Pollination efficiency of cockroaches and other floral visitors of Clusia blattophila.

Cockroaches have rarely been documented as pollinators. In this paper we examine whether this is because they might be inefficient at pollination compared to other pollinators. Clusia blattophila, a dioecious shrub growing on isolated rocky outcrops in French Guiana, is pollinated by Amazonina platystylata cockroaches and provides a valuable system for the study of cockroach pollination efficiency. We examined the species composition of the visitor guild and visitation rates by means of camcorder recordings and visitor sampling. Then, we investigated the capacity for pollen transfer of principal visitors and found correlations between visitation rates and pollen loads on stigmas. In an exclusion experiment we determined the contributions of individual species to pollination success. Amazonina platystylata, crickets and two species of Diptera transferred pollen, but the number of transferred pollen grains was only related to visitation rates in the case of cockroaches. Crickets visited and rarely carried pollen. Dipterans were as frequent as cockroaches, carried similar pollen loads, but transferred much less pollen. An estimated 41% and 17% of ovules were pollinated by cockroaches and dipterans, respectively. The remaining ovules were not pollinated. There was no spatial variation in pollinator guild composition, but cockroaches visited flowers less frequently at the smaller study site. We demonstrate that cockroaches pollinate a large proportion of ovules. Their pollination service is not confined to one study site and, unlike that provided by dipterans, is not limited to certain years. We suggest that cockroach pollination has been overlooked and that cockroach-pollinated plants, which share certain floral features, possess adaptations to pollination by cockroaches.

The Vulnerability of Tropical Ectotherms to Warming Is Modulated by the Microclimatic Heterogeneity.

Most tropical ectotherms live near their physiological limits for temperature. Substantial ecological effects of global change are predicted in the tropics despite the low amplitude of temperature change. These predictions assume that tropical ectotherms experience air temperature as measured by weather stations or predicted by global circulation models. The body temperature of ectotherms, however, can deviate from ambient air when the organism samples the mosaic of microclimates at fine scales. The thermal heterogeneity of tropical landscapes has been quantified only rarely in comparison to temperate habitats, limiting our ability to infer the vulnerability to warming of tropical ectotherms. Here, we used thermal imaging to quantify the heterogeneity in surface temperatures across spatial scales, from the micro- up to landscape scale, at the top of an Inselberg in French Guiana. We measured the thermal heterogeneity at the scale of Clusia nemorosa leaves, by categorizing leaves in full sun versus leaves in the shade to quantify the microclimatic variance available to phytophagous insects. Then, we measured the thermal heterogeneity at the scales of the single shrub and the landscape, for several sites differing in their orientation toward the sun to quantify the microclimatic heterogeneity available for larger ectotherms. All measurements were made three times per day over four consecutive days. There was a high level of thermal heterogeneity at all spatial scales. The thermal variance varied between scales, increasing from the within-leaf surface to the landscape scale. It also shifted across the day in different ways depending on the spatial scale. Then, using a set of published data, we compared the critical temperature (CTmax) of neo-tropical ectotherms and temperature distributions. The portion of space above the CTmax varied substantially depending on spatial scale and taxa. Insects were particularly at risk at the surface of leaves exposed to solar radiation but not on shaded leaves. By contrast, ants tolerated elevated surface temperatures and can survive almost anywhere in the habitat. We suggest that the fine scale mosaic of microclimates in the tropics modulates the vulnerability of ectotherms to warming. By moving just a few meters, or even a few centimeters, small tropical ectotherms can radically change their microclimatic temperature and escape overheating.

Facultative crassulacean acid metabolism (CAM) plants: powerful tools for unravelling the functional elements of CAM photosynthesis.

Facultative crassulacean acid metabolism (CAM) describes the optional use of CAM photosynthesis, typically under conditions of drought stress, in plants that otherwise employ C3 or C4 photosynthesis. In its cleanest form, the upregulation of CAM is fully reversible upon removal of stress. Reversibility distinguishes facultative CAM from ontogenetically programmed unidirectional C3-to-CAM shifts inherent in constitutive CAM plants. Using mainly measurements of 24h CO2 exchange, defining features of facultative CAM are highlighted in five terrestrial species, Clusia pratensis, Calandrinia polyandra, Mesembryanthemum crystallinum, Portulaca oleracea and Talinum triangulare. For these, we provide detailed chronologies of the shifts between photosynthetic modes and comment on their usefulness as experimental systems. Photosynthetic flexibility is also reviewed in an aquatic CAM plant, Isoetes howellii. Through comparisons of C3 and CAM states in facultative CAM species, many fundamental biochemical principles of the CAM pathway have been uncovered. Facultative CAM species will be of even greater relevance now that new sequencing technologies facilitate the mapping of genomes and tracking of the expression patterns of multiple genes. These technologies and facultative CAM systems, when joined, are expected to contribute in a major way towards our goal of understanding the essence of CAM.

Leaf anatomical traits which accommodate the facultative engagement of crassulacean acid metabolism in tropical trees of the genus Clusia.

Succulence and leaf thickness are important anatomical traits in CAM plants, resulting from the presence of large vacuoles to store organic acids accumulated overnight. A higher degree of succulence can result in a reduction in intercellular air space which constrains internal conductance to CO2. Thus, succulence presents a trade-off between the optimal anatomy for CAM and the internal structure ideal for direct C3 photosynthesis. This study examined how plasticity for the reversible engagement of CAM in the genus Clusia could be accommodated by leaf anatomical traits that could facilitate high nocturnal PEPC activity without compromising the direct day-time uptake of CO2 via Rubisco. Nine species of Clusia ranging from constitutive C3 through C3/CAM intermediates to constitutive CAM were compared in terms of leaf gas exchange, succulence, specific leaf area, and a range of leaf anatomical traits (% intercellular air space (IAS), length of mesophyll surface exposed to IAS per unit area, cell size, stomatal density/size). Relative abundances of PEPC and Rubisco proteins in different leaf tissues of a C3 and a CAM-performing species of Clusia were determined using immunogold labelling. The results indicate that the relatively well-aerated spongy mesophyll of Clusia helps to optimize direct C3-mediated CO2 fixation, whilst enlarged palisade cells accommodate the potential for C4 carboxylation and nocturnal storage of organic acids. The findings provide insight on the optimal leaf anatomy that could accommodate the bioengineering of inducible CAM into C3 crops as a means of improving water use efficiency without incurring detrimental consequences for direct C3-mediated photosynthesis.

Aspects of reproductive ecology of Clusia valerioi Standl. and Clusia peninsulae Hammel (sp. nov.), two Central American species of Clusiaceae with resin flowers.

Clusia valerioi Standl. and C. peninsulae Hammel, sp. nov. (formally established in the Appendix), two Central American species of Clusiaceae offering resin as a floral reward, were studied in the Piedras Blancas National Park, SW Costa Rica. Basic data on phenology, flower structure, course of anthesis, flower visitors, flower visitation and pollination processes, fruit development and seed dispersal are communicated. Resin collection and pollen release are reported and documented in greater detail. The significance of stingless bees for pollination is confirmed, but honeybees were also observed to visit the flowers and to collect resin. The seeds of C. valerioi, exhibiting a clearly ornithochorous character syndrome, were observed to be eaten and dispersed by four species of the tanager family (Thraupidae) and one species of finch (Fringillidae). Ants were also observed to carry away the seeds.

Photosynthetic efficiency of Clusia arrudae leaf tissue with and without Cecidomyiidae galls.

Leaf galls induced by a still undescribed new species of Cecidomyiidae (Diptera) are frequent on leaves of Clusia arrudae Planchon & Tirana (Clusiaceae) in the rupestrian fields at 1400 m a.s.l. in Serra do Cipó, Minas Gerais, Brazil. Galls were 7.1 ± 0.7 mm in diameter, one chambered with only one larva inside. Gall tissue is green and soft. Assessments of photosynthetic capacity using chlorophyll-a fluorescence measurements revealed that photosynthetic performance of gall tissue and healthy leaf tissue were rather similar. Hence, the morphological changes due to gall development were not associated with significant changes in the photosynthetic capacity of the tissue.

Adaptation of the obligate CAM plant Clusia alata to light stress: Metabolic responses.

In the Crassulacean acid metabolism (CAM) plants Clusia alata Triana and Planch., decarboxylation of citrate during phase III of CAM took place later than malate decarboxylation. The interdependence of these two CO(2) and NADPH sources is discussed. High light accelerated malate decarboxylation during the day and lowered citrate levels. Strong light stress also activated mechanisms that can protect the plant against oxidative stress. Upon transfer from low light (200micromol m(-2)s(-1)) to high light (650-740micromol m(-2)s(-1)), after 2 days, there was a transient increase of non-photochemical quenching (NPQ) of fluorescence of chlorophyll a of photosystem II. This indicated acute photoinhibition, which declined again after 7 days of exposure. Conversely, after 1 week exposure to high light, the mechanisms of interconversion of violaxanthin (V), antheraxanthin (A), zeaxanthin (Z) (epoxydation/de-epoxydation) were activated. This was accompanied by an increase in pigment levels at dawn and dusk.

Dinámica del daño foliar en plántulas de Drimys granadensis (Winteraceae) y Clusia multiflora (Clusiaceae) en el bosque altoandino de la Cordillera Oriental colombiana

Leaf damage dynamics of Drimys granadensis (Winteraceae) and Clusia multiflora (Clusiaceae) seedlings in the High-Andean Forest. Because of their slow growth, shade-tolerant species remain exposed to foliar damage long before reproductive age. Foliar damage can be controlled through synchronous leaf production and specialized phytochemical strategies. in this study, the dynamics of foliar damage in different cohorts of seedlings were evaluated to determine if the High-Andean species, Clusia multiflora (Clusiaceae) and Drimys granadensis (Winteraceae) appeal to the synchronous leaf production for controlling the herbivory and pathogenical damage, and to establish the possible relations between the healthy state, growth and mortality of seedlings. Since a recently-emerged seedling could not supply the physiological costs of specialized strategies, we expected the highest synchronous leaf production in the youngest individuals, and differences between cohorts in foliar damage. Four variables were measured to evaluate the health state along time, in three cohorts of seedlings: Proportion of predated leaves (Pp), proportion of healthy leaves (Ps), proportion of leaves with symptoms of disease or punctual damage (Pe) and growing (% increment of height). Both species showed significant differences between periods in the proportion of healthy leaves, but there was not an effect of time-cohort interaction, therefore synchronic production of leaves was not a strategy more used for any particular cohort. Foliar damage oscillated along time, fact that can be explained by the pulses of leaf production. However, this strategy had little efficiency to control the pathogen attack. in general, the unified behavior of all variables was affected by cohort, time, species an all the different interactions. Association between growing and foliar damage were conditioned by climate. The highest mortality ocurred during the dry season, and one fourth of the D. granadensis deaths were caused by the joint action of herbivory and drought. Results suggest that in spite of the synchronous leaf production in all cohorts, this strategy quickly loses the efficiency for controlling foliar damage, because the means of Ps were below of 0.25 at the end of the monitoring period. The differences between species in the dynamics of health state should explain partially their coexistence in the High-Andean forest. Rev. Biol. Trop. 56 (3): 1087-1100. Epub 2008 September 30.

Además de las estrategias fitoquímicas especializadas, las plantas pueden usar la producción sincrónica de hojas como un método de saciado de patógenos y herbívoros. Con el fin de determinar si las especies del bosque altoandino colombiano Clusia multiflora (Clusiaceae) y Drimys granadensis (Winteraceae) recurren a la producción sincrónica de hojas para controlar los efectos de la herbivoría y el ataque microbiano, y establecer que relación existe entre el estado de salud, el crecimiento y la mortalidad de plántulas, se evaluó la dinámica del daño foliar sobre diferentes cohortes. Dado que una plántula tolerante a la sombra recientemente emergida no puede suplir los costos fisiológicos de una estrategia especializada, se esperaba una alta sincronía en la producción de hojas en las plántulas más jóvenes, y diferencias en el daño foliar entre cohortes. Se midieron cuatro variables que evaluaban el estado de salud a lo largo del tiempo, en tres cohortes de plántulas: Proporción de hojas predadas, proporción de hojas sanas, proporción de hojas enfermas o con daño puntual y crecimiento. Ambas especies mostraron diferencias significativas entre épocas, en la proporción de hojas sanas; pero no hubo un efecto de la interacción tiempo-cohorte, por lo tanto la producción sincrónica de hojas no fue una estrategia más usada por alguna cohorte en particular. El daño foliar osciló a través del tiempo, lo cual puede ser explicado por los pulsos en la producción de hojas. Sin embargo, ésta estrategia tuvo poca eficiencia para controlar el ataque por patógenos. En general, el comportamiento unificado de todas las variables fue afectado por la cohorte, el tiempo, la especie y todas las diferentes interacciones. La relación entre crecimiento y daño foliar fue condicionado por el clima. La mayor mortalidad se dio durante la estación seca, y un cuarto de las muertes en D. granadensis fueron causadas por la acción conjunta de herbivoría y sequía. Los resultados sugieren que a pesar de la producción sincrónica de hojas en todas las cohortes, fue poca la eficiencia para controlar el daño foliar, ya que las medias de Ps estuvieron por debajo de 0.25 al final del seguimiento. Las diferencias en la dinámica del estado de salud entre especies podrían explicar parcialmente la coexistencia en el bosque altoandino.

Cockroaches as pollinators of Clusia aff. sellowiana (Clusiaceae) on inselbergs in French Guiana.

BACKGROUND AND AIMS: A report is made on a new species of Clusia related to C. sellowiana that dominates the vegetation of the Nouragues inselberg in French Guiana. The focus is on the pollination biology and on the remarkable relationship of this plant species to Amazonina platystylata, its cockroach pollinator. This appears to be only the second record of pollination by cockroaches. METHODS: Pollination ecology was investigated by combining morphological studies, field observations and additional experiments. Floral scent was analysed by gas chromatography-mass spectrometry. The role of acetoin, the major component of the scent of this species of Clusia, in attracting pollinators was examined in field attraction experiments. The ability of cockroaches to perceive acetoin was investigated by electroantennography (EAG). KEY RESULTS: The Clusia species studied produces seeds only sexually. Its nocturnal flowers are visited by crickets, ants, moths and cockroaches. A species of cockroach, Amazonina platystylata, is the principal pollinator. The reward for the visit is a liquid secretion produced by tissues at the floral apex and at the base of the ovary. Although the cockroaches have no structures specialized for pollen collection, their body surface is rough enough to retain pollen grains. The cockroaches show significant EAG reactions to floral volatiles and acetoin, suggesting that the floral scent is a factor involved in attracting the cockroaches to the flowers. CONCLUSIONS: The results suggest that the plant-cockroach interaction may be quite specialized and the plant has probably evolved a specific strategy to attract and reward its cockroach pollinators. Acetoin is a substance involved in the chemical communication of several other cockroach species and it seems plausible that the plant exploits the sensitivity of cockroaches to this compound to attract them to the flowers as part of the pollination syndrome of this species.

[Leaf damage dynamics of Drimys granadensis (Winteraceae) and Clusia multiflora (Clusiaceae) seedlings in the High-Andean Forest]. / Dinámica del daño foliar en plántulas de Drimys granadensis (Winteraceae) y Clusia multiflora (Clusiaceae) en el bosque altoandino de la Cordillera Oriental colombiana.

Because of their slow growth, shade-tolerant species remain exposed to foliar damage long before reproductive age. Foliar damage can be controlled through synchronous leaf production and specialized phytochemical strategies. In this study, the dynamics of foliar damage in different cohorts of seedlings were evaluated to determine if the High-Andean species, Clusia multiflora (Clusiaceae) and Drimys granadensis (Winteraceae) appeal to the synchronous leaf production for controlling the herbivory and pathogenical damage, and to establish the possible relations between the healthy state, growth and mortality of seedlings. Since a recently-emerged seedling could not supply the physiological costs of specialized strategies, we expected the highest synchronous leaf production in the youngest individuals, and differences between cohorts in foliar damage. Four variables were measured to evaluate the health state along time, in three cohorts of seedlings: Proportion of predated leaves (P(p)), proportion of healthy leaves (P(s)), proportion of leaves with symptoms of disease or punctual damage (P(e)) and growing (% increment of height). Both species showed significant differences between periods in the proportion of healthy leaves, but there was not an effect of time-cohort interaction, therefore synchronic production of leaves was not a strategy more used for any particular cohort. Foliar damage oscillated along time, fact that can be explained by the pulses of leaf production. However, this strategy had little efficiency to control the pathogen attack. In general, the unified behavior of all variables was affected by cohort, time, species an all the different interactions. Association between growing and foliar damage were conditioned by climate. The highest mortality ocurred during the dry season, and one fourth of the D. granadensis deaths were caused by the joint action of herbivory and drought. Results suggest that in spite of the synchronous leaf production in all cohorts, this strategy quickly loses the efficiency for controlling foliar damage, because the means of P(s) were below of 0.25 at the end of the monitoring period. The differences between species in the dynamics of health state should explain partially their coexistence in the High-Andean forest.

Photosynthetic flexibility and ecophysiological plasticity: questions and lessons from Clusia, the only CAM tree, in the neotropics.

The discovery of crassulacean acid metabolism (CAM) in the trees of Clusia: arrival in the limelight of international research 8 II. Phylogeny 8 III. Photosynthetic physiotypes 10 IV. Metabolic flexibility: organic acid variations 12 V. The environmental control of photosynthetic flexibility 13 VI. Phenotypic plasticity: physiotypes and morphotypes 16 VII. Ecological amplitude and habitat impact 16 VIII. Conclusions and outlook 21 Acknowledgements 22 References 22 Summary It is the aim of this review to present a monographic survey of the neotropical genus Clusia on scaling levels from molecular phylogeny, metabolism, photosynthesis and autecological environmental responses to ecological amplitude and synecological habitat impact. Clusia is the only dicotyledonous genus with real trees performing crassulacean acid metabolism (CAM). By way of introduction, a brief historical reminiscence describes the discovery of CAM in Clusia and the consequent increase in interest in studying this particular genus of tropical shrubs and trees. The molecular phylogeny of CAM in the genus is compared with that in Kalanchoë and the Bromeliaceae. At the level of metabolism and photosynthesis, the great plasticity of expression of photosynthetic physiotypes, i.e. (i) C(3) photosynthesis, (ii) CAM including CAM idling, (iii) CAM cycling and (iv) C(3)/CAM-intermediate behaviour, as well as metabolic flexibility in Clusia is illustrated. At the level of autecology, the factors water, irradiance and temperature, which control photosynthetic flexibility, are assessed. The phenotypic plasticity of physiotypes and morphotypes is described. At the level of synecology, the ecological amplitude of Clusia in the tropics and the relations to habitat are surveyed.