Natural selection in novel environments: predation selects for background matching in the body colour of a land fish

The invasion of a novel habitat often results in a variety of new selective pressures on an individual. One pressure that can severely impact population establishment is predation. The strategies that animals use to minimize predation, especially the extent to which those strategies are habitat or predator specific, will subsequently affect individuals' dispersal abilities. The invasion of land by a fish, the Pacific leaping blenny, Alticus arnoldorum, offers a unique opportunity to study natural selection following the colonization of a novel habitat. Various studies have examined adaptations in respiration and locomotion, but how these fish have responded to the predation regime on land was unknown. We studied five replicate populations of this fish around the island of Guam and found their body coloration converged on the terrestrial rocky backgrounds on which the fish were most often found. Subsequent experiments confirmed that this background matching significantly reduced predation. Natural selection has therefore selected for background matching in the body coloration of the Pacific leaping blenny to minimize predation, but it is a strategy that is habitat specific. A subsequent comparative study of closely related blenny species suggested that the evolutionary ancestor of the Pacific leaping blenny might have resembled the rocky backgrounds on land prior to invasion. The ancestors of the Pacific leaping blenny may therefore have already been ideally suited for the predator regime on land. More generally our results imply that animals must either already possess antipredator strategies that will be effective in new environments, or must adapt very quickly to new predation pressures if successful establishment is to occur. Ó 2013 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. Adaptive divergence among taxa often arises when populations invade new environments (reviewed by Schluter 2001). This is because changes in the selection regime experienced by invaders can lead to changes in phenotype (adaptation). The colonization of novel environments has therefore been of special interest to evolutionary biologists because of the opportunity it brings to study natural selection in the wild (e.g. If an individual is indistinguishable from other aspects of the environment, it is less likely to be attacked than one that is not. Tactics used to reduce detection and recognition by predators in this way include masquerading as an unpalatable food item Contents lists available at ScienceDirect Animal Behaviour j o u r n a l h o me p a g e : w w w . e l s e v i e r . c o m / l o ca t e / a n b e h a v establishment does occur, animals may be restricted to certain areas within that habitat where individuals are less conspicuous. Predation may still be a problem, but selection has the opportunity to drive the evolution of greater crypsis or some other strategy to minimize predation. Species in this latter scenario offer a means to study how predation can affect the colonization process and provide a wonderful opportunity to study the process of natural selection more generally (e.g. The primary goal of our study was to test the general hypothesis that visually oriented predators on land have selected for a body coloration in the Pacific leaping blenny that matches the rocky backgrounds against which the fish are typically found. We tested this hypothesis in two ways. First, we examined five populations of blenny around Guam and determined the extent to which the body coloration of each population matched their environments (we measured both the hue (chromatic) and brightness (achromatic) properties of fish and backgrounds). We replicated our study across five populations because initial observations suggested habitat backgrounds varied subtly from location to location. Given this, we predicted that populations would converge on the colour properties specific to their location. To provide a suitable benchmark for this colour comparison, we also quantified the colour of the dorsal fin, which is an important signal in social interactions for both males and females (Ord & Hsieh 2011) and should therefore be conspicuous in the environment (e.g. To provide some resolution of the evolutionary history of body coloration, and whether it might have facilitated or challenged the invasion of land by the Pacific leaping blenny, we supplemented these two studies with an ad hoc examination of body coloration in representative specimens of several closely related marine species found around the island. This comparative study was not meant to provide a formal phylogenetic reconstruction of ancestor phenotype, which would require detailed and extensive sampling of species across the blenny phylogeny (as well as their environments). Rather, the goal was to reveal the extent to which the Pacific leaping blenny differed or resembled its marine relatives and, by extension, the likelihood that the fish has evolved its presentday body coloration prior to, or following, the colonization of land. METHODS Population Colour Analysis Adult male and female Pacific leaping blennies and specimens of closely related species were captured using hand nets at five locations around Guam between June and August 2011 (overlapping with the probable breeding season of this genus; see Full body photographs were taken of individuals positioned side-on to the camera with the dorsal fin raised against a white standard background (X-Rite ColorChecker White Balance Card) and beside a ruler and a Munsell colour chart (X-Rite mini ColorChecker; Colour analysis was performed using the inCamera plug-in for Photoshop CS4. The images that were analysed for a given individual were those photographs that exhibited the lowest standard deviation for the red, green and blue (RGB) colour channels of the colour squares of the Munsell colour chart (i.e. those photographs with the least amount of within-image variance in lighting). The colour and brightness of these images were then standardized using the known RGB values of the colour squares in the Munsell chart with the inCamera plug-in (see To quantify achromatic properties or the brightness of colour, we took the average value of all three colour channels and divided this number by 255 to compute a value between 0 (corresponding to black or zero brightness) and 1 (corresponding to white or maximum brightness; NB: white has a value of 255 for the R, G and B channels, whereas black has a value of 0 for all three channels). We quantified the colour of fish for a common section of the dorsal fin and a representative, similarly sized area of the body This type of standardized colour analysis makes several assumptions about the spectral properties of the object being measured and, subsequently, the most relevant spectral sensitivities of the visual system of the organism viewing the object. Like most digital cameras, the one we used relied on image sensors that captured reflected light over a wavelength range of 400 to 700 nm, which is designed to match the wavelengths visible to humans. Actual data on the spectral sensitivity of these sensors for the make and model of the camera we used was not available. However, peak sensitivities of the sensors most likely occur at (or close to) 475, 550 and 625 nm, with sensitivity curves around these peaks overlapping extensively to ensure consistent colour representation across the visible spectrum in captured images (this is based on specifications published by Canon, the colour processing tests of DxO Image Science for the same make and model of camera (www. dxo.com), and the spectral sensitivities of other digital cameras that have been reported by Whether or not UV reflectance is relevant is dependent on the visual system of the predator viewing the blenny. We anticipated most predation occurred from birds, land crabs or lizards. Many birds and lizards do see into the UV To compare body, fin and background colour and brightness, we used the degree of overlap between the 95% confidence intervals of means and the magnitude of effect sizes (R/G and brightness ratios were normally distributed for all populations). Means with 95% confidence intervals that did not overlap were considered statistically different from one another (equivalent to P < 0.05). For effect size magnitude, we computed effects for two sample comparisons (body versus background colour or brightness; fin versus background colour or brightness) as a standardized mean difference (Cohen's d). This value and its 95% confidence interval were then converted into an r value. A biological effect was interpreted if the confidence intervals of r did not overlap zero. Equations for effect size computations are given in Predation Experiment We used highly realistic plasticine models made from casts of euthanized male and female Pacific leaping blennies to test the relative predation pressure between two environments: intertidal rocks and sandy beach. We chose Taga'chang to perform the experiment because it was a site where both habitat types occurred immediately adjacent to each other and were infrequently used by people. The blenny was found in both habitats, but densities were heavily skewed towards the rocky environment. Observations of blennies on the beach were generally limited to areas of wet sand within several metres of isolated rock outcrops that were within the intertidal zone. As a method of quantifying predation, the use of plasticine or clay models has been successfully used in a variety of taxa (e.g. Note that we assumed that predators were equally abundant in both environments. We had no reason to believe that this assumption was not correct prior to conducting the experiment: models and controls were positioned in rocky and beach habitat that were immediately adjacent to each other (e.g. within several metres of each other) and observations of birds, land crabs and lizards (likely predators) were made in both habitats. If anything, predator density may have been slightly skewed towards the rocky habitat: while birds were frequently observed in both habitats, we often observed large land crabs and lizards on the rocks but less so on the beach. Nevertheless, the subsequent frequency of attack rates recorded during the experiment was generally consistent with the notion that predators were equally likely to target stimuli in both habitats (see Results). Both models and controls were of similar size; photos of both stimuli positioned in the environment are shown in Models and controls were placed alternately along transects parallel to the shoreline at intervals of approximately 1.5 m. In the rocky habitat, models and controls were attached to rocks using fishing line and in areas that were above the high tide waterline, but otherwise within the splash zone (i.e. areas frequented by blennies but where stimuli would not be washed away by the tide). In the beach habitat, models and controls were secured by lengths of fishing line to plastic lids that were buried in the sand and positioned above the high tide waterline. The integrity of stimuli was checked daily and evidence of predation was tallied after 3 days, following which all stimuli were removed from the environment. On occasion, unusually large swells buried stimuli on the beach and these were replaced daily. On day 3, stimuli were categorized on the following criteria: (1) no marks; (2) single or multiple small nicks; (3) large punctures or nicks; (4) entire portions missing; or (5) only the anchor point remaining. For our analyses, we focused on categories 3 and 4 as evidence of predation. Category 2 seemed to reflect the inspection of stimuli by small scavenging organisms rather than predator attacks (e.g. ants nibbling at stimuli). Category 5 was exempt from analysis as it was not possible to exclude wave action or human interference as reasons for model disappearance. To make monitoring manageable, the experiment was conducted in two halves. Consecutive batches of stimuli were dispatched in nonoverlapping areas of each environment, for a final total of 70 models and 70 controls. The experiment was run over 8 days (2 days were devoted to the removal and positioning of stimuli between batches). Our final tally based on the recovery rates of stimuli was 52 models and 63 controls in the rocky habitat and 58 models and 64 controls from the beach habitat. The experiment was conducted from 6 July to 12 August 2011. Differences in predation rate between models and controls, and between environments for a given stimulus type, were evaluated through a comparison of 95% CIs of the proportion of stimuli exhibiting predation and relevant effect sizes (see previous section, Population Colour Analysis). Confidence intervals for proportions were computed using formula presented in Zar (2010). Comparisons in which the 95% CIs of proportions did not overlap were considered to be statistical different from one another (i.e. equivalent to P < 0.05). We also calculated effect sizes by computing an odds ratio and its associated 95% CI, and then converting this value into an r value using formula presented in . Comparative Study To explore the extent to which body coloration might have changed following the colonization of land, we compared the colour morphology of the Pacific leaping blenny to 12 closely related blenny species. These 12 species covered the full diversity of intertidal blenny species around Guam. Species ranged from exclusively marine (seven species) to amphibious (five species). These behavioural categorizations were based on observations made of fish behaviour during collection. Marine species were always observed fully immersed in water (e.g. swimming about in open water), while amphibious species were observed immersed in water and above the waterline in rock holes or (more rarely) out in the open on rocks. The Pacific leaping blenny was the only species that remained exclusively out of the water at all times. The assessment of species colour morphology relied largely on a qualitative comparison of coloration among species, coupled with a single estimate of the chroma and brightness of the specimen examined for each species. This comparison was made with reference to a preliminary phylogeny created using maximum parsimony and based on two mitochondrial DNA genes (ATPase 6 and 8) and four nuclear DNA genes (RAG1, ZiC, Sreb2 and Ptr; G. M. Cooke & T. J. Ord, unpublished data). A formal ancestor state reconstruction of chroma and hue was inappropriate given that the species found on Guam were only a subset of the species found in the entire C. L. Morgans, T. J. Ord / Animal Behaviour 86 Nevertheless, a general comparison of the colour morphology among our subset of species still provides a reasonable picture of the probable history of colour evolution in the group. For example, if the Pacific leaping blenny appears very similar in colour to its marine and amphibious relatives, then it likely evolved from an ancestor that was also very similar in appearance. Otherwise, the extent to which the Pacific leaping blenny differs in colour morphology from its immediate relatives provides a general indication of the extent to which colour evolution has likely changed following, or in conjunction with, the colonization of land. RESULTS Background Matchin

Evaluating the effectiveness of palm oil certification in delivering multiple sustainability objectives

Industrial oil palm plantations in South East Asia have caused significant biodiversity losses and perverse social outcomes. To address concerns over plantation practices and in an attempt to improve sustainability through market mechanisms, civil society organisations and industry representatives developed the Roundtable on Sustainable Palm Oil (RSPO) in 2004. The effectiveness of RSPO in improving the sustainability of the palm oil industry is frequently debated and to date, few quantitative analyses have been undertaken to assess how successful RSPO has been in delivering the social, economic and environmental sustainability outcomes it aims to address. With the palm oil industry continuing to expand in South East Asia and significant estates being planted in Africa and South America, this paper evaluates the effectiveness of RSPO plantations compared to non-certified plantations by assessing the relative performance of several key sustainability metrics compared to business as usual practices. Using Indonesian Borneo (Kalimantan) as a case study, a novel dataset of RSPO concessions was developed and causal analysis methodologies employed to evaluate the environmental, social and economic sustainability of the industry. No significant difference was found between certified and non-certified plantations for any of the sustainability metrics investigated, however positive economic trends including greater fresh fruit bunch yields were revealed. To achieve intended outcomes, RSPO principles and criteria are in need of substantial improvement and rigorous enforcement

Impact of palm oil sustainability certification on village well-being and poverty in Indonesia

The Roundtable on Sustainable Palm Oil (RSPO) has emerged as the leading sustainability certification system to tackle socio-environmental issues associated with the oil palm industry. To date, the effectiveness of RSPO certification for achieving its socioeconomic objectives remains uncertain. We evaluate the impact of certification on village-level well-being across Indonesia by applying counterfactual analysis to multi-dimensional government poverty data. We compare poverty across 36,311 villages between 2000 and 2018, tracking changes from before oil palm plantations were first established to several years after plantations were certified. Certification was associated with reduced poverty in villages with primarily market-based livelihoods, but not with those in which subsistence livelihoods were dominant before switching to oil palm. We highlight the importance of baseline village livelihood systems in shaping local impacts of agricultural certification, and assert that oil palm certification in certain village contexts may require additional resources to ensure socioeconomic objectives are realised

Data from: Natural selection in novel environments: predation selects for background matching in the body colour of a land fish

The invasion of a novel habitat often results in a variety of new selective pressures on an individual. One pressure that can severely impact population establishment is predation. The strategies that animals use to minimize predation, especially the extent to which those strategies are habitat or predator specific, will subsequently affect an individuals’ dispersal ability. The invasion of land by a fish, the Pacific leaping blenny, Alticus arnoldorum, offers a unique opportunity to study natural selection following the colonization of a novel habitat. Various studies have examined adaptations in respiration and locomotion, but how these fish have responded to the predation regime on land was unknown. We studied five replicate populations of this fish around the island of Guam and found their body coloration converged on the terrestrial rocky backgrounds on which the fish were most often found. Subsequent experiments confirmed that this background matching significantly reduced predation. Natural selection has therefore selected for background matching in the body coloration of the Pacific leaping blenny to minimize predation, but it is a strategy that is habitat specific. A subsequent comparative study of closely related blenny species suggested that the evolutionary ancestor of the Pacific leaping blenny might have resembled the rocky backgrounds on land prior to invasion. The ancestors of the Pacific leaping blenny may therefore have already been ideally suited for the predator regime on land. More generally our results imply that animals must either already possess antipredator strategies that will be effective in new environments, or must adapt very quickly to new predation pressures if successful establishment is to occur

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Data from: How populations differentiate despite gene flow: sexual and natural selection drive phenotypic divergence within a land fish, the Pacific leaping blenny

Background: Divergence between populations in reproductively important features is often vital for speciation. Many studies attempt to identify the cause of population differentiation in phenotype through the study of a specific selection pressure. Holistic studies that consider the interaction of several contrasting forms of selection are more rare. Most studies also fail to consider the history of connectivity among populations and the potential for genetic drift or gene flow to facilitate or limit phenotypic divergence. We examined the interacting effects of natural selection, sexual selection and the history of connectivity on phenotypic differentiation among five populations of the Pacific leaping blenny (Alticus arnoldorum), a land fish endemic to the island of Guam. Results: We found key differences among populations in two male ornaments—the size of a prominent head crest and conspicuousness of a coloured dorsal fin—that reflected a trade-off between the intensity of sexual selection (male biased sex ratios) and natural selection (exposure to predators). This differentiation in ornamentation has occurred despite evidence suggesting extensive gene flow among populations, which implies that the change in ornament expression has been recent (and potentially plastic). Conclusions: Our study provides an early snapshot of divergence in reproductively important features that, regardless of whether it reflects genetic or plastic changes in phenotype, could ultimately form a reproductive barrier among populations

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All data associated with Morgans et al. 201

Not more, but strategic collaboration needed to conserve Borneo's orangutan

In conservation, Collaboration is thought to improve returns from investment and is frequently encouraged, however not all collaborations are equal and may therefore lack characteristics important for addressing collective action problems. Furthermore, partnerships that are advantageous for a collective may not necessarily be advantageous for an individual. This study investigated collaboration within the Bornean orangutan (Pongo pygmaeus) conservation sector - a system with reported inefficiencies and for which there has been a renewed call for collaborative partnerships. Collaborative partnerships were conceptualised as a social network and analysed using exponential random graph modelling. The prevalence of structural attributes associated with social processes considered to be important for solving collective action problems such as trust and innovation were investigated. Qualitative surveying techniques were used to measure the perceptions of collaboration held by individual actors within the network and the impact of organizational attributes on network formation and perceptions was assessed. Collaboration was found to be occurring within the conservation network and was positively perceived at the individual organisational level. At the collective level, the current collaborative network contains some structural characteristics important for addressing the collective-action problem of orangutan conservation, particularly through innovation and knowledge sharing. However efforts to develop trust between organisations may be needed. To improve returns on investment, future collaborative partnerships must be strategically implemented with individual roles and desired overall outcomes explicitly articulated. Increased operational transparency and improved performance evaluation will be critical for achieving improved collaborative efficiency. (C) 2017 The Authors. Published by Elsevier B.V