Using a phenological network to assess weather influences on first appearance of butterflies in the Netherlands

Phenological responses of butterflies to temperature have been demonstrated in several European countries by using data from standardized butterfly monitoring schemes. Recently, phenological networks have enabled volunteers to record phenological observations at project websites. In this study, the quality of the first appearance data of butterflies from the Dutch phenological network ‘De Natuurkalender’ was examined and these data were then used to analyze trends in butterfly appearance between 2001 and 2013, the effects of climatic factors on appearance of butterflies as well as the phenological interaction of one butterfly species, Anthocharis cardamines, and its two major host plants. Although phenological networks are relatively unstructured, this study shows that data from De Natuurkalender were highly comparable to more standardized data collected by the Dutch Butterfly Monitoring Scheme. No trend in first appearance of any butterfly species was found during the time period 2001–2013. The first appearance dates of most butterflies showed, however, a clear relationship with spring temperature. Higher temperatures, especially in March and April, advanced the first appearance of butterflies. Therefore, with climatic warming in the future, earlier appearance of butterflies is expected. Although climate warming is a potential threat for phenological mismatches between different trophic levels, this study shows a similar temperature response of A. cardamines and its main host plants in the Netherlands. However, as only few phenological interactions between species are examined, further research including rarer monophagous butterfly species and their host plants is needed.     

Effect of regional climate warming on the phenology of butterflies in boreal forests in Manitoba, Canada

We examined the effect of regional climate warming on the phenology of butterfly species in boreal forest ecosystems in Manitoba, Canada. For the period 1971-2004, the mean monthly temperatures in January, September, and December increased significantly, as did the mean temperatures for several concurrent monthly periods. The mean annual temperature increased ≈ 0.05°C/yr over the study period. The annual number of frost-free days and degree-day accumulations increased as well. We measured the response of 19 common butterfly species to these temperature changes with the date of first appearance, week of peak abundance, and the length of flight period over the 33-yr period of 1972-2004. Although adult butterfly response was variable for spring and summer months, 13 of 19 species showed a significant (P < 0.05) increase in flight period extending longer into the autumn. Flight period extensions increased by 31.5 ± 13.9 (SD) d over the study period for 13 butterfly species significantly affected by the warming trend. The early autumn and winter months warmed significantly, and butterflies seem to be responding to this warming trend with a change in the length of certain life stages. Two species, Junonia coenia and Euphydryas phaeton, increased their northerly ranges by ≈ 150 and 70 km, respectively. Warmer autumns and winters may be providing opportunities for range extensions of more southerly butterfly species held at bay by past climatic conditions.     

Extended season for northern butterflies

Butterflies are like all insects in that they are temperature sensitive and a changing climate with higher temperatures might effect their phenology. Several studies have found support for earlier flight dates among the investigated species. A comparative study with data from a citizen science project, including 66 species of butterflies in Sweden, was undertaken, and the result confirms that most butterfly species now fly earlier during the season. This is especially evident for butterflies overwintering as adults or as pupae. However, the advancement in phenology is correlated with flight date, and some late season species show no advancement or have even postponed their flight dates and are now flying later in the season. The results also showed that latitude had a strong effect on the adult flight date, and most of the investigated species showed significantly later flights towards the north. Only some late flying species showed an opposite trend, flying earlier in the north. A majority of the investigated species in this study showed a general response to temperature and advanced their flight dates with warmer temperatures (on average they advanced their flight dates by 3.8 days/°C), although not all species showed this response. In essence, a climate with earlier springs and longer growing seasons seems not to change the appearance patterns in a one-way direction. We now see butterflies on the wings both earlier and later in the season and some consequences of these patterns are discussed. So far, studies have concentrated mostly on early season butterfly–plant interactions but also late season studies are needed for a better understanding of long-term population consequences.     

Flight endurance in relation to adult age in the green‐veined white butterfly Pieris napi

• 1 The flight apparatus in butterflies, as well as in other insects, is costly to manufacture. Since most animals live in a world where resources are limited, trade‐offs are expected and available resources must thus be allocated between flight and other functions, such as reproduction.
• 2 To mitigate this trade‐off, previous studies have shown that butterflies can break down flight muscles in the thorax as they age in order to use muscle nutrients for reproduction.
• 3 Although breakdown of flight muscles is expected to reduce flight ability, relative flight muscle mass (thorax mass/body mass) in many butterfly species does not decrease with age. The aim of the present study was to test the relationship between flight endurance and adult age in the green‐veined white butterfly Pieris napi (L.). The tests were performed in the laboratory at five different temperatures.
• 4 The results showed that age has a significant influence on butterfly flight endurance; older butterflies showed reduced flight endurance. Male butterflies fly for a longer time than females and flight endurance increases with temperature in both sexes.

     

The Ultrastructure of the Indirect Flight Muscles of the Monarch Butterfly,Danaus plexippus (L.) with Implications for Fuel Utilization

The fine structure of the dorsal longitudinal flight muscle of the monarch butterfly, Danaus plexippus (L.), is described. The high actin: myosin filament ratio in this fast muscle is likely related to extensive actin-myosin filament interaction which must occur when tension is increased and maintained by repeated nervous stimulation as demonstrated by Kammer (1967) during the long downstroke of the wingbeat cycle. Glycogen particles are present in the granular fraction of the interfibrillar sacroplasm and among the myofilaments of the flight muscle of young butterflies. The distribution of the granules appears to be related to spatial forces within the muscle fibril for in resting butterflies the intermyofilament particles are generally located in rows parallel to the myofilaments, while they are in transverse bands in the H and I zones of animals fixed immediately after flight. Since the glycogen particles were not depleted during flight, this redistribution does not appear to be related to glycogen metabolism. Glycogen in the flight muscle was depleted during eight days of adulthood in butterflies fed on honey solutions, but lipid reserves increased in the same period.     

BIRD PREDATION AS A SELECTIVE AGENT IN A BUTTERFLY POPULATION

In a population of the checkerspot butterfly, Euphydryas chalcedona, the detached wings of 309 individuals that had been attacked and eaten by birds were collected during a single flight season. During this time period a representative sample of 296 live butterflies in this population was photographed. Comparison of sex ratio and coloration of those butterflies that had been attacked with those that had not showed, first, that birds attacked slightly more females than males; and second, that among males, which are extremely variable in the amount of red on the forewing, birds attacked the less red individuals.     

The aerodynamic costs of warning signals in palatable mimetic butterflies and their distasteful models

Bates hypothesized that some butterfly species that are palatable gain protection from predation by appearing similar to distasteful butterflies. When undisturbed, distasteful butterflies fly slowly and in a straight line, and palatable Batesian mimics also adopt this nonchalant behaviour. When seized by predators, distasteful butterflies are defended by toxic or nauseous chemicals. Lacking chemical defences, Batesian mimics depend on flight to escape attacks. Here, I demonstrate that flight in warning-coloured mimetic butterflies and their distasteful models is more costly than in closely related non-mimetic butterflies. The increased cost is the result of differences in both wing shape and kinematics. Batesian mimics and their models slow the angular velocity of their wings to enhance the colour signal but at an aerodynamic cost. Moreover, the design for flight in Batesian mimics has an additional energetic cost over that of its models. The added cost may cause Batesian mimics to be rare, explaining a general pattern that Bates first observed.     

Less input same output: simplified approach for population size assessment in Lepidoptera

With the aim of creating a simplified sampling scheme that would retain the accuracy of standard mark–release–recapture (MRR) sampling, but at a greatly reduced cost, we analysed 23 capture–recapture data sets from spatially closed populations of six Lepidoptera species according to the constrained Cormack–Jolly–Seber models. Subsequently the relationships between the estimates of population parameters were investigated in order to develop a regression equation that would enable us to calculate seasonal population size without sampling the population throughout the entire flight period. The proportion of individuals flying at peak population was highly variable (CV=0.39), but the variation decreased considerably (CV=0.14) after different life span and flight period length were accounted for. Over 90% of the variance of this proportion was explained by the life span:flight period length ratio. Simulations of hypothetical sampling schemes proved that schemes covering the second and third quarter of the flight period performed much better than those restricted to the second quarter only. The accuracy of seasonal population size estimated with the regression equation developed was comparable for intensive schemes (daily sampling) and non-intensive ones (sampling once in 2 or 3 days). We propose a simplified method of surveying butterfly populations that should be based on checking the presence of flying adults at the beginning and end of the flight period to assess its length, and MRR sampling covering its middle part, with intervals between capture days corresponding to the average life span of investigated butterflies.     

Temperature‐related shifts in butterfly phenology depend on the habitat

Many species are becoming active earlier in the season as the climate becomes warmer. In parallel to phenological responses to climate change, many species have also been affected by habitat changes due to anthropogenic land use. As habitat type can directly affect microclimatic conditions, concurrent changes in climate and habitat could have interacting effects on the phenology of species. Temperature‐related shifts in phenology, however, have mostly been studied independent of habitat types. Here, I used long‐term data from a highly standardized monitoring program with 519 transects to study how phenology of butterflies is affected by ambient temperature and habitat type. I compared forests, agricultural areas and settlements, reflecting three major land use forms, and considered butterfly species that were observed in all three of these habitats. Seasonal appearance of the butterflies was affected both by the ambient temperature and the habitat type. As expected, warmer temperatures led to an overall advancement of the appearance and flight period of most species. Surprisingly, however, phenology of species was delayed in settlement habitats, even though this habitat type is generally associated with higher temperatures. A possible explanation is dispersal among habitat types, such that source–sink effects affect local phenology. When there is little productivity in settlement areas, observed butterflies may have immigrated from forest or agricultural habitats and thus appear later in settlements. My findings suggest that a spillover of individuals among habitats may affect phenology trends and indicate that phenological studies need to be interpreted in the context of habitat types. This becomes especially important when defining strategies to prevent or mitigate effects of climate and land‐use changes on phenology and abundance of species.     

Effects of Light Intensity on the Flight Behaviour of Adult <Emphasis Type="Italic">Tirumala limniace</Emphasis> (Cramer) (Lepidoptera: Nymphalidae: Danainae)

Light intensity significantly affects insect flight behaviour. Mating of butterflies is significantly associated with flight frequency. However, no research has elucidated the effects of light intensity on butterfly flight. Thus, a clear understanding of the effects of light intensity on flight has significant theoretical implications for the cultivation and utilization of butterflies. We observed the flight behaviour of adult Tirumala limniace (Cramer) exposed to light intensities from 243 to 2240 lx and measured the frequency of flight, take-off rhythm, thoracic temperature excess (△T) when perching and flying, and the tendency for thoracic temperature to increase. Results showed that high-intensity light significantly increased flight activity, and males were more active than females under similar light intensities; strong light (1280–2240 lx) resulted in female and male butterflies taking flight earlier compared with weak light (243–864 lx); and a similar pattern was observed for flight duration, with flights by males being significantly longer than those by females at 864–2240 lx; △T of adults flying in strong light was significantly higher than in weak light, whereas the thoracic temperature of perching adults was similar to the air temperature. Compared with other light intensities, the equilibrium thoracic temperature of adults exposed to 2240 lx was higher, and the time to reach it was shorter; in addition, the △T and rate of thoracic temperature increase were higher and achieved more quickly, respectively. Thus, of the 243–2240 lx range, 2240 lx was the most optimal light intensity for adult T. limniace flight and captive rearing.     

Large‐sized insects show stronger seasonality than small‐sized ones: a case study of fruit‐feeding butterflies

Animal species have a restricted period during the year when conditions for development are optimal, and this is known as the temporal window. Duration of the temporal window can vary among species, although the causes of variation are still poorly understood. In the present study, examining butterflies, we assume that the temporal window duration is correlated with the seasonal period of flight (termed seasonality). To understand how species characteristics are correlated with this, we examine whether there is a relationship between body size and length of flight period of fruit‐feeding butterflies in forest fragments, and whether these two parameters have a phylogenetic signal. Using wing size as a measure of body size and the period of adult flight as a measure of seasonality, we found significant positive correlations between body size and seasonality among subfamilies but not within subfamilies. We also found a clear phylogenetic signal in size but not in seasonality. The results obtained suggest the existence of a trade‐off between insect size and seasonality, with size limiting flight period length. The relationship between body size and seasonality and the synchrony with their resources may be one factor explaining the vulnerability of large insects to forest fragmentation. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 104 , 820–827.     

Thermal biology of flight in a butterfly: genotype,flight metabolism,and environmental conditions

Knowledge of the effects of thermal conditions on animal movement and dispersal is necessary for a mechanistic understanding of the consequences of climate change and habitat fragmentation. In particular, the flight of ectothermic insects such as small butterflies is greatly influenced by ambient temperature. Here, variation in body temperature during flight is investigated in an ecological model species, the Glanville fritillary butterfly (Melitaea cinxia). Attention is paid on the effects of flight metabolism, genotypes at candidate loci, and environmental conditions. Measurements were made under a natural range of conditions using infrared thermal imaging. Heating of flight muscles by flight metabolism has been presumed to be negligible in small butterflies. However, the results demonstrate that Glanville fritillary males with high flight metabolic rate maintain elevated body temperature better during flight than males with a low rate of flight metabolism. This effect is likely to have a significant influence on the dispersal performance and fitness of butterflies and demonstrates the possible importance of intraspecific physiological variation on dispersal in other similar ectothermic insects. The results also suggest that individuals having an advantage in low ambient temperatures can be susceptible to overheating at high temperatures. Further, tolerance of high temperatures may be important for flight performance, as indicated by an association of heat‐shock protein (Hsp70) genotype with flight metabolic rate and body temperature at takeoff. The dynamics of body temperature at flight and factors affecting it also differed significantly between female and male butterflies, indicating that thermal dynamics are governed by different mechanisms in the two sexes. This study contributes to knowledge about factors affecting intraspecific variation in dispersal‐related thermal performance in butterflies and other insects. Such information is needed for predictive models of the evolution of dispersal in the face of habitat fragmentation and climate change.     

Thermoregulation and flying habits of the Japanese sulfur butterfly Colias erate (Lepidoptera: Pieridae) in an open habitat

This study evaluated the impact of the thermal environment on the flying behavior of male Japanese sulfur butterflies Colias erate searching for females in an open habitat. Thoracic temperature was monitored before and after flight. Mean thoracic temperature of butterflies immediately after landing was consistently higher than, but independent of, ambient temperature. Although ground speed of flying butterflies was different between flight types, air speed against the butterfly was similar across flight types. The excess of thoracic over ambient temperature was lower in flying butterflies than in basking ones, as predicted by a model. This difference appeared to be due to air current, which enhanced heat loss. In a laboratory study, newly eclosed male butterflies were placed under an incandescent lamp to measure their thoracic temperature at different air current speeds. The excess of thoracic over ambient temperature decreased as the speed of air currents increased. When the air current was similar to the air speed against flying butterflies in the field, a substantial decrease occurred in the operative thoracic temperature.     

Who flies first? – habitat‐specific phenological shifts of butterflies and orthopterans in the light of climate change: a case study from the south‐east Mediterranean

1. Insects undergo phenological change at different rates, showing no consistent trend between habitats, time periods, species or groups. Understanding how and why this variability occurs is crucial. 2. Phenological patterns of butterflies and Orthoptera were analysed using a novel approach of standardised major axis (SMA) analysis. It was investigated whether: (i) phenology (the mean date and duration of flight) of butterflies and Orthoptera changed from one survey (1998 and 1999 respectively) to another (2011), (ii) the rate at which phenology changed differed between taxa and (iii) phenological change was significantly different across habitat types (agriculture fields, grasslands, and forests). Using the 2011 dataset, we investigated relationships between habitat‐specific variables and species phenology. 3. For both groups, late‐emerging species had an advanced onset on the second survey while the duration showed no consistent trend for butterflies and did not change for Orthoptera. Although the rate at which phenology changed was consistent between the two groups, at the habitat level, a longer duration of flight period emerged for butterflies in agriculture fields while Orthoptera showed no differentiation in flight duration between habitats. We found an earlier emergence of butterflies in grasslands compared to forests, attributed to habitat‐specific temperature, whereas spatial variation in humidity had a significantly lower effect on butterflies' phenology in grasslands compared to forests. A gradual delay of butterfly appearances as the canopy cover increased was also found. 4. The utility of SMA analysis was demonstrated in phenological studies and evidence was detected that both habitat type and habitat‐specific variables refine species' phenological responses.     

Behavioural mimicry in flight path of Batesian intraspecific polymorphic butterfly Papilio polytes

Batesian mimics that show similar coloration to unpalatable models gain a fitness advantage of reduced predation. Beyond physical similarity, mimics often exhibit behaviour similar to their models, further enhancing their protection against predation by mimicking not only the model''s physical appearance but also activity. In butterflies, there is a strong correlation between palatability and flight velocity, but there is only weak correlation between palatability and flight path. Little is known about how Batesian mimics fly. Here, we explored the flight behaviour of four butterfly species/morphs: unpalatable model Pachliopta aristolochiae, mimetic and non-mimetic females of female-limited mimic Papilio polytes, and palatable control Papilio xuthus. We demonstrated that the directional change (DC) generated by wingbeats and the standard deviation of directional change (SDDC) of mimetic females and their models were smaller than those of non-mimetic females and palatable controls. Furthermore, we found no significant difference in flight velocity among all species/morphs. By showing that DC and SDDC of mimetic females resemble those of models, we provide the first evidence for the existence of behavioural mimicry in flight path by a Batesian mimic butterfly.     

Optimal strategies for insects migrating in the flight boundary layer: mechanisms and consequences

Directed aerial displacement requires that a volant organism'sairspeed exceeds ambient wind speed. For biologically relevantaltitudes, wind speed increases exponentially with increasedheight above the ground. Thus, dispersal of most insects isinfluenced by atmospheric conditions. However, insects thatfly close to the Earth's surface displace within the flightboundary layer where insect airspeeds are relatively high. Overthe past 17 years, we have studied boundary-layer insects byfollowing individuals as they migrate across the Caribbean Seaand the Panama Canal. Although most migrants evade either droughtor cold, nymphalid and pierid butterflies migrate across Panamanear the onset of the rainy season. Dragonflies of the genusPantala migrate in October concurrently with frontal weathersystems. Migrating the furthest and thereby being the most difficultto study, the diurnal moth Urania fulgens migrates between Centraland South America. Migratory butterflies and dragonflies arecapable of directed movement towards a preferred compass directionin variable winds, whereas the moths drift with winds over water.Butterflies orient using both global and local cues. Consistentwith optimal migration theory, butterflies and dragonflies adjusttheir flight speeds in ways that maximize migratory distancetraveled per unit fuel, whereas the moths do not. Moreover,only butterflies adjust their flight speed in relation to endogenousfat reserves. It is likely that these insects use optic flowto gauge their speed and drift, and thus must migrate wheresufficient detail in the Earth's surface is visible to them.The abilities of butterflies and dragonflies to adjust theirairspeed over water indicate sophisticated control and guidancesystems pertaining to migration.     

Butterfly visual characteristics and ontogeny of responses to butterflies by a specialized tropical bird

The responses of two adult and three hand-reared, naive young rufous-tailed jacamars (Galbula ruficauda) to local butterflies were studied in feeding experiments. Four behavioural characteristics distinguish jacamars from other less specialized avian predators: (1) Exposed to butterflies for the first time, naive young jacamars would attack butterflies without showing signs of inhibition. Unacceptable butterflies, once captured, were taste-rejected quickly, and most survived the sampling. The few presumably unacceptable butterflies consumed by the birds were not observed to cause vomiting. (2) After gaining some familiarity with butterflies, young birds, like the adults, developed a reluctance to attack. They visually rejected certain classes of butterflies, often failing to attack them during an entire four-hour feeding trial. However, occasional attacks were made on butterflies in these ‘rejected’ classes. When this did occur, the insects proved to be actually easier to catch than those that were more often attacked. Once captured, however, the majority of these butterflies were taste-rejected. (3) For a given butterfly species, most individuals were either consumed or rejected. Thus, each species could be clearly classified as either acceptable or unacceptable to the jacamars. This consistency in jacamar responses resulted in a bimodal acceptability distribution of sympatric butterflies. (4) Young jacamars were capable of rapid associative learning and their responses were closely associated with butterfly visual characteristics in which colour pattern, flight behaviour, and morphology were also closely correlated. Thus, a single butterfly morphological parameter termed body shape (body length/thoracic diameter ratio) can adequately predict the feeding responses of jacamars. Visually detectable traits associated with butterflies possessing chemical defences may represent a balance between the need to signal unambiguously to specialized and/or experienced predators and the need to escape attacks by generalized and/or opportunistic predators. Since the proportion of specialized predators is higher in the tropical rainforest than in other habitat types, we expect greater divergence of morphological and behavioural characteristics between palatable and unpalatable butterflies in rainforest habitats.     

EXPERIMENTAL ANALYSES OF WING SIZE,FLIGHT, AND SURVIVAL IN THE WESTERN WHITE BUTTERFLY

Butterflies have distinctively large wings relative to body size, but the functional and fitness consequences of wing size for butterflies are largely unknown. I use natural and experimentally generated variation in wing surface area to examine how decreased wing size affects flight and survival in a population of the western white butterfly, Pontia occidentalis. In the laboratory, experimental reductions in wing area (reduced-wings manipulation) significantly increased wingbeat frequencies of hovering butterflies, whereas a control manipulation had no detectable effects. In contrast, behavioral observations and mark-release-recapture (MRR) studies in the field detected no significant differences in flight activity, initial dispersal rates, or recapture probabilities among treatment groups. Estimated selection coefficients indicated that natural variation in wing size, body mass, and wing loading in the population were not significantly correlated with survival in the two MRR studies. In two mark-recapture studies with manipulated butterflies, survival probabilities were not significantly different for reduced-wings individuals compared with control or unmanipulated individuals. In summary, experimental reductions in wing area significantly altered aspects of flight in the laboratory, but did not detectably alter flight or survival in the field for this population. The large wing size typical of butterflies may reduce the functional and survival consequences of wing size variation within populations.     

Weight Loading and Reproductive Status Affect the Flight Performance of Pieris napi Butterflies

Weight-induced mobility reductions can have dramatic fitness consequences and winged animals are especially sensitive to the trade-off between mass and locomotion. Data on how natural weight fluctuations influence a flying insect’s ability to take off are scarce. We therefore quantified take-off flight ability in Pieris napi butterflies in relation to reproductive status. Take-off flight ability (velocity and take-off angle) under suboptimal temperature conditions was recorded with a 3D-tracking camera system and was predicted to decrease with relatively larger weight loads. Our results show that relatively larger weight loads generally reduce flight speed in male butterflies and lower take-off angles in females. However, despite having a lower wing loading, mated male butterflies flew slower than unmated males. Our study suggests that retention of weight loads associated with reproduction impairs insect flight performance.