Lay Summaries

The summaries below are provided by our authors to help put their research into context for the wider scientific community and the general public. Lay summaries for the current issue are here. You can also find all the previous lay summaries by issue, as well as summaries for articles on Early View, in the lay summaries archive.

Lay summaries for the current issue.

 

You can also find all the previous lay summaries by issue, as well as summaries for articles on Early View, in the lay summaries archive.

 

Mothers increase yolk oestrogen levels and the production of female offspring across the nesting season

Amanda W. Carter, Rachel M. Bowden, Ryan T. Paitz Mothers increase yolk oestrogen levels and the production of female offspring across the nesting season .

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Moms can permanently affect the phenotype of their offspring through a variety of causes termed “maternal effects,” (e.g., health during gestation affecting offspring growth rates, or the amount of care provided to young after birth impacting offspring stress). Maternal effects can help match the phenotype of the offspring to the offspring’s environment to enhance fitness, but sometimes the phenotype that is most advantageous differs between sons and daughters. Therefore, conditions that enable females to either directly manipulate the sex of their offspring or match maternal effects to a predictable pattern of sex ratio variation would be advantageous.

We investigated the ability of red-eared slider turtles to match maternal effects to offspring sex. Turtles are a great system for investigating sex-specific maternal effects because females transfer steroids to the eggs which may affect hatchling phenotype, including sex. In our species, females deposit higher concentrations of oestrogens in late season eggs, compared to early season eggs, which could result in a seasonal sex ratio shift. Also, in many turtles, incubation temperatures determine whether offspring develop as male or female. Turtle nest temperatures fluctuate daily, however, and we don’t know how even slight increases in fluctuating temperatures, as would occur across the nesting season, affect sex determination.

We collected turtle eggs early and late in the nesting season and incubated them under fluctuating incubation temperatures. We found that late season eggs, which contain higher concentrations of maternally derived oestrogens, are more likely to produce female hatchlings than early season eggs. Combined with even a slight increase in incubation temperature (0.5°C), late season eggs produce up to 49% more female hatchlings than early season eggs.

These findings demonstrate a seasonal shift in sex ratios driven by maternal effects and subtle increases in incubation temperatures. This predictable pattern of sex ratio variation creates the potential for sex-specific maternal effects mediated by oestrogens, and furthers our understanding of how moms may influence offspring.

Image caption: Mothers increase yolk oestrogen levels and the production of female offspring across the nesting season .
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

The wind, the wind, the heaven-born wind! Forest windthrow effects on soil carbon dynamics

Mathias Mayer, Hans Sandén, Boris Rewald, Douglas L. Godbold, Klaus KatzensteinerImage provided by authors.

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Forests are the predominant terrestrial sinks for atmospheric carbon dioxide (CO2). However, forest disturbances, such as insect attacks or windthrows (from storm events) can negatively affect the carbon (C) balance of a forest ecosystem. Climate change is likely to intensify these disturbance regimes in the future. A precise quantification of disturbance effects on the C dynamics of forests is key to lower uncertainties of their C sink capacities.

Soils are the largest C pool in forests and the CO2 efflux from soils represents the largest C flux to the atmosphere. Our understanding of how forest disturbance affects the sources of soil CO2 efflux, namely autotrophic (from roots and associated microorganisms) and heterotrophic soil respiration (from decomposition of dead organic matter), is however poor.

In this study we investigated the impact of forest windthrow on the sources of soil CO2 efflux, underlying biotic and abiotic drivers (i.e. plant community composition, soil organic matter properties and soil temperature and moisture), and consequences for soil organic C stocks in a temperate forest ecosystem in the European Alps.

We found that windthrow had no obvious effect on soil CO2 efflux in the first years after disturbance, because a reduction in autotrophic soil respiration was offset by a ~60% increase in heterotrophic soil respiration. Since all trees were blown over at the research site, an increase in heterotrophic soil respiration was principally related to higher soil temperatures. Autotrophic soil respiration was mainly driven by grasses and herbs rather than young trees in the first six years after disturbance. However, abundant symbiotic soil fungi (ectomycorrhiza) suggests an important indirect tree contribution to autotrophic soil respiration after windthrow. Soil C stocks significantly declined over the post-windthrow period.

Our results show that heterotrophic soil respiration was by far the dominant source of soil CO2 efflux after forest windthrow. Since C losses from heterotrophic soil respiration and soil organic C stocks were of the same order of magnitude, this study demonstrates that a decline in soil C stocks after windthrow was mainly driven by a temperature-related increase in heterotrophic soil respiration and thus decomposition.

Image caption: Image provided by authors.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Shade tolerance and the functional trait – demography relationship in temperate and boreal forests

Aitor Ameztegui, Alain Paquette, Bill Shipley, Michael Heym, Christian Messier and Dominique GravelImage provided by authors.

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Although shade tolerance is a fundamental concept in forest ecology, its definition is complex, and there is still open debate about what confers the ability of species to withstand shade conditions, and how shade tolerance is related to growth and mortality. Here, we hypothesize that shade tolerance can be achieved by alternative combinations of traits depending on the type of tree (deciduous vs. evergreen), and that its relationship with growth and mortality will also vary across these groups. We collected data on 48 tree species (23 evergreen and 25 deciduous species) from 10 sites in temperate or boreal forests across 4 continents. We identified the main traits (leaf characteristics, seed mass, wood density, etc.) that helped predict species growth and mortality, and whether these traits were related to shade tolerance. To test different hypotheses about the relationship between traits, shade tolerance, growth and mortality we used a technique called “structural equation modelling”. This technique allowed us to confirm that the traits involved in shade tolerance are different for evergreen than for deciduous trees, making an interesting contribution to the debate on the nature of shade tolerance. For instance, according to our results shade tolerance may be a good example of convergent evolution, that is, the parallel adaptation of evolutionarily distant species to the same condition (shade) but possibly using different strategies. Moreover, if researchers want to use shade tolerance as a predictor of forest dynamics and species coexistence, they should first be sure about the role it plays in the demography of the species under study.

Image caption: Image provided by authors.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

Plant-Pollinator Interactions from Flower to Landscape

Landscape impacts on pollinator communities in temperate systems: evidence and knowledge gaps

Deepa Senapathi, Mark A Goddard, William E Kunin and Katherine C R BaldockAgricultural field. Photo provided by authors.

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This review assesses current knowledge about the interplay between landscape and pollinator communities. Our primary aim is to provide an evidence base, identify key gaps in knowledge and highlight initiatives that will help to develop and improve strategies for pollinator conservation. Human-dominated landscapes can have detrimental impacts on pollinator richness and abundance but these negative effects can be ameliorated by proximity to semi-natural habitat and habitat corridors. There is also evidence to suggest that increased landscape heterogeneity and landscape configuration can play an important role in the maintenance of diverse pollinator communities. Landscape characteristics have direct impacts on pollinator communities but can also influence abundance and richness through interaction with other drivers such as changing climate or increased chemical inputs in land management. The majority of the existing literature focuses on specific groups of bees but there is a lack of information on the impact of landscape changes on other pollinators. Research is also needed on the effectiveness of management interventions for pollinators and multiple year observations are required for both urban and rural initiatives. Current policies and monitoring schemes could contribute data that will plug gaps in knowledge, thus enabling greater understanding of relationships between landscapes and pollinator populations. This would in turn help to design mitigation and adaptation strategies for pollinator conservation.

Image caption: Agricultural field. Photo provided by authors.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Honest floral colour change to maintain a long-lasting relationship with pollinators

Takashi T. Makino and Kazuharu Ohashi A bumblebee collecting nectar from an artificial flower. (photo by Takashi T. Makino).

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Floral colour change, reported in hundreds of plant species, is a well-known example of ‘honest signalling’ in plant–pollinator interactions. It occurs in fully turgid flowers, and usually correlates with a cessation of reward production (such as nectar) in individual flowers. The question is “Why do these plants honestly tell pollinators which flowers are rewarding?” In previous studies, the trait has been considered a plant strategy that enhances distant pollinator attraction, while minimizing visits to non-reproductive flowers at close range.

Here, we propose an additional benefit of floral colour change, which emerges when we consider the spatial learning ability of pollinators to avoid unprofitable plants. If a plant retains rewardless flowers without colour change, it is difficult for pollinators to visually locate the rewarding flowers. Although the enhanced display initially attracts more pollinators, its low profitability for foraging may discourage them from returning to the plant. This plant-level avoidance resulting from rewardless flowers may be prevented by floral colour change because it helps pollinators to find rewarding flowers. To test this possibility, we observed the behavioural changes of bumblebees foraging in an array of artificial plants.

We found that the retention of rewardless flowers without colour change could initially attract bees by increasing the plant’s display size, but their lack of reward resulted in plant-level avoidance by those bees that used spatial memories when choosing plants. The colour change in rewardless flowers, in contrast, encouraged bees to return by helping them to find rewards on plants. Consequently, honest plants with floral colour change received more visits by bees than those dishonest plants that did not display colour change. Floral colour change thus can prevent plant-level avoidance, and thereby enable plants to maintain a long-lasting relationship with experienced pollinators. For employing learning pollinators such as bumblebees, honesty may be the best policy.

Image caption: A bumblebee collecting nectar from an artificial flower. (photo by Takashi T. Makino).
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

The structure of flower-visitor networks in relation to pollination across an agricultural to urban gradient

Panagiotis Theodorou, Karoline Albig, Rita Radzevičiūtė, Josef Settele, Oliver Schweiger, Tomás E. Murray and Robert J. PaxtonImage provided by authors.

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Pollination is a major ecosystem service in which insects play an important role for the reproduction of most flowering plants, including crops. Among the major threats to insect pollinators, and consequently pollination services, is land use change. However, few studies have addressed the relative effects of (i) local habitat and (ii) anthropogenic land use on local plant-flower visitor community structure, the architecture of flower-visitor mutualistic networks and potential knock-on effects for the ecosystem service of pollination.

In our study, we performed a landscape-scale experiment using insect pollinator-dependent plant communities as ‘pollinometers’ and empirically examined the relative effects of local and landscape drivers on pollination. Using a statistical technique termed Structural Equation Modelling to analyse our empirical data, we found that plant-flower-visitor communities and their mutualistic networks were largely influenced by local factors. In addition, there were positive and correlated effects on the ecosystem service of pollination of (i) increasing urbanization in the surrounding landscape, (ii) flying insect abundance and (iii) bee richness. Yet, we surprisingly found that mutualistic network metrics were themselves largely independent of pollination service provision.

Our findings show that, in moderately urbanized areas providing rich floral resources, positive effects on both bee richness and plant reproduction can be observed. From a theoretical perspective, it is noteworthy that we did not find a relationship between flower-visitor network metrics and pollination of four experimental plant species, challenging the notion that flower-visitor networks can be used as surrogates for the ecosystem service of pollination. From an applied perspective, and as cities expand worldwide, the strong effects of local habitat on pollinator communities further emphasize the potential for local management as a tool for biodiversity conservation in urbanized areas.

Image caption: Image provided by authors.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

Plant-Pollinator Interactions from Flower to Landscape

Assessment of pollen rewards by foraging bees

Elizabeth Nicholls and Natalie Hempel de IbarraApis dorsata. Photo provided by authors.

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Plants that are pollinated by insects use brightly coloured or strongly scented flowers to attract insects’ attention. In addition they provide pollinators with food in the form of pollen and nectar to reward them for landing on the flower and encourage them to make repeated visits, transferring pollen between plants of the same species and pollinating them in the process. Until recently, much of our understanding of how these food rewards affect pollinator behaviour and pollen transfer has been based on the study of insects, mainly bees, visiting flowers to collect nectar. We know that bees are very sensitive to the sugar content and amount of nectar that flowers produce, and use this information to help them decide which flowers to visit. However almost nothing is known about if and how pollinators might assess the quality of pollen available and how this might guide their flower choices. Here we describe recent advances in our understanding of pollen collecting behaviour, and discuss the challenges involved in studying pollen rewards. Pollen produced by different plants varies across multiple dimensions, from visual appearance and odour, which affect bees’ sensory experience during collection, to nutritional content, which influences bee development and their ability to reproduce. Since pollen is the bees’ main source of protein it is thought that they would benefit by choosing to visit plants producing pollen with the highest protein concentration. However the relationship between bees’ preferences and the protein content of the pollen they collect is not simple. Bees do not eat pollen at the flower, but collect it on their body and transport it back to the nest, so it is not clear if or how bees would assess how nutritious pollen is. We suggest that bees are likely to use multiple factors to guide their flower choices, such as the visual and olfactory cues provided by pollen and the flower, as well as monitoring the physical effort required for them collect pollen in the first place. For bees that live in colonies such as honeybees and bumblebees, information from their nest-mates may also be important.

Image caption: Apis dorsata. Photo provided by authors.
Read the article here.

 

To bask or not to bask? Lizards do not follow current theory

Christine H. Basson, Ofir Levy, Michael J. Angilletta Jr., Susana Clusella¬TrullasBasking lizard. Image provided by authors.

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One means by which lizards can maintain favourable body temperatures is by thermoregulating. For example, they can shuttle back and forth between sites with sun and shade. However, depending on the availability and distribution of favourable sites, basking may become a costly activity. Longer distances or more time spent moving and searching for optimal sites should involve higher energetic costs. According to theory, lizards should abandon searching for favourable sites when the costs of doing so surpass the benefits and when this net difference is higher than when lizards passively track their surrounding temperatures. In this study, we compared data from a virtual (computer-simulated) lizard that either used an optimal behaviour by maximizing the net benefit of shuttling between available basking sites or used a passive behaviour. We simulated two environments: a ‘poor’ environment which only had one suitable basking site versus a ‘good’ environment which had multiple basking opportunities shifting throughout the day. We then compared the results of these simulations to the results for real lizards placed in experimental arenas with a single or multiple basking sites in the laboratory. Surprisingly, we found that our real lizards do not follow the predictions of the theoretical model. In both environments, lizards searched for basking sites despite the high costs of doing so in the ‘poor’ environment. We revealed that costs were associated with missed opportunities, such as less time available to explore the arena, rather than costs associated with energy spent moving between basking sites. These results highlight that the prediction of thermoregulatory behaviour, to bask or not to bask, depends on the complexity of the habitat mosaic formed by sun and shade sites in the landscape. Flat arid areas, deserts or dense tropical forests are likely to impose high energetic costs if optimal sites are scarce, while temperate and more variable environments may impose non-energetic costs, such as missed opportunities.

Image caption: Basking lizard. Image provided by authors.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Stay cool or warm up? Individual differences in energy-saving have consequences for survival and reproduction

Melanie Dammhahn, Manuelle Landry-Cuerrier, Denis Réale, Dany Garant and Murray M. HumphriesEastern Chipmunk (Tamias striatus).

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Energy is in short supply for most animals. Therefore, individuals have to find a balance between investing energy into growth, body maintenance and reproduction. During times of food scarcity and unfavorable temperatures many mammals go “on stand-by” and reduce their energy and water requirements by entering into torpor, a reversible state of reduced body temperature, metabolism and activity. Here, we asked whether individual variation in torpor use has consequences for survival and reproduction. We recorded body temperature of individuals of free-ranging eastern chipmunk (Tamias striatus), a small squirrel species that hoards food in a burrow and hibernates during winter. Using small temperature loggers, placed around the neck of animals, we continuously recorded skin temperature over the whole winter. We found that individuals of the same population differ from each other in how much torpor they use on average over the winter, even though they are exposed to similar environmental conditions. This among-individual variation had consequences for winter survival and reproductive success in the following breeding season. Individuals using less torpor at the beginning of the winter had decreased survival in resource-rich but not in resource-poor years, and higher reproductive success in the subsequent breeding season. Thus, whether it is beneficial for an individual chipmunk to stay cool and save energy, or to warm up and reduce the costs of torpor and prepare for reproduction, depends on local environmental conditions. Since individuals are the target of selection, we think that considering individual variation in eco-physiology can contribute to a more thorough understanding of the evolution of energy-saving strategies in mammals.

Image caption: Eastern Chipmunk (Tamias striatus).
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Functional traits of marine macrophytes predict primary production

Holger Jänes, Jonne Kotta, Merli Pärnoja, Tasman P. Crowe, Fabio Rindi and Helen Orav-KottaImage provided by authors.

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Large seaweeds and higher plants (macrophytes) are commonly found in coastal marine habitats where they photosynthesise i.e. they build up their own organic compounds by using the sun’s energy. Primary production underpins aquatic food webs, plays an important role in the global carbon cycle and connects the life from surface ocean layers with the species at the seabed. However, the rate of primary production can greatly vary between species, communities, ecosystems, seas and oceans, simply because species differ in terms of their functional setup and oceans in their environmental settings. Here we investigated the possibility to link functional traits (i.e. biological characteristics) of macrophytes from the major European seas to primary production and we asked if there were specific functional traits that could be effectively used to predict primary production of macrophyte communities.

We first measured primary production of macrophyte communities and then quantified how large fractions of the total community biomass different traits compose. By linking community production and trait information we found out that primary production mostly depended on the amount of large epilithic seaweeds of marine origin in the community. Interestingly, we also found that several traits were clustered together meaning that the occurrence of one trait increased the likelihood of another. Our findings suggest that functional traits of macrophytes can be effectively used to monitor primary production. Furthermore, taxonomically distinct species might possess similar traits meaning that functional aspects of ecosystems can be analysed without extensive taxonomic knowledge. This could result in simplification of the general procedure of production estimations and establish transparent framework how to link community structure with functioning.

Image caption: Image provided by authors.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Are certain types of plumage colours more likely to differ between males and females?

Kaspar Delhey & Anne PetersImage provided by authors.

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In many birds males and females show different colours and often males are more colourful than females, a phenomenon called sexual dichromatism. More colourful males are generally favoured by females. But why would females choose males based on their colours? One hypothesis states that females choosing colourful males are selecting mates of higher quality. Consequently, sexual selection should lead to the elaboration of colours that honestly signal quality and these should be more sexually dichromatic.

Certain types of plumage colours, for physiological reasons, may constitute better signals of male quality. Among these are carotenoid-based colours. Carotenoids are yellow to red plant pigments that animals need to ingest in their food and which also play important roles in immune function and health maintenance. These links with food and health, which are particularly strong for red carotenoids, make them good candidates to be sexually selected and dichromatic. Other pigments, such as melanins, are produced within the body and are considered cheaper to produce. Colours can also be produced by the interaction between light and feather microstructure, known as structural colours, which often have blue, violet or ultraviolet hues.

Here we quantify sexual dichromatism for colours produced by different mechanisms (including carotenoids) in a large sample of Australian birds. By measuring plumage colours on museum specimens and using models of bird colour vision we could estimate how different male and female plumage colours look to birds.

In general, sexual dichromatism was highest when males and females had plumage coloured by different mechanisms of colour production (e.g. males by carotenoids and females by melanins). This is not surprising, since colours caused by different mechanisms are usually quite different. We also found that, as predicted, red carotenoid plumage had higher sexual dichromatism and that species with a higher proportion of their plumage coloured with red carotenoids showed higher levels of sexual dichromatism. However, these correlations did not explain a large amount of variation in sexual dichromatism. We conclude that knowing the mechanisms behind the different types of colours has only limited utility in predicting which colours should be sexually selected in birds.

Image caption: Image provided by authors.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Plant communication in a widespread goldenrod: keeping herbivores on the move

André Kessler and Kimberly Morrell Photograph provided by authors.

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Plants can exchange information with neighbouring plants and a complex network of herbivores, predators and parasitoids. The language that plants use for such information transfer is, to a great extent, chemical - released into the rhizosphere (the soil immediately surrounding the roots) or into the air surrounding the plant. Chemical communication between neighbouring plants through airborne volatile organic compounds (VOCs) has to date been documented in over 35 plant species spanning 16 families; however, the underlying mechanisms through which it shapes plants’ ecological interactions remain less clear. Using a combination of field/laboratory bioassays and airborne volatile and leaf chemical analyses in tall goldenrod (Solidago altissima), we tested the hypothesis that plant-to-plant communication affects the performance, feeding and movement behaviour of herbivores by changing plants’ chemical phenotypes. We found that plant communication accelerates herbivore movement between host plants while simultaneously reducing herbivory. This suggests that plant communication can limit herbivore loads by keeping herbivores on the move between host plants.

We also demonstrate that volatile chemicals emitted from herbivore-attacked plants are sufficient to explain metabolic responses in, and ecological consequences for, the exposed neighbour plant. Thus, volatile organic compounds emitted by stressed plants provide neighbouring plants with specific information about herbivores in the vicinity. The attacking herbivores, in turn, respond similarly to directly damaged plants and plants exposed to VOCs from damaged neighbours, as if they were of equivalently poor quality.

This study suggests that by enlarging the spatial scale at which induced resistance affects the distribution of plant chemical phenotypes in plant populations, VOC-mediated plant communication alters the movement behaviour and performance of herbivores.

Image caption: Photograph provided by authors.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Plant genotype identity and intra-specific diversity trump soil nutrient availability to shape old-field structure and function

Lara Souza, Katharine L. Stuble and Aimeé T. ClassenPhoto provided by authors.

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Biodiversity, often measured as the number of species in a community, can promote services within ecosystems such as sequestration of carbon from the atmosphere. Biodiversity within a species, or specifically the number of genotypes within a species, may be just as important in promoting ecosystem services, especially when considering a common species. Solidago altissima, also known as tall goldenrod, is a commonly found plant in abandoned agricultural fields ranging from Florida into northern Canada. Tall goldenrod can make up almost half of the total productivity of old fields and is associated with a large number of insects including herbivores, predators and pollinators. To explore the role of biodiversity within tall goldenrod, and how the environment may influence biodiversity effects on ecosystem services, we established a field experiment where Solidago genotypes occurred in monocultures vs. mixtures under ambient vs. added soil nutrients, to mimic the variability of resources found across space and time. Our findings indicate that plant genetic variation, and to some extent plant genotypic diversity, strongly influence carbon sequestration in old fields, and such effects took place regardless of soil nutrient availability.

Image caption: Photo provided by authors.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Fire ant queen choices are behind fire ant success

Walter Tschinkel and Joshua KingThe experimental plots in the Apalachicola National Forest in Florida. Several tilled plots and shade covers are apparent.

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One of the basic questions of ecology is how and why particular sets of species (called communities) live together; to what degree does the physical nature of the habitat limit the species present, and to what degree do species' interactions? Solid answers to such questions cannot be derived from the existing species co-occurrence, but must be derived from experiments.

The fire ant, Solenopsis invicta, is an exotic, invasive ant found primarily in human-disturbed habitats, and is absent from most undisturbed, native habitat such as the coastal plains pine forests of northern Florida. However, fire ants quickly colonize soil and vegetation disturbances in these forests and thrive until these revert in time to a less disturbed condition. We previously showed that soil disturbance reduces the native ant populations. Newly-mated, dispersing fire ant queens locate these disturbances while in flight and settle in them preferentially to try to establish new colonies. The question is, do they know what they are doing? Does settling in such sites improve their chances of success?

We set up experimental plots in a Florida pine forest with all combinations of soil tilling, shading and reduction of the native ant community (using poison baits). We then planted newly-mated fire ant queens, incipient colonies and small colonies in these plots and followed their survival. Survival of newly-mated queens and incipient colonies was extremely low, but those that did survive were exclusively in plots in which native ants had been reduced and/or the soil disturbed. Planted small colonies fared much better: in plots with reduced native ants, 21 of the 108 planted colonies (19%) were still alive 15 months later, while in plots with an intact native ant population, less than 2% of the 108 colonies survived.

By choosing to land in disturbed habitat with its reduced native ant population, newly mated fire ants queens increase their chances of successful colony establishment. This ant community is thus assembled primarily by queen habitat choice and secondarily by competition. Queens do know what they are doing.

Image caption: The experimental plots in the Apalachicola National Forest in Florida. Several tilled plots and shade covers are apparent.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Tree height, not fruit shape or weight, predicts how far wind dispersed seeds fly

Carol K. Augspurger, Susan E. Franson, and Katherine C. Cushman A representative dispersal unit of each of 12 wind-dispersed study species in Panama.  The results show that tree height and number of dispersal units, and not how fast the dispersal unit falls, explain the pattern of seeds distributed around the parent tree.Image provided by authors.

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Seeds that disperse further from their parent tree often have a better chance of survival. Seed dispersal may send a parent’s offspring to areas with more light, and therefore improved growth. Also, offspring may arrive in areas of lower seed density and away from the parent tree where fungi and herbivores are less likely to attack them. However, how a parent controls where its offspring are dispersed is unclear. This study provides insights into factors critical in predicting the pattern of seeds that fall around a parent tree. This pattern is important because dispersal determines how many of a parent’s offspring survive.

Here, we studied wind-dispersal by 12 Panamanian tree species. Our results showed that dispersal units with a higher weight to area ratio fell faster in still air. However, this speed of fall did not predict dispersal distance when many dispersal units were released from a 40 m tower in the forest. Likewise, these traits did not explain how far a seed landed after natural dispersal from the parent tree.

The pattern of seeds around parent trees of the 12 species differed greatly. We found that taller trees had greater average and maximum seed dispersal distances. Trees dispersing a greater number of seeds also had a greater average dispersal distance. In contrast, a seed’s speed of fall in still air, which is related to how long it is exposed to winds, was not important. Generally, the tree variables predicted dispersal distance well, but unaccounted factors about the dispersal unit or the parent tree, or, more likely, variation in wind speeds that seeds experienced after release, were also important.

Therefore, tree traits explained dispersal distances of these wind-dispersed species, particularly over long distances where offspring survival is enhanced. Apparently, a taller tree exposes its seeds to stronger winds, particularly updrafts after they are released, and carries them to farther distances and lower densities, and perhaps to higher light where some offspring may survive. Future studies should focus on wind strengths needed to release the seeds from the tree, as well as wind patterns after release, to improve our understanding of dispersal.

Image caption: A representative dispersal unit of each of 12 wind-dispersed study species in Panama. The results show that tree height and number of dispersal units, and not how fast the dispersal unit falls, explain the pattern of seeds distributed around the parent tree. Image provided by authors.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Intraspecific trait variation across multiple scales: the leaf economics spectrum in coffee

Adam Martin, Bruno Rapidel, Olivier Roupsard, Karel Van den Meersche, Elias de Melo Virginio Filho, Mirna Barrios and Marney Isaac Photograph provided by authors.

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Ecologists are interested in knowing how changes in biodiversity affect ecosystems. Specifically, they are often interested in understanding how biodiversity losses reduce the “services” that ecosystems provide. In agricultural systems for example, we are interested in knowing how reduced diversity affects crop yield, pest outbreaks, or crop responses to climate change. For a long time, ecologists have measured biodiversity simply as the number of species in an ecosystem. But more recently they are interested in “functional diversity”: in other words, the range of leaf, root and stem types that are present in an ecosystem.

Generally, functional diversity is a better predictor of ecosystem services than simply the number of species, so it has become important to know which are the most ecologically important functional traits in plants. Leaf functional traits – notably, photosynthetic rates, the amount of nitrogen in a leaf, and leaf mass per area – get the most attention. One main way ecologists have come to know these traits are ecologically important is by examining how they relate to one another. Looking at the leaves of hundreds of species, they have uncovered general trends in plants globally: as leaf nitrogen goes up, photosynthesis goes up, and leaf mass per area goes down.

While we know this happens across plant species in natural ecosystems (or “wild” plants), we are still unsure i) if these relationships occur when we look across different individuals of the same species, or ii) if these relationships in wild plants also occur in crops, which have been domesticated over many years.

We looked at these questions in coffee, one of the world’s most common (and well-loved) crops. We found that the same leaf traits that are ecologically important in wild plants are also ecologically important in coffee. Specifically, we found that across nearly 400 leaves from 100 coffee plants, as leaf nitrogen goes up, photosynthesis goes up, and leaf mass per area goes down. But in coffee, these relationships are not the same as in wild plants, possibly because coffee has been bred to have a lot of caffeine, much of which may be in leaves.

Image caption: Photograph provided by authors.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Climate and tree vigour control the timing of wood formation in deciduous oaks

Gonzalo Pérez-de-Lis, José Miguel Olano, Vicente Rozas, Sergio Rossi, Rosa Ana Vázquez-Ruiz and Ignacio García-GonzálezTransverse section of wood from pedunculate oak (Quercus robur). Dividing cells in the cambial zone (centre) give rise to new phloem (top) and xylem (bottom) tissues.

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Trees produce new wood during their whole lifespan. Tissue known as ‘vascular cambium’ generates a new tree ring that is disposed over the existing wood tissues every year. To sustain the machinery of growth, trees need to invest large amounts of carbohydrates produced in the leaves via photosynthesis. Trees adjust how they function in different climates by shifting the timing of growth (i.e. phenology), although this can influence the capability of trees to produce wood. Understanding how phenology affects wood production is of special relevance in the context of climate warming, which is modifying phenological patterns in terrestrial plants.

We monitored wood and leaf formation, and the content of non-structural carbohydrates (NSC), in the stems of two deciduous species, pedunculate oak (Quercus robur) and Pyrenean oak (Quercus pyrenaica), in three sites located along a humidity gradient in northwestern Spain. Although Pyrenean oak is better adapted to drought than pedunculate oak, both species coexist along the transition between the temperate and Mediterranean regions. We also assessed the impact of the number of cambial cells in winter (higher in more vigorous trees) on wood production and phenology during the following growing season.

Pedunculate oak was more productive and had a longer growing season than Pyrenean oak, but both species showed comparable seasonal changes in growth activity and carbon reserves. We show that, under warm and dry conditions, deciduous oaks reduce or even stop growth in summer, but extend the growing season in spring and autumn. Stem NSC dropped in spring simultaneously with the onset of growth, and recovered in summer after the formation of new leaves. Trees with more cambial cells in winter had a longer growing season and produced more wood. This result indicates that tree vigour acts as a predisposing factor for growth, modulating carbon demands throughout the year.

Image caption: Transverse section of wood from pedunculate oak (Quercus robur). Dividing cells in the cambial zone (centre) give rise to new phloem (top) and xylem (bottom) tissues.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Integrating intraspecific variation in community ecology unifies theories on bodysize shifts along climatic gradients

Alice Classen, Ingolf Steffan-Dewenter, William J. Kindeketa, Marcell K. PetersImage provided by the authors.

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Species traits, like the size and shape of organisms, change along broad-scale climatic gradients. Probably the most famous biogeographical pattern in this context is Bergmann’s rule, which says that species tend to get larger in cooler environments. This has been explained by the fact that species with larger body sizes are energetically favoured because they lose less heat, in relative terms, due to a reduced surface-to-volume ratio. An alternative hypothesis is that energy availability effectively limits the maximum size of organisms. Absolute energy requirements of larger organisms are higher than those of smaller organisms, i.e. they need more energy and space to maintain critical population sizes and are predicted to face higher extinction risks in energy-limited environments. Thus, the predictions concerning body size distributions are contradictory.

Tropical mountains provide excellent conditions to study the patterns and drivers of species traits, as here potential drivers like temperature, area and resource availability change rapidly, making ecological studies feasible. In this study we analysed the body size distributions of wild bees on the highest free-standing mountain in the world, Mount Kilimanjaro (Tanzania). As we assumed that different drivers may operate at different levels of biological organization we studied trends in body size at both the community and species level.

We show that Bergmann´s rule and energy-based predictions are both evident in bee communities along the elevational gradient of Mt. Kilimanjaro. While individuals within species became on average larger with increasing elevation, communities in cooler habitats were increasingly dominated by smaller species. Thus, whether evidence for one or the other hypothesis is found depends on the level of biological organization. We conclude that the integration of intraspecific variation into community ecology can unify conflicting theories on body size shifts along temperature gradients.

Image caption: Image provided by the authors.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Wood anatomy reflects different ecological strategies in tropical rainforest lifeforms

Deborah M.G. Apgaua, David Y.P. Tng, Lucas A. Cernusak, Alexander W. Cheesman, Rubens M. Santos, Will J. Edwards and Susan G.W. LauranceAnatomy of a rainforest liana Strychnos minor showing large and largely solitary vessels. Image provided by the authors.

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Tropical rainforests harbour a large portion of the world’s plant diversity, yet many scientists fear these communities are at risk from increasing drought events. In order to understand how forests with thousands of species will respond to droughts, we explored how plants that live in different parts of the forest differ in form and function.

We studied 90 plant species in a lowland rainforest in northeast Australia that differed in their habitat preferences, ranging from the dark understorey to the tops of trees. These species formed six ecological groups: mature-phase trees, understorey trees, pioneer trees, understorey shrubs, pioneer shrubs and vines. We sampled wood from these species to collect data on anatomical features related to water transport, such as vessel sizes, frequency and distribution. We also collected leaves from each species to quantify leaf intrinsic water use efficiency through carbon isotope ratios, a measure of how much carbon could be taken up by photosynthesis for a given amount of water lost to transpiration.

Across our study species, we found a spectrum of different wood characteristics. Large climbing plants called lianas, for instance, had low wood densities and exhibited large solitary vessels, indicating an ecological strategy that maximizes water transport at the expense of mechanical support. At the other end of the spectrum, understorey shrubs and trees had high wood densities and numerous small vessels, possibly reflecting a higher investment in structural support, and the reduced need for high water transport. Vessel size was also a strong predictor of water use efficiency across our 90 study species, indicating that plants with larger vessels, and thus a higher potential for water transport, are able to fix more carbon per unit of water transpired. We therefore provide a framework for understanding plant performance through wood functional anatomy and a plant functional group approach.

Image caption: Anatomy of a rainforest liana Strychnos minor showing large and largely solitary vessels. Image provided by the authors.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Mosses in Californian grasslands in a changing environment

Risto Virtanen, Anu Eskelinen and Susan Harrison A view over the experimental site at McLaughlin Nature Reserve (Inner Coastal Ranges, California) with harsh serpentine (background) and non-serpentine grassland (foreground). The green grassland patches in the middle of harsh serpentine are created by simulated eutrophication and increased rainfall. In these grasslands, typical bryophytes include Didymodon vinealis (left insert) and Fissidens sublimbatus (right insert). Photos by Anu Eskelinen and Risto Virtanen.

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Bryophytes (mosses) are small spore-producing plants that occur in most global ecosystems. Even where they are relatively scarce, such as in semiarid grasslands, bryophytes still may play important roles in various processes such as nutrient cycling, surface water dynamics or vascular plant regeneration. Human impacts such as projected climate shifts and nutrient deposition are likely to change both the abundances and the ecological role of bryophytes.

We simulated two environmental changes, increased springtime rainfall and increased nutrient availability, in a semiarid grassland in California. Both of these changes are already known to make grassland plant communities more productive and more strongly dominated by tall vascular plant species such as exotic annual grasses. In turn, this increase in productivity has been shown to suppress the abundance and diversity of smaller vascular plants, many of which are native annual forbs (“wildflowers”). We asked whether bryophytes would show this same competitive suppression of abundance and diversity under enhanced rainfall and nutrients.

As predicted, both bryophytes and small vascular plants declined under our rainfall and nutrient addition treatment as biomass and tall plant dominance increased. In contrast, adding water alone benefited bryophytes but not small vascular plants, while adding nutrients alone benefited small vascular plants but not bryophytes. In general, our results support the idea that environmental changes that enhance grassland productivity and dominance of tall vascular plants are likely to harm grassland diversity, including bryophytes as well as small vascular plants.

Image caption: A view over the experimental site at McLaughlin Nature Reserve (Inner Coastal Ranges, California) with harsh serpentine (background) and non-serpentine grassland (foreground). The green grassland patches in the middle of harsh serpentine are created by simulated eutrophication and increased rainfall. In these grasslands, typical bryophytes include Didymodon vinealis (left insert) and Fissidens sublimbatus (right insert). Photos by Anu Eskelinen and Risto Virtanen.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

How will climate change affect predatory invasive species?

Brian S Cheng, Lisa M Komoroske and Edwin D GrosA predatory Atlantic oyster drill rests upon an Olympia oyster. In many parts of the world, oyster drills have been accidentally introduced and may pose a problem for native oysters. These negative effects may intensify with climate change. Oyster drill egg capsules can also be seen on the right side of the photo. Photo credit: Brian Cheng.

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The spread of invasive species has resulted in tremendous economic impacts and losses to biodiversity across the planet. There is concern that climate change may worsen the impacts of invaders, partly because many of these species appear to be more tolerant of changing environmental conditions than their native counterparts. However, most of our knowledge in this area is from alien species that are taxonomically related to or that compete with natives. Invasive predators are among the most disruptive non-native species, yet we know almost nothing of how these animals may respond to climate change. To address this, we examined the physiology of two invasive predators (oyster drills – predatory sea snails) and their native prey (oysters) to understand how these species may respond to warming and extreme flood events. We found that these predators were generally less tolerant of extreme climate change conditions as compared to their prey. However, when animals were exposed to conditions representing near-term warming, predator performance and foraging on prey oysters increased greatly. These observations are supported by previous field measurements that indicate intense predation on oysters at the warmest sites. In addition, both invasive predators exhibited different temperatures of peak performance, suggesting that there is a broad temperature range over which predators will consume prey oysters.

Although extreme events appear to favor prey oysters, near-term warming trends may ultimately reduce their abundance in nature. This is a concern, because wild oysters have experienced declines of up to 88% over the last century due to overfishing and habitat degradation. In response, there are active efforts to conserve and restore oyster populations in many parts of the world. Our work suggests that climate change and the invasion of non-native species may severely hamper the recovery of oysters. Future efforts to assist native oysters should consider attempting to eradicate invasive predators that may benefit from climate change.

Image caption: A predatory Atlantic oyster drill rests upon an Olympia oyster. In many parts of the world, oyster drills have been accidentally introduced and may pose a problem for native oysters. These negative effects may intensify with climate change. Oyster drill egg capsules can also be seen on the right side of the photo. Photo credit: Brian Cheng.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Does differential processing of coral and algal exudates by reef sponges influence dissolved organic matter cycling via the “sponge loop”?

Laura Rix, Dick van Oevelen, Ulrick Struck, Fuad Al-Horani, Christian Wild and Malik NaumannImage provided by authors.

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The efficient recycling of nutrients on coral reefs contributes to the characteristic high productivity of these diverse underwater ecosystems. The main primary producers on coral reefs, corals and algae, release large quantities of their excess products from photosynthesis as energy-rich dissolved organic matter (DOM). This DOM represents the largest source of organic matter produced on coral reefs, but most reef organisms that rely on organic matter as a source of energy cannot directly utilize DOM as a food source. Sponges are not only able to consume DOM, but they also transform and release a fraction of the DOM they assimilate as particulate detritus, which can then be used as a food source by many other reef organisms. This sponge-mediated DOM recycling pathway has been termed the “sponge loop” and plays a key role in transferring the energy and nutrients in DOM to higher trophic levels on coral reefs. Interestingly, the DOM released by corals and algae differs in composition and nutritional quality, but the influence of these different DOM sources on recycling by sponges has not been investigated.

We used incubation experiments to compare the processing of coral- and algal-derived DOM by three coral reef sponge species from the Red Sea: Chondrilla sacciformis, Hemimycale arabica, and Mycale fistulifera. We found that the sponges took up and assimilated both coral- and algal-derived DOM into their tissue biomass, but that uptake rates were significantly higher for algal-derived DOM. A substantial fraction (15–49%) of the coral- and algal-derived DOM assimilated by the sponges was subsequently converted into and released as particulate detritus. However, algal-derived DOM was released as detritus at a higher rate. These findings suggest that sponges process and recycle algal-DOM more rapidly than coral-derived DOM. As coral reefs are increasingly threatened by anthropogenic impacts, many corals reefs are undergoing community shifts from coral to algal dominance. By demonstrating that the DOM produced by algae enhances DOM recycling via the sponge loop, our findings have potential consequences for both nutrient cycling and the transfer of energy through food webs on coral reefs.

Image caption: Image provided by authors.
Read the article in full here.

 

Moose in disturbed forests: impacts on plant regeneration, litter decomposition and soil composition

Nichola Ellis and Shawn LerouxImage provided by authors.

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Herbivores, such as moose, can play an important role in ecosystems. By selectively feeding on certain plant species, herbivores can reduce the growth of their preferred plants and promote growth in those plant species they avoid. Herbivores usually consume plants that are relatively high in nitrogen and phosphorus and avoid plants that are relatively high in carbon and non-palatable toxins. Most of the plant material not consumed by herbivores dies and becomes litter which then decomposes in the soil. Depending on feeding preferences, herbivores can dramatically change the concentrations of carbon, nitrogen and phosphorus in the soil. This could influence plant growth, and the insects, birds and other animals that depend on plants.

Evidence from studies in boreal forests in North American show that moose, via their feeding activities, can change plant communities, decrease the amount of carbon, nitrogen, and phosphorus in soils and decrease the time it takes for litter to decompose. We tested the influence of moose and abiotic conditions, such as climate, on plant communities and soils in Newfoundland, Canada, a temperate marine island with different climatic and environmental history from that in other studies.

We used 10 large fenced areas to exclude moose and found that after 15-20 years of moose absence, both preferred and non-preferred plants were able to grow taller, and produce more litter compared to areas where moose were feeding. However, concentrations of carbon, nitrogen, and phosphorus in soils and litter decomposition time were not impacted by moose, while soil depth and soil pH were higher and lower respectively. Our results suggest that, in Newfoundland, environmental conditions such as moisture and disturbance history may have a greater impact on soil quality and litter decomposition than moose presence. We show that future studies of herbivore impacts on forests should consider the importance of environmental conditions. In Newfoundland, Parks Canada should continue to monitor moose populations and forests to see if the effect of moose on forest ecosystems changes over time.

Image caption: Image provided by authors.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

The outcome of competition between two parasitoid species is influenced by a facultative symbiont of their aphid host

Ailsa H.C. McLean & H. Charles J. GodfrayAphelinus abdominalis parasitizing Acyrthosiphon pisum. Photo by Jan Hrček.

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Many insects have close and ongoing relationships with symbiotic bacteria, which can provide a number of different benefits, including defence against natural enemies. In this study, we asked whether this protection can affect how different natural enemies interact with one another; specifically, can symbiont-mediated protection alter the outcome of competition between natural enemies?

We studied aphids which carry a symbiotic bacterium that can provide protection against parasitoid wasps. The wasps lay their eggs inside aphids, and the developing wasp larva eventually kills the aphid, but not until the very end of its development. The symbiotic bacteria can act to kill the wasp at an early stage, but the symbionts are not equally effective against all wasp species. We used a symbiont strain which is known to provide strong resistance against one species, Aphelinus abdominalis, but much weaker resistance against a second species, Aphidius ervi. We asked how this asymmetric protection affects the outcome of competition between these two different wasp species when they lay eggs in the same aphid. In these interactions, only one wasp can develop successfully.

We allowed a female of first one wasp species, then a female of the other wasp species, to lay one egg each in a single aphid and compared the outcome for aphids with and without the symbiont. We asked which wasp species successfully developed, or did the aphid survive? We found that, in symbiont-free aphids, the first wasp to oviposit gained an advantage. However, A. abdominalis never survived in the presence of the symbiont. This allowed A. ervi, which would normally have been the inferior competitor, to develop successfully in aphids with the symbiont, even when it parasitized the aphid second. Our results show that protective symbionts do not only affect the interaction between the host and a natural enemy, but also the outcome of competition at the next trophic level.

Image caption: Aphelinus abdominalis parasitizing Acyrthosiphon pisum. Photo by Jan Hrček.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

Special Feature: Plant–Pollinator Interactions from Flower to Landscape

Specialization and generalization in pollination mutualisms

William ArmbursterA male Euglossa cf. dilemma collecting eugenol from blotter-paper (bait) in Yucatan, Mexico.  This species of bee is a floral generalist in foraging for nectar (males and females) and pollen (females) resources but a floral specialist in foraging for fragrant compounds for mate attraction (males) and resins for use in nests (females).  Note orange hairs on front feet, blue velvet pads on mid legs, and enlarged hind legs, which are used in fragrance collection, transfer, and storage, respectively. The bee is about 12 mm long. (Photo: WS Armbruster).

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The role of specialization in pollination ecology is a central question in contemporary research on plant evolution and the ecology of flower-visiting animals. However, there are several different uses of the term specialization in ecology and evolutionary biology, and organizing these into a comprehensive framework is an overdue task, earlier attempts notwithstanding. At least three different meanings can be distinguished: ecological (pollination by one or a few kinds of animals or visiting one of few kinds of flowers), phenotypic (having specialized flowers or structures), and evolutionary (evolving towards greater specialization). Additional complexities include scope and scaling. The relationships among these various meanings are nuanced and can be a source of confusion. For example, specialized floral phenotypes do not necessarily indicate specialized pollination ecology.

The natural history of specialized plant-pollinator interactions is the stuff of classic nature films. Tight associations and coevolution abound, but are not by any means the rule. Instead, plants often respond genetically to selection generated by their pollinators, while pollinating animals themselves remain little changed. For example, recent studies of the pollination of specialized orchids and other flowers pollinated by male euglossine bees (photo) have shown that the plants have responded evolutionarily to the relationship, but the bees have not. This is despite the fact that many of these bees depend on certain flowers for fragrance compounds that are essential for attracting female bees of their species, and thus for passing on their genes.

Earlier studies have suggested that specialized pollination is expected to increase plant diversity by increasing speciation rates. However, support for this mechanism is weak, and other mechanisms explaining the association exist, including specialization reducing extinction rates or being a result of selection generated by competition with related plant species in the local environment.

The intimate relationships between plants and pollinating animals can be viewed both as ecosystem services (e.g. for crop pollination) and as processes essential for the reproduction of plants and the animals they host, and thus long-term viability of natural communities. We need to better understand the natural history and degree of specialization in such relationships to assess the vulnerability of natural ecosystems to the challenges being inflicted on the planet by growing human populations.

Image caption: A male Euglossa cf. dilemma collecting eugenol from blotter-paper (bait) in Yucatan, Mexico. This species of bee is a floral generalist in foraging for nectar (males and females) and pollen (females) resources but a floral specialist in foraging for fragrant compounds for mate attraction (males) and resins for use in nests (females). Note orange hairs on front feet, blue velvet pads on mid legs, and enlarged hind legs, which are used in fragrance collection, transfer, and storage, respectively. The bee is about 12 mm long. (Photo: WS Armbruster).
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Competition shaping the phytoplankton communities, judged from the functional properties of the species

Riina Klais, Veera Norros, Sirpa Lehtinen, Timo Tamminen and Kalle OlliMorphological diversity of phytoplankton, from single cells to different colonies and chains. Photo credit: Dr. Richard Kirby.

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Understanding the rules of species coexistence is central for ecological research. Phytoplankton – free-living phototrophic protists and cyanobacteria (the bluegreens) – are known to be controlled by temperature, salinity, light, and nutrients. Species’ environmental preferences define the biogeography and seasonality of phytoplankton functional groups (the most well known being diatoms, dinoflagellates and blue-greens). This knowledge is already used to inform global plankton models. Much less is known about the role of biotic interactions – especially competition – between phytoplankton species in the assembly of natural communities.

We analysed a large coastal phytoplankton dataset, consisting of nearly 8000 samples, collected from the Baltic Sea over the last 30 years, and covering the seasonal cycle and wide salinity and temperature gradients. We first estimated the preferred habitat of every species. From that information, we constructed the simulated communities – as they should be, if only the environment determines community composition. These simulated communities were then compared against the actually observed communities.

We investigated whether the species in the observed community were functionally more or less similar to each other than the simulation predicted. The similarity was judged from characteristics such as body size, ability to fix atmospheric nitrogen, whether they are both auto- and heterotrophic at the same time, whether they swim around, make colonies or chains to change the body shape and avoid predators, and the composition of accessory pigments that phytoplankton use to harvest all the different wavelengths of light that penetrate the water.

When comparing the simulated and observed communities, we found that one in every four communities was notably shaped by competition, because species in it were either too similar, or too dissimilar to each other for their coexistence to be explained only by the environment.

Image caption: Morphological diversity of phytoplankton, from single cells to different colonies and chains. Photo credit: Dr. Richard Kirby.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Which are the drivers of animal personality: hormone levels or metabolic rates?

Benedikt Holtmann, Malgorzata Lagisz and Shinichi NakagawaColour-ringed dunnock (Prunella modularis) from the Dunedin Botanic Garden, New Zealand. Photo credit Stefanie Grosser.

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Animals of the same population often show individual variation in their behaviours, which are consistent over time (i.e. repeatable). For example, some individuals are consistently more active, more explorative or more aggressive than others. While these repeatable behavioural differences, referred to as animal personality, have been described in various species, we still know very little about their underlying mechanisms and how personality differences are maintained. Recent studies in the field of animal personality have proposed that consistent individual differences in hormone levels and/or metabolic rates may be responsible for mediating consistent behavioural differences. Thus, here we investigate the relationship between behavioural and the two proposed physiological traits by testing the hypothesis that physiological traits (hormones vs. metabolism) that mediate consistent individual differences in behaviour exhibit similar or higher time-consistency (i.e. repeatability) compared to behavioural traits.

We systematically reviewed published (and unpublished) data from bird species on the repeatability of hormone levels, metabolic rates and behavioural traits, combining results from all relevant articles. Our analyses revealed that both metabolic rates and behavioural traits were highly repeatable and that repeatability estimates of both traits were of similar magnitude. Conversely, the repeatability of hormone levels was three times lower, suggesting that individual hormone levels are more variable over time. These results indicate that individual differences in metabolic rates, rather than hormone levels, are likely a key mechanism involved in generating consistent individual differences in behaviour.

Moreover, additional analyses revealed three more notable findings. First, repeatability estimates of hormone levels and behavioural traits decrease with increasing interval time between two consecutive measurements. Second, males and females differ in repeatability for behavioural traits. And third, hormone level measurements, taken within a few minutes after the capture of an individual (baseline levels) show higher variation than hormone levels taken at least 30 minutes after capture (stress-induced levels).

By conducting meta-analyses, we show that metabolic rates are likely one of the mechanisms underlying consistent individual differences in behaviour. Future studies are now needed to investigate the relationship between metabolic rates and personality traits in more detail.

 

Aphid-generated indirect interaction network

Yoshino Ando, Shunsuke Utsumi and Takayuki OhgushiFigure showing how aphid created an interaction network through ant-mediated and plant-mediated indirect effects.

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A wide variety of herbivorous insects may share a host plant. Since the strength and direction of an interaction between two species can be indirectly altered by a third species, multiple insect herbivores on plants can interact directly and indirectly with each other.

Herbivory can induce morphological and/or chemical changes in plants, thereby affecting interactions with subsequent insect herbivores, called a plant-mediated indirect effect. Although past studies have focused on interactions between co-occurring species, plant-mediated indirect effects can affect plant-associated arthropod communities by connecting species that are separated in time and space. However, little is known about how and to what extent multiple direct/indirect interactions can create an interaction network through plant-mediated indirect effects.

We focused on the potential role of an aphid in creating an interaction network on tall goldenrods, and used an aphid exclusion experiment to examine how the aphid affects the interaction network through aphid-generated indirect effects and its consequence for plant reproductive success .

The aphid played a critical role as a network creator in determining the interaction network. The aphid indirectly decreased co-occurring insects through their removal by ants (an ant-mediated indirect effect). Also, late in the season when the aphid was no longer present, it still indirectly decreased scale insects but increased grasshoppers through aphid-induced leaf regrowth. As a result, aphid-induced leaf regrowth greatly contributed to an increase in the interaction diversity and complexity by connecting co-occurring and temporally-separated herbivores. Moreover, the aphid-generated interaction network could improve the reproductive success of tall goldenrods by increasing seed production.

Image caption: Figure showing how aphid created an interaction network through ant-mediated and plant-mediated indirect effects.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Insects adapt in real-time to cold but not hot temperatures

Mads Fristrup Schou, Marie Brandt Mouridsen, Jesper Givskov Sørensen & Volker Loeschcke To measure the cold tolerance of small insects, they are distributed individually to small numbered glass tubes, which are lowered into a fluid with a low freezing point (<10°C). Hereafter, several machines work together to perform a controlled decrease in temperature, while every single fly is monitored through the glass. The temperature at which all movement of a fly stops is noted, and is a measure of the cold tolerance. Photograph credit: Mads F. Schou.

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The ability of insects to evolve and adapt to an increased or a decreased temperature is receiving a great deal of attention, as a consequence of current and future climate change. But adaptation through evolutionary change, which typically requires multiple generations, is not the only way organisms can adapt. Organisms have a remarkable ability to adjust important traits during their lifetime, to stay well aligned with the environment at hand. One example among many is the drastic change in fur color of snowshoe hares from brown to white before the arrival of winter. Do insects also have the ability to readily adjust their physiology or morphology? If insects can increase their cold tolerance when winter is coming, and increase their heat tolerance as the temperature increases during summer, this may be a short-cut for dealing with the expected changes in temperature during the next century. In an attempt to answer this question we investigated 13 species of fruit flies, with distributions that are either world-wide or restricted to deserts, the cold northern climate or the tropical climate. Throughout the entire life cycle, the flies were reared at one of several different temperatures spanning their entire tolerable temperature range. We then estimated the ability to adjust their physiology and thereby align their tolerance according to the given temperature. All 13 species had a surprisingly strong ability to readily adjust their cold tolerance as a response to rearing temperature. This ability is without doubt central for their ability to survive in natural habitats. Conversely, all species had very limited ability to increase their heat tolerance when reared in warmer temperatures, and some species even suffered a decrease in heat tolerance, likely because the high temperatures stressed them. In conclusion, heat tolerance is a highly fixed trait which is unlikely to be rapidly adjusted within generations as an adaptive response during a changing climate, at least in comparison to the strong response with respect to cold tolerance.

Image caption: To measure the cold tolerance of small insects, they are distributed individually to small numbered glass tubes, which are lowered into a fluid with a low freezing point (<10°C). Hereafter, several machines work together to perform a controlled decrease in temperature, while every single fly is monitored through the glass. The temperature at which all movement of a fly stops is noted, and is a measure of the cold tolerance. Photograph credit: Mads F. Schou.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Handbook of protocols for standardized measurement of terrestrial invertebrate functional traits

Marco Moretti, André T.C. Dias, Francesco de Bello, Florian Altermatt, Steven L. Chown, Francisco M. Azcárate, James R. Bell, Bertrand Fournier, Michael Hedde, Joaquín Hortal, Sébastien Ibanez, Erik Öckinger, José Paulo Sousa, Jacintha Ellers and Matty P. BergPhotographs of Isopoda  by Theodoor Heijerman.

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Traits are simply species characters that can be measured or observed directly and are commonly a descriptor of a behavioural or morphological adaptation. The first well known observation was made by Charles Darwin who famously described the shape of finch bills and their functional relationship with seed size and form. Beyond shape and form, traits strike at the very heart of how individuals increase their survival and fitness in relation to environmental conditions - Darwin’s theory of natural selection brilliantly illustrated that. Relating traits to functions can ultimately provide a measure of how key ecosystem processes and services, like nutrient cycling and pollination, might be affected if communities were to change. Perhaps not surprisingly, the practical side of trait ecology is little different to how taxonomists collect measurements to describe new species: ecologists collect measurements like body size, life span, eye morphology and these are then mapped using a standardized protocol. Measurements are projected in a ‘trait space’ that displays the range and variability of traits of interest, and in doing so, seemingly unrelated species are linked to identify general principles and emergent ideas. Traits have yet to realize their full potential because the methodology is rarely standardized outside of plant ecology, an issue that we try to resolve in this paper for terrestrial invertebrates. We propose the first handbook of protocols for standardized measurements of 29 terrestrial invertebrate traits known to be sensitive to global stressors and to affect key ecosystem processes and services. As has been the case with plants, standardized functional traits will be used in the future to explain invertebrate community assembly, species diversity patterns, and ecosystem processes and services within and across taxa and trophic levels. Meta-analyses across regions and ecosystems will likely highlight future weaknesses and vulnerabilities in communities, as they have done to some extent with pollination. Importantly, we have left room for new knowledge to be incorporated into the trait protocols, using a standard format within which researchers can further provide methodological input for additional special cases.

Image caption: Photographs of Isopoda by Theodoor Heijerman.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

Special Feature: Plant–Pollinator Interactions from Flower to Landscape

How do anthropogenic volatile pollutants affect the olfactory communication between plants and their pollinators?

Andreas Jürgens & Mascha BischoffAnthropogenic air pollution sources (e.g. industries, traffic, urban areas, and crops) and their putative effect on olfactory communication between plants (signal emitters) and animals (signal receivers). Image provided by authors.

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Floral scent has been shown to play a key role as a signal in interactions between flowering plants and flower-visiting animals. However, human activities such as industrialisation, urbanization and the expansion of agricultural areas may disrupt this olfactory communication in complex ways. The overall result of all these effects could be a reduced diversity of signals within flowering communities, i.e. a dominance of species that communicate efficiently with pollinators mostly via visual signals.

In this paper, we review how anthropogenic activities that introduce volatile chemicals into the environment may interfere with olfactory information transfer between flowering plants and flower visiting insects. Both natural and anthropogenic “odour landscapes” are highly variable in space and time. We are just beginning to understand how signal emitters (plants) and signal receivers (insects) are affected by odour landscape dynamics and what the ecological and evolutionary responses may be. Changes in the levels of air pollution can affect plants and their visitors on four fundamental levels: (i) by causing changes in plant metabolic processes, thus inducing plant stress and changes in signal emission, (ii) by interacting with infochemicals, thus ‘garbling’ the message, (iii) by increased levels of airborne ‘background noise’ hampering signal detection and finally, (iv) by affecting pollinator signal perception and behaviour. Air pollution may already be causing an overall loss of information in plant-pollinator communities leading to mismatches between interaction partners. The consequences of such information-impoverished plant-pollinator communities are reduced pollination efficiency for plants, lower foraging efficiency for animals, and higher competition between species.

These impacts are expected to intensify in the coming decades. Understanding how relevant factors affect the biological fitness of plants and flower visitors and the overall resilience/stability of plant-pollinator networks is therefore important for the development of conservation strategies and crucial to ensure food security and pollinator health.

Image caption: Anthropogenic air pollution sources (e.g. industries, traffic, urban areas, and crops) and their putative effect on olfactory communication between plants (signal emitters) and animals (signal receivers). Image provided by authors.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

Special Feature: The Ecology of De-Extinction

Using palaeoecology to determine baseline ecological requirements and interaction networks for de-extinction candidate species

Jamie R. Wood, George L. W. Perry, Janet M. WilmshurstCoprolites, such as this of an extinct New Zealand moa, are a source of detailed information on the habitat and dietary requirements, microbiota and parasite communities of extinct species. Photo by J. R. Wood.

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One of the main drivers for research into de-extinction (or reviving extinct species) is the potential for returning lost processes and function to modern-day ecosystems. For example, some extinct animals may have been the sole pollinators or seed dispersers for particular plant species, which have now declined themselves as a result of the extinction. Other extinct animals may have played key roles in nutrient deposition, and their extinction may have had major flow-on effects for nutrient cycles. Restoring such species is seen as likely to have beneficial results for ecosystems.

However, this viewpoint focusses mainly on what de-extinction candidates can do for ecosystems. We must also understand and provide the ecological requirements of candidate species, as this will play a key role in determining the success of a de-extinction. Aspects of these include: (i) habitat requirements; (ii) dietary requirements; (iii) microbiota communities; and (iv) parasite communities. Information on these can be challenging to obtain for extinct species, but here we review how different palaeoecological sample types and analytical techniques can be used to gain insights into such requirements. Although palaeoecological data have an important role in guiding and informing the selection of suitable de-extinction candidates, they can only ever provide an incomplete picture, and therefore must complement, rather than replace, observational or experimental data on the resurrected organisms themselves.

Image caption: Coprolites, such as this of an extinct New Zealand moa, are a source of detailed information on the habitat and dietary requirements, microbiota and parasite communities of extinct species. Photo by J. R. Wood.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Physiological maturity at a critical life-history transition and flight ability at fledging

Allison Cornell, Kate F. Gibson and Tony D WilliamsA fledgling European starling (Sturnus vuglaris) attempts to take off in flight, photo by A. Cornell.

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It’s a dangerous world out there for young birds leaving the nest. When songbirds fledge, they make a permanent transition from the sedentary lifestyle of a nestling to a highly active, free-flying fledgling. Outside the nest they have to look for food, escape from predators, and navigate in their habitat. Reported rates of survival show that nearly half of chicks that make this transition die almost immediately, largely due to predators who mark them as easy prey. It’s no surprise that predators choose to go after these juvenile birds; they’re relatively slow to take off, and have poor flight ability.

We investigated the maturity of fledglings on the day they leave the nest, to measure just how developed these young birds are. Consistent with other studies, we found that the values of somatic traits, such as body size and wing length, were smaller than adults. However, when we measured physiological traits that indicate the body’s ability to transport oxygen, we found more than just low trait values. Our fledglings were highly variable in these traits, indicating that this might be a good way to measure the quality of individuals. When we measured the birds’ flight ability, we found that physiological traits were helpful as predictors of take-off angle and energy produced during flight.

When scientists typically study fledglings, only measurements of body size are taken. Our results show that measuring physiological traits might help us distinguish between low and high quality fledglings, because these traits have high individual variation and help predict flight ability. The physiological traits we measured are relatively easy to obtain, and recording these values could greatly impact the way we understand fledglings. If physiological traits are the mechanism driving fledgling flight ability, then for a juvenile bird, physiological maturity could mean the difference between life and death.

Image caption: A fledgling European starling (Sturnus vuglaris) attempts to take off in flight, photo by A. Cornell.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

Review

Does biomass-growth increase in the largest trees? Flaws, fallacies and alternative analyses.

Douglas Sheil, Chris Eastaugh, Mart Vlam, Pieter Zuidema, Peter Groenendijk, Peter van der Sleen, Alex Jay and Jerome VanclayImage provided by authors.

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Trees play a major role in the global carbon cycle and our understanding of tree growth informs forest science and management. Yet the characteristic growth pattern of most tree species remains unknown. Until recently most researchers thought that biomass-growth declined at large stem sizes. But recent studies claim to show that biomass-growth increases throughout a tree’s life with no ultimate decline both in forests and in open-grown competition-free environments. Such contrasting views merit careful assessment. Here we examine how methodological issues can influence the detection and interpretation of biomass-growth trends.

Growth studies of large trees pose various challenges. These challenges range from finding enough of such trees (they typically occur at low densities) to measuring them in an accurate and consistent manner (see figure). Correcting stem measurement errors can itself cause biases that increase perceived biomass-growth with tree size. To estimate biomass change from tree measurements requires the size-biomass relationship to be well characterised (calibrated) but for most species and for large stems in general, these relationships remain unknown. Using general species-averaged size-biomass relationships leads to large uncertainties regarding biomass and biomass-growth at large sizes in each species. A problem arises when growth patterns within and among stems are confused (these patterns can be distinct as they reflect distinct ecological processes).

To explore and illustrate some of our concerns we use growth-rings to examine the lifetime growth of 14 tropical tree species. Our examination of estimated biomass-growth in 706 stems indicates similar numbers of positive and negative trends with most trees having relatively flat growth (i.e., without marked trends) over extended periods. Nonetheless, when we compare stems all but one of our 14 species indicate higher biomass-growth in the larger stems. Individual stems and patterns across stems thus lead to contrasting conclusions: any confusion of these would constitute a so called “Ecological Fallacy”.

We note that recent studies concluding that biomass-growth increases as stems grow larger do not in fact examine patterns in individual stems but compare variation in growth among stems. Patterns among stems themselves remain uncertain too, due to errors and possible artefacts. We describe how these problems can be avoided or reduced so as to provide reliable results and conclusions.

Image caption: Image provided by authors.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Plants direct the dispersal of their seeds towards suitable sites

Merel B. Soons, G. Arjen de Groot , M. Teresa Cuesta Ramirez, Rob G. A. Fraaije, Jos T.A. Verhoeven & Monique de JagerImage provided by authors.

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Plants cannot move to find new places to live in – instead, they produce seeds that disperse to sites away from the parent plant. Seed dispersal usually involves the transportation of the seeds by animals, water or wind. Animals may purposely or accidentally pick up seeds and deposit them at another site when they are moving. Depending on the behaviour of the animal, this mode of transportation may be very efficient for plants. For example, the seeds of wetland plants may be ingested by ducks in one pond and excreted after a couple of hours in the next pond visited by the bird. In this way, seeds are transported to new sites that are suitable for the plant species to grow in. Such efficient transportation of seeds towards suitable sites is called ‘directed dispersal’.

Directed dispersal is known mostly for animal-dispersed plant species. However, most plant species are not dispersed by animals but by water or wind. Wouldn’t it be highly efficient for these species as well, if their seeds were dispersed predominantly towards suitable sites? We investigated whether directed dispersal also exists in water-dispersed and wind-dispersed wetland plant species. To this purpose, we studied a range of wetland plant species growing in shorelines, from the permanently inundated, aquatic part to the permanently dry, upland part. We discovered that plants growing under permanently inundated, wet conditions produce large seeds that sink immediately in water. These seeds are transported at the bottom of the pond, stream or ditch by water flows that take them only to other inundated, wet sites. In contrast, plants growing at the waterline produce seeds that float for extensive periods of time until they are eventually washed ashore in… the waterline. In these ways, plants growing in the reach of water use the transportation capacity of water in very different ways to direct the dispersal of their seeds towards suitable sites.

Plants growing on the uplands have seeds that are best dispersed by wind, facilitating their transportation across wet areas to reach dry sites.

Image caption: Image provided by authors.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

 

Movement ability of an invasive beetle is related to leg length but not body size nor metabolic rate

Pieter A. Arnold, Phillip Cassey, Craig R. White Red flour beetle moving through wheat flour. Schematic of the maze used to assess movement is inset in the top left. Photo: Pieter Arnold.

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Individuals within a species can vary greatly in their ability to move around and disperse within their environment. This variation in movement ability can often be described by physiological, morphological and behavioural traits that are related to dispersal, but the associations among such traits are not always clear-cut or predictable. Previous studies, including work on the invasive cane toad in Australia, have identified that individuals that are larger and have longer legs relative to their body size are able to move farther and faster than smaller or proportionate individuals. In our study, we used an invasive insect species, the red flour beetle, as a model to investigate how movement characteristics related to morphological and physiological traits. Individual beetles were run through a maze that simulated a complex environment, to assess their movement. We identified that movement ability could be described along an axis; individuals that scored positively on this axis moved at higher speed, travelled longer distances, moved continuously, and reached the edge of the maze quicker. Leg length relative to body size was strongly related to movement ability. That is, beetles with relatively long legs had positive movement ability scores, which we hypothesised was because longer legs allow for longer stride length and therefore a greater movement ability. Surprisingly, body size and metabolic rate (energy expenditure) were unrelated to movement ability. This result suggests that dispersal may be more strongly related to the muscles and structures that directly affect locomotion, rather than body size overall or energy-related traits. It will be important for future studies to consider locomotor morphology as a foundation for studying variation in movement and dispersal, especially when investigating the ecology and evolution of traits in invasive or pest species.

Image caption: Red flour beetle moving through wheat flour. Schematic of the maze used to assess movement is inset in the top left. Photo: Pieter Arnold.
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. You can find the As Accepted version here.

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