientation, olfactory guidance towards kairomones and pheromones as well as the recognition and avoidance of the antagonists visual and olfactory cues to those. This was tested with D. ponderosae and D. psedostugae in a test were both attractants as well as anti-aggregation compounds were applied to visually distinctly painted funnels (Campbell & Borden, 2006) obtaining significant results on how these species are attracted to dark objects but avoid with colored ones, giving a indication of how these insects integrate the two sets of information into their host selecting process. This could explain how they choose between two populations within their range one for instance of lighter non-host Birch or Aspen and the other of darker host lodgepole or ponderosa pines. Their positive wavelength- dependent phototaxis to violet-blue and green light and positive chemotaxis was reinforced by the addition of an element of anti-aggregation compounds which further reduced captures reinforcing this theory and their potential application in the management of their outbreaks. Olfaction in this group is simply amazing and very complicated to the point that is not fully comprehended in some of the species; research in this area is improving with time and is of much importance in the development of techniques to control these pests. The mechanisms to detect density after colonization are partially understood, but the hypotheses about this appear congruent, and suggest and advance process of evolution on the genus. The sound producing capacity of females in this genus has not been found in other genera in the sub-family Scolytinae. Finally, an ethogram which integrated the different cues involved in the life cycle of this genus 9

10 could not be found for this review, for that see figure two for an elementary approach to an example. Figure 2. Ethogram of the life cycle of Dendroctonus species References Atkins, M.D. (1969). Lipid loss with flight in Douglas Fir Beetle. CANADIAN ENTOMOLOGIST, 101(2): Atkins, M.D. (1975). On factors affecting the size, fat content and behavior of a scolytid. Zeitschrift fur Angewandte Entomolgie. 78: Bentz, B., Logan, J. &Amman, G. (1991). Temperature-dependent development of the Mountain Pine Beetle (Coleoptera: Sclolytidae) and simulation of its phenology. CANADIAN ENTOMOLOGIST, 123(5): Bedard, W. D., Lindahl, K. Q., Tilden, P. E., & Wood, D. L. (1985). Behavior of the western pine beetle during host colonization. Journal of Chemical Ecology, 11(9): Bertram, S. L., & Paine, T. D. (1994). Influence of aggregation inhibitors (verbenone and ipsidenol) on landing and attack behavior of Dendroctonus brevicomis (Coleoptera: Scolytidae). Journal of Chemical Ecology, 20(7):

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