High road mortality during female-biased larval dispersal in an iconic beetle.

ABSTRACT: Animals often disperse from one habitat to another to access mates or suitable breeding sites. The costs and benefits of such movements depend, in part, on the dispersing individuals' phenotypes, including their sex and age. Here we investigated dispersal and road-related mortality in larvae of a bioluminescent beetle, the European common glow-worm, Lampyris noctiluca, in relation to habitat, sex and proximity of pupation. We expected these variables to be relevant to larval dispersal because adult females are wingless, whereas adult males fly when searching for glowing females. We found that dispersing glow-worm larvae were almost exclusively females and close to pupation. The larvae were often found on a road, where they were able to move at relatively high speeds, with a tendency to uphill orientation. However, each passing vehicle caused a high mortality risk, and we found large numbers of larvae run over by cars, especially close to covered, forest-like habitat patches. In contrast, adult females in the same area were most often found glowing in more open rocky and grassy habitats. These findings demonstrate an underappreciated ecological strategy, sex-biased dispersal at larval phase, motivated by different habitat needs of larvae and wingless adult females. The results are also consistent with roads being an ecological trap, facilitating dispersal and presumably females' signal visibility but causing severe larval mortality just before the reproductive stage. Hence, in addition to the previously recognised threats of urbanisation, even low traffic volumes have a high potential to negatively affect especially females of this iconic beetle. SIGNIFICANCE STATEMENT: Animals sometimes need to move from one habitat to another to find mating partners or breeding sites. We found this need to result in strongly female-biased larval dispersal in the European common glow-worm, a beetle known for the glow of wingless females that attract flying males to mate. Female larvae moving between habitats often used a road or trail but perished in high numbers when run over by cars. Hence, roads are likely to be ecological traps for the female glow-worm larvae, attracting them during dispersal, but causing grave mortality. The sex-biased larval dispersal, demonstrated in this study, is a poorly known ecological strategy that was found to be very risky in a human-modified landscape. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s00265-020-02962-6.

Reproduction under light pollution: maladaptive response to spatial variation in artificial light in a glow-worm.

The amount of artificial light at night is growing worldwide, impacting the behaviour of nocturnal organisms. Yet, we know little about the consequences of these behavioural responses for individual fitness and population viability. We investigated if females of the common glow-worm Lampyris noctiluca-which glow in the night to attract males-mitigate negative effects of artificial light on mate attraction by adjusting the timing and location of glowing to spatial variation in light conditions. We found females do not move away from light when exposed to a gradient of artificial light, but delay or even refrain from glowing. Further, we demonstrate that this response is maladaptive, as our field study showed that staying still when exposed to artificial light from a simulated streetlight decreases mate attraction success, while moving only a short distance from the light source can markedly improve mate attraction. These results indicate that glow-worms are unable to respond to spatial variation in artificial light, which may be a factor in their global decline. Consequently, our results support the hypothesis that animals often lack adaptive behavioural responses to anthropogenic environmental changes and underlines the importance of considering behavioural responses when investigating the effects of human activities on wildlife.

Identification and characterisation of common glow-worm RNA viruses.

The common glow-worms (Lampyris noctiluca) are best known for emission of green light by their larvae and sexually active adult females. However, both their DNA and RNA viruses remain unknown. Glow-worms are virologically interesting, as they are non-social and do not feed as adults, and hence their viral transmission may be limited. We identified viral sequences from 11 different virus taxa by the RNA-sequencing of two Finnish populations of adult glow-worms. The viruses represent nine different virus families and have negative, positive, or double-stranded RNA genomes. We also found a complete retroviral genome. Similar viral sequences were found from the sequencing data of common eastern firefly of North America, a species belonging to the same family (Lampyridae) as that of the common glow-worm. On average, an individual glow-worm had seven different RNA virus types and most of them appeared to establish a stable infection since they were found from glow-worms during two consecutive years. Here we present the characterization of load, prevalence, and interactions for each virus. Most of the glow-worm RNA viruses seem to be transmitted vertically, which may reflect the biology of glow-worms as non-social capital breeders, i.e., they invest stored resources in reproduction.

I'm sexy and I glow it: female ornamentation in a nocturnal capital breeder.

In many species, males rely on sexual ornaments to attract females. Females, by contrast, rarely produce ornaments. The glow-worm (Lampyris noctiluca) is an exception where wingless females glow to attract males that fly in search of females. However, little is known about the factors that promote the evolution of female ornaments in a sexual selection context. Here, we investigated if the female ornament of the glow-worm is a signal of fecundity used in male mate choice. In support of this, we found brightness to correlate with female fecundity, and males to prefer brighter dummy females. Thus, the glow emitted by females is a reliable sexual signal of female fecundity. It is likely that male preference for the fecundity-indicating ornament has evolved because of large variation among females in fecundity, and because nocturnal males cannot directly assess female size and fecundity. These results indicate that female ornamentation may evolve in capital breeders (i.e. those in which stored resources are invested in reproduction) when females vary significantly in fecundity and this variation cannot be assessed directly by males.

Acute impacts of the deer ked (Lipoptena cervi) infestation on reindeer (Rangifer tarandus tarandus) behaviour.

Blood-sucking ectoparasites have often a strong impact on the behaviour of their hosts. The annual insect harassment of reindeer (Rangifer tarandus tarandus) has increased in the southern part of the Finnish reindeer herding area because of the recent invasion of a blood-feeding ectoparasitic louse-fly, the deer ked (Lipoptena cervi). We studied the impact of the deer ked on the behaviour of reindeer. Twelve reindeer were infested with a total of 300 keds/reindeer on six occasions in a 5-week period during the deer ked flight season in autumn, while six non-infested reindeer were used as controls. Behavioural patterns indicating potential stress were monitored by visual observation from August to December. The infested reindeer displayed more incidences of restless behaviour than the controls. Shaking and scratching were the most common forms of restless behaviour after infestation of deer keds. Increased grooming was also observed after the transplantation and also later, 1 month after the infestation. Based on the results, the deer ked infestation can cause acute behavioural disturbance in reindeer and, thus, could pose a potential threat to reindeer welfare. Antiparasitic treatment with, e.g. ivermectin, may increase the welfare of parasitized reindeer by reducing deer keds. If the deer ked infestation intensity on the reindeer herding area increases and restless behaviour of reindeer becomes more common, the present results can help in further evaluation of the duration and magnitude of behavioural changes.

Months of asynchrony in offspring production but synchronous adult emergence: the role of diapause in an ectoparasite's life cycle.

Off-host stages of temperate zone ectoparasites must overcome two challenges: coping with unfavorable seasons and synchronizing their life cycles with host availability. In general, little is known about the seasonal cycles of insect ectoparasites of warm-blooded animals. The current study investigates the unusual phenology of a viviparous hippoboscid fly, the deer ked (Lipoptena cervi L.), that parasitizes boreal cervids. Despite months of asynchrony in offspring production, the adults emerge synchronously in mid-August across the northern boreal zone. We examined the role of diapause variation in the synchronization of life cycles by testing adult emergence success and time in relation to offspring birth month (October to April) and with respect to chilling time and photoperiod. Unexpectedly, we found that photoperiod had no role in regulating the life cycle, but diapause was maintained as long as pupae were exposed to cold. Pupae born before February needed a slightly longer exposure to high temperatures to terminate diapause if the cold period was short. Despite the apparent importance of a long period of chilling for life cycle synchrony, it was not required to terminate diapause. This finding of cold mainly preventing, rather than promoting, diapause termination is not novel among temperate insects, but it is rare. Slow diapause termination as a response to exceptionally long exposure to high, not low, temperatures seems to be a cornerstone for synchronizing the life cycle in the deer ked.

Unexpected seasonal variation in offspring size and performance in a viviparous ectoparasite.

Offspring size and performance in invertebrates often decrease with maternal age or as a response to seasonal environment. In viviparous ectoparasites maternal provision may wholly determine offspring performance outside the host. The viviparous deer ked (Lipoptena cervi), an ectoparasite of cervids, breeds from autumn to spring. We reared deer ked pupae through the reproductive period to investigate whether offspring size and performance vary according to maternal age and offspring environment. We expected that, in autumn, young females would produce the largest offspring to ensure that early-born pupae would survive a long period of winter diapause, and that offspring size would decrease with maternal age and decreasing diapause length. Diapause was associated with a significant weight loss, which reduced survival through post-diapause development. It was thus surprising that the early-born offspring were the smallest, and that size and survival (eventually) increased towards the spring. The variability among offspring in the length of off-host period seems to be an important component of life-history evolution in this ectoparasite, and should be studied further. Unexpected seasonal variation in the offspring size of this blood-feeding ectoparasite may result from changes in female resources due to weakening host condition as the winter progresses.

High cold tolerance through four seasons and all free-living stages in an ectoparasite.

Off-host stages of temperate parasites must cope with low temperatures. Cold tolerance is often highest in winter, as a result of diapause and cold acclimation, and low during the active summer stages. In some blood-feeding ectoparasites, offspring provisioning determines cold tolerance through all the non-feeding, off-host stages. Large size increases survival in the cold, but so far seasonal variation in within-female offspring size has not been associated with offspring cold tolerance. The deer ked (Lipoptena cervi) reproduces on cervids from autumn to spring. Newborn pupae drop off the host, facing frosts without any acclimation. We examined cold tolerance through 4 seasons and from birth to adulthood by means of short- and long-term frost exposure. We expected females to produce more tolerant offspring in winter than in spring. Large spring pupae survived prolonged frosts better than did small winter pupae. Thus more tolerant offspring were not produced when the temperature outside the host is at its lowest. Unexpectedly, the freezing points were -20 °C or below all year round. We showed that high cold tolerance is possible without acclimation regardless of life stage, which presumably correlates with other survival characteristics, such as the starvation resistance of free-living ectoparasites.

Geographical variation in host use of a blood-feeding ectoparasitic fly: implications for population invasiveness.

Invasive generalist ectoparasites provide a tool to study factors affecting expansion rates. An increase in the number of host species may facilitate geographic range expansion by increasing the number of suitable habitats and by affecting local extinction and colonization rates. A geographic perspective on parasite host specificity and its implications on range expansion are, however, insufficiently understood. We conducted a field study to explore if divergent host specificity could explain the observed variation in expansion rates between Fennoscandian populations of the deer ked (Lipoptena cervi), which is a blood-feeding ectoparasitic fly of cervids. We found that the rapidly expanding eastern population in Finland appears to specialize on moose, whereas the slowly expanding western population in Norway breeds successfully on both moose and roe deer. The eastern population was also found to utilize the wild forest reindeer as an auxiliary host, but this species is apparently of low value for L. cervi in terms of adult maintenance, reproductive output and offspring quality. Abundant numbers of roe deer and white-tailed deer were observed to be apparently uninfected in Finland, suggesting that host use is not a plastic response to host availability, but rather a consequence of population-level evolutionary changes. Locally compatible hosts were found to be the ones sharing a long history with the deer ked in the area. Cervids that sustained adult deer keds also allowed successful reproduction. Thus, host use is probably determined by the ability of the adult to exploit particular host species. We conclude that a wide host range alone does not account for the high expansion rate or wide geographic distribution of the deer ked, although loose ecological requirements would increase habitat availability.

Experimental infection of the deer ked (Lipoptena cervi) has no negative effects on the physiology of the captive reindeer (Rangifer tarandus tarandus).

The deer ked (Lipoptena cervi) is a haematophagous parasitic fly of cervids that spread to Finland in the early 1960's. Presently its northern distribution limit lies at approximately 65°N and it is gradually spreading northwards. In Finland the principal host species has been the moose (Alces alces), but the deer ked is about to establish contact with another potential host, the semi-domesticated reindeer (Rangifer tarandus tarandus) causing possible threats to reindeer health and management. The aim of this study was to investigate if the deer ked would have an influence on the welfare of the reindeer. Eighteen adult reindeer were divided into three experimental groups: the control group and two infected groups with 300 deer keds per reindeer introduced in August-September. One of the infected groups was treated with subcutaneous ivermectin in November. To gather comprehensive data on potential health hazards caused by the deer ked a wide array of physiological variables was measured during and at the end of the experiment in December. The keds caused no clear changes in the complete blood count, plasma clinical chemistry, amino acids, endocrinology, energy stores, enzyme activities or tissue fatty acid profiles of the host. The haematological, clinical chemical and endocrinological values displayed changes that could be related to the seasonal physiological adaptations of the species. In conclusion, at the duration and intensity of infection that were employed, the effects of the deer ked on the measured physiological variables of the reindeer were insignificant.

Fennoscandian distribution of an important parasite of cervids, the deer ked (Lipoptena cervi), revisited.

The deer ked [Lipoptena cervi (L. 1758) (Dipt., Hippoboscidae)] is a blood-sucking ectoparasite of cervids. The species has been resident in Sweden for more than two centuries, whereas in Finland ( approximately 50 years) and Norway ( approximately 30 years), it has established itself relatively recently. L. cervi may cause serious health problems in its natural hosts, act as a vector for zoonotic diseases, and pose a socioeconomic threat to forest-based activity. In this paper, we review the distribution and former expansion of the species in Fennoscandia. The current distribution of L. cervi appears bimodal, and the geographical range expansion of the species shows notable differences across Fennoscandia. The western population in Norway and Sweden has its northern edge of range at respective latitudes of 61 degrees N and 62 degrees N, whereas the eastern population in Finland reaches 65 degrees N. The future expansion of L. cervi is dependent on several interdependent extrinsic and intrinsic factors. International multidisciplinary collaboration is needed to achieve a synthesis on the factors affecting expansion rates and to understand the effects of L. cervi on wildlife, human health, and the rural societies of Fennoscandia.

Seasonal clines of evolutionarily stable reproductive effort in insects.

For ectotherms, growth and reproduction are possible only during a limited period of the year in seasonal environments. In insects, fitness is generally maximized by producing as many generations as possible within a season, and in many species, the number of generations produced (voltinism) increases with increasing season length. In this study, we analyzed variation in adult life histories in insects along a climatic gradient. The analyzed trait is reproductive effort (resource allocation to reproduction). We begin by formalizing the trade-off between current reproduction and subsequent survival generated by reproductive effort. It appeared that reproductive effort is correlated positively with early fecundity and negatively with lifetime fecundity and life span. Then, deriving from that trade-off, we analyze the evolutionary stability of different schedules of age-specific fecundity that are generated by divergent reproductive effort. The analysis was carried out in season lengths that promote either univoltine or bivoltine phenology. The evolutionarily stable reproductive effort decreases with increasing season length in both phenologies, with a sudden increase when a change from univoltine to partially bivoltine phenology takes place. Reproductive effort responds strongly to changing phenology when density-dependent mortality occurs during diapause and weakly when juvenile mortality is density dependent.