Evolutionary ecology of the bark beetles Ips typographus and Pityogenes chalcographus.

Ips typographus (L.) and Pityogenes chalcographus (L.) (Coleoptera: Curculionidae) are two common bark beetle species on Norway spruce in Eurasia. Multiple biotic and abiotic factors affect the life cycles of these two beetles, shaping their ecology and evolution. In this article, we provide a comprehensive and comparative summary of selected life-history traits. We highlight similarities and differences in biotic factors, like host range, interspecific competition, host colonization, reproductive behaviour and fungal symbioses. Moreover, we focus on the species' responses to abiotic factors and compare their temperature-dependent development and flight behaviour, cold adaptations and diapause strategies. Differences in biotic and abiotic traits might be the result of recent, species-specific evolutionary histories, particularly during the Pleistocene, with differences in glacial survival and postglacial recolonization. Finally, we discuss future research directions to understand ecological and evolutionary pathways of the two bark beetle species, for both basic research and applied forest management.

Facultative and obligate diapause phenotypes in populations of the European spruce bark beetle Ips typographus.

The bark beetle Ips typographus is the most destructive insect pest in Norway spruce-dominated forests. Its potential to establish multiple generations per year (multivoltinism) is one major trait that makes this beetle a severe pest. Ips typographus enters diapause to adjust its life cycle to seasonally changing environments. Diapause is characterized by developmental and reproductive arrest; it prolongs generation time and thus affects voltinism. In I. typographus a facultative, photoperiod-regulated diapause in the adult stage has been described. In addition, the presence of an obligate, photoperiod-independent, diapause has been hypothesized. The diapause phenotype has important implications for I. typographus voltinism, as populations with obligate diapausing individuals would be univoltine. To test for the presence of different I. typographus diapause phenotypes, we exposed Central and Northern European individuals to a set of photoperiodic treatments. We used two ovarian traits (egg number and vitellarium size) that are associated with gonad development, to infer reproductive arrest and thus diapause. We found a distinct effect of photoperiod on ovarian development, with variable responses in Central and Northern European beetles. We observed obligate diapausing (independent of photoperiod) individuals in Northern Europe, and both facultative (photoperiod-regulated) as well as obligate diapausing individuals in Central Europe. Our results show within-species variation for diapause induction, an adaptation to match life cycles with seasonally fluctuating environmental conditions. As the diapause phenotype affects the potential number of generations per season, our data are the basis for assessing the risk of outbreaks of this destructive bark beetle. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s10340-021-01416-w.

Diapause and overwintering of two spruce bark beetle species.

Diapause, a strategy to endure unfavourable conditions (e.g. cold winters) is commonly found in ectothermic organisms and is characterized by an arrest of development and reproduction, a reduction of metabolic rate, and an increased resistance to adversity. Diapause, in addition to adaptations for surviving low winter temperatures, significantly influences phenology, voltinism and ultimately population growth. We review the literature on diapause and overwintering behaviour of two bark beetle species that affect spruce-dominated forests in the northern hemisphere, and describe and compare how these strategies can influence population dynamics. The European spruce bark beetle Ips typographus (L.) (Coleoptera, Curculionidae) is the most important forest pest of Norway spruce in Europe. It enters an adult reproductive diapause that might be either facultative or obligate. Obligate diapausing beetles are considered strictly univoltine, entering this dormancy type regardless of environmental cues. Facultative diapausing individuals enter diapause induced by photoperiod, modified by temperature, thus being potentially multivoltine. The spruce beetle Dendroctonus rufipennis (Kirby) (Coleoptera: Curculionidae) infests all spruce species in its natural range in North America. A facultative prepupal diapause is averted by relatively warm temperatures, resulting in a univoltine life cycle, whereas cool temperatures induce prepupal diapause leading to a semivoltine cycle. An adult obligate diapause in D. rufipennis could limit bi- or multivoltinism. We discuss and compare the influence of diapause and overwinter survival on voltinism and population dynamics of these two species in a changing climate and provide an outlook on future research.

Do water-limiting conditions predispose Norway spruce to bark beetle attack?

Drought is considered to enhance susceptibility of Norway spruce (Picea abies) to infestations by the Eurasian spruce bark beetle (Ips typographus, Coleoptera: Curculionidae), although empirical evidence is scarce. We studied the impact of experimentally induced drought on tree water status and constitutive resin flow, and how physiological stress affects host acceptance and resistance. We established rain-out shelters to induce both severe (two full-cover plots) and moderate (two semi-cover plots) drought stress. In total, 18 sample trees, which were divided equally between the above treatment plots and two control plots, were investigated. Infestation was controlled experimentally using a novel 'attack box' method. Treatments influenced the ratios of successful and defended attacks, but predisposition of trees to infestation appeared to be mainly driven by variations in stress status of the individual trees over time. With increasingly negative twig water potentials and decreasing resin exudation, the defence capability of the spruce trees decreased. We provide empirical evidence that water-limiting conditions impair Norway spruce resistance to bark beetle attack. Yet, at the same time our data point to reduced host acceptance by I. typographus with more extreme drought stress, indicated by strongly negative pre-dawn twig water potentials.

Inhibition of juvenile hormone esterase activity in Lymantria dispar (Lepidoptera, Lymantriidae) larvae parasitized by Glyptapanteles liparidis (Hymenoptera, Braconidae).

Glyptapanteles liparidis is a gregarious, polydnavirus (PDV)-carrying braconid wasp that parasitizes larval stages of Lymantria dispar. In previous studies we showed that parasitized hosts dramatically increase juvenile hormone (JH) titers, whereas JH degradation is significantly inhibited in the hemolymph. Here we (i) quantified the effects of parasitism on JH esterase (JHE) activity in hemolymph and fat body of penultimate and final instars of L. dispar hosts and (ii) assessed the relative contribution of individual and combined wasp factors (PDV/venom, teratocytes, and wasp larvae) to the inhibition of host JHE activity. The effects of PDV/venom was investigated through the use of gamma-irradiated wasps, which lay non-viable eggs (leading to pseudoparasitization), while the effects of teratocytes and wasp larvae were examined by injection or insertion of these two components in either control or pseudoparasitized L. dispar larvae. Parasitism strongly suppressed host JHE activity in both hemolymph and fat body irrespective of whether the host was parasitized early (premolt-third instar) or late (mid-fourth instar). Down-regulation of JHE activity is primarily due to the injection of PDV/venom at the time of oviposition, with only very small additive effects of teratocytes and wasp larvae under certain experimental conditions. We compare the results with those reported earlier for L. dispar larvae parasitized by G. liparidis and discuss the possible role of JH alterations in host development disruption.

Parasitism-induced effects of Glyptapanteles liparidis (Hym., Braconidae) on the juvenile hormone titer of its host, Lymantria dispar: the role of the parasitoid larvae.

Parasitization by the gregarious larval endoparasitoid Glyptapantles liparidis induces a dramatic increase in the hemolymph juvenile hormone (JH) titer (especially JH III) of its host larva, Lymantria dispar. Here, we investigated the role of the parasitoid larvae in JH synthesis and release by in vitro and in vivo experiments. GC-MS analyses confirmed that the rising hemolymph JH titer coincided with the time at which the parasitoids molt to the second larval instar. Peak values in host hemolymph titers were observed prior to parasitoid emergence, and titers dropped to negligible levels within 24 h after parasitoid emergence. Whole body extracts from excised second instar parasitoids yielded JH III and trace amounts of JH II. The in vitro secretory activity of the corpora allata (CA) of L. dispar larvae was not enhanced by parasitization. When the host's CA were separated by neck ligation, we found elevated JH III titers, but no JH II in the hemolymph of the posterior section, which contained the parasitoids. Parasitoids that were kept in in vitro culture produced and released only JH III. The parasitoids' ability to secrete JH and to molt independently from their host's molting cycles indicates that at least second instar parasitoids are hormonally self-reliant.

Alterations in carbohydrate and fatty acid levels of Lymantria dispar larvae caused by a microsporidian infection and potential adverse effects on a co-occurring endoparasitoid, Glyptapanteles liparidis.

Infection of Lymantria dispar host larvae by the entomopathogenic microsporidium Vairimorpha sp. has a negative impact on the performance of the endoparasitic braconid Glyptapanteles liparidis. To investigate possible causes for this effect, we studied to what extent nutritional host suitability is altered by the microsporidium. Therefore, we analyzed carbohydrates and fatty acids in host larvae after Vairimorpha infection and/or parasitism by G. liparidis. Trehalose levels were significantly reduced in the hemolymph of infected hosts. After day five post infection, it was detected only in traces. Four to six days later, the glycogen resources were depleted in infected larvae. Parasitism by G. liparidis, on the other hand, led to increased hemolymph trehalose levels during the early endoparasitic phase but to a significant decrease at the end of its larval development. No effect of parasitism on the glycogen content was ascertained. Hemolymph levels of the fatty acids analyzed, such as palmitic, stearic, oleic, linoleic, and linolenic acid, were significantly reduced in microsporidia-infected L. dispar. Vairimorpha sp. develops as an intracellular parasite in the fat body of the host larva and synthesis of trehalose and fatty acids may be disturbed. Moreover, microsporidia may also harness metabolites or energy produced by host cells. We conclude that the microsporidia-induced decrease in hemolymph carbohydrates and fatty acids adversely affects growth and development of parasitoid larvae.