Deceptive female oviposition behaviour elicits male ejaculation in the European bitterling

In European bitterling Rhodeus amarus , fish that lay their eggs in the gill chambers of living freshwater mussels, females perform conspicuous behaviours associated with spawning that increases the probability of males performing ejaculatory behaviour and participating in a spawning. A significant positive association was detected between behaviour in which a female performs a spawning action but without releasing eggs, here termed 'deceptive female oviposition', and ejaculatory behaviour by courting males.     

A proximate cue for oviposition site choice in the bitterling (Rhodeus sericeus)

1. We investigated two possible proximate cues used for oviposition site choice by females of the bitterling ( Rhodeus sericeus ), a freshwater fish that spawns on the gills of live unionid mussels. The two cues were the flow velocity and/or oxygen content of water emerging from the exhalant siphon of a mussel.
2. Field observations showed that female bitterling always inspected the exhalant siphons of mussels before they spawned in them. Siphon inspection was not always a prelude to spawning and it may serve as a means of assessing mussel quality. Female skimming behaviour, swimming over a mussel without spawning, may also be used to assess mussel quality, although the mechanism for this is unclear.
3. Measurements of the flow velocity of water emerging from the exhalant siphons of four mussel species ( Anodonta anatina, A. cygnea, Unio pictorum and U. tumidus ) showed a significant difference among species, with U. tumidus having the highest mean flow velocity and U. pictorum the lowest.
4. Measurements of the change in oxygen concentration of water entering a mussel inhalant siphon and leaving its exhalant siphon in field and laboratory studies showed a significant difference among the four mussel species, with A. cygnea exhibiting a significantly higher change in oxygen concentration than the other species.
5. The presence of bitterling embryos in the gills of a mussel significantly increased its oxygen consumption whereas larval glochidia had no significant effect. We discuss oxygen availability as a possible proximate cue for oviposition site choice in bitterling.     

The cost of polyphagy: oviposition decision time vs error rate in a butterfly

Neural constraints on information processing have emerged as a possible general explanation for why a majority of plant-feeding insects are relative specialists. According to the hypothesis, acquiring and processing information necessary to make fast and accurate oviposition decisions will carry a cost. As plants constitute a vast but diverse resource, the cost can be expected to increase with increasing host range. The cost can be paid in two currencies: time or accuracy. Both types of costs have been demonstrated, using a variety of taxa including butterflies. However, all studies have measured either one of the two currencies. Hence, there is the possibility that a decrease in one of the currencies can be compensated by an increase in the other, in which case the net outcome may not be a cost at all. Poor oviposition decisions could then be counterbalanced by shorter decision times, which could lead to higher realized fecundity. Using two strains of butterflies ( Polygonia c-album ) with different degrees of specificity, I test the hypothesis that the previously reported higher error rates in the more polyphagous butterflies are compensated by shorter decision times at oviposition. Post-alighting decision times were measured while the females evaluated a preferred plant ( Urtica dioica ) for oviposition. Contrary to the expectations, the polyphagous butterflies actually had longer decision times than the specialized butterflies, giving no support for the quality vs. quantity hypothesis. Instead, the results suggests that the polyphagous butterflies do pay a real cost for their wide host range and thus gives increased support for the information processing hypothesis as a general explanation for the widespread host specificity among plant-feeding insects.     

Host plant constituents as oviposition stimulants for a generalist herbivore: European corn borer

Oviposition response of the polyphagous European corn borer,Ostrinia nubilalis (Hübner) (Lepidoptera: Pyralidae), to chemical constituents in host plants was investigated in the laboratory using two-choice bioassays. Foliar extracts of corn (Zea mays L.), pepper (Capsicum annuum L.) and potato (Solanum tuberosum L.) were prepared using the solvents pentane, acetone and methanol. In all three host plants, chemicals soluble in pentane stimulated oviposition. In potato, chemicals extractable in acetone also elicited a positive oviposition response. When presented with a choice between pentane extracts of corn and pepper, females preferred corn. No preferences were exhibited between pentane extracts of corn and potato or pepper and potato. Pentane extracts of corn husks, tassels, silk, and corn leaves from plants at early whorl and tassel (pre-pollen shed) stages of development also stimulated oviposition. Similar extracts from plants at 2-leaf and blister (when kernels resemble blisters) stages were not stimulatory. This indicates that plant phenology affects chemically mediated oviposition response in European corn borer. The potential use of plant chemicals for management ofO. nubilalis in the field is suggested.     

Development of European bitterling in the gills of freshwater mussels

The development of bitterling embryos within the unique environment of a freshwater mussel's gills requires a departure from typical cyprinid embryological development. Eggs are large (2·6×1·7 mm), illustrating the low risk of predation, and elliptical; a response to unionid gill morphology and a way of increasing the transfer rates of respiratory and excretory products to and from the tissues. The yolk sac develops elongated lateral processes during early ontogeny; these secure the embryo into the host's interlamellar space. Once the larva is capable of movement (8·2 mm) the lateral processes are lost and the larva becomes less dependent of the host's gills for the provision of oxygen. Hatching (3·3 mm) and pigmentation of the blood (6·4 mm) occur relatively early; this may increase the rate of oxygen supply to the tissues. Pigmentation of the eyes and appearance of the melanophores occurs relatively late (7·4 mm and 7·9 mm, respectively); embryos are not required to detect or avoid predators. Bitterling larvae generally emerge from the host once the yolk sac has been consumed (10·5 mm); this may mark a change in respiratory and nutritional requirements.     

A morphological and genetic analysis of the European bitterling species complex

Bitterling fishes lay their eggs on the gills of living freshwater mussels and are valuable models in behavioural and evolutionary ecology. We used morphological and genetic data to resolve the taxonomic relationships of bitterling in Europe. Previous studies have suggested the European bitterling is either a single species with a wide but discontinuous geographic distribution, or a complex of species. Morphometric and meristic data identified differences between three putative species; with a clear distinction between the eastern Asian Rhodeus sericeus, western European bitterling Rhodeus amarus, and colchian bitterling, Rhodeus colchicus. Polymorphism in the mitochondrial DNA control region was predominantly due to insertion/deletion events, making phylogenetic inference difficult, but the single haplotype found in R. sericeus populations was detected at low frequency (one of 24 individuals) in R. amarus and R. colchicus populations. Eight control region haplotypes were found in R. amarus populations, which were distinct from the two haplotypes in a R. colchicus population. Cytochrome b data produced a phylogeny with strongly‐supported differentiation between a clade of two R. sericeus haplotypes and a clade of six R. amarus/colchicus haplotypes. The star‐like topology of the R. amarus/colchicus haplotypes in a minimum spanning network suggested a rapid radiation in this clade. Our results are consistent with an hypothesis of relatively ancient divergence of R. sericeus from R. amarus/colchicus and more recent and rapid differentiation between R. amarus and R. colchicus. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 95 , 337–347.     

Characterizing the cost of oviposition in insects: a dynamic model

The development of a consensus model of insect oviposition has been impeded by an unresolved controversy regarding the importance of time costs versus egg costs in mediating the trade-off between current and future reproduction. Here I develop a dynamic optimization model that places time and egg costs in a common currency (opportunity costs expressed as decreased lifetime reproductive success) so that their relative magnitudes can be compared directly. The model incorporates stochasticity in host encounter and mortality risk as well as behavioral plasticity in response to changes in the age and egg load of the ovipositing female. The dynamic model's predictions are congruent with those of a simpler, static model: both time- and egg-mediated costs make important contributions to the overall cost of oviposition. Modest quantitative differences between the costs predicted by the static versus dynamic models show that plasticity of oviposition behavior modulates the opportunity costs incurred by reproducing females. The relative importance of egg-mediated costs increases substantially for oviposition events occurring later in life. I propose that the long debate over how to represent the cost of oviposition should be resolved not by advocating the pre-eminence of one sort of cost above all others, but rather by building models that represent the complementary roles of different costs. In particular, both time and egg costs must be recognized to produce a general model of insect oviposition that incorporates a realistic representation of the cost of reproduction. This revised version was published online in July 2006 with corrections to the Cover Date.     

Seasonal dynamics in population characteristics of European bitterling Rhodeus amarus in a small lowland river

The seasonal dynamics of biological traits in a population of European bitterling Rhodeus amarus from a small river in central Europe (River Kyjovka, Czech Republic) were investigated from April 2007 to March 2008. The reproductive season lasted from early April to mid-June, with a peak in late April when > 50% of females possessed ripe eggs in their ovaries. The sex ratio was female-biased, with a higher bias following the peak in reproduction, suggesting higher mortality of males than females over the reproductive period. The population was effectively annual, with a major decrease in adult fish abundance at the end of the reproductive period. Highest relative lipid content and condition factor were observed in February, both decreasing with an increase in investment into gonads. Seasonal dynamics in somatic condition, relative lipid content and gonad mass, and their comparison with other R. amarus populations, suggest that the study population allocated a disproportionally high level of resources to reproduction.     

Molecular cytogenetic study of the European bitterling Rhodeus amarus (Teleostei: Cyprinidae: Acheilognathinae)

The European bitterlings (Rhodeus amarus) from the Eastern locations were cytogenetically examined by conventional and molecular techniques. All analyzed individuals presented invariably the same chromosomal constitution of 2n = 48, with 8 metacentrics + 20 submetacentrics + 20 subtelo-acrocentrics and C-banding positive heterochromatin at the pericentromeric regions in most of the chromosomes. Moreover, some of the chromosomes had short arms entirely built with heterochromatin. GC-rich Ag-NORs (nucleolus organizer regions) were located at the short arms of two submetacentric chromosomes, and the length polymorphism of these regions was found. Multiple location of 28S rDNA sequences with fluorescence in situ hybridization signals was observed on the long and/or short arms of three submetacentric chromosomes including NOR regions and short arms of three to five acrocentric chromosomes in the studied fish. 5S rDNA sites were found on the short arms of two subtelocentric chromosomes, and telomeric repeats were localized at the ends of all chromosomes. Provided results have expanded our knowledge concerning genetic characteristics of the European bitterlings that may be profitable in the conservation programs of this endangered species.     

Dancing for a decision: a matrix model for nest-site choice by honeybees

A mathematical model is formulated for decision making by honeybees during nest-site choice, using a population matrix model. This model explains how the observed dynamics of the nest-site scouts' dancing can reliably lead to a choice of the best nest site available.     

A possible evolutionary lag in the relationship between freshwater mussels and European bitterling

The coevolutionary dynamics between European bitterling Rhodeus amarus and freshwater unionid mussels, which the former parasitize by laying eggs on their gills, were tested. In a series of experiments fish preferences and mussel responses were compared in parasites and hosts of recent (Europe) and ancient (Asia) sympatry. Rhodeus amarus readily oviposited on the gills of all mussel species tested. Fish that laid their eggs on the gills of Asian Anodonta woodiana, however, suffered a dramatic reduction in reproductive success compared to fish that oviposited on the gills of European mussels: Unio pictorum , Unio tumidus , Anodonta anatina and Anodonta cygnea . This difference was the result of egg ejection behaviour by mussels rather than the unsuitability of the internal gill environment for European bitterling embryo development. The ejection response of mussels with a long sympatry with European bitterling was considerably more pronounced than that of mussels with a substantially shorter sympatry. The data support a coevolutionary arms race between bitterling and mussels and point to an evolutionary lag in the relationship between R. amarus and its European mussel hosts.     

The decision to reject an oviposition site: sequential analysis of the post-alighting behaviour of Delia floralis

Abstract.The post-alighting behaviour of gravid female turnip root fly, Delia floralis (Fallén) (Diptera: Anthomyiidae), was observed in the laboratory, using four plant genotypes differing in antixenotic resistance, to stimulate a range of oviposition-related behavioural events. Analysis of the behavioural sequences of individual female flies suggested that during the post-alighting behaviour of D. floralis , the decision to reject a highly resistant plant was predominantly based on plant cues received during a stationary period immediately after landing on the leaf (the leaf contact phase). Female flies that rejected a plant immediately after the leaf contact phase did so after spending approximately twice as long in the leaf contact phase as those flies that continued to explore the plant. On a plant genotype of intermediate susceptibility, D. floralis females on the stem of the plants increased proboscis extension. The mechanisms involved in early host plant rejection decisions and the possible ecological advantages of such behaviour patterns to female flies seeking suitable oviposition sites are explored. The potential advantages of using detailed studies of individual behaviour sequences to focus studies seeking to elucidate chemical oviposition stimuli on the plant's surface are also discussed.     

Male coloration signals direct benefits in the European bitterling (Rhodeus amarus)

Female mating preferences are frequently associated with exaggerated male sexual traits. In the European bitterling, Rhodeus amarus, a fish with a resource-based mating system, male coloration is not associated with indirect genetic benefits of female mate choice, and does not reliably signal spawning site quality. We tested a link between the extent of male carotenoid-based coloration and testis size and number of spermatozoa stripped from the testes. Male body size predicted spermatozoa number, but less reliably than the extent of male coloration. Male color was a highly significant predictor of spermatozoa number, with approximately 26 % of variance in the number of spermatozoa stripped from males predicted from male color after controlling for male body size. Body size, but not coloration, predicted teste size. Female bitterling often risk sperm limitation, especially during pair spawnings, and male nuptial coloration may be under direct selection through female mate choice as a signal of male fertilization efficiency.     

Sexual signaling in the European bitterling: females learn the truth by direct inspection of the resource

In many taxa females appear to base their mate choice on multipletraits. But the relative importance of different traits inmate choice has rarely been determined. Here we show that femalesof a freshwater fish, the European bitterling, Rhodeus sericeus,base their mate choice on multiple traits that differ in theirreliability as indicators of expected reproductive successand are used at different stages of the decision process. Theinitial decision to inspect a male is based on male behaviorand red coloration, whereas the final spawning decision isbased on the quality of the live unionid mussel, Anodonta anatina,that the male is defending as an oviposition site. Male traitsmay indicate which males are worth inspecting by reflectingmale quality, such as reproductive condition and genetic constitution.Male traits do not, however, reflect mussel quality, as bright males also court females vigorously toward mussels that yielda low probability of survival of the offspring. Females, onthe other hand, are choosier than males in their choice ofspawning site and seem to gain reliable information about thesurvival probability of the eggs by inspecting the mussel directly.     

The first record of endophytic insect oviposition from the Tartarian of European Russia

The first endophytic oviposition in a plant leaf from the Tatarian of European Russia (Isady locality) is formally described as Paleoovoidus rasnitsyni, sp. nov. This find supplements considerably the data on plant-insect interaction recorded in this locality.     

The function of multiple ejaculations in bitterling

In some taxa, males perform multiple ejaculations, which may function in sperm competition or in maintaining a baseline density of spermatozoa in the female reproductive tract to ensure fertilization, a process that has been termed ‘topping up’. We investigated the function of multiple ejaculations in two species of bitterling, the European bitterling (Rhodeus amarus) and Chinese rose bitterling (Rhodeus ocellatus). Bitterling oviposit in living freshwater mussels, with fertilization taking place within the mussel gill cavity. Thus, although fertilization is external, the mussel is analogous to the female reproductive tract in an internally fertilizing species. We measured the frequency of ejaculations and mussel inspections by individual males of two bitterling species in 28 replicated mesocosms and examined focal male responses to rival ejaculations and the presence of females in spawning condition. We used a model of ejaculatory behaviour to simulate the temporal abundance of spermatozoa in mussels. Male R. amarus exhibited high rates of ejaculation and inspection of the siphons of mussels and increased their ejaculation rate in response to the presence of females in spawning condition. Rhodeus ocellatus showed lower overall rates of ejaculation, but significantly elevated ejaculation rate in response to rival ejaculations. The ejaculatory strategy of R. amarus is one that maintains a minimum level of spermatozoa in mussels, which is elevated when the probability of oviposition increases. In contrast, R. ocellatus engages more directly in sperm competition with rivals. We discuss these results in the context of the function of multiple ejaculations and male mating tactics.