Costs of two non-mutualistic species in a yucca/yucca moth mutualism

Mutualisms often involve significant costs for participants. Costs are inflicted by mutualists themselves, as well as by associated, non-mutualistic species. These costs are rarely quantified, however, particularly the ones extrinsic to the pairwise interaction. We compare costs inflicted by an obligate mutualist pollinator and two common exploiters of an Arizona yucca over a 2-year period. The magnitude of seed damage from seed and fruit-feeding beetle larvae (Carpophilus longus, Nitidulidae) was similar to damage from the seed-eating larvae of Yucca schottii's pollinator moth Tegeticula yuccasella (Prodoxidae), averaging about 15 seeds destroyed per fruit in each case. The two seed predators usually fed within the same fruits, although rarely side by side. In contrast, the presence of fruit-galling moth larvae (Prodoxusy-inversus, Prodoxidae) appeared to benefit the yucca: individual Tegeticula destroyed only half as many seeds in galled fruits as they did in ungalled fruits. We discuss three general implications of these results. Firstly, the costs of non-mutualists to the two mutualistic partners are not necessarily parallel. Secondly, measurable costs of non-mutualists do not necessarily translate into an impact on the success of the mutualism itself, because they may be incurred after mutualistic activities take place. Finally, the costs of mutualists to each other can differ substantially depending on the presence or absence of non-mutualistic species. Received:17 July 1996 / Accepted:10 June 1997     

Gas exchange and chlorophyll fluorescence responses of three south-western Yucca species to elevated CO2 and high temperature

The ability of seedlings to tolerate temperature extremes is important in determining the distribution of perennial plants in the arid south-western USA, and the manner in which elevated CO₂ impacts the ability of plants to tolerate high temperatures is relatively unknown. Whereas the effects of chronic high temperature (30–38°C) and elevated CO₂ are comparatively well understood, little research has assessed plant performance in elevated CO₂ during extreme (> 45 °C) temperature events. We exposed three species of Yucca to 360 and 700 μmol CO₂ mol^–1 for 8 months, then 9 d of high temperature (up to 53 °C) to evaluate the impacts of elevated CO₂ on the potential for photosynthetic function during external high temperature. Seedlings of a coastal C₃ species (Yucca whipplei), a desert C₃ species (Yucca brevifolia), and a desert CAM species (Yucca schidigera), were used to test for differences among functional groups. In general, Yuccas exposed to elevated CO₂ showed decreases in carboxylation efficiency as compared with plants grown at ambient before the initiation of high temperature. The coastal species (Y. whipplei) showed significant reductions (33%) in CO₂ saturated maximum assimilation rate (A_max), but the desert species (Y. brevifolia and Y. schidigera) showed no such reductions in A_max. Stomatal conductance was lower in elevated CO₂ as compared with ambient throughout the temperature event; however, there were species-specific differences over time. Elevated CO₂ enhanced photosynthesis in Y. whipplei at high temperatures for a period of 4 d, but not for Y. brevifolia or Y. schidigera. Elevated CO₂ offset photoinhibition (measured as F_v/F_m) in Y. whipplei as compared with ambient CO₂, depending on exposure time to high temperature. Stable F_v/F_m in Y. whipplei occurred in parallel with increases in the quantum yield of photosystem II (ΦPSII) at high temperatures in elevated CO₂. The value of ΦPSII remained constant or decreased with increasing temperature in all other treatment and species combinations. This suggests that the reductions in F_v/F_m resulted from thermal energy dissipation in the pigment bed for Y. brevifolia and Y. schidigera. The greater efficiency of photosystem II in Y. whipplei helped to maintain photosynthetic function at high temperatures in elevated CO₂. These patterns are in contrast to the hypothesis that high temperatures in elevated CO₂ would increase the potential for photoinhibition. Our results suggest that elevated CO₂ may offset high-temperature stress in coastal Yucca, but not in those species native to drier systems. Therefore, in the case of Y. whipplei, elevated CO₂ may allow plants to survive extreme temperature events, potentially relaxing the effects of high temperature on the establishment in novel habitats.     

Variation in the costs and benefits of mutualism: the interaction between yuccas and yucca moths

Summary Yucca moths are both obligate pollinators and obligate seed predators of yuccas. I measured the costs and net benefits per fruit arising for eight species of yuccas from their interaction with the yucca moth Tegeticula yuccasella. Yucca moths decrease the production of viable seeds as a result of oviposition by adults and feeding by larvae. Oviposition through the ovary wall caused 2.3–28.6% of ovules per locule to fail to develop, leaving fruit with constrictions, and overall, 0.6–6.6% of ovules per fruit were lost to oviposition by yucca moths. Individual yucca moth larvae ate 18.0–43.6% of the ovules in a locule. However, because of the number of larvae per fruit and the proportion of viable seeds, yucca moth larvae consumed only 0.0–13.6% of potentially viable ovules per fruit. Given both oviposition and feeding effects, yucca moths decreased viable seed production by 0.6–19.5%. The ratio of costs to (gross) benefits varied from 0% to 30%, indicating that up to 30% of the benefits available to yuccas are subsequently lost to yucca moths. The costs are both lower and more variable than in a similar pollinator-seed predator mutualism involving figs and fig wasps.There were differences between species of yuccas in the costs of associating with yucca moths. Yuccas with baccate fruit experienced lower costs than species with capsular fruit. There were also differences in costs between populations within species and high variation in costs between fruit within populations. High variability was the result of no yucca moth larvae being present in over 50% of the fruit in some populations, while other fruit produced up to 24 larvae. I present hypotheses explaining both the absence and high numbers of larvae per fruit.     

Leaf anatomy is not correlated to CAM function in a C3+CAM hybrid species,Yucca gloriosa

Background and AimsCrassulacean acid metabolism (CAM) is often considered to be a complex trait, requiring orchestration of leaf anatomy and physiology for optimal performance. However, the observation of trait correlations is based largely on comparisons between C₃ and strong CAM species, resulting in a lack of understanding as to how such traits evolve and the level of intraspecific variability for CAM and associated traits.MethodsTo understand intraspecific variation for traits underlying CAM and how these traits might assemble over evolutionary time, we conducted detailed time course physiological screens and measured aspects of leaf anatomy in 24 genotypes of a C₃+CAM hybrid species, Yucca gloriosa (Asparagaceae). Comparisons were made to Y. gloriosa’s progenitor species, Y. filamentosa (C₃) and Y. aloifolia (CAM).Key ResultsBased on gas exchange and measurement of leaf acids, Y. gloriosa appears to use both C₃ and CAM, and varies across genotypes in the degree to which CAM can be upregulated under drought stress. While correlations between leaf anatomy and physiology exist when testing across all three Yucca species, such correlations break down at the species level in Y. gloriosa.ConclusionsThe variation in CAM upregulation in Y. gloriosa is a result of its relatively recent hybrid origin. The lack of trait correlations between anatomy and physiology within Y. gloriosa indicate that the evolution of CAM, at least initially, can proceed through a wide combination of anatomical traits, and more favourable combinations are eventually selected for in strong CAM plants.     

Trends in floral scent chemistry in pollination syndromes: floral scent composition in hummingbird-pollinated taxa

We studied an assemblage of 17 species of bird-pollinated Ecuadorian plants (from 14 angiosperm families), including taxa pollinated by short-billed (trochiline) and sickle-billed (hermit) hummingbirds. Hummingbirds are widely supposed to ignore fragrance while visiting flowers. We collected floral headspace odours in order to test the general prediction that specialist hummingbird-pollinated flowers are scentless. In nine out of 17 of these species we failed to detect any odours using gas chromatography-mass spectrometry (GC-MS), whereas the remaining eight species produced trace levels of volatile compounds. Most of these odour compounds were of terpenoid or lipoxygenase derivation and are commonly emitted by vegetative as well as floral plant tissues. Further studies will be required to determine whether these weak odours attract alternative pollinators, repel enemies or represent vestiges of a scented ancestry.  © 2004 The Linnean Society of London, Botanical Journal of the Linnean Society , 2004, 146 , 191–199.     

The scent of age

In many species, older males are often preferred mates because they carry 'good' genes that account for their viability. How females discern a male's age is a matter of question. However, for animals that rely heavily on chemical communication there is some indication that an animal's age can be determined by its scent. To investigate whether there are changes in body odours with age, and if so their composition, mice were trained in a Y-maze to discriminate urine odours of donor mice of different ages: Adult (3-10 months old) and Aged (more than 17 months old). Trained mice could discriminate between these two age groups by odour alone. To determine the chemical basis for these discriminations, studies were performed using gas chromatography and mass spectrometry. These analyses demonstrated differences in the ratio of urinary volatiles with age. The most prominent differences involved significantly greater amounts of 2-phenylacetamide and significantly lower amounts of methylbutyric acids in Aged animals relative to Adult animals. Fractionating and manipulating the levels of these compounds in the urine demonstrated that the mice can distinguish age based on variation in amounts of these specific compounds in the combined urine.     

The scent of fear

In this study we tried to find out if fear can be detected from human body odours. Female subjects wore under-arm axillary pads while watching a terrifying film. Saliva cortisol samples were taken before and after the film presentation as a hormonal measure for the fear response. The fear experience itself was measured by Spielberger's State-Trait Anxiety Inventory. A "neutral" film, shown one day after the "fear" film, was used as a control in a repeated measures design. In part two of the experiment, the axillary pads were presented to female subjects in a triple forced choice test. Results show that subjects were able to discriminate between fear and non-fear axillary pads, suggesting that women are indeed able to detect "the scent of fear". A direct correlation between induced fear, changes in cortisol levels and smell ratings could not be established. Thus cortisol levels are probably not the inducer of the scent of fear and a hypothetical fear pheromone could have other origins.     

Floral scent and intrafloral scent differentiation inMoneses andPyrola (Pyrolaceae)

Floral scent was collected by headspace methods from intact flowers, petals, and stamens of four species ofPyrolaceae. The scent samples were analyzed by coupled gas chromatography-mass spectrometry (GC-MS). The floral scent inPyrola spp. is differentiated into a characteristic petal scent—phenyl propanoids and a characteristic stamen scent—methoxy benzenes. InMoneses the scent is characterized by isoprenoids and benzenoids, with a larger proportion of benzenoids in the stamens compared to the petals. Specific anther scents may promote foraging efficiency in buzz-pollinated species and enhance flower fidelity. Variation in floral scent composition is consistent with the taxonomic relationships among the genera and species examined.     

Trends in floral scent chemistry in pollination syndromes: floral scent composition in moth-pollinated taxa

KNUDSEN, J. T. & TOLLSTEN, L., Trends in floral scent chemistry in pollination syndromes: floral scent composition in moth-pollinated taxa. Floral scent from 15 moth-pollinated species in nine families was collected by head-space adsorption. The chemical composition was determined by coupled gas chromatography-mass spectrometry (GC-MS). The typical floral scent of moth-pollinated flowers contains some acyclic terpene alcohols, their corresponding hydrocarbons, benzenoid alcohols and esters and small amounts of some nitrogen compounds. The floral scent composition of sphingophilous flowers can be distinguished from that of phalaenophilous flowers by the presence of oxygenated sesquiterpenes. The flowers of three of the studied species had the general appearance and floral scent composition of moth-pollinated flowers, but contained no nectar reward. These species probably rely on deceptive pollination by naive visitors, which are deceived by the similarity of the flowers' morphological and scent chemistry to that of rewarding moth flowers. The finding of similar or structurally closely related floral scent compounds in both temperate and tropical species from both the Old and New worlds suggests that floral scent composition has been selected by a specific group of pollinators, moths that have similar sensory preferences. The functions of floral scent in moth-pollinated flowers are discussed in relation to an often observed over-representation of male moth visitors.     

王朗自然保护区中大熊猫发情场的嗅味树和嗅味标记调查

2004年2月底至4月中旬,我们对四川省王朗国家自然保护区内大熊猫(Ailuropodamelanoleuca)发情场的嗅味标记和嗅味树进行了调查,以了解王朗大熊猫的发情时间和发情场位置,为确定保护区内的重点保护区域和时间段提供证据,同时增加对大熊猫生物学特性的了解。在海拔2500–3200m间,共对10条样带进行了36次调查,测量并记录了山脊上1801株乔木的种类、高度、胸径和嗅味标记状况。调查共发现24株被大熊猫标记的嗅味树,其中54%位于种群分布中心区域内两侧都有森林分布的山脊上,70.8%分布于海拔2700–3000m之间。嗅味树的平均胸径为37.2±17.8cm(N=24),其中92%为岷江冷杉(Abiesfargesiivar.faxoniana),96%树皮粗糙或比较粗糙。嗅味标记中,75%的嗅味标记为肛周腺分泌物,标记中心的平均高度为51.8±15.6cm(N=18),25%为尿液,尿液上沿的平均高度为64.5±14.5cm(N=6)。此外,从调查结果初步得知,春季王朗最重要的大熊猫发情场所是长白沟-解放沟等区域,这里是大熊猫种群的关键栖息地。目前保护区对这些关键栖息地加强了保护力度。     

Cutaneous blood vessels in scent pigs

The purpose of this study was to systematically provide anatomic data for flap research in plastic surgery on the cutaneous blood vessels. Seven scent pigs used in this study were killed anesthetically, and their carotid vessels were intubated and injected with a black liquid rubber. Twenty-four hours later, the integument of the scent pig was removed, and the perforating points of the cutaneous vessels were recorded. The different-sized pieces of integument became transparent. Part of this transparent skin tissue was cut into cross-sectional strips. There were three types of the cutaneous vascular source, the same as in humans. Six division levels of vessels in the skin were identified, which formed five vascular plexuses and two systems (the perforating vessel system and the cutaneous vessel system). There were two sets of vein systems: the concomitant vein and the oscillating vein; the latter can be divided into regular and irregular types. The structures of the perforating vessel system and the cutaneous vessel system were the morphological basis for choosing flaps. Two anatomic points have been emphasized: the preserved vascular plexus in thin flaps (not the subcutaneous vascular network reported previously) and the dependency of vascular structure on its location. Otherwise, this study has also provided two new kinds of flaps used in experimental study: the arterial loop flap and the intermuscular septal perforator flap. Although there were differences as well as similarities in skin vasculature between humans and the scent pig, the scent pig is still suitable for flap research.     

The adult scent glands and scent of nine bugs of the superfamily Coreoidea

In most of the six coreoid genera examined there are differences in the scent gland complex. This comprises a median, ventral, metathoracic reservoir with either one, two, or three pairs of accessory glands.

The nine adult bugs examined all produced a colourless, single-phase scent, the components of which were similar although the relative proportions varied. Either n-hexanal or n-hexyl acetate, or both, were usually the major constituents (about 90 per cent of the total) and n-hexanol and acetic acid were also present in amounts varying from traces to about 10 per cent. In one species n-butanal was detected and in two species n-butyl butyrate and (probably) butyric acid were present.

The characteristic, ester odour of these coreoid bugs is quite unlike that of pentatomid bugs examined so far and the two groups do not possess a single component in common; nevertheless there are interesting analogies between the scent components of both groups.     

Genetic consequences of specialization: yucca moth behavior and self-pollination in yuccas

Reciprocal specialization in interspecific interactions, such as plant-pollinator mutualisms, increases the probability that either party can have detrimental effects on the other without the interaction being dissolved. This should be particularly apparent in obligate mutualisms, such as those that exist between yucca and yucca moths. Female moths collect pollen from yucca flowers, oviposit into floral ovaries, and then pollinate those flowers. Yucca moths, which are the sole pollinators of yuccas, impose a cost in the form of seed consumption by the moth larvae. Here we ask whether there also is a genetic cost through selfish moth behavior that may lead to high levels of self fertilization in the yuccas. Historically, it has been assumed that females leave a plant immediately after collecting pollen, but few data are available. Observations of a member of the Tegeticula yuccasella complex on Yucca filamentosa revealed that females remained on the plant and oviposited in 66% of all instances after observed pollen collections, and 51% of all moths were observed to pollinate the same plant as well. Manual cross and self pollinations showed equal development and retention of fruits. Subsequent trials to assess inbreeding depression by measuring seed weight, germination date, growth rate, and plant mass at 5 months revealed significant negative effects on seed weight and germination frequency in selfed progeny arrays. Cumulative inbreeding depression was 0.475, i.e., fitness of selfed seeds was expected to be less than half that of outcrossed seeds. Single and multilocus estimates of outcrossing rates based on allozyme analyses of open-pollinated progeny arrays did not differ from 1.0. The discrepancy between high levels of behavioral self-pollination by the moths and nearly complete outcrossing in mature seeds can be explained through selective foreign pollen use by the females, or, more likely, pollen competition or selective abortion of self-pollinated flowers during early stages of fruit development. Thus, whenever the proportion of pollinated flowers exceeds the proportion that can be matured to ripe fruit based on resource availability, the potential detrimental genetic effects imposed through geitonogamous pollinations can be avoided in the plants. Because self-pollinated flowers have a lower probability of retention, selection should act on female moths to move among plants whenever moth density is high enough to trigger abortion. Received: 18 March 1996 \Accepted: 30 July 1996     

Diurnal regulation of scent emission in rose flowers

Previous studies have shown diurnal oscillation of scent emission in rose flowers with a peak during the day (Helsper in Planta 207:88–95, 1998; Picone in Planta 219:468–478, 2004). Here, we studied the regulation of scent production and emission in Rosa hybrida cv. Fragrant Cloud during the daily cycle and focused on two terpenoid compounds, germacrene D and geranyl acetate, whose biosynthetic genes have been characterized by us previously. The emission of geranyl acetate oscillated during the daily light/dark cycle with a peak early in the light period. A similar daily fluctuation was found in the endogenous level of this compound and in the expression of its biosynthetic gene, alcohol acetyl transferase (RhAAT). The rhythmic expression of RhAAT continued under conditions of constant light or darkness, indicating regulation by the endogenous circadian clock. However, the accumulation and emission of geranyl acetate ceased under continuous light. Our results suggest that geranyl acetate production is limited by the level of its substrate geraniol, which is suppressed under constant light conditions. The emission of germacrene D also oscillated during the daily cycle with a peak early in the light period. However, the endogenous level of this compound and the expression of its biosynthetic gene germacrene D synthase (RhGDS) were constant throughout the day. The diurnal oscillation of germacrene D emission ceased under continuous light, suggesting direct regulation by light. Our results demonstrate the complexity of the diurnal regulation of scent emission: although the daily emission of most scent compounds is synchronized, various independently evolved mechanisms control the production, accumulation and release of different volatiles. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Dimorphism in inflorescence scent of dioecious wild grapevine

Wild grapevine (Vitis vinifera subsp. sylvestris) is the dioecious ancestral form of grapevine, from which the domesticated cultivars have derived (V. vinifera subsp. vinifera). Little is known about the floral scent compounds of wild grapevine that is considered as being partly insect pollinated. The knowledge of volatiles released by male and female inflorescence may contribute to the understanding of the pollination biology of this endangered taxon. Inflorescence scents of male and female individuals were collected by dynamic headspace and analysed by thermal desorption-GC/MS. A total of 17 compounds of C5-branched chain alcohols, aliphatics, aromatics, and terpenoids were identified with benzyl alcohol being most abundant in both sexes. Eight of the compounds were sex-specific and differences in 1,2-dimethoxybenzene were most obvious. This aromatic compound was a main constituent in the scent of females (30%), but it did not occur in males. Some of the main compounds of the scent samples are known to be detected by beetles (Cerambycidae) or attract sweat bees (Halictidae) and honey bees (A. mellifera), all well-known inflorescence visitors in wild grapevine. The data presented here are an important step in understanding the chemical communication between wild grapevine and its inflorescence visitors/potential pollinators.     

Characterization of polymorphic microsatellite loci in Yucca filamentosa

Yuccas and their pollinator moths are a textbook example of mutualism, yet we lack sufficiently variable markers to properly study the population genetics of the plants. We characterized 13 polymorphic microsatellite loci for Yucca filamentosa by screening primers derived from an expressed sequence tag database. We found four to 13 alleles per locus and the observed heterozygosity ranged from 0.31 to 1. These markers will be useful in future ecological studies of Y. filamentosa.     

On the scent of sexual attraction

A study in the current issue of BMC Biology has identified a mouse major urinary protein as a pheromone that attracts female mice to male urine marks and induces a learned attraction to the volatile urinary odor of the producer. See research article