Determinants of foraging profitability in two nectarivorous butterflies

ABSTRACT.

• 1 I studied flower selection and foraging energetics of Agraulis vanillae L. (Nymphalidae) and Phoebis sennae (Pieridae), two butterfly species common to north central Florida. I identified the major nectar resources exploited by several populations of these butterflies and, for each plant species, measured available nectar volumes and concentrations, corolla lengths, and density. I quantified foraging behaviour of each butterfly species at each nectar source (flower visitation rate and percentage of foraging time in flight), and used these data to estimate the net rate of energy intake of each butterfly species at each nectar source.
• 2 Estimated mean energy contents of individual flowers of the eleven exploited plant species spanned three orders of magnitude, ranging between 0.015 and 9.27 joules. Mean energy content of individual flowers was strongly correlated with mean foraging profit of both butterfly species.
• 3 Mean nectar volume strongly influenced energy content and varied widely within and among species, ranging from 0.0076 to 1.853 μ1. Nectar concentration varied between 17.1% and 40.4% sucrose-equivalents. Nectar volume was the best single predictor of foraging profitability (correlation coefficients of 0.994 and 0.984 for Phoebis and Agraulis respectively). Corolla length also strongly affected foraging profitability for both butterfly species; flower species with longer corollas were generally more profitable.
• 4 Flower density and nectar concentration showed weak or nonsignificant associations with foraging profitability.
• 5 The usefulness and limitations of these floral characteristics as bases for foraging selectivity, and the selective pressures foraging butterflies might place on the visited plants are discussed.

     

A Comparative Analysis of Mating Recognition Signals in Graylings: Hipparchia statilinus vs. H. semele (Lepidoptera: Nymphalidae, Satyrinae)

Courtship is an important character linked to fitness and can evolve in response to female mate choice, to ensure sex identity and quality of a potential mate. It can also be a major pre-mating isolating mechanism in butterflies and many other species. In this paper, aspects of the reproductive behaviour of Hipparchia statilinus are described. First, the ethogram and the sequential structure of courtship leading to copulation and female refusal behaviour are showed; second, the results are compared with the behaviour of the sympatric and syntopic species, H. semele. Sequential analysis of H. statilinus courtship showed that, once a male has started the sequence, the following steps most likely follow up to the end. Courtship seems to reflect female behaviour: the male can repeat the whole sequence or part of it more than once, waiting for female signals. The general pattern of sexual behaviour in H. semele and in H. statilinus is mainly identical: perching strategy, flight pursuit, courtship. In both species, courtship consists of a highly stereotypic sequence, and differences between sequences are primarily related to presence/absence, order and performance of steps. This study is the first step of an experimental design addressed to a better understanding of mating recognition signals in Hipparchia and provides more details to define the relative roles of phylogeny and environment in shaping boundaries among species.     

Foraging behaviour of honey bees (Apis mellifera L.) on transgenic oilseed rape (Brassica napus L.var. oleifera)

The impact of genetically modified oilseed rape (Brassica napus L.) on the foraging behaviour of honey bees (Apis mellifera L.) was evaluated on two different lines transformed to express constitutively heterologous chitinase in somatic tissue for enhanced disease resistance. Experiments were conducted in confinement in an indoor flight room with controlled conditions and in an outdoor flight cage with conditions more representative of the open environment. Foraging behaviour was analysed by observations of general bee behaviour (total number of visits) and of individual bee behaviour (using a video camera coupled with a special software program to process the data). The plants were analysed in terms of nectar quantity and quality (nectar volume and sugar content). The results showed no effects on bee foraging behaviour due to the modification of the genome of these plants by the introduction of a chitinase gene even though some differences between lines were found in the nectar. The methods applied in this original approach for the evaluation of the impact of genetically modified oilseed rape were shown to be sufficiently sensitive to detect changes in bee behaviour resulting from differences between plants.     

Behavioural traits mediating effects of two plant-ants on their specific myrmecophyte host

Summary. Symbiotic ant species vary in their effects on the same host plant, and some ant species are exploiters. These can destabilise the interaction. The behavioural repertoire of ant associates should be important in determining their effects on the host. We examined several traits of foraging behaviour of two ant species associated with the African understorey tree Leonardoxa africana africana – the protective mutualist Petalomyrmex phylax and the parasite Cataulacus mckeyi – to examine the mechanistic basis of the difference in their effects on the plant. These two ant species displayed significant differences not only in activity rhythms, P. phylax patrolling leaves day and night while C. mckeyi was strictly diurnal, but also in their predatory behaviour (P. phylax killed more herbivores) and recruitment dynamics (C. mckeyi recruited at a lower level). For all traits examined, C. mckeyi expressed behaviours reflecting an opportunistic exploitation of the nectar produced by the host plant, whereas those displayed by P. phylax contribute to conferring effective protection of the host plant. Our results suggest that prey capture may be important as a source of food for Petalomyrmex, in addition to its function in increasing plant-provided resources through protection.Received 27 August 2004; revised 11 November 2004; accepted 16 November 2004.     

Pollen amino acids—an additional diet for a nectar feeding butterfly?

The increase of the amino acid concentration over different time intervals in artificial nectar (i.e., a sucrose solution) due to pollen contamination was investigated in four Californian plant species (Aesculus californica, Amsinckia lunaris, Brodiaea pulchella, Carduus pycnocephalus), which are important nectar resources for a Californian colony of the butterflyBattus philenor as well as for other insects. The increase of the amino acid concentration in the medium is different in all four species and seems to be determined by a variety of factors including permeability of the pollen grain wall and presence or absence of pores. The results suggest a passive diffusion process of the free pollen amino acids into the medium rather than an active release. Implications from the experiments forBattus philenor and for other nectar feeding pollinators are discussed. A possible complementary effect of free pollen and nectar amino acids is proposed for plant species in which pollen is likely to be knocked into nectar by their flower visitors. A possible evolutionary pathway from nectar feeding butterflies such asBattus philenor to the complex derived pollen feeding habit in theHeliconius butterflies is proposed.     

Preference of cabbage white butterflies and honey bees for nectar that contains amino acids

Summary Amino acids occur in most floral nectars but their role in pollinator attraction is relatively unstudied. Nectars of butterfly-pollinated flower tend to have higher concentrations of amino acids than do flowers pollinated by bees and many other animals, suggesting that amino acids are important attractants of butterflies to flowers. In order to determine whether amino acids are important in attracting butterflies and bees, we tested the preference of cabbage white butterflies (Pieris rapae) and honey bees (Apis mellifera) by allowing them to feed from artificial flowers containing sugar-only or sugar-amino acid mimics ofLantana camara nectar. Honey bees and female cabbage white butterflies consumed more sugar-amino acid nectar than sugar-only nectar. In addition, female cabbage white butterflies visited artificial flowers containing sugar-amino acid nectars more frequently than flowers containing sugar-only nectars; honey bees spent more time consuming the sugar-amino acid nectar. Male cabbage white butterflies did not discriminate between the two nectars. These results support the hypothesis that the amino acids of nectar contribute to pollinator attraction and/or feeding.     

Male courtship cycles in three species of tropical Ilyoplax crabs (Decapoda,Brachyura, Ocypodidae)

The courtship behaviour and cycles of male courtship activity and colouration of Ilyoplax orientalis, I. delsmani and I. gangetica were studied in the field in Malaysia and Thailand. Each species had a distinctive chela waving or beckoning display. Depending on species, the chelipeds, carapaces, or both of waving males blanched to white in contrast to the cryptic colour of nonwaving males and females. All three of these tropical Ilyoplax exhibited semilunar cycles in male waving activity at the colony level. It was confirmed for I. orientalis that individual males cycled each semilunar period between waving and non-waving phases and exhibited different behaviour toward females during these two behavioural phases.     

Butterfly habitats, broad-scale biotope affiliations, and structural exploitation of vegetation at finer scales: the matrix revisited

Abstract. 1. Biotope and resources data are rarely attached to arthropod (butterfly) synoptic monitoring systems, and invariably not linked to behavioural exploitation of vegetation substrates. Yet, these data allow us to examine resource use within different biotopes and to distinguish more clearly between habitat and the matrix. 2. Comparative data on vegetation exploitation for different behaviours (search flight, direct flight, tactile inspections, perching, feeding, interactions, oviposition) were collected using transect sections over a range of biotopes from bare ground to mature woodland for two closely related satyrine butterflies, Maniola jurtina and Pyronia tithonus with overlapping flight times. Occupancy data were obtained on Pararge aegeria as a marker for the woodland end of the biotope spectrum. 3. There were clear distinctions in biotope occupancy between M. jurtina (grassland bias) and P. tithonus (shrub bias); significant differences in exploitation of vegetation substrates (except for nectar feeding) coincided with this bias in transect sections which comprise both grassland and shrubs. The exception (nectar feeding) is explained by the decline in shrub (Rubus fruticosus) nectar and increase in herb nectar during the later emergence of P. tithonus. 4. Direct flight increased in unsuitable biotopes for both species. However, resource‐exploiting behaviour (>70%) predominated even in biotopes that would be regarded as completely unsuitable for supporting the species and where less than 2% of individuals for each species were observed. 5. Simultaneous collection of biotope, resources, and behavioural data is needed for monitoring affinities of butterflies to vegetation structures and using butterflies as indicators of environmental changes. 6. Much of the landscape is shown to comprise valuable resources for butterflies, even when classified for metapopulation studies as empty matrix.     

Role of morphological variables of the visitor butterfly species in relation to their foraging behaviour on Lantana camara: Implication for conservation

The study of foraging behaviour of butterflies has been an important focus among the lepidopterists for years. Although established as invasive weed plant, the role Lantana camara as an important host plant as well as a food plant for the butterfly species is now well-known. The present study aims to interpret the role of morphological variables of the visitor butterflies in relation to their foraging behaviour on Lantana camara. Butterflies with longer proboscis were more efficient in foraging on flowers of Lantana camara than the butterflies with shorter ones, when the species containing proboscis same as or longer than their body length were excluded. Longer relative proboscis length (RPL) have selective advantage for foraging over Lantana camara up to a certain point (RPL = 0.881) and after that larger relative proboscis length often obstructs foraging behaviour as the handling time increases and these butterflies face more resistance against incoming nectar than the others.The residuals (body weight-wing span) also act as important factor.The handling time of the butterflies on Lantana camara shows a negative relationship with the residuals. The findings suggests that in case of Lantana camara as a nectaring plant butterfly species with longer proboscis have selective advantage for exploitation of the resource than the species with shorter ones and plantation of Lantana camara may be useful for conserving the long tongued butterfly species.     

Effects of temperature on courtship and copulatory behaviours of a wolf spider Pardosa astrigera (Araneae: Lycosidae)

Spiders possess a suit of characteristics, which play important roles in the fields of sensory modalities and sexual selection. Although the effects of temperature on spider prey-hunting, web-building, sexual signaling and habitat selection are well-documented, the effects of environmental temperature on spider courtship and copulatory behaviours are largely unexplored. In order to determine the effects of temperature on the sexual behaviours of the wolf spider Pardosa astrigera, we subjected pairs of male and female to five temperatures from 16 to 32 °C at an interval of 4 °C in a controlled laboratory conditions. Results indicated that in males most behavioural parameters, except the number of hematodochal expansions, were significantly influenced by environmental temperature. Male P. astrigera courtship latency, courtship duration, and copulatory duration declined gradually with increasing temperature within the range of 16–28 °C, whereas the number of pedipalp insertions and frequencies of both pedipalp insertions and hematodochal expansions increased gradually with temperature.     

Untersuchungen zur Blütenaffinität der Schachbrettweibchen (Agapetes galathea L.)

Rhopaloceran butterflies are well known to visit distinct species of flowers in order to extract nectar, normally leaving again after a short time to continue their foraging flights. Females of Agapetes galathea, however, often show a different behaviour, which is the subject of the following analysis. The dynamics of sugar production by flowers and the foraging pattern of the galathea- ♂♂ have been studied under natural conditions. Special consideration is given to the aggressive behaviour of the females towards approaching insects during their flower resting periods.     

Hybrid disadvantage in the larval foraging behaviour of the two neotropical species of <Emphasis Type="Italic">Drosophila pavani</Emphasis> and <Emphasis Type="Italic">Drosophila gaucha</Emphasis>

Flies from two populations of the Chilean endemic neotropical species Drosophila pavani and two populations of its sibling species Drosophila gaucha were crossed reciprocally to obtain intra- and interspecific hybrids. The developmental pathways of locomotor activity and feeding rate were analysed for eleven of twelve possible genotype groups. The hybrids showed reduced fitness indicated by a decrease in the measured traits. Hybrid disadvantage was strongest in interspecific hybrids, especially with respect to feeding behaviour. This evidence supports the contention that D. pavani and D. gaucha have evolved different coadapted gene pools controlling the developmental pathways for behavioural traits expressed during larval foraging; but genetic divergence affecting these behaviours has also taken place between locally adapted populations within each species.     

The role of host species, age and defensive behaviour on ovipositional decisions in a solitary specialist and gregarious generalist parasitoid (Cotesia species)

The main objective of this study was to determine the extent to which host acceptance behaviour as related to host species, age, and defensive behaviour might explain the differences in host use that exist between two congeneric and sympatric species of parasitic wasps. Cotesia glomerata (L.) (Hymenoptera: Braconidae) is gregarious and generalist on several species of Pieridae, whereas C. rubecula (Marshall) is solitary and specific to Pieris rapae (L.). Cotesia species differed in their responses to host species (P. brassicae (L.), P. napi (L.) and P. rapae) and developmental stage (early and late 1st, 2nd and 3rd instars). In no-choice tests, host acceptance by C. rubecula was higher for p. rapae and females did not distinguish among the 6 host ages. In contrast, when foraging for P. brassicae and P. napi, C. rubecula females more readily attacked early first instar. Cotesia glomerata showed a higher degree of behavioural plasticity towards acceptance of Pieris host species and host age than did C. rubecula. Cotesia glomerata females parasitized the three Pieris species and showed higher acceptance of first and second instars over third instar. Oviposition success was also influenced by host defensive behaviour. The frequency and the effectiveness of defensive behaviour rose with increasing age of the host, P. brassicae being the most aggressive Pieris species. Furthermore, the mean duration of C. glomerata oviposition was significantly reduced by the defensive reactions of P. brassicae, which would likely affect parasitoid fitness as oviposition time is positively correlated to clutch size in C. glomerata. Acceptance frequencies corresponded well to field reports of Pieris-Cotesia associations and to patterns of parasitoid larval performance, suggesting that the acceptance phase might be used as a reliable indicator of Cotesia host-specificity.     

Can nectar properties explain sex‐specific flower preferences in the Adonis Blue butterfly Lysandra bellargus?

1. Field observations in the Swiss Jura mountains showed that males and females of the bivoltine Adonis Blue butterfly Lysandra bellargus Rott. differed significantly in their flower visitation patterns. 2. In both generations, females visited a broader range of available nectar plants than did males. The specific flower visitation patterns of males and females were not affected by the general availability and abundance of potential nectar plant species during both flight periods, indicating high selectivity for nectar plants by both males and females. 3. In addition, the sexes differed in their nectar foraging behaviours: distances between successively visited flowers were significantly longer in males than in females, indicating that male and female butterflies have different foraging strategies. 4. Investigations of nectar characteristics showed that the sexes preferred flowers with different nectar compositions. Males of both generations preferred flowers with high proportions of sucrose and high amounts of total sugar, whereas females preferred flowers with high portions of glucose in their nectar, and, in the spring generation, flowers rich in amino acids. 5. Flowers visited exclusively by males or females in spring differed significantly in their amino acid composition. 6. This clear‐cut pattern did not hold for the autumn generation, most probably due to the limited availability of flowers. 7. The observed nectar foraging patterns underline the importance of adult feeding for longevity and reproduction in butterflies. The findings are particularly relevant for conservation, because L. bellargus is an increasingly threatened species in many European countries.     

Honeydew feeding in the solitary bee Osmia bicornis as affected by aphid species and nectar availability

Like honey bees (Apis mellifera), non-Apis bees could exploit honeydew as a carbohydrate source. In addition to providing carbohydrates, this may expose them to potentially harmful plant products secreted in honeydew. However, knowledge on honeydew feeding by solitary bees is very scarce. Here we determine whether the polylectic solitary bee Osmia bicornis (=O. rufa) collects honeydew under semi-field conditions, and whether this is affected by aphid species and presence of floral nectar. Bees were provided with oilseed rape plants containing flowers and/or colonies of either Myzus persicae or Brevicoryne brassicae. We used the total sugar level of the bee crop as a measure of the individual's nutritional state and the oligosaccharide erlose as indicator for honeydew consumption. Erlose was present in honeydews from both aphid species, while absent in oilseed rape nectar, nor being synthesized by O. bicornis. When bees were confined to a single honeydew type as the only carbohydrate source, consumption of M. persicae honeydew was confirmed for 47% of the bees and consumption of B. brassicae honeydew for only 3%. Increased mortality in the latter treatment provided further evidence that B. brassicae honeydew is an unsuitable food source for O. bicornis. All bees that were given the choice between honeydew and floral nectar showed significantly increased total sugar levels. However, the fact that no erlose was detected in these bees indicates that honeydew was not consumed when suitable floral nectar was available. This study demonstrates that honeydew exploitation by O. bicornis is dependent on honeydew type and the presence of floral nectar.     

Nectar exploitation by herbivores and their parasitoids is a function of flower species and relative humidity

In conservation biological control, diversification of the agro ecosystem with flowering vegetation is seen as an important tool to support the broad range of predators and parasitoids that require nectar and pollen sources to survive and reproduce. In order to identify flowering plants that provide suitable food sources for natural enemies without supporting the pest species, we analyzed the exploitation of 19 flowering plants by two important lepidopteran cabbage pests, Pieris rapae and Plutella xylostella, and their hymenopteran parasitoids, Cotesia glomerata and Diadegma semiclausum. The experiments were conducted at 90% r.h., while Pieris rapae was tested both at 45% r.h. and at 90% r.h. At 45 ± 5% r.h., corresponding with field conditions at which P. rapae is predominantly active, the butterfly was unable to feed on a number of exposed floral nectar sources whose nectar was successfully exploited at 90% r.h. The broader nectar exploitation by P. rapae at the high humidity is presumably explained by the resulting decrease in nectar viscosity. When comparing D. semiclausum and its herbivorous host P. xylostella, the herbivore exploited a broader range of plants. However, those plants that benefited both the parasitoid and the herbivore had a much stronger effect on the longevity of the parasitoid. The results from the accessibility bioassay suggest that flowers where nectar is not accessible can have a negative impact on insect survival presumably by stimulating foraging without providing accessible nectar. Our results underline the importance of considering species-specific environmental conditions when fine-tuning the choice of nectar sources to be used in conservation biological control programs.     

Non-lethal presence of predators modifies morphology and movement rates in <Emphasis Type="Italic">Euplotes</Emphasis>

Many species are able to modify aspects of their behaviour and morphology in the presence of predators. The aim of this study was to investigate the relationship between the expression of morphological and behavioural defences according to the framework proposed by DeWitt et al (1999). Experiments were carried out using hypotrich ciliates of the genus Euplotes as prey and turbellarians of the genus Stenostomum as predators. The smaller species Euplotes octocarinatus showed a greater proportional increase in width, a reduction in foraging movement rates and an increase in maximum movement rates following exposure to predator cues. The larger Euplotes aediculatus induced lesser changes in width, similar reductions in movement during foraging and no change in maximum speed following predator exposure. These results provide evidence of a cospecialised relationship between morphological and behavioural defences. Despite substantial differences in the absence of predators, movement rates and lateral body width were similar in both species following predator exposure. The observed changes may be considered adaptive, gape limited flatworm predators are unable to ingest large Euplotes and a reduction in movement rates during foraging reduces predator encounter rates, while an increase in maximal movement rates increases chances of predator evasion. Handling editor: S. I. Dodson     

Nectary structure and nectar characteristics in someBignoniaceae

The nectary structure and chemical nectar composition of 15 species belonging to 12 genera ofBignoniaceae are analyzed. All taxa bear a conspicuous nuptial nectary surrounding the ovary base. The secretory tissue is mostly supplied by phloem branches. The stomata are located in the middle and upper part of the nectary epidermis with an homogeneous distribution. The nuptial nectary is proportionally large in relation to the ovary (15–30%), disregarding the nectary volume. Most species have extranuptial nectaries in both inner and outer surfaces of the calyx. Both kinds of nectaries lack a vascular tissue that straightly supplies them. Nuptial nectar concentration (wt/wt) ranges from 19 to 68%. Sugars and amino acids are found in all species. Half of the species have hexose predominant nectars, the remaining sucrose predominant. Phenols are detected in only three species, whereas reducing acids exclusively inTecoma stans. Alkaloids and lipids were never detected. Extranuptial nectar chemical composition is analyzed in two species:Dolichandra cynanchoides andPodranea ricasoliana. Bees constitute the main flower visitors of the species studied whereas hummingbirds were seen visiting three species. A correlation analysis is performed with the data obtained. There are a few significant correlations which indicate a parallel increase of three parameters: the longer the flower length, the more voluminous the nectary and the higher stomata number, independently of the floral biotype. Phenograms are obtained using 24 floral characters including nectary and nectar data. The clusters obtained do not reflect taxonomic relationships but are useful in the understanding of animal-plant interactions when the flower biotype is considered.This paper is based on a chapter of a doctoral thesis presented at the University of Córdoba (Argentina).     

Foraging activity and behaviour of two goatfish species (Perciformes: Mullidae) at Fernando de Noronha Archipelago, tropical West Atlantic

The goatfishes (Mullidae) include about 50 bottom-foraging fish species. The foraging activity of the yellow goatfish, Mulloidichthys martinicus, and the spotted goatfish, Pseudupeneus maculatus, was studied comparatively at Fernando de Noronha Archipelago, off coast of Northeast Brazil tropical West Atlantic. Pseudupeneus maculatus fed over a larger variety of substrate types, had lower feeding rate, roamed more per given time, spent less time in a feeding event, and displayed a more diverse repertoire of feeding modes than M. martinicus. The differences in the foraging activity and behaviour between the two species possibly minimize a potential resource overlap, as already recorded for other sympatric mullids. Pseudupeneus maculatus had lower feeding rate most likely because it feeds on larger items, and roamed over greater distance per time. Possibly this is because it foraged over a greater variety of substrate distributed over a larger area than that used by M. martinicus. Notwithstanding the overall morphological and behavioural similarity of goatfishes in general, they do differ in their substrate preferences and foraging activity, which indicates that these fishes should not be simply considered generalized bottom foragers.     

The role of foraging behaviour in the sexual segregation of the African elephant

Elephants (Loxodonta africana) exhibit pronounced sexual dimorphism, and in this study we test the prediction that the differences in body size and sociality are significant enough to drive divergent foraging strategies and ultimately sexual segregation. Body size influences the foraging behaviour of herbivores through the differential scaling coefficients of metabolism and gut size, with larger bodied individuals being able to tolerate greater quantities of low-quality, fibrous vegetation, whilst having lower mass-specific energy requirements. We test two distinct theories: the scramble competition hypothesis (SCH) and the forage selection hypothesis (FSH). Comprehensive behavioural data were collected from the Pongola Game Reserve and the Phinda Private Game Reserve in South Africa over a 2.5-year period. The data were analysed using sex as the independent variable. Adult females targeted a wider range of species, adopted a more selective foraging approach and exhibited greater bite rates as predicted by the body size hypothesis and the increased demands of reproductive investment (lactation and pregnancy). Males had longer feeding bouts, displayed significantly more destructive behaviour (31% of observations, 11% for females) and ingested greater quantities of forage during each feeding bout. The independent ranging behaviour of adult males enables them to have longer foraging bouts as they experience fewer social constraints than females. The SCH was rejected as a cause of sexual segregation due to the relative abundance of low quality forage, and the fact that feeding heights were similar for both males and females. However, we conclude that the differences in the foraging strategies of the sexes are sufficient to cause spatial segregation as postulated by the FSH. Sexual dimorphism and the associated behavioural differences have important implications for the management and conservation of elephant and other dimorphic species, with the sexes effectively acting as distinct “ecological species”.