Pollen metabarcoding as a tool for tracking long‐distance insect migrations

Insects account for a large portion of Earth's biodiversity and are key players for ecosystems, notably as pollinators. While insect migration is suspected to represent a natural phenomenon of major importance, remarkably little is known about it, except for a few flagship species. The reason for this situation is mainly due to technical limitations in the study of insect movement. Here, we propose using metabarcoding of pollen carried by insects as a method for tracking their migrations. We developed a flexible and simple protocol allowing efficient multiplexing and not requiring DNA extraction, one of the most time‐consuming part of metabarcoding protocols, and apply this method to the study of the long‐distance migration of the butterfly Vanessa cardui, an emerging model for insect migration. We collected 47 butterfly samples along the Mediterranean coast of Spain in spring and performed metabarcoding of pollen collected from their bodies to test for potential arrivals from the African continent. In total, we detected 157 plant species from 23 orders, most of which (82.8%) were insect‐pollinated. Taxa present in Africa–Arabia represented 73.2% of our data set, and 19.1% were endemic to this region, strongly supporting the hypothesis that migratory butterflies colonize southern Europe from Africa in spring. Moreover, our data suggest that a northwards trans‐Saharan migration in spring is plausible for early arrivals (February) into Europe, as shown by the presence of Saharan floristic elements. Our results demonstrate the possibility of regular insect‐mediated transcontinental pollination, with potential implications for ecosystem functioning, agriculture and plant phylogeography.     

Migration in butterflies: a global overview

Insect populations including butterflies are declining worldwide, and they are becoming an urgent conservation priority in many regions. Understanding which butterfly species migrate is critical to planning for their conservation, because management actions for migrants need to be coordinated across time and space. Yet, while migration appears to be widespread among butterflies, its prevalence, as well as its taxonomic and geographic distribution are poorly understood. The study of insect migration is hampered by their small size and the difficulty of tracking individuals over long distances. Here we review the literature on migration in butterflies, one of the best-known insect groups. We find that nearly 600 butterfly species show evidence of migratory movements. Indeed, the rate of ‘discovery’ of migratory movements in butterflies suggests that many more species might in fact be migratory. Butterfly migration occurs across all families, in tropical as well as temperate taxa; Nymphalidae has more migratory species than any other family (275 species), and Pieridae has the highest proportion of migrants (13%; 133 species). Some 13 lines of evidence have been used to ascribe migration status in the literature, but only a single line of evidence is available for 92% of the migratory species identified, with four or more lines of evidence available for only 10 species – all from the Pieridae and Nymphalidae. Migratory butterflies occur worldwide, although the geographic distribution of migration in butterflies is poorly resolved, with most data so far coming from Europe, USA, and Australia. Migration is much more widespread in butterflies than previously realised – extending far beyond the well-known examples of the monarch Danaus plexippus and the painted lady Vanessa cardui – and actions to conserve butterflies and insects in general must account for the spatial dependencies introduced by migratory movements.     

The effects of long‐distance migration on the evolution of moult strategies in Western‐Palearctic passerines

Although feathers are the unifying characteristic of all birds, our understanding of the causes, mechanisms, patterns and consequences of the feather moult process lags behind that of other major avian life‐history phenomena such as reproduction and long‐distance migration. Migration, which evolved in many species of the temperate and arctic zones, requires high energy expenditure to endure long‐distance journeys. About a third of Western‐Palearctic passerines perform long‐distance migrations of thousands of kilometres each year using various morphological, physiological, biomechanical, behavioural and life‐history adaptations. The need to include the largely non‐overlapping breeding, long‐distance migration and feather moult processes within the annual cycle imposes a substantial constraint on the time over which the moult process can take place. Here, we review four feather‐moult‐related adaptations which, likely due to time constraints, evolved among long‐distance Western‐Palearctic migrants: (i) increased moult speed; (ii) increased overlap between moult and breeding or migration; (iii) decreased extent of plumage moult; and (iv) moult of part or all of the plumage during the over‐wintering period in the tropics rather than in the breeding areas. We suggest that long‐distance migration shaped the evolution of moult strategies and increased the diversity of these strategies among migratory passerines. In contrast to this variation, all resident passerines in the Western Palearctic moult immediately after breeding by renewing the entire plumage of adults and in some species also juveniles, while in other species juvenile moult is partial. We identify important gaps in our current understanding of the moult process that should be addressed in the future. Notably, previous studies suggested that the ancestral moult strategy is a post‐breeding summer moult in the Western Palearctic breeding areas and that moult during the winter evolved due to the scheduling of long‐distance migration immediately after breeding. We offer an alternative hypothesis based on the notion of southern ancestry, proposing that the ancestral moult strategy was a complete moult during the ‘northern winter’ in the Afro‐tropical region in these species, for both adults and juveniles. An important aspect of the observed variation in moult strategies relates to their control mechanisms and we suggest that there is insufficient knowledge regarding the physiological mechanisms that are involved, and whether they are genetically fixed or shaped by environmental factors. Finally, research effort is needed on how global climate changes may influence avian annual routines by altering the scheduling of major processes such as long‐distance migration and feather moult.     

The frequency of wing damage in a migrating butterfly

The ability to fly is crucial for migratory insects. Consequently, the accumulation of damage on the wings over time can affect survival, especially for species that travel long distances. We examined the frequency of irreversible wing damage in the migratory butterfly Vanessa cardui to explore the effect of wing structure on wing damage frequency, as well as the mechanisms that might mitigate wing damage. An exceptionally high migration rate driven by high precipitation levels in their larval habitats in the winter of 2018–2019 provided us with an excellent opportunity to collect data on the frequency of naturally occurring wing damage associated with long-distance flights. Digital images of 135 individuals of V. cardui were collected and analyzed in Germany. The results show that the hindwings experienced a greater frequency of damage than the forewings. Moreover, forewings experienced more severe damage on the lateral margin, whereas hindwings experienced more damage on the trailing margin. The frequency of wing margin damage was higher in the painted lady butterfly than in the migrating monarch butterfly and in the butterfly Pontia occidentalis following artificially induced wing collisions. The results of this study could be used in future comparative studies of patterns of wing damage in butterflies and other insects. Additional studies are needed to clarify whether the strategies for coping with wing damage differ between migratory and nonmigratory species.     

Phytophagous insect-woody sprout interactions in tropical eucalypt forest. II. Insect community structure

Abstract Sucking insects constituted 79% of all phytophagous insects collected from woody sprouts in the ground layer of a tropical eucalypt forest. Mobile insect groups such as non-psyllid Hemiptera and Orthoptera were relatively frequent in this environment compared to temperate, Eucalyptus-dominated vegetation. The high fire frequency of the tropical eucalypt forest may favour mobile insect groups. The capture of sucking insects and caterpillars peaked in dry season samples. Other patterns of abundance of phytophagous insect groups showed little consistency in their seasonal trends between host species or between vegetation types within host species. Disparities between chewing insect abundance in daytime samples and the damage chewing insects cause, may result from disproportionate consumption by large, mainly nocturnal insects, such as members of the Orthoptera. In this study, 21% of insect species were specialists on single plant species. This study suggested that insect abundance reflected the growth patterns of woody sprouts after regular burning, rather than that plant growth and development were tuned to the pressures of insect herbivory.     

Effects of landscape and management on ground‐dwelling insect assemblages of farmland in Jeju Island,Korea

Granite‐derived soils are widespread in the farmland of Korea in general. In contrast, Jeju Island has mainly volcanic ash soils. Soils and weather condition in Jeju Island created a unique agricultural system. We identified the features of ground‐dwelling insects in farmlands of Jeju Island. This study was conducted in four areas (Samdal‐ri and Susan‐ri in Seogwipo city, and Dongmyeong‐ri and Suwon‐ri in Jeju city) in Jeju Island, Korea. Field surveys were carried out twice in summer (June) and autumn (September) in 2013. Ground‐dwelling insects were sampled quantitatively by using pitfall traps. As a result, in total 3322 individuals, 137 species, 48 families and 8 orders were investigated in farmlands of Jeju Island. Especially, members of Coleoptera and Hymenoptera accounted for a large proportion of ground‐dwelling insect communities. The numbers of species and individuals for major taxonomic groups showed significant regional and seasonal differences. This study implied that the seasonal and regional differences of ground‐dwelling insect communities were affected by surrounding land use patterns, life history patterns of each taxonomic group and farmland management.     

Migration strategies and annual space‐use in an Afro‐Palaearctic aerial insectivore – the European nightjar Caprimulgus europaeus

Obligate insectivorous birds breeding in high latitudes travel thousands of kilometres during annual movements to track the local seasonal peaks of food abundance in a continuously fluctuating resource landscape. Avian migrants use an array of strategies when conducting these movements depending on e.g. morphology, life history traits and environmental factors encountered en route. Here we used geolocators to derive data on the annual space‐use, temporal pattern and migratory strategies in an Afro‐Palaearctic aerial insectivorous bird species – the European nightjar Caprimulgus europaeus. More specifically, we aimed to test a set of hypothesises pertaining to the migration of a population of nightjars breeding in south‐eastern Sweden. We found that the birds wintered across the central and western parts of the southern tropical Africa almost entirely outside the currently described wintering range of the species. The nightjars performed a narrow loop migration across Sahara, with spring Sahel stopovers significantly to the west of autumn stops indicative to an adaptive response to winds during migration. To our surprise, the migration speed was faster in the autumn (119 km d^{? 1}) than in the spring (99 km d^{? 1}), possibly due to the prevailing wind regimes over the Sahara. The estimated flight fraction in both autumn (14%) and spring (12%) was almost exactly as the theoretically predicted 1:7 time relationship between flights and stopovers for small birds. The temporal patterns within the annual cycle indicate that individuals follow alternative spatiotemporal schedules that converge towards the breeding season. The positive relationship between the spatially and temporally distant winter departure and breeding arrival suggests that individuals´ temporal fine‐tuning to breeding may be constrained, leading to potential negative fitness consequences.     

Niche-tracking migrants and niche-switching residents: evolution of climatic niches in New World warblers (Parulidae)

Differences in life-history traits between tropical and temperate lineages are often attributed to differences in their climatic niche dynamics. For example, the more frequent appearance of migratory behaviour in temperate-breeding species than in species originally breeding in the tropics is believed to have resulted partly from tropical climatic stability and niche conservatism constraining tropical species from shifting their ranges. However, little is known about the patterns and processes underlying climatic niche evolution in migrant and resident animals. We evaluated the evolution of overlap in climatic niches between seasons and its relationship to migratory behaviour in the Parulidae, a family of New World passerine birds. We used ordination methods to measure seasonal niche overlap and niche breadth of 54 resident and 49 migrant species and used phylogenetic comparative methods to assess patterns of climatic niche evolution. We found that despite travelling thousands of kilometres, migrants tracked climatic conditions across the year to a greater extent than tropical residents. Migrant species had wider niches than resident species, although residents as a group occupied a wider climatic space and niches of migrants and residents overlapped extensively. Neither breeding latitude nor migratory distance explained variation among species in climatic niche overlap between seasons. Our findings support the notion that tropical species have narrower niches than temperate-breeders, but does not necessarily constrain their ability to shift or expand their geographical ranges and become migratory. Overall, the tropics may have been historically less likely to experience the suite of components that generate strong selection pressures for the evolution of migratory behaviour.     

Histories of host shifts and cospeciation among free‐living parasitoids of Rhagoletis flies

Host shifts by specialist insects can lead to reproductive isolation between insect populations that use different hosts, promoting diversification. When both a phytophagous insect and its ancestrally associated parasitoid shift to the same novel host plant, they may cospeciate. However, because adult parasitoids are free living, they can also colonize novel host insects and diversify independent of their ancestral host insect. Although shifts of parasitoids to new insect hosts have been documented in ecological time, the long‐term importance of such shifts to parasitoid diversity has not been evaluated. We used a genus of flies with a history of speciation via host shifting (Rhagoletis [Diptera: Tephritidae]) and three associated hymenopteran parasitoid genera (Diachasma, Coptera and Utetes) to examine cophylogenetic relationships between parasitoids and their host insects. We inferred phylogenies of Rhagoletis, Diachasma, Coptera and Utetes and used distance‐based cophylogenetic methods (ParaFit and PACo) to assess congruence between fly and parasitoid trees. We used an event‐based method with a free‐living parasitoid cost model to reconstruct cophylogenetic histories of each parasitoid genus and Rhagoletis. We found that the current species diversity and host–parasitoid associations between the Rhagoletis flies and parasitoids are the primary result of ancient cospeciation events. Parasitoid shifts to ancestrally unrelated hosts primarily occur near the branch tips, suggesting that host shifts contribute to recent parasitoid species diversity but that these lineages may not persist over longer time periods. Our analyses also stress the importance of biologically informed cost models when investigating the coevolutionary histories of hosts and free‐living parasitoids.     

Multi‐decadal trends in spring arrival of avian migrants to the central Arctic coast of Alaska: effects of environmental and ecological factors

Warming in the Arctic has caused the transition from winter to summer to occur weeks earlier over the last half century, yet little is known about whether avian migrants have altered their timing of arrival on breeding areas to match this earlier seasonal transition. Over a 50‐yr period, we examined trends in the timing of the first arrival for 16 avian migrant species at the terminus of their northward migration along the central Arctic coast of Alaska and compared these trends to factors potentially influencing migration phenology. Date of first arrival occurred an average of 0.12 d yr^?1 or 6 d (range = 3–10 d) earlier across all species and did not differ significantly among species between 1964 and 2013. Local climatic variables, particularly temperature, had a greater effect on a species first arrival date than did large‐scale climatic predictors. First arrival date was 1.03 d earlier for every 1°C annual change in temperature, but there was nearly a 2‐fold difference in the range of responses across species (0.69–1.33 d °C^?1), implying that some species did better than others at timing their arrival with changing temperature. There was weak support for an influence of foraging strategy, migration distance, and flight path on timing of first arrival. Our findings, like others from temperate latitudes, indicate that avian migrants are responsive to changing environmental conditions, though some species appear to be more adaptive than others.     

Long‐range seasonal migration in insects: mechanisms,evolutionary drivers and ecological consequences

Myriad tiny insect species take to the air to engage in windborne migration, but entomology also has its ‘charismatic megafauna’ of butterflies, large moths, dragonflies and locusts. The spectacular migrations of large day‐flying insects have long fascinated humankind, and since the advent of radar entomology much has been revealed about high‐altitude night‐time insect migrations. Over the last decade, there have been significant advances in insect migration research, which we review here. In particular, we highlight: (1) notable improvements in our understanding of lepidopteran navigation strategies, including the hitherto unsuspected capabilities of high‐altitude migrants to select favourable winds and orientate adaptively, (2) progress in unravelling the neuronal mechanisms underlying sun compass orientation and in identifying the genetic complex underpinning key traits associated with migration behaviour and performance in the monarch butterfly, and (3) improvements in our knowledge of the multifaceted interactions between disease agents and insect migrants, in terms of direct effects on migration success and pathogen spread, and indirect effects on the evolution of migratory systems. We conclude by highlighting the progress that can be made through inter‐phyla comparisons, and identify future research areas that will enhance our understanding of insect migration strategies within an eco‐evolutionary perspective.     

Flies on vacation: evidence for the migration of Australian Syrphidae (Diptera)

1. Hover flies (Syrphidae: Diptera) are a cosmopolitan group of insects that provide important ecosystem services including pollination and pest control. The seasonal migration of hover flies is probably best known in Europe, but it remains unstudied in many other parts of the world. 2. Australia is believed to be home to around 160 hover fly species, some of which are common in urban and agricultural environments. The current evidence for hover fly migration in Australia is scarce and anecdotal, yet migration may be critical to the success of pollination and the biological control of aphids. 3. In this study, species occurrence records from an online biodiversity database (Atlas of Living Australia) were used to look for evidence of migratory behaviours in all Australian hover flies with more than 200 occurrence records. 4. Four of the 10 species displayed seasonal changes in their distribution consistent with migration, including Australia's two most abundant species: Melangyna viridiceps and Simosyrphus grandicornis. This work is an important first step in understanding the prevalence of migration in Australian hover flies. However, confirmation of our findings requires additional evidence to rule out other plausible explanations for the observed patterns. 5. Based on changes in summer and winter latitudinal distribution, it is estimated that some Australian hover flies may make annual migrations of 400–1800 km. 6. This work suggests that the management of beneficial insects requires consideration of factors at both local and continental scales, as landscape use changes may have an impact on ecosystem services delivered hundreds of kilometres away.     

The Relationship Between Habitat Selection and Preference for Adult and Larval Food Resources in the Polyphagous Butterfly <Emphasis Type="Italic">Vanessa cardui</Emphasis> (Lepidoptera: Nymphalidae)

Search strategies can have profound fitness-effects for plant-feeding insects. Here I focus on the potential conflict between searching for nectar plants and for larval food plants. I test if the butterfly Vanessa cardui, which can use some of its larval food plants as nectar sources, is able to rationalize this search problem by combining the two search tasks. Lab-experiments revealed a higher oviposition preference for Cirsium arvense over Urtica dioica and a corresponding difference in larval performance. Contrary to predictions, there was no effect of inflorescences on oviposition. However, experiments in large outdoor cages showed a higher occupancy and a higher level of oviposition in patches with access to nectar sources, even on U. dioica. Hence, while there was no preference for individual plants with flowers, the results suggests that V. cardui is simplifying its search task to primarily search for hosts in nectar-rich patches. This strategy allows females to increase oviposition rate, but it is likely that it comes at the expense of not always using optimal host plants in terms of offspring performance.     

Testing the host‐finding ability of a monophagous caterpillar in the field

1. Relatively few studies of the host‐finding ability of specialised, phytophagous insects involve direct observations of individual insects moving among intact hosts and non‐hosts. Information from such studies can inform the design of restoration programmes for species of conservation concern. 2. The movement of caterpillars of the threatened Oregon silverspot butterfly, Speyeria zerene hippolyta (Edwards) (Lepidoptera: Nymphalidae) was studied in the field in cleared arenas with 10 cm radii. Caterpillars were placed in the centre, surrounded by three individuals of their host, Viola adunca, and three different non‐host individuals, separated by bare ground. In a second experiment, second instars were placed between a host and a non‐host, 3–6 cm away. Caterpillars were observed to determine if they walked to their host more often than expected by chance. 3. Caterpillars walked to vegetation significantly more often than expected by chance. They did not, however, reach their hosts more often than expected, based on plant availability. 4. It is concluded that S. z. hippolyta caterpillars can distinguish vegetation from bare ground from 10 cm away. There is no evidence that they can distinguish their host plant from other herbaceous species at distances of 3 cm.     

Breeding cues in a wetland‐dependent Australian passerine of the seasonally wet‐dry tropics

The Capricorn yellow chat Epthianura crocea macgregori (Aves: Meliphagidae) occurs in the seasonal wet‐dry tropics. This region, although coastal, is typified by highly variable annual rainfall. The Capricorn yellow chat breeds in wetlands, predominantly in the summer–autumn period, but has the capacity to breed in response to out‐of‐season rainfall events, consistent with an opportunistically breeding species. Most studies of breeding cues in passerines have been on species centred on temperate climates with predictable rainfall season, arid biomes with a highly variable rainfall quantity and season, and the relatively non‐seasonal wet tropics. This study was focused on a species that occurs in an intermediate situation with a highly variable but summer dominant rainfall season. It aimed to identify which proximal cues are used by birds in such environments to prepare for breeding. Monthly observations at a breeding ground over a 45‐month period were regressed against environmental and climatic variables. There was a significant positive relationship of chat abundance with average minimum monthly air temperature and the extent of inundation. Invertebrate food availability was also sampled. Cross‐correlation with prior monthly rainfall showed that abundance of insects (Diptera, Hemiptera and Lepidoptera) and semi‐aquatic invertebrates peaked 1–2 months following large rainfall events, coinciding with peaks in presence of dependent young of Capricorn yellow chats. Thus, the Capricorn yellow chat matches the model for arid‐adapted birds in which seasonal cues (e.g. increasing day‐length or temperature) in spring lead to breeding preparedness, but breeding only occurs in response to proximal factors such as rainfall. However, the Capricorn yellow chat differs in that breeding is delayed until rainfall is sufficient to inundate its wetland habitat and stimulate the production of food resources associated with the low vegetation and muddy margins of the temporarily flooded pools and channels; suggesting that inundation may be the most important breeding cue.     

Seasonal migration of male red deer (<Emphasis Type="Italic">Cervus elaphus</Emphasis>) in southern Sweden and consequences for management

Red deer Cervus elaphus is a highly appreciated and intensively managed game species throughout Europe. A common management objective is a sustainable harvest of large trophies. In southern Sweden, management has mainly aimed at preserving the nominate subspecies C. elaphus elaphus. Seasonal migration of red deer males may, however, complicate both harvest management as well as conservation efforts. I used individually identified male red deer in southern Sweden to observe distance travelled from rutting areas to areas used by males in summer and winter. Adult males were identified by antler shape and photo-documented during rut. Photos from the rut were compared to trophies of deer harvested or found dead, to found cast antlers and to stags photographed during summer. From 1969 to 2007, a distance between rutting ground and summer/winter quarters was established for 96 identified stags. An average distance of 14 km and a maximum distance of 47 km were recorded between rut and summer/winter observations. The seasonal migration of males increases the risk of overexploitation of males with harvest in both rutting areas and wintering areas. Harvest management and conservation efforts may fail if males seasonally migrate outside the management unit. The results suggest that seasonal migration must be considered in harvest management and conservation and that there is a need for a regulation of male harvest. Furthermore, the study stresses that the success in deer management of single hunting units, may be largely dependent on the harvest policies in the near surroundings as well as in areas tenths of kilometres away, suggesting that a successful management must rely on co-operation and co-ordination on a landscape scale.