Protein self-marking by emerald ash borer: an evaluation of efficacy and persistence

Understanding the dispersal ability of invasive insects provides useful insights for developing effective management strategies. Historically, methods for marking insects for dispersal studies have been expensive, time-consuming, labor-intensive, and oftentimes ineffective, especially for woodboring beetles. Also, capturing or rearing insects requires human handling, which can alter behavior. Protein immunomarking is a well-established technique for studying the dispersal of insects; however, it has not been applied to woodborers. This study evaluates the potential for using protein immunomarkers applied directly to woodborer-infested trees to mark emerging beetles. Specifically, in the first experiment, we sprayed varying concentrations of ovalbumin (egg white) solution directly onto logs infested with emerald ash borer (EAB), Agrilus planipennis Fairmaire (Coleoptera: Buprestidae, Agrilini). In turn, an enzyme-linked immunosorbent assay was used to detect the presence of protein on emerged beetles. To test the persistence of the mark, we applied varying concentrations of albumin to freeze-killed beetles, mounted them on pins, and placed them over various time intervals in an exposed location outdoors. Adult EAB self-marked as they emerged from protein-treated trees, with higher protein concentrations persisting for longer on the cuticle. This technique offers a convenient, inexpensive, and durable means of marking woodborers and circumvents the need for human handling, allowing for more natural behavior and more realistic estimates of dispersal. Protein self-marking may find application in studies of woodborer dispersal within natural forest environments.     

High dispersal ability and low genetic differentiation in the widespread butterfly species <Emphasis Type="Italic">Melanargia galathea</Emphasis>

Agricultural intensification caused a fragmentation of flower-rich extensively used meadows which resulted in the reduction of the abundance of species of these habitats. The abundance pattern and the dispersal behaviour of species influence the connectivity of local populations. In this context exchange rates can be directly measured by mark release recapture (MRR) studies and indirectly by genetic analysis. Both approaches are used in our study in a comparative way. As a test species to investigate the influence of habitat interconnectivity on a local and regional scale, we selected the butterfly Melanargia galathea (Lepidoptera, Nymphalidae), a widely distributed species, which is common on flower-rich meadows in our study area in western Germany. We marked 3,175 individuals of four neighbouring sites in a mark-release-recapture study and analysed 18 allozyme loci for 644 individuals sampled over 17 sites. Only 3.3% of the total genetic variance was found among samples, thus supporting the detected between-patch movements. Both approaches revealed a high exchange rate among local populations. Moderate between- and high within-patch movements were recorded by MRR analysis, dependent on the geographical distance. The two analytical tools showed high estimated effective population sizes for all populations. In the light of conservation biology, the combination of the MRR and allozyme data support the assumption that high dispersal ability and habitat interconnectivity countervail genetic differentiation and enable the maintenance of a high level of genetic differentiation.     

Marking behaviour of the bahaman hutia (Geocapromys ingrahami)

The marking behaviour of a rare hystricomorph rodent, the Bahaman hutia (Geocapromys ingrahami), was studied in captivity. Hutias were more likely to mark urine-scented sticks than to mark unscented controls. The odour of conspecific urine readily induced marking and the sight and/or odour of an animal marking often immediately led to marking by other animals. Marking was exhibited by both males and females regardless of whether females were in oestrus. Olfactory investigation and marking by males was more intense, however, in the presence of oestrous females or their scent. Marking appears to be primarily a non-agonistic, social behaviour which may be important in the social organization of this gregarious, nocturnal species.     

Handstand Scent Marking in the Dwarf Mongoose (Helogale parvula)

Many mammal species adopt marking postures that elevate their scent deposits. The most extreme of these is handstand marking, in which an individual reverses against an upright object, flings its hind legs into the air above its back and balances bipedally on its fore feet. The resulting anogenital deposit is thus raised one full body length above ground level. It has been suggested that this energetically costly form of marking serves to provide conspecifics with information about the marker's body size and hence competitive ability. However, this explanation assumes that the height of an individuals’ deposit does reflect accurately its body size, an assumption that has never been tested in any hand‐standing species. This study investigated the relationship between body size and handstand mark height in a wild population of dwarf mongooses (Helogale parvula) in South Africa. We found that although body size and marking height were correlated positively for female dwarf mongooses, they were not related for males. Male dwarf mongooses (who are subject to intrasexual competition from outside their group) invested more heavily in anogenital range marking, marking at three times the female frequency and placing their deposits significantly higher than females (although they were not dimorphic). Males that were particularly vulnerable to rivals (i.e. those that were small for their age) tended to mark higher than more robust age‐mates, in keeping with the predictions of Adams & Mesterton‐Gibbons’ (1995, J. Theor. Biol.175, 405–421). model of deceptive threat communication. These findings suggest strongly that the height of anogenital scent deposits is of social significance to dwarf mongooses.     

Dispersal and gene flow in the rare, parasitic Large Blue butterfly Maculinea arion

Dispersal is crucial for gene flow and often determines the long‐term stability of meta‐populations, particularly in rare species with specialized life cycles. Such species are often foci of conservation efforts because they suffer disproportionally from degradation and fragmentation of their habitat. However, detailed knowledge of effective gene flow through dispersal is often missing, so that conservation strategies have to be based on mark–recapture observations that are suspected to be poor predictors of long‐distance dispersal. These constraints have been especially severe in the study of butterfly populations, where microsatellite markers have been difficult to develop. We used eight microsatellite markers to analyse genetic population structure of the Large Blue butterfly Maculinea arion in Sweden. During recent decades, this species has become an icon of insect conservation after massive decline throughout Europe and extinction in Britain followed by reintroduction of a seed population from the Swedish island of Öland. We find that populations are highly structured genetically, but that gene flow occurs over distances 15 times longer than the maximum distance recorded from mark–recapture studies, which can only be explained by maximum dispersal distances at least twice as large as previously accepted. However, we also find evidence that gaps between sites with suitable habitat exceeding ～20 km induce genetic erosion that can be detected from bottleneck analyses. Although further work is needed, our results suggest that M. arion can maintain fully functional metapopulations when they consist of optimal habitat patches that are no further apart than ～10 km.     

Inter-population dispersal by adult stoneflies detected by stable isotope enrichment

1. Dispersal of adult stream insects may be of considerable importance in regional population dynamics and colonisation of new sites, but quantifying the rate and extent of dispersal is difficult. 2. We used stable isotope (¹⁵N) enrichment to mark more than 1.5 million larval stoneflies (Leuctra inermis) before they emerged from an upland stream in the Plynlimon area of mid‐Wales, in order to determine directly the rate and pattern of inter‐site dispersal. 3. A small number of isotopically enriched adult stoneflies were captured in samples taken at adjacent streams between 800 m and 1.1 km away from the source population, including a headwater of a different river system. 4. The distribution of marked individuals suggested that wind influences dispersal direction in the uplands, but the low number of captures limits our ability to draw firm conclusions. 5. This is the first direct demonstration of dispersal of insects between streams. The dispersal distances recorded were significantly greater than those suggested by previous direct studies, but much more consistent with indirect studies based on genetic differentiation of populations.     

How limited is dispersal in the rare beetle, Cryptocephalus decemmaculatus (Chrysomelidae, Cryptocephalinae)?

As suitable habitat becomes increasingly fragmented the ability of a species to reach new areas may often dictate whether populations persist or perish. An understanding of dispersal ability is a prerequisite for informed management decisions. This is particularly true for species that have become restricted to one or a small number of sites, as is the case for several species of Cryptocephalus beetle in the UK. Using mark–release–recapture, host-plant marking and direct observations we investigated population size, movement through suitable habitat and the flight behaviour of Cryptocephalus decemmaculatus. In the UK this species is known from only two sites and it is listed as a priority species on the UK Biodiversity Action Plan. At the time of the study, the one known English site for this species supported a population of ~500 individuals. The adult beetles move through their habitat using suitable host-plants as ‘stepping stones’. There appears to be no interchange of adults between sub-populations that are separated by small areas of unsuitable habitat (e.g. small tracts of woodland or areas devoid of scrub), a result reinforced by studies of genetic differentiation between sub-populations. The small population size of this beetle and its association with, mid-successional habitats makes it vulnerable to local extinction. Furthermore, its limited dispersal ability means that other habitat patches are unlikely ever to be colonised naturally.     

Population Structure of the Chagas Disease Vector Triatoma infestans in an Urban Environment

Chagas disease is a vector-borne disease endemic in Latin America. Triatoma infestans, a common vector of this disease, has recently expanded its range into rapidly developing cities of Latin America. We aim to identify the environmental features that affect the colonization and dispersal of T. infestans in an urban environment. We amplified 13 commonly used microsatellites from 180 T. infestans samples collected from a sampled transect in the city of Arequipa, Peru, in 2007 and 2011. We assessed the clustering of subpopulations and the effect of distance, sampling year, and city block location on genetic distance among pairs of insects. Despite evidence of genetic similarity, the majority of city blocks are characterized by one dominant insect genotype, suggesting the existence of barriers to dispersal. Our analyses show that streets represent an important barrier to the colonization and dispersion of T. infestans in Arequipa. The genetic data describe a T. infestans infestation history characterized by persistent local dispersal and occasional long-distance migration events that partially parallels the history of urban development.     

Non-Invasive Genetic Mark-Recapture as a Means to Study Population Sizes and Marking Behaviour of the Elusive Eurasian Otter (Lutra lutra)

Quantifying population status is a key objective in many ecological studies, but is often difficult to achieve for cryptic or elusive species. Here, non-invasive genetic capture-mark-recapture (CMR) methods have become a very important tool to estimate population parameters, such as population size and sex ratio. The Eurasian otter (Lutra lutra) is such an elusive species of management concern and is increasingly studied using faecal-based genetic sampling. For unbiased sex ratios or population size estimates, the marking behaviour of otters has to be taken into account. Using 2132 otter faeces of a wild otter population in Upper Lusatia (Saxony, Germany) collected over six years (2006–2012), we studied the marking behaviour and applied closed population CMR models accounting for genetic misidentification to estimate population sizes and sex ratios. We detected a sex difference in the marking behaviour of otters with jelly samples being more often defecated by males and placed actively exposed on frequently used marking sites. Since jelly samples are of higher DNA quality, it is important to not only concentrate on this kind of samples or marking sites and to invest in sufficiently high numbers of repetitions of non-jelly samples to ensure an unbiased sex ratio. Furthermore, otters seemed to increase marking intensity due to the handling of their spraints, hence accounting for this behavioural response could be important. We provided the first precise population size estimate with confidence intervals for Upper Lusatia (for 2012: N^ = 20 ± 2.1, 95% CI = 16–25) and showed that spraint densities are not a reliable index for abundances. We further demonstrated that when minks live in sympatry with otters and have comparably high densities, a non-negligible number of supposed otter samples are actually of mink origin. This could severely bias results of otter monitoring if samples are not genetically identified.     

Quantifying interspecific variation in dispersal ability of noctuid moths using an advanced tethered flight technique

Dispersal plays a crucial role in many aspects of species' life histories, yet is often difficult to measure directly. This is particularly true for many insects, especially nocturnal species (e.g. moths) that cannot be easily observed under natural field conditions. Consequently, over the past five decades, laboratory tethered flight techniques have been developed as a means of measuring insect flight duration and speed. However, these previous designs have tended to focus on single species (typically migrant pests), and here we describe an improved apparatus that allows the study of flight ability in a wide range of insect body sizes and types. Obtaining dispersal information from a range of species is crucial for understanding insect population dynamics and range shifts. Our new laboratory tethered flight apparatus automatically records flight duration, speed, and distance of individual insects. The rotational tethered flight mill has very low friction and the arm to which flying insects are attached is extremely lightweight while remaining rigid and strong, permitting both small and large insects to be studied. The apparatus is compact and thus allows many individuals to be studied simultaneously under controlled laboratory conditions. We demonstrate the performance of the apparatus by using the mills to assess the flight capability of 24 species of British noctuid moths, ranging in size from 12–27 mm forewing length (~40–660 mg body mass). We validate the new technique by comparing our tethered flight data with existing information on dispersal ability of noctuids from the published literature and expert opinion. Values for tethered flight variables were in agreement with existing knowledge of dispersal ability in these species, supporting the use of this method to quantify dispersal in insects. Importantly, this new technology opens up the potential to investigate genetic and environmental factors affecting insect dispersal among a wide range of species.     

A comparison of mark–release–recapture methods for estimating colony size in the wood ant Formica lugubris

Colony size can be considered the analogue of the body size of a superorganism. Just as body size is important to the physiology of an individual animal, colony size correlates with the life-history and ecology of social insects. Although nest excavation and counting all individuals is the most accurate method for estimating colony size (or nest size), it has the major drawback of being destructive. Alternatively, mark–release–recapture (MRR) can be used repeatedly to measure the size of the same colony or nest. We compared the accuracy and feasibility of four MRR methods and a Mound-Volume method with complete counts from nest excavation for estimating the nest size of F. lugubris, a mound-building wood ant of the Formica rufa group, during the early spring in Scotland. We found that our After-Disturbing method, in which we performed marking and recapturing after gentle disturbance to the top of nest mound, has the best balance between accuracy, non-destructiveness, and time required. We also found that mound volume can be an index of ant nest size under certain conditions. Both non-destructive methods can be used on the same colony or nest repeatedly to monitor nest dynamics.     

Field Methods for Capturing and Marking Azarai Night Monkeys

Long-term behavioral studies require the permanent identification of individuals. The need for individual identification is even more crucial for sexually monomorphic species since not even the sexes can be differentiated by the field observer. Owl monkeys (Aotus spp.) are sexually monomorphic primates inhabiting the forests of Central and South America. We report here on the methods and drug dosages used to capture, mark, and identify individual owl monkeys (Aotus azarai azarai) in Eastern Formosa, Argentina. We successfully captured 70 owl monkeys using blowpipes or a CO₂ rifle, but attempts to capture them with baited traps proved unsuccessful. During the marking and collaring procedures, we gave individuals on average a total of 50 mg of ketamine hydrochloride, including the dose in the dart. To mark them, we freeze-branded portions of their tails and fitted them with radio or bead collars. There was no death or physical life-threatening injury while capturing or marking individuals. The procedures we describe should allow one to safely capture and to mark small arboreal primates when trapping is not possible.     

Foraging Area Marking in Two Related Tetramorium Ant Species (Hymenoptera: Formicidae)

The related ants Tetramorium caespitum and T. impurum mark their foraging area in a species-specific, home range and short-lasting manner. Indeed, ants reaching a new area have a slow linear speed which increases during the marking. Conspecific ants are arrested and attracted by marked areas, while heterospecific ants are reluctant to visit them. However, when the latter do visit marked areas, they move more quickly and less sinuously than conspecific ants and do not stay on the areas. The marking is performed in about 3 min by T. caespitum and in 3 to 6 min by T. impurum. If not reinforced, the marking vanishes in the same time intervals. Neither poison gland nor last sternite extracts reproduce the activity of naturally marked areas, whereas a Dufour gland extract does exactly that. Foraging ants touch the ground with the tip of their gaster. Consequently, we can postulate that the workers mark their foraging area with the contents of this gland, which is associated with the sting apparatus, and that they deposit with the extremity of the gaster. Alien conspecific ants are seldom aggressive to one another, even on marked areas. When encountering each other on unmarked areas, heterospecific ants present some aggressive reactions. On marked areas, their aggressiveness is enhanced and intruder ants are restless, while resident ones walk freely. On ground marked by T. impurum, ants of this species are more aggressive than antagonistic T. caespitum workers. The marking of foraging areas thus induces defense against heterospecifics but not against conspecific ants.     

Who are we sampling? Apparent survival differs between methods in a secretive species

Survival is a fundamental parameter in population dynamics with increasing importance in the management and conservation strategies of wildlife populations. Survival probability in vertebrates is usually estimated by live‐encounter data obtained by means of physical mark–capture–recapture protocols. Non‐invasive acoustic marking relying on individual‐specific features of signals has been alternatively applied as a marking technique, especially in secretive species. Nevertheless, to date no research has compared survival rate estimates obtained by acoustic and physical marking. We estimated half‐yearly and annual survival and recapture rates of a secretive and threatened passerine, the Dupont's lark Chersophilus duponti, using two separate live‐encounter data sets of males collected simultaneously by physical and acoustic marking in the same study area. The separate analysis of both methods led to different model structures, since transient individuals had to be accounted for in the acoustic marking but not in the physical marking data set. Furthermore, while reencounter probabilities did not differ between methods, survival estimates employing physical marking were lower than those obtained acoustically, especially between the postbreeding and the breeding period when the apparent survival of colour‐banded birds was twice as low as for acoustic marking. The combination of marking methods suggested the existence of different subsets of individuals differentially sampled within the population: whereas colour‐banded males seemed to represent the territorial fraction of the population, both resident and floater individuals were probably detected by acoustic marking. Using traditional mark–recapture methods exclusively could have misled our estimates of survival rates, potentially affecting prospective predictions of population dynamics. Acoustic marking has been poorly applied in mark–recapture studies, but might be a powerful complement to obtain accurate estimates of fundamental demographic parameters such as survival and dispersal.     

Marking of Nest Entrances and Vicinity in Two Related Tetramorium Ant Species (Hymenoptera: Formicidae)

Workers of the related ants Tetramorium impurum and T. caespitum mark the vicinity of their nest entrances in a species-specific manner, as seen by similarities between the behavior of nestmates and that of alien conspecifics (e.g., concerning aggregation, locomotion, orientation, tendency to move, and agonistic behavior). Additionally, they mark the inside of their nest entrances in a colony-specific manner, as seen by the following differences in behavior. Nestmates aggregate on these areas, walk rather slowly, but freely and essentially in the middle of the areas, come toward and very near such areas, are not inclined to escape, and are ready to attack possible intruders. Alien conspecifics do not aggregate, walk quickly, and are reluctant to stay on the areas, come neither toward nor very near the areas, are inclined to escape, and often open their mandibles, mainly when in front of a resident. The marking of the nest entrances is performed by T. impurum in 30 min and by T. caespitum in 15 min. If not reinforced, the marking by both species vanishes in 60 and 50 min, respectively. Extracts of hindlegs, metathorax, or metapleural glands produce in unmarked areas the ethological effect of marked entrances. It may be hypothesized that the marking factor is produced by the workers' metapleural glands and deposited onto the ground, via the hindlegs of ants leaving the nest. A worker's head has a species- but not a colony-specific ethological effect. An isolated alien conspecific's head is never attacked, whereas a thorax with abdomen is. This explains why, by opening its mandibles (and then presumably emitting a mandibular gland pheromone), a conspecific ant momentarily inhibits the attack of a nonnestmate. According to Hölldobler and Wilson (1990), the marking of the inside of T. impurum and T. caespitum nest entrances is a territorial and nest-entrance marking, whereas the marking of the close vicinity of the entrances is a home-range marking, as is the marking of the foraging area. These markings are in accordance with the fact that T. impurum foragers deposit their trail pheromone as far as the opening of the nest entrance.     

Understanding Bactrocera dorsalis trapping to calibrate area-wide management

Knowing the dispersal of released insects and estimating the size of field populations are keys to the successful implementation of area-wide management (AWM) programmes based on the sterile insect technique (SIT), as they determine the release strategy of sterile males. Mark–release–recapture (MRR) is a common method used to estimate field populations and spatiotemporal dynamics. However, the extent to which the pest is attracted to lures is often difficult to identify, thereby biasing extrapolation to movement patterns and population size. We performed MRR experiments on the Oriental fruit fly, Bactrocera dorsalis (Hendel) (Diptera: Tephritidae), in a fruit-growing area in Senegal. Methyl eugenol and protein baits were used to trap males and females, respectively. After studying the suitability of marking B. dorsalis with fluorescent pigments at the laboratory, two releases of marked sterile flies were organized in the centre of an organic mango orchard, first in the late mango fruiting stage and second in the fruit setting stage. Traps were placed symmetrically along a 250 and 500 m radius from the release point. A very small fraction of the released individuals was recaptured: 0.45% in the first release and 3.08% in the second. Trapping of both sterile and wild flies was completely anisotropic. Sterile flies were mostly trapped at a relatively short distance (250 m) from the release point, in the first two days. Male trapping using methyl eugenol was highly effective, whereas the response of females to food bait traps was low. The direction of the wind was the main driver of recapture, with flies heading upwind. The results underline the importance of taking the odour plume around the traps into account when estimating populations, and the heterogeneous spread of the wild population in the landscape for the set-up of the release strategy of sterile insects for SIT-based AWM.     

Where have all the tadpoles gone? Individual genetic tracking of amphibian larvae until adulthood

Reliably marking larvae and reidentifying them after metamorphosis is a challenge that has hampered studies on recruitment, dispersal, migration and survivorship of amphibians for a long time, as conventional tags are not reliably retained through metamorphosis. Molecular methods allow unique genetic fingerprints to be established for individuals. Although microsatellite markers have successfully been applied in mark–recapture studies on several animal species, they have never been previously used in amphibians to follow individuals across different life cycle stages. Here, we evaluate microsatellites for genetic across‐stages mark–recapture studies in amphibians and test the suitability of available software packages for genotype matching. We sampled tadpoles of the dendrobatid frog Allobates femoralis, which we introduced on a river island in the Nature Reserve ‘Les Nouragues’ in French Guiana. In two subsequent recapture sessions, we searched for surviving juveniles and adults, respectively. All individuals were genotyped at 14 highly variable microsatellite loci, which yielded unique genetic fingerprints for all individuals. We found large differences in the identification success of the programs tested. The pairwise‐relatedness‐based approach, conducted with the programs kingroup or ML‐Relate, performed best with our data set. Matching ventral patterns of juveniles and adult individuals acted as a control for the reliability of the genetic identification. Our results demonstrate that microsatellite markers are a highly powerful tool for studying amphibian populations on an individual basis. The ability to individually track amphibian tadpoles throughout metamorphosis until adulthood will be of substantial value for future studies on amphibian population ecology and evolution.     

Measuring the dispersal of saproxylic insects: a key characteristic for their conservation

In the discipline of nature conservation it is important to understand under which circumstances populations can survive by compensating local extinctions with colonizations. Many saproxylic (= wood-dwelling) insect species have declining populations and are regarded as threatened due to low habitat availability in managed forests. Several methods have been used to better understand the dispersal biology and colonization ability of saproxylic insects with declining populations. The present article summarizes and compares the results of such studies. When the same species have been studied using several methods, the results are consistent, but different aspects of dispersal biology are revealed with different methods. Capture-recapture and telemetry are direct methods that can be used to quantify dispersal rate and range in the field. Studies of genetic structure and occupancy patterns are complementary, as they reveal the consequences of dispersals that have taken place over a larger spatial and temporal scale than is possible to study with direct methods. Because colonization, rather than dispersal, is important for population persistence, colonization experiments provide useful information. To obtain information relevant for conservation work, dispersal studies should be conducted on model species that are representative of threatened species. Colonization ability probability differs between common and rare species, and therefore it is important to also study the dispersal of rare species, even if it is more difficult.     

Marking through molts: An evaluation of visible implant elastomer to permanently mark individuals in a lower termite species

1. Advances in individual marking methods have facilitated detailed studies of animal populations and behavior as they allow tracking of individuals through time and space. Hemimetabolous insects, representing a wide range of commonly used model organisms, present a unique challenge to individual marking as they are not only generally small‐bodied, but also molt throughout development, meaning that traditional surface marks are not persistent.
2. Visible implant elastomer (VIE) offers a potential solution as small amounts of the inert polymer can be implanted under the skin or cuticle of an animal. VIE has proved useful for individually marking fish, crustaceans, and amphibians in both field and laboratory studies and has recently been successfully trialed in laboratory populations of worms and fly larvae. We trialed VIE in the single‐piece nesting termite Zootermopsis angusticollis, a small hemimetabolous insect.
3. We found that there was no effect of VIE on survival and that marks persisted following molting. However, we found some evidence that marked termites performed less allogrooming and trophallaxis than controls, although effect sizes were very small.
4. Our study suggests that VIE is an effective technique for marking small hemimetabolous insects like termites but we advocate that caution is applied, particularly when behavioral observation is important.

     

Migration and dispersal patterns of bats and their influence on genetic structure

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