Implications of geometric plasticity for maximizing photosynthesis in branching corals

Reef-building corals are an example of plastic photosynthetic organisms that occupy environments of high spatiotemporal variations in incident irradiance. Many phototrophs use a range of photoacclimatory mechanisms to optimize light levels reaching the photosynthetic units within the cells. In this study, we set out to determine whether phenotypic plasticity in branching corals across light habitats optimizes potential light utilization and photosynthesis. In order to do this, we mapped incident light levels across coral surfaces in branching corals and measured the photosynthetic capacity across various within-colony surfaces. Based on the field data and modelled frequency distribution of within-colony surface light levels, our results show that branching corals are substantially self-shaded at both 5 and 18 m, and the modal light level for the within-colony surface is 50 μmol photons m^?2 s^?1. Light profiles across different locations showed that the lowest attenuation at both depths was found on the inner surface of the outermost branches, while the most self-shading surface was on the bottom side of these branches. In contrast, vertically extended branches in the central part of the colony showed no differences between the sides of branches. The photosynthetic activity at these coral surfaces confirmed that the outermost branches had the greatest change in sun- and shade-adapted surfaces; the inner surfaces had a 50 % greater relative maximum electron transport rate compared to the outer side of the outermost branches. This was further confirmed by sensitivity analysis, showing that branch position was the most influential parameter in estimating whole-colony relative electron transport rate (rETR). As a whole, shallow colonies have double the photosynthetic capacity compared to deep colonies. In terms of phenotypic plasticity potentially optimizing photosynthetic capacity, we found that at 18 m, the present coral colony morphology increased the whole-colony rETR, while at 5 m, the colony morphology decreased potential light utilization and photosynthetic output. This result of potential energy acquisition being underutilized in shallow, highly lit waters due to the shallow type morphology present may represent a trade-off between optimizing light capture and reducing light damage, as this type morphology can perhaps decrease long-term costs of and effect of photoinhibition. This may be an important strategy as opposed to adopting a type morphology, which results in an overall higher energetic acquisition. Conversely, it could also be that maximizing light utilization and potential photosynthetic output is more important in low-light habitats for Acropora humilis.     

Mutualist-induced morphological changes enhance growth and survival of corals

Species interactions can induce morphological changes in organisms that affect their subsequent growth and survival. In Moorea, French Polynesia, epibiotic gammaridean amphipods induce the formation of long, branch-like coral “fingers” on otherwise flat, encrusting, or plating Montipora coral colonies. The fingers form as corals encrust tubes built by the amphipods and lead to significant changes in colony morphology. This study examines the costs and benefits of this association to the amphipods and corals and demonstrates that the interaction is a mutualism. Amphipods gain protection from predators by living within corals, and corals benefit by enhanced growth and survival. Benefits to the coral arise through direct effects due to the amphipods’ presence as well as through benefits derived from the altered colony morphology. This study demonstrates that induced morphological plasticity can be a mechanism for facilitation, adding to our knowledge of the roles mutualism, and phenotypic plasticity play in ecology.     

Variation in colony geometry modulates internal light levels in branching corals, <Emphasis Type="Italic">Acropora humilis</Emphasis> and <Emphasis Type="Italic">Stylophora pistillata</Emphasis>

Colonial photosynthetic marine organisms often exhibit morphological phenotypic plasticity. Where such plasticity leads to an improved balance between rates of photosynthesis and maintenance costs, it is likely to have adaptive significance. To explore whether such phenotypic plasticity leads to more favourable within-colony irradiance for reef-building branching corals, this relationship was investigated for two coral species Acropora humilis and Stylophora pistillata, along a depth gradient representing light habitats ranging from 500 to 25 μmol photons m⁻² s⁻¹, during 2006 at Heron Island, Great Barrier Reef (23.44°S, 151.91°E). In the present study changes in flow-modulated mass transfer co-varied with light as a function of depth. In low-light (deep) habitats, branch spacing (colony openness) in A. humilis and S. pistillata was 40–50% greater than for conspecifics in high-light environments. Also, branches of A. humilis in deep water were 40–60% shorter than in shallow water. Phenotypic changes in these two variables lead to steeper within-colony light attenuation resulting in 38% higher mean internal irradiance (at the tissue surface) in deep colonies compared to shallow colonies. The pattern of branch spacing was similar for S. pistillata, but this species displayed an alternate strategy with respect to branch length: shade adapted deep and cave colonies developed longer and thinner branches, allowing access to higher mass transfer and irradiance. Corals in cave habitats allowed 20% more irradiance compared to colonies found in the deep, and had a 47% greater proportion of irradiance compared to colonies in the shallow high-light environment. Such phenotypic regulation of internal light levels on branch surfaces partly explains the broad light niches of many branching coral species. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Effects of photoacclimation on the light niche of corals: a process-based approach

The ecology of photosynthetic organisms is influenced by the need to adjust the photosynthetic apparatus to variable light environments (photoacclimation). In this study, we quantified different components of the photoacclimation process for a reef-building coral (Turbinaria mesenterina, Lamarck, 1816): including, variation in absorption cross-section, size of photosynthetic units, turnover time, chlorophyll content, and colony respiration. We used these calibrations to characterize this species’ light niche, and to determine the sensitivity of the niche boundaries to different processes of photoacclimation. Results showed that the breadth of the light niche was most sensitive to the size of the photosynthetic unit, absorption cross-section, and rates of respiration. Habitats with the highest light availability did not lead to maximal energy acquisition. This was because, although corals acclimated to high light have high rates of photosynthesis per unit chlorophyll, their chlorophyll content was strongly reduced. This suggests that potential energetic benefits that could be achieved through increased light harvesting (i.e., increased chlorophyll content) in high-light habitats are outweighed by costs associated with photoprotection. Such costs appear to place an upper bound on the habitat distributions of coral species. Our approach reveals how the photophysiological processes involved in photoacclimation interact to determine the light niche.     

Flesh or bone? Quantifying small-scale coral morphology using with-tissue and without-tissue techniques

The quantification of small-scale coral morphology using tissue-free skeletons often requires colonies, or colony sections, to be removed from the reef. This undesirable destruction can be reduced by using a with-tissue technique based on photographic images of living corals. The results of this study indicate that with-tissue multivariate morphometric data contain similar information to skeleton-derived data and can help identify phenotypic plasticity in the massive coral Favia speciosa. With-tissue data can also be used to discern changes with time in individual polyps exposed to new environments.Communicated by O. Kinne, Oldendorf/Luhe     

Effects of eutrophication on reef-building corals

Fourteen environmental variables were monitored at seven locations along the west coast of Barbados on a weekly basis over a one-year period, 1981 to 1982. The physicochemical and biological data indicate that an environmental gradient exists as a result of increased eutrophication of coastal waters. Growth rates (linear extension) of Montastrea annularis (Ellis and Solander), measured along the environmental gradient, exhibit high correlation with a number of water quality variables. Concentration of suspended particulate matter is the best univariate estimator of M. annularis skeletal extension rates (r ²=0.79, P<0.0001). The results suggest that suspended particulate matter may be an energy source for reef corals, increasing growth up to a certain maximum concentration. After this, reduction of growth occurs due to smothering, reduced light levels and reduced zooxanthellae photosynthesis.     

Behavioral evolution in the major worker subcaste of twig-nesting <Emphasis Type="Italic">Pheidole</Emphasis> (Hymenoptera: Formicidae): does morphological specialization influence task plasticity?

Polymorphism frequently correlates with specialized labor in social insects, but extreme morphologies may compromise behavioral flexibility and thus limit caste evolution. The ant genus Pheidole has dimorphic worker subcastes in which major workers appear limited due to their morphology to performing defensive or trophic functions, thus providing an ideal model to investigate specialization and plasticity. We examined worker morphology, brood-care flexibility, and subcaste ratio in 17 species of tropical twig-nesting Pheidole by quantifying nursing by major workers in natural colonies and in subcolonies lacking minors, in which we also measured brood survival and growth. Across species, majors performed significantly less brood care than minors in intact colonies, but increased rates of brood care 20-fold in subcolonies lacking minors. Brood nursed by majors had lower survival than brood tended by minors, although rates of brood growth did not vary between subcastes. Significant interspecific variation in rates of brood care by major workers did not lead to significant differences in brood growth or survival. Additionally, we did not find a significant association between the degree of major worker morphometric specialization and rates of nursing, growth, or survival of brood among species. Therefore, major workers showed reduced efficacy of brood care, but the degree of morphological specialization among species did not directly compromise task plasticity. The compact nests and all-or-nothing consequences of predation or disturbance on colony fitness may have influenced the evolution of major worker brood-care competency in twig-nesting Pheidole. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users. Dedicated to Professor Edward O. Wilson on the occasion of his 80th birthday.     

Evaluating the causal basis of ecological success within the scleractinia: an integral projection model approach

Many tropical corals have declined in abundance in the last few decades, and evaluating the causal basis of these losses is critical to understanding how coral reefs will change in response to ongoing environmental challenges. Motivated by the likelihood that marine environments will become increasingly unfavorable for coral growth as they warm and become more acidic (i.e., ocean acidification), it is reasonable to evaluate whether specific phenotypic traits of the coral holobiont are associated with ecological success (or failure) under varying environmental conditions including those that are adverse to survival. Initially, we asked whether it was possible to identify corals that are resistant or sensitive to such conditions by compiling quantitative measures of their phenotypic traits determined through empirical studies, but we found only weak phenotypic discrimination between ecological winners and losers, or among taxa. To reconcile this outcome with ecological evidence demonstrating that coral taxa are functionally unequal, we looked beyond the notion that phenotypic homogeneity arose through limitations of empirical data. Instead, we examined the validity of contemporary means of categorizing corals based on ecological success. As an alternative means to distinguish among functional groups of corals, we present a demographic approach using integral projection models (IPMs) that link organismal performance to demographic outcomes, such as the rates of population growth and responses to environmental stress. We describe how IPMs can be applied to corals so that future research can evaluate within a quantitative framework the extent to which changes in physiological performance influence the demographic underpinnings of ecological performance.     

New aspect in seagrass acclimation: leaf mechanical properties vary spatially and seasonally in the temperate species Cymodocea nodosa Ucria (Ascherson)

Seagrasses may acclimate to environmental heterogeneity through phenotypic plasticity. In contrast to leaf morphology, which has been a central point in seagrass acclimation studies, plasticity in leaf biomechanics and fibre content is poorly understood, despite being crucial in plant ecological performance, especially regarding physical forces. We hypothesised that mechanical traits (e.g. breaking force, strength, toughness, and stiffness) and fibre content of seagrass leaves vary as morphology does under differential environments. Cymodocea nodosa was seasonally monitored at three locations around Cádiz Bay (southern Spain) with hydrodynamic regime as the most noticeable difference between them. Leaves showed plasticity in both morphology and mechanical traits, with wave-exposed individuals presenting short but extensible and tough leaves. Leaf fibre content was invariant along the year and with little spatial variability. Cross-sectional area rather than material properties or fibre content differentiates leaf mechanical resistance. Seagrass capacity to thrive under a range of mechanical forces may be dictated by their plasticity in morpho-biomechanical traits, a key element for the hydrodynamical performance and, hence, for species colonisation and distribution.     

Behavioural flexibility in reef fishes responding to a rapidly changing wave environment

Flexible traits can be crucial in helping animals meet the challenges of a highly variable environment. We examined whether coral reef fishes systematically alter their swimming behaviour in response to temporal changes in hydrodynamic conditions. Exploiting site-based differences in wave energy impinging on reef habitats over calm and rough weather, we found many reef fishes changed their swimming behaviour alongside increases in wave-driven water motion. Most fishes tended to orient their bodies parallel to oncoming wave-driven flow and recruited additional stabilising fins during rough weather; such changes in swimming behaviour aid stability and minimise drag. However, not all species displayed such flexibility, with fishes possessing highly tapered pectoral fins and high levels of swimming performance continuing to successfully navigate reef habitats without significantly altering their swimming behaviour. We highlight how labile behaviours augment the morphology and performance of species to underpin their occupation of habitats subject to variable environmental conditions.     

Multivariate morphometric analysis of two varieties of Littorina saxatilis from the Swedish west coast

Shell variation in Littorina saxatilis Olivi (=L. rudis) is examined with different techniques of multivariate analysis (canonical variate-, multiple discriminant-, principal component-, and principal coordinate analysis). In bivariate projections of the analyses, two populations, spatially only 60 m apart, but from different habitats, showed a phenotypic separation without overlap. One habitat is a boulder shore, while the other is a rocky cliff. A sample, geographically and environmentally intermediate to the exposed and sheltered populations, covered completely the morphologic gap between the two former groups, indicating a clinal variation in morphology over the environmental gradient exposed — sheltered. From this it is concluded that the two phenotypically distinct populations belong to the same species.     

Flow,flapping, and photosynthesis ofNereocystis leutkeana: a functional comparison of undulate and flat blade morphologies

A number of species of macroalagae possess a flat, strap-like blade morphology in habitats exposed to rapidly-moving water whereas those at protected sites have a wider, undulate blade shape. We have explored the functional consequences of flat, narrow vs. wide, undulate blade morphologies in the giant bull kelpNereocystis luetkeana. Our study focused on the behavior of blades in ambient water currents and the consequences of that behavior to breakage and to photosynthesis. In flowing water, the narrow, flat blades flap with lower amplitude and collapse together into a more streamlined bundle than do wide, undulate blades, and hence experience lower drag per blade area at a given flow velocity. If the algae at current-swept sites had ruffled blades, drag forces would sometimes be sufficient to break the stipes. However, flat blades in a streamlined bundle experience more self-shading than do undulate blades, which remain spread out in water currents. Thus, there is a morphological trade-off between reducing drag and reducing self-shading. Photosynthetic¹⁴C-HCO₃ uptake rates decrease in slow flow when the boundary layer along the blade surface across which diffusion takes place is relatively thick. However, blade flapping, which stirs water near the blade surface, enhances carbon uptake rates in slow water currents for both the undulate and the flat morphologies.     

Past predation risk induces an intertidal whelk (Nucella lamellosa) to respond to more dilute concentrations of its predator’s scent

Unless sensory control is coupled with developmental flexibility, organisms are unable to produce adaptive phenotypes in response to environmental risk cues. However, empirical examples of adaptive phenotypic plasticity focus largely on development and rarely on sensory control. Here, I ask whether past exposure to predation cues affects an intertidal whelk’s (Nucella lamellosa) sensitivity to the scent of a known predatory crab (Cancer productus). I pre-conditioned whelks for 30 days with the smell of crabs eating other whelks and then, after a period of rest (14 days in fresh seawater free of predator effluent), re-introduced them to different concentrations of waterborne crab scent. Relative to controls, pre-conditioned whelks expressed crab-defences at significantly lower concentrations of crab effluent, suggesting the pre-conditioning reduced their risk–response threshold. Results remind us that the full scope of factors controlling adaptive phenotypic plasticity in natural populations remains underappreciated.     

丛枝菌根对盐胁迫的响应及其与宿主植物的互作

丛枝菌根真菌(Arbuscular Mycorrhizae Fungi,AMF)作为陆地生态系统的组成部分之一,在促进宿主植物对土壤养分和水分的吸收、提高植物生物量生产、调节种群和群落的结构、维持生态系统的稳定性等方面发挥了重要作用。其中,盐渍化是自然生态系统中广泛存在的一种胁迫生境条件,全球盐渍化土地约占耕地总面积的10%,因而探讨AM菌根在此胁迫生境下对宿主植物生长的影响具有重要意义。从以下几个方面,围绕盐胁迫条件、AM菌根和宿主植物三者之间的关系对当前国际上相关领域的研究进展进行了综述:1)AM真菌对盐胁迫的响应,包括菌根共生体形成、菌根侵染率、AM真菌的分布、菌丝体生长发育、孢子的形成和分布等;2)盐胁迫条件下AM菌根对宿主植物的效应,包括AM菌根促进宿主植物对P、N等元素的吸收、降低植物体内Na 的含量、提高光合作用能力,进而提高植物的生物量和对植物的群落结构产生影响等;3)AM菌根提高宿主植物耐盐性的机理,分别从植物根系形态的改变、水分吸收能力的加强、细胞内营养物质的平衡,以及细胞生理代谢的调节等方面对AM菌根促进植物抗盐性的机理进行了剖析。     

Estimating the footprint of pollution on coral reefs with models of species turnover

Ecological communities typically change along gradients of human impact, although it is difficult to estimate the footprint of impacts for diffuse threats such as pollution. We developed a joint model (i.e., one that includes multiple species and their interactions with each other and environmental covariates) of benthic habitats on lagoonal coral reefs and used it to infer change in benthic composition along a gradient of distance from logging operations. The model estimated both changes in abundances of benthic groups and their compositional turnover, a type of beta diversity. We used the model to predict the footprint of turbidity impacts from past and recent logging. Benthic communities far from logging were dominated by branching corals, whereas communities close to logging had higher cover of dead coral, massive corals, and soft sediment. Recent impacts were predicted to be small relative to the extensive impacts of past logging because recent logging has occurred far from lagoonal reefs. Our model can be used more generally to estimate the footprint of human impacts on ecosystems and evaluate the benefits of conservation actions for ecosystems.     

Contest behaviour in the speckled wood butterfly (Pararge aegeria): seasonal phenotypic plasticity and the functional significance of flight performance

Although contemporary animal contest theory emphasises the importance of physical asymmetries in resolving disputes, such asymmetries do not obviously settle fights in all groups. Territorial male butterflies, for example, compete via elaborate non-contact aerial interactions in which success is determined by relative persistence. Prior research suggests that the resolution of these contests is not clearly related to physical variables such as body size or energy reserves. However, given that the contests involve elaborate aerial manoeuvres, one long-standing suggestion is that asymmetries in flight performance, and thus flight morphology, may be important. We addressed this hypothesis via a manipulative investigation into the biophysical correlates of contest success in the speckled wood butterfly, Pararge aegeria. This species possesses the ability for significant adaptive phenotypic plasticity in relevant flight morphological parameters. We took advantage of this plasticity to rear 90 individuals of markedly varying flight morphologies, which we then pitted against each other in a semi-controlled experimental fashion. Multiple logistic and lognormal analyses provided little evidence for the relevance of morphological parameters, including relative flight musculature, wing loading and wing aspect ratio (wing length relative to area), to the outcome and/or duration of experimental contests. Instead, we found a positive effect of age upon contest success. Given that ability for high acceleration is strongly linked to variation in these morphological parameters, our findings suggest that flight performance is not a strong determinant of resource-holding potential in this notably territorial butterfly.     

Latitude or biogeographic breaks? Determinants of phenotypic (co)variation in fitness-related traits in Betaeus truncatus along the Chilean coast

Ectothermal organisms distributed along environmental gradients in a wide geographical distribution display extensive phenotypic variation. This is particularly pervasive along latitudinal clines, which are linked to gradual changes in environmental factors. Widespread species may also be distributed among biogeographic breaks, which in contrast to smooth clines, often show abrupt changes in phenotypic traits. In species with widespread latitudinal distribution that also encompass important biogeographical breaks, it is not clear which of those factors prevails on shaping the phenotypic variation or if some traits are particularly more sensitive to one or the other. To evaluate this, we measured 4 fitness-related traits in 6 populations of the intertidal snapping shrimp Betaeus truncatus, as its distribution along Chile expands over 40° in latitude and three major biogeographical provinces. Here, we statistically evaluated the role of both, latitude and biogeographic breaks, on mean population values of fitness-related traits but also on the variances and covariances (i.e., P-matrix) between them. Overall, our results (1) indicate that latitude is more important than breaks in shaping the phenotypic variation of most of these fitness-related traits, (2) show that the differences in the variance–covariance relationship among traits between the extremes of the gradient arises from gradual increases in variance and rather sharp changes in covariance at mid-latitudes and (3) show that at present, it is difficult to unambiguously determine whether natural selection or plasticity is responsible for the observed pattern in means, variances and covariances and only further work might disentangle these possibilities.     

Serial patterns of biodiversity change in corals across shallow reef flats in Ko Phuket,Thailand, due to the effects of local (sedimentation) and regional (climatic) perturbations

A 17-year monitoring programme of reef flats at Ko Phuket, Thailand afforded an opportunity to evaluate both univariate and multivariate measures of environmental stress in an assessment of change on coral reef ecosystems. The sites at Ko Phuket suffered the effects of dredging in 1986-1987 and then anomalously low sea levels in 1997-1998 as a result of climate-related events in the Indian Ocean. Univariate measures of species diversity and taxonomic distinctness ((*) increased across the reef flat, reflecting the greater effects of physical stresses on the inner reef flats (compared with outer reef flats) at all sites, with more congeneric species present on the inner reef and more confamilial species on the outer reef. Multivariate measures showed a clear breakdown in seriation patterns at all sites during the dredging in 1987 and in 1998, as a result of earlier negative sea-level anomalies. Recovery from environmental disturbances was obvious within 12 months in each case. The domination of the reefs by massive coral species, which are physiologically adapted to intertidal living and which display partial rather than total colony mortality, may be a factor contributing to the apparent resilience of the reef flats together with continued recruitment and survival of juvenile corals during adverse environmental conditions. Elevated sea temperatures and extensive bleaching of corals in 1991, 1995, and 1998 had no effect upon coral community measures, with many corals recovering their zooxanthellae numbers within 3-5 months of the bleaching events.     

Morphological variation and phenotypic plasticity of buoyancy in the macroalga Turbinaria ornata across a barrier reef

Many aspects of morphology of benthic algae (length, surface area-to-volume ratio, and blade undulation) are plastic traits that vary in response to physical factors (such as light or water flow environment). This study examines whether frond buoyancy is a plastic trait, and whether differences in morphology including buoyancy affect the potential persistence of macroalgae in habitats characterized by different water flow regimes. Fronds of the tropical alga Turbinaria ornata in protected backreef environments in Moorea, French Polynesia possess pneumatocysts (gas-filled floats) and experience positive buoyant forces, whereas fronds in wave-exposed forereef sites either lack pneumatocysts entirely or have very small, rudimentary pneumatocysts and experience negative buoyant forces. Forereef fronds transplanted to the backreef developed pneumatocysts and experienced increased buoyant force indicating that buoyancy is a phenotypically plastic trait in T. ornata. In comparing the potential for dislodgement by drag, drag was greater on forereef fronds at low flow speeds as these fronds were stiffer and did not bend over at low flow speeds and therefore were less streamlined in the flow than backreef algae, which bent easily. The environmental stress factor (ESF) (a measure of the likelihood of detachment for a frond in its habitat) was higher for forereef than backreef fronds at all flow speeds. When examined with respect to the flow velocities likely in their respective habitats however, the chance of detachment for backreef and forereef was similar. Neither backreef nor forereef fronds were predicted to break under normal, non-storm conditions, but both were predicted to break in storms. Strong forereef morphologies are well suited to habitats characterized by rapid flow, whereas the weaker, buoyant, tall backreef fronds are well suited to habitats where crowding and shading is common but hydrodynamic forces are low.     

Invasive Microstegium populations consistently outperform native range populations across diverse environments

Plant species introduced into novel ranges may become invasive due to evolutionary change, phenotypic plasticity, or other biotic or abiotic mechanisms. Evolution of introduced populations could be the result of founder effects, drift, hybridization, or adaptation to local conditions, which could enhance the invasiveness of introduced species. However, understanding whether the success of invading populations is due to genetic differences between native and introduced populations may be obscured by origin x environment interactions. That is, studies conducted under a limited set of environmental conditions may show inconsistent results if native or introduced populations are differentially adapted to specific conditions. We tested for genetic differences between native and introduced populations, and for origin x environment interactions, between native (China) and introduced (U.S.) populations of the invasive annual grass Microstegium vimineum (stiltgrass) across 22 common gardens spanning a wide range of habitats and environmental conditions. On average, introduced populations produced 46% greater biomass and had 7.4% greater survival, and outperformed native range populations in every common garden. However, we found no evidence that introduced Microstegium exhibited greater phenotypic plasticity than native populations. Biomass of Microstegium was positively correlated with light and resident community richness and biomass across the common gardens. However, these relationships were equivalent for native and introduced populations, suggesting that the greater mean performance of introduced populations is not due to unequal responses to specific environmental parameters. Our data on performance of invasive and native populations suggest that post-introduction evolutionary changes may have enhanced the invasive potential of this species. Further, the ability of Microstegium to survive and grow across the wide variety of environmental conditions demonstrates that few habitats are immune to invasion.