Not only the butterflies: managing ants on road verges to benefit Phengaris (Maculinea) butterflies

Obligate myrmecophilic butterfly species, such as Phengaris (Maculinea) teleius and P. nausithous, have narrow habitat requirements. Living as a caterpillar in the nests of the ant species Myrmica scabrinodis and M. rubra, respectively, they can only survive on sites with both host ants and the host plant Great Burnet Sanguisorba officinalis. After having been reintroduced into a nature reserve in the Netherlands in 1990, both butterfly species expanded their distribution to linear landscape elements such as road verges and ditch edges outside this reserve. As additional habitat of both butterfly species, vegetation management of these landscape elements became important. Our results show that a management beneficial for Phengaris butterflies should aim to increase the nest density of Myrmica species, at the same time reducing the density of nests of the competitor Lasius niger or at least keeping them at a low density. Unfavourable grassland management under which L. niger thrives, includes not mowing or flail-cutting the grass, or depositing dredgings along the side of the ditch. Management favourable for the two Myrmica species differs, demanding some flexibility if both species are to benefit. M. scabrinodis is best supported with early mowing of the road verge vegetation or late mowing in the nature reserve, both of which result in an open vegetation and warm microclimate. In contrast, the nest sites of M. rubra should be left undisturbed during the summer, and mown in late autumn. Mowing of butterfly habitat should be avoided between mid-June and mid-September as this would remove the flowerheads of the Sanguisorba plants, on which the butterflies lay their eggs.     

Resource use of specialist butterflies in agricultural landscapes: conservation lessons from the butterfly Phengaris (Maculinea) nausithous

Most of the European grassland butterfly species are dependent on species rich grasslands shaped by low intensity farming. Conservation of these specialist species in agricultural landscapes relies on knowledge of their essential resources and the spatial distribution of these resources. In The Netherlands, the dusky large blue Phengaris (Maculinea) nausithous butterflies were extinct until their reintroduction in 1990. In addition, a spontaneous recolonization of road verges in an agricultural landscape occurred in 2001 in the southern part of The Netherlands. We analyzed the use of the essential resources, both host plants and host ants, of the latter population during the summers of 2003 and 2005. First we tested whether the distribution of the butterflies during several years could be explained by both the presence of host plants as well as host ants, as we expected that the resource that limits the distribution of this species can differ between locations and over time. We found that oviposition site selection was related to the most abundant resource. While in 2003, site selection was best explained by the presence of the host ant Myrmica scabrinodis, in 2005 it was more strongly related to flowerhead availability of the host plant. We secondly compared the net displacement of individuals between the road verge population and the reintroduced population in the Moerputten meadows, since we expected that movement of individuals depends on the structure of their habitat. On the road verges, butterflies moved significantly shorter distances than on meadows, which limits the butterflies in finding their essential resources. Finally we analyzed the availability of the two essential resources in the surroundings of the road verge population. Given the short net displacement distances and the adverse landscape features for long-distance dispersal, this landscape analysis suggests that the Phengaris population at the Posterholt site is trapped on the recently recolonized road verges. These results highlight the importance of assessing the availability of essential resources across different years and locations relative to the movement of the butterflies, and the necessity to careful manage these resources for the conservation of specialist species in agricultural landscapes, such as this butterfly species.     

Population isolation rather than ecological variation explains the genetic structure of endangered myrmecophilous butterfly Phengaris (=Maculinea) arion

Genetic variation of the globally threatened obligatorily myrmecophilous Large Blue butterfly Phengaris (Maculinea) arion (Lepidoptera) was studied, using six microsatellite markers, in a country where its decline is dramatic (Poland). Material was collected on 13 sites showing considerable ecological variation as far as biotope, larval food plant and host ants of the butterfly were concerned. Genetic variability, estimated in terms of number of alleles and heterozygosity, was the lowest in the most isolated populations. However on sites localized in areas where suitable biotopes were extensive and interconnected, P. arion still held relatively high genetic diversity. Pairwise F _ST values indicated small and moderate differentiation among samples (F _ST = 0.01–0.15), with the exceptions of two isolated localities (0.20). We did not find clear evidence of isolation by distance. The presence of four or five genetic clusters was indicated. Analysis of the membership of each individual to each cluster showed that the vast majority of individuals from three isolated populations were clustered in three separate genetic groups. The most distinct population was the one, which had been found to be specialized towards Myrmica lobicornis in previous studies. Individuals from the remaining populations could not be clustered in separate genetic groups, however some dominance of different clusters in geographical regions was observed. Some portion of the population’s genetic variability could be explained by geographical distribution, however the percentage of variation, explaining the differences between two main regions (S and NE Poland), was very low. We conclude that the main factor shaping the current genetic structure of P. arion in Poland is the recent isolation of populations related to habitat fragmentation but local ecological specializations may be also a potential factor. Therefore the necessity of activities aiming to halt the further reduction of genetic variability, as well as the monitoring of priority populations (e.g. those belonging to unique host races), should be emphasized in future action plans in Central Europe.     

The social parasite Phengaris (Maculinea) nausithous affects genetic diversity within Myrmica rubra host ant colonies

Evolutionary theory predicts that high genetic variation maintains plasticity in a species’ response to parasite pressure. However, higher genetic diversity might also cause easier infiltration by social parasites, because odour diversity is high and nest-mate recognition poor. Here we test if the obligate myrmecophile Lycaenid butterfly Phengaris nausithous, a parasite of colonies of the highly polygynous ant Myrmica rubra causes local adaptation by enhancing genetic variance in parasitized versus non parasitized ant populations M. rubra colonies from six infested and three uninfested sites were assayed at five microsatellite loci to quantify genetic variation. Our results reveal isolation by distance and a significantly enhanced intracolonial variance due to the parasite pressure.     

Interspecific differences in cuticular hydrocarbon profiles of Myrmica ants are sufficiently consistent to explain host specificity by Maculinea (large blue) butterflies

The chemical signatures on the cuticles of five common Myrmica ant species were analysed (49 colonies of M. rubra, M. ruginodis, M. sabuleti, M. scabrinodis and M. schencki), each ant being the specific host of one of the five threatened European species of Maculinea butterfly. The cuticular hydrocarbon profile (based on the relative abundance of each chemical) of each ant species was highly distinctive, even between the morphologically similar species M. sabuleti and M. scabrinodis. There was no significant difference in the chemical profiles of workers and larvae from any colony. Nor was there much pattern in the intraspecific variation: colonies from the same populations were significantly, but only slightly, more similar to each other than to colonies from distant populations. M. rubra showed remarkably little variation between populations sampled widely from northern Russia, Ukraine, Scotland and southern England. The data were compared with published profiles of M. rubra and two North American Myrmica species, and with a quantitative reanalysis of data for Maculinea rebeli caterpillars. We conclude that the hydrocarbon profiles of Myrmica species are sufficiently and consistently different for chemical mimicry to explain the pattern of host specificity recorded for the European Maculinea butterflies. The optimum strategy for chemical mimicry in each of the two life-styles of Maculinea larvae is discussed: we suggest that predatory species might benefit from mimicking the median profile of their model whereas the cuckoo species would benefit when variation between siblings encompasses a large range of the variation recorded within a local population of the model species.     

Species-specific distribution of two sympatric Maculinea butterflies across different meadow edges

An important consequence of habitat fragmentation is the increase of edge habitats. Environmental factors in the edges are different from those in the interiors, which causes changes in the distribution of plant and animal species. We aimed to study how edges affect the distribution of two butterfly species within meadow fragments. We therefore investigated the effect of distance from edge and edge type (road edge versus tree edge) on two sympatric large blue species (Maculinea teleius and M. nausithous). Our results showed that edge type had contrasting effects on the two species. M. teleius favoured both interiors and road edges, while M. nausithous preferred the tree edges. In the case of the latter species a strong positive edge effect was also found. This kind of within-habitat niche segregation is probably related to the different microenvironmental conditions at the edges. Foodplant density did not seem to limit the distribution of these species. Our results suggest that interiors of meadows are important for M. teleius, while tree edges maintain the habitats of the regionally rarer butterfly, M. nausithous.     

The ecology of Myrmica ants in relation to the conservation of Maculinea butterflies

Maculinea butterflies in Europe, and probably most of Asia, are host specific social parasites of various species of Myrmica ants. The latest summary of field data showing the pattern of host specificity by Maculinea is presented. Myrmica ants have been well studied in the laboratory but much less is known about the ecology of their natural populations. While the former is important in understanding the adaptive evolution of Maculinea larval behaviours, the latter is of more practical importance to conservationists charged with the protection of specific populations of Maculinea. The current knowledge of habitat partition, colony growth and colony reproduction within communities of Myrmica ants is summarized in relation to the ecology of Maculinea species. Concepts used in current population simulation models are explained. A key concept is the idea that community structure (both number of species and size and abundance of nests) is controlled by the quantity and quality of suitable nest sites. Some advice is given to conservationists who might need to manipulate Myrmica ant populations in order to maintain a robust population of a Maculinea species. © Rapid Science Ltd. 1998     

Isolation and genetic diversity of endangered grey nurse shark (Carcharias taurus) populations

Anthropogenic impacts are believed to be the primary threats to the eastern Australian population of grey nurse sharks (Carcharias taurus), which is listed as critically endangered, and the most threatened population globally. Analyses of 235 polymorphic amplified fragment length polymorphisms (AFLP) loci and 700 base pairs of mitochondrial DNA control region provide the first account of genetic variation and geographical partitioning (east and west coasts of Australia, South Africa) in C. taurus. Assignment tests, analysis of relatedness and Fst values all indicate that the Australian populations are isolated from South Africa, with negligible migration between the east and west Australian coasts. There are significant differences in levels of genetic variation among regions. Australian C. taurus, particularly the eastern population, has significantly less AFLP variation than the other sampling localities. Further, the eastern Australian sharks possess only a single mitochondrial haplotype, also suggesting a small number of founding individuals. Therefore, historical, rather than anthropogenic processes most likely account for their depauperate genetic variation. These findings have implications for the viability of the eastern Australian population of grey nurse sharks.     

Polymorphic growth in larvae of Maculinea butterflies, as an example of biennialism in myrmecophilous insects

The presence of annual and biennial individuals within the same population has been recently demonstrated in the myrmecophilous butterflies Maculinea rebeli and Maculinea alcon, which present a cuckoo strategy inside Myrmica nests, and Maculinea arion which is a predatory species. Here, we present field and laboratory data on polymorphic larval growth in two other predatory species of Maculinea: M. teleius and M. nausithous. Body mass distributions of pre-pupation larvae were bimodal in both species. These results point to the existence of larvae that develop in 1 or 2 years. We also showed that the probability of pupation depended on larval body mass. In the case of M. teleius, the critical body mass at which larvae have a 50% probability of pupation is about 80 mg. We suggest that polymorphism in Maculinea may have evolved as an adaptation to life in ant nests, a habitat which protects them from predators and provides food. However, the quality of this resource is highly variable and unpredictable. According to the bet-hedging hypothesis, if the habitat is unpredictable, females should have an advantage by producing more variable offspring. In the case of Maculinea butterflies, this may involve maintaining larvae that develop in 1 or 2 years.     

Comparative unpalatability of mimetic viceroy butterflies (Limenitis archippus) from four south-eastern United States populations

Viceroy butterflies (Limenitis archippus), long considered palatable mimics of distasteful danaine butterflies, have been shown in studies involving laboratoryreared specimens to be moderately unpalatable to avian predators. This implies that some viceroys are Müllerian co-mimics, rather than defenseless Batesian mimics, of danaines. Here, I further test this hypothesis by assessing the palatability of wild-caught viceroys from four genetically and ecologically diverse populations in the southeastern United States. Bioassays revealed that viceroys sampled from three sites in Florida and one in South Carolina were all moderately unpalatable to captive redwinged blackbird predators, which ate fewer than half of the viceroy abdomens presented. Red-wings commonly exhibited long manipulation times and considerable distress behavior when attempting to eat a viceroy abdomen, and they taste-rejected over one-third of viceroys after a single peck. These findings, the first based on wild-caught butterflies, support the hypothesis that the viceroy-danaine relationship in some areas represents Müllerian mimicry, prompting a reassessment of selective forces shaping the interaction. Moreover, considerable variation in palatability of individual viceroys, and in behavior of individual birds, contributes to the complexity of chemical defense and mimicry in this system.     

Comparison of genetic population structure of the large blue butterflies Maculinea nausithous and M. teleius

We investigated the genetic population structure of two rare myrmecophilous lycaenid butterflies, Maculinea nausithous and M. teleius, which often live sympatrically and have similar biology. In Europe, both species occur in highly fragmented populations and are vulnerable to local extinction. The proportion of variable allozyme loci, average heterozygosity and genetic differentiation among populations was higher in M. nausithous than in sympatrically living M. teleius populations. We hypothesise that the differences in heterozygosity are mainly due to the known higher efficiency of typical host ant nests in rearing M. nausithous pupae compared to M. teleius pupae. This implies a larger probability of larval survival in M. nausithous, which buffers populations against environmental and demographic stochasticity. In contrast, the lower carrying capacity of ant nests in rearing M. teleius pupae requires higher nest-densities and makes M. teleius populations more prone to losing genetic variation through drift if this condition is not fulfilled. The single investigated Russian population of M. teleius showed much higher levels of heterozygosity than any of the Polish populations, suggesting a more viable and still intact metapopulation structure.     

Viability analysis of endangered crayfish populations

The noble crayfish Astacus astacus L. is a threatened freshwater invertebrate. Many of the remaining populations are isolated and there is considerable concern that diseases and the increased frequency of flooding events may drive these remnant populations to extinction. We performed a population viability analysis for a typical isolated noble crayfish population. We quantified the extinction risk by the mean time to extinction within 1000 years for several scenarios (flooding events, restocking of adults). For a set of parameters derived from field estimates, we estimated the mean time to extinction to be 240 years. However, the median was only 80 years. Multiple sensitivity analysis by logistic regression revealed that spawning probability, juvenile and adult mortality were the important parameters for the survival of the population. The mean time to extinction decreased with increasing frequency of floodings. This is alarming, considering the magnitude of the effect and the expectation of an increasing number of floodings with global warming. Restocking, however, was found to have only a minor effect on the mean time to extinction. Overall, our simulations suggested that for the long-term and self-sustaining survival of the noble crayfish, particularly where they remain isolated, we have to improve the extent and quality of habitats. Nevertheless, additional measures are necessary, especially the removal of dispersal barriers to allow some exchange of individuals between populations. However, this also calls for a control of invasive crayfish species.     

Rampant drift in artificially fragmented populations of the endangered tidewater goby (Eucyclogobius newberryi)

Habitat fragmentation and its genetic consequences are a critically important issue in evaluating the evolutionary penalties of human habitat modification. Here, we examine the genetic structure and diversity in naturally subdivided and artificially fragmented populations of the endangered tidewater goby (Eucyclogobius newberryi), a small fish restricted to discrete coastal lagoons and estuaries in California, USA. We use five naturally fragmented coastal populations from a 300‐ km spatial scale as a standard to assess migration and drift relative to eight artificially fragmented bay populations from a 30‐ km spatial scale. Using nine microsatellite loci in 621 individuals, and a 522‐base fragment of mitochondrial DNA control region from 103 individuals, we found striking differences in the relative influences of migration and drift on genetic variation at these two scales. Overall, the artificially fragmented populations exhibited a consistent pattern of higher genetic differentiation and significantly lower genetic diversity relative to the naturally fragmented populations. Thus, even in a species characterized by habitat isolation and subdivision, further artificial fragmentation appears to result in substantial population genetic consequences and may not be sustainable.     

Local adaptation in European populations of Arabidopsis lyrata (Brassicaceae)

We studied local adaptation to contrasting environments using an organism that is emerging as a model for evolutionary plant biology-the outcrossing, perennial herb Arabidopsis lyrata subsp. petraea (Brassicaceae). With reciprocal transplant experiments, we found variation in cumulative fitness, indicating adaptive differentiation among populations. Nonlocal populations did not have significantly higher fitness than the local population. Experimental sites were located in Norway (alpine), Sweden (coastal), and Germany (continental). At all sites after one year, the local population had higher cumulative fitness, as quantified by survival combined with rosette area, than at least one of the nonlocal populations. At the Norwegian site, measurements were done for two additional years, and fitness differences persisted. The fitness components that contributed most to differences in cumulative fitness varied among sites. Relatively small rosette area combined with a large number of inflorescences produced by German plants may reflect differentiation in life history. The results of the current study demonstrate adaptive population differentiation in A. lyrata along a climatic gradient in Europe. The studied populations harbor considerable variation in several characters contributing to adaptive population differentiation. The wealth of genetic information available makes A. lyrata a highly attractive system also for examining the functional and genetic basis of local adaptation in plants.     

Genetic structure of wild populations of the endangered Desert Pupfish complex (Cyprinodontidae: Cyprinodon)

Data from 10 microsatellite DNA loci were used to describe the genetic structure of the two extant species (Cyprinodon macularius and C. eremus) of the endangered Desert Pupfish complex of southwestern United States and northwestern Mexico. Variation at microsatellite loci was significantly correlated (Mantel test) with that of previous mtDNA results, both for the complex and for the relatively wide-ranging C. macularius alone. Both species showed unusually high levels of microsatellite diversity for non-marine fish (H _e = 0.84–0.93; A_R = 11.9–17.0). There was evidence (R _ST > F _ST) that the two extant populations of C. eremus have been isolated sufficiently long for mutation to contribute significantly to genetic divergence, whereas divergence among the nine assayed populations of C. macularius could be attributed to genetic drift alone. Correspondingly, 10% of the diversity in C. eremus was attributable to differences between the two populations, whereas, for C. macularius, only 2.7% was attributable to among-population variation. Within C. macularius, a small (0.8%), but statistically significant, portion was attributable to differences between populations in the Salton Sea area and those on the lower Colorado River delta. The two populations of C. eremus and five groups of populations of C. macularius are recommended as management units for conservation genetics management of the two species.     

Patterns of differentiation among endangered pondberry populations

Pondberry, Lindera melissifolia, is an endangered and partially clonally reproducing shrub species found in isolated populations that inhabit seasonally wet depressions in forested areas of the lower Mississippi River alluvial valley and southeastern regions of the United States. With eleven microsatellite loci, we quantified population genetic differentiation and diversity among 450 genets in 10 locations distributed across pondberry’s range. We used estimates of F _st and Jost’s D _est to measure genetic differences between populations and between geographic regions. The largest pairwise regional difference was found between eastern and western regional population groups (F _st = 0.23, D _est = 0.67), with the northern-most population groups in each region exhibiting larger divergence from each other than the southern-most population groups. Genetic diversity was lowest in the Sand Pond Conservation Area (A _e = 1.9, H _e = 0.36), which was the northern-most pondberry population, and highest in the Francis Marion National Forest (A _e = 4.1, H _e = 0.69), although we identified only 17 genets in that admixed population. Following adjustments for estimated null allele frequencies, we identified heterozygote excess in four eastern populations and found no evidence for inbreeding in any population. The observed patterns of differentiation indicate a phylogeography that exhibits an Appalachian Mountain discontinuity coupled with northward migrations along the Southern Atlantic Coastal Plain and into the Mississippi Alluvial Plain. The genetic consequences of this proposed phylogeographical structure may affect selection of germplasm sources for population reestablishment programs across pondberry’s range.     

Conservation implications of source-sink dynamics within populations of endangered <Emphasis Type="Italic">Maculinea</Emphasis> butterflies

Conservation programmes are often based on snapshot information on animal abundance. However, land fragments with high numbers of individuals do not necessarily represent their natal areas, which are crucial for species persistence. A classic example of the above principle are source-sink systems, in which excess individuals emigrate from source areas during their lifetime and gather in sink areas. We demonstrated the existence of source-sink dynamics in two species of endangered Maculinea (=Phengaris) butterflies. Sympatrically occurring M. nausithous and M. teleius were investigated with mark-recapture sampling during the entire flight period. In the first half of the season a great majority of butterflies were captured within the relatively small central part of the site, while later their numbers became similar between the site centre and its peripheries. The analysis of movements indicated that most individuals captured in the peripheral zone eclosed in the central zone. Moreover, the timing of the sharp increase in movements from the site centre to its peripheries corresponded well with the period when the number of eggs laid in the former area reached carrying capacity, defined by the number of the Sanguisorba officinalis foodplant flowerheads available for oviposition. Within the peripheral zone the foodplant availability greatly exceeded the egg load, but in contrast the abundance of host ants (i.e. the other essential resource) was low, which presumably results in low Maculinea larval survival there. Our findings imply that setting conservation priorities over different land fragments should take into account dispersion of individuals among them.     

Mitochondrial DNA diversity and phylogeography of endangered green turtle (Chelonia mydas) populations in Africa

We analysed the genetic structure of seven nesting sites of the endangered green turtle (Chelonia mydas) in Africa using mitochondrial DNA control region sequences. Tissue samples were collected from 188 nesting females at six sites in West Africa and one in the Indian Ocean. A 488 bp fragment of the control region revealed 14 different haplotypes, 10 of which are previously undescribed. The most common haplotype (CM8) was observed in 157 individuals. All other haplotypes were closely related, except two divergent lineages: CM38, removed by four substitutions, and the three Indian Ocean haplotypes, distinguished by 31 substitutions. Significant differences in haplotype and nucleotide diversity were observed between Atlantic rookeries and among ocean basins. Analysis of molecular variance revealed high levels of differentiation between the Atlantic and the Indian Ocean populations but a much shallower Atlantic substructuring. Green turtle population genetic structure is thought to have been shaped by a dynamic succession of extinction and recolonisation of rookeries, by natal homing and occasional breakdown in nest-site fidelity. Mismatch distributions of pairwise differences between haplotypes at each rookery were found to be consistent with recent population expansion. We argue that demographic histories can be explained by scenarios at several temporal scales, including geological events, sea level fluctuations and more recent patterns of exploitation. We discuss management and conservation implications of our results for these threatened populations, identifying two ESUs (one in the Atlantic and one in the Indian ocean) and three MUs within the Atlantic.