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Plant Camouflage: Ecology, Evolution, and Implications

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Abstract

Camouflage is a key defensive strategy in animals, and it has been used to illustrate and study evolution for 150 years. It is now evident that many camouflage concepts likely also apply to plants, attracting greatly increased attention. Here, we review the hypotheses and evidence for different camouflage strategies used by plants and conceptualise the state of play in plant concealment under a general framework of camouflage theory. In addition, we compare the camouflage strategies used by plants and animals, outline key factors promoting and constraining the evolution of concealment, and highlight the evolutionary and ecological implications of plant camouflage. Ultimately, we show how plant camouflage exhibits many commonalities with animals and how this understudied parallel phenomenon can inform key questions in ecology and evolution.

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... Part of the diverse defensive arsenal of land plants against herbivores is anti-herbivory coloration and morphology (Lev-Yadun, 2016), including among many tactics mimicry, masquerade and camouflage. Defensive (anti-herbivory) mimicry in plants received little attention in the past, especially in comparison with defensive or aggressive mimicry in animals (Ruxton, Sherratt & Speed, 2004;Lev-Yadun, 2016;Quicke, 2017;Niu, Sun, & Stevens, 2018). Notable exceptions are host resemblance in Australian parasitic mistletoes (Barlow & Wiens, 1977;Canyon & Hill, 1997), host-tree leaf mimicry in the liana Boquila trifoliolata (DC.) ...
... Decne. (Gianoli & Carrasco-Urra, 2014), background matching leaf colours (Lev-Yadun, 2006, 2016Niu et al., , 2018 and the proposed Batesian mimicry between two species from New Zealand [the chemically defended leaves of the model Pseudowintera colorata (Raoul) Dandy, which is visually mimicked by the leaves of the non-defended Alseuosmia pusilla Colenso; Yager, Schaefe & Gould, 2016]. ...
... Camouflage, 'potentially the best of all defences' (Lev-Yadun, 2016), enables the organism to become less detectable to a predator by means of crypsis, e.g. by countershading, disruptive coloration and/ or background matching (e.g. Cott, 1940;Ruxton et al., 2004;Merilaita & Lind, 2005;Niu et al., , 2018. A special case of background matching in plants consists of sticky trichomes, enabling the plant organism to be covered with small particles of the surrounding soil (Jürgens, 1996;Lev-Yadun, 2006). ...
Article
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We revisit a case of mimicry in Amorphophallus involving visual mimicry of lichens and colonies of cyanobacteria on their tree-trunk sized petioles. We investigate the entire genus for similar defensive coloration types and report a defensive leaf coloration strategy in several Amorphophallus spp. that involves mimicry, camouflage and plant-mimicking that results in defensive visual masquerade. We propose that the visual expression of lichen and cyanobacteria mimicry enables the huge and fleshy petioles to look like solid non-edible tree trunks, a classic case of masquerade, probably as defence against herbivores. The results are discussed in a phylogenetic and evolutionary context.
... Since 2000, following a wave of interest in various types and cases of defensive plant coloration, plant camouflage has received more theoretical and experimental attention (e.g. Lev-Yadun, 2006a, 2016bKlooster et al., 2009;Fadzly et al., 2009Fadzly et al., , 2016Burns, 2010;Schaefer & Ruxton, 2011;Lev-Yadun & Ne'eman, 2013;Porter, 2013;Farmer, 2014;La Rocca et al., 2014;Niu et al., 2014Niu et al., , 2017Niu et al., , 2018Niu et al., , 2021Aviezer & Lev-Yadun, 2015;Strauss et al., 2015;Quicke, 2017). Wiens (1978) proposed that light coloration, achieved by sand attached to sticky glandular trichomes, may camouflage plants from herbivores, an issue further discussed by Lev-Yadun (2006a) and LoPresti & Karban (2016). ...
... Cook et al., 1971;Saracino et al., 1997Saracino et al., , 2004Lev-Yadun & Ne'eman, 2013;Porter, 2013;Aviezer & Lev-Yadun, 2015;Lev-Yadun, 2016b). In various seeds camouflage is achieved not only by background matching, but also by disruptive coloration (Aviezer & Lev-Yadun, 2015;Niu et al., 2018) predators. The evolution of aposematic signalling is based on the ability of target enemies to associate the signals with the risk, damage or non-profitable handling, and later to avoid such organisms as prey (Cott, 1940;Edmunds, 1974;Ruxton et al., 2004). ...
... The defensive strategy known as masquerade, or camouflage without crypsis, has until recently received very little scientific attention even in animals (e.g. Allen & Cooper, 1985; Ruxton et al., 2004;Skelhorn et al., 2010a, b, c;Skelhorn, 2015;Quicke, 2017), and concerning plants very little (Lev-Yadun, 2014a, 2016bSkelhorn, 2015;Quicke, 2017;Niu et al., 2018;Claudel et al., 2019). Masquerade by animals is a situation when prey, parasite or predator resembles inedible objects such as leaves, twigs, stones, birddroppings or any other relevant object. ...
Article
A common idea is that resisting or blocking herbivore attacks by structural, chemical and molecular means after they have commenced is the first line of plant defence. However, these are all secondary defences, operating only when all the various methods of avoiding attack have failed. The real first line of plant defence from herbivory and herbivore-transmitted pathogens is avoiding such attacks altogether. Several visual, chemical and ‘statistical’ methods (and commonly their combined effects) have been proposed to allow avoidance of herbivore attacks. The visual types are camouflage, masquerade, aposematic coloration of toxic or physically defended plants (including Müllerian/Batesian mimicry), undermining herbivorous insect camouflage, delayed greening, dazzle and trickery coloration, heterophylly that undermines host identification, leaf movements, and signalling that colorful autumn leaves are soon to be shed. The mimicry types include: herbivore damage, insects and other animals, fungal infestation, dead/dry leaves or branches, animal droppings, and stones and soil. Olfactory-based tactics include odour aposematism by poisonous plants, various repelling volatiles, mimicry of faeces and carrion odours, and mimicry of aphid alarm pheromones. The ‘statistical’ methods are mast fruiting, flowering only once in many years and being rare. In addition to the theoretical aspects, understanding these mechanisms may have considerable potential for agricultural or forestry applications.
... Several potential physiological advantages of variegation have been proposed in plants. For example, it was reported that leaf variegation is involved in plant defense from enemies including aposematic coloration, mimicry of dead or infested plants, masquerade and camouflage [16][17][18][19]. It can also play physiological roles such as improved water or gas transport [20], mitigation of UV radiation [21] and thermoregulation [22]. ...
... Nine DEGs, all being heat shock proteins (HSP) were detected within this pathway. Notably, we observed that all the small HSP genes (15)(16)(17)(18)(19)(20)(21)(22) were down-regulated while the high molecular weight HSP genes (70-90 kDa) were up-regulated in the variegated leaves (Table 5). This result highlights the weight dependent roles of HSP genes for a stout cold response in variegated P. tobira. ...
... The natural occurrence of variegation in plants suggests that the trait might play some adaptive functions beyond their aesthetic value [32]. It has been suggested that leaf variegation plays several physiological and ecological functions such as defense from enemies, adaptations to light, temperature, etc. [16][17][18][19][20][21][22][23][24][25]. We tested the hypothesis that leaf variegation plays a low temperature protective function in P. tobira, which is an ornamental shrub widely grown in temperate climate and therefore is annually subjected to cold stress. ...
Article
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Leaf variegation has been demonstrated to have adaptive functions such as cold tolerance. Pittosporum tobira is an ornamental plant with natural leaf variegated cultivars grown in temperate regions. Herein, we investigated the role of leaf variegation in low temperature responses by comparing variegated “Variegatum” and non-variegated “Green Pittosporum” cultivars. We found that leaf variegation is associated with impaired chloroplast development in the yellow sector, reduced chlorophyll content, strong accumulation of carotenoids and high levels of ROS. However, the photosynthetic efficiency was not obviously impaired in the variegated leaves. Also, leaf variegation plays low temperature protective function since “Variegatum” displayed strong and efficient ROS-scavenging enzymatic systems to buffer cold (10 °C)-induced damages. Transcriptome analysis under cold conditions revealed 309 differentially expressed genes between both cultivars. Distinctly, the strong cold response observed in “Variegatum” was essentially attributed to the up-regulation of HSP70/90 genes involved in cellular homeostasis; up-regulation of POD genes responsible for cell detoxification and up-regulation of FAD2 genes and subsequent down-regulation of GDSL genes leading to high accumulation of polyunsaturated fatty acids for cell membrane fluidity. Overall, our results indicated that leaf variegation is associated with changes in physiological, biochemical and molecular components playing low temperature protective function in P. tobira.
... Color signals are then seen by mutualist and antagonist alike (Schaefer et al. 2004). Through color, flowers can be conspicuous (Schaefer et al. 2004), camouflaged (Niu et al. 2018) and even aposematic (Lev-Yadum 2011), but it all depends on who is looking and their sensory capabilities. ...
... Flowers of Eucomis autumnalis and Eucomis comosa (Asparagaceae) are visually cryptic by having a similar color to leaves, attracting pollinators solely by smell (Shuttleworth & Johnson 2009). Unfortunately, camouflage is a poorly studied topic in plants (Niu et al. 2018). Previously, dull-colored bat pollinated flowers were considered as camouflaged from other visitors (Fleming et al. 2009), but bats and other pollinators can use visual cues from these flowers (Domingos-Melo et al. 2021). ...
Article
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Diversity and distribution of flower coloration is a puzzling topic that has been extensively studied, with multiple hypotheses being proposed to account for the functions of coloration, such as pollinator attraction, protection against herbivory, and prevention of damage by ultraviolet light. Recent methodologies have allowed studies to consider the visual system of animals other than humans, helping to answer questions regarding the distribution of flower coloration. A survey of keywords in Web of Science shows floral color to be mainly studied in relation to macroevolutionary traits and biochemistry of pigments, focusing on pollination and anthocyanins, respectively. The present paper reviews mechanisms that determine the color of flowers. First, it is discussed how pigment, visual systems and signaling environments influence flower color; secondly, patterns of convergent evolution of flower color is debated, including evolutionary history, pollinator preference, flower color change, flowering season, and habitat. Third and last, patterns of flower coloration that have been found around the globe are addressed. In short, the aim is to contribute to ongoing research, by underlining mechanisms that lead to global patterns of coloration and indicating perspectives for future study on the topic. Keywords: floral color; flower coloration; color vision; pollination ecology; sensory drive; flower color change; pollinator preference; color preference; flowering season
... Defensive plant colouration gained much more attention in the 21 st century (e.g. Archetti, 2000Archetti, , 2009bArchetti et al., 2009a;Burns, 2010;Cooney et al., 2012;Fadzly et al., 2009;Farmer, 2014;Hughes & Lev-Yadun, 2015;Lev-Yadun, 2001, 2021Lev-Yadun et al., 2004;Lev-Yadun & Gould, 2007Lev-Yadun & Holopainen, 2009;Lev-Yadun & Ne'eman, 2012Maskato et al., 2014;Niu et al., 2018;Quicke, 2017;Ruxton et al., 2004Ruxton et al., , 2018Schaefer & Ruxton, 2009. Altogether, yellow autumn leaf colouration and red autumn leaf colouration are just two related phenomena out of many cases and mechanisms of anti-herbivory plant colouration. ...
... (2) Plants camouflage themselves (Klooster et al., 2009;Lev-Yadun, 2006a, 2021Niu et al., 2018). ...
Article
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Yellow and red autumn leaves are typical of many temperate/boreal woody plants. Since the 19th century, it has been either considered the non‐functional outcome of chlorophyll degradation that unmasks the pre‐existing yellow and red pigments or that the de novo synthesis of red anthocyanins in autumn leaves indicated that it should have a physiological function, although it was commonly ignored. Defending free amino acids and various other resources released especially following the breakdown of the photosynthetic system, and mobilizing them for storage in other organs before leaf fall, is the cornerstone of both the physiological and anti‐herbivory hypotheses about the functions of yellow and red autumn leaf colouration. The complicated phenomenon of conspicuous autumn leaf colouration has received significant attention since the year 2000, especially because ecologists started paying attention to its anti‐herbivory potential. The obvious imperfection of the hypotheses put forth in several papers stimulated many other scientists. Hot debates among physiologists, among ecologists, and between physiologists and ecologists have been common since the year 2000, first because the various functions of yellow and red autumn leaf colouration are non‐exclusive, and second because many scientists were trained to focus on a single subject. Here, I will review the debates, especially between the photoprotective and the anti‐herbivory hypotheses, and describe both the progress in their understanding and the required progress. Yellow and red autumn leaves typical to temperate/boreal trees defend important resources released following the photosynthetic system breakdown, and mobilized for storage to be used in the next spring. This coloration, especially red, defends from excess light and oxidative stress and against herbivores. I describe the hypotheses, findings and disagreements about the functions and evolution of yellow/red autumn leaves.
... When a prey encounters a predator, it will produce anti-predator responses, such as camouflage [13][14][15], seeking refuge [16][17][18], etc. Faced with these anti-predation responses, predators also look for ways to restrain them, such as hunting cooperation. ...
... where E is defined in (19). According to (15), we can obtain that LV ≤ −1 for all (x, y) ∈ W 2 . Case 3. ...
Article
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This paper proposes a stochastic predator–prey model with hunting cooperation and nonlinear stochastic disturbance, and focuses on the effects of nonlinear white noise and hunting cooperation on the populations. First, we present the thresholds R1 and R2 for extinction and persistence in mean of the predator. When R1 is less than 0, the predator population is extinct; when R2 is greater than 0, the predator population is persistent in mean. Moreover, by establishing suitable Lyapunov functions, we investigate the threshold R0 for the existence of a unique ergodic stationary distribution. At last, we carry out the numerical simulations. The results show that white noise is harmful to the populations and hunting cooperation is beneficial to the predator population.
... A possible way to circumvent this trade-off, particularly relevant in the context of floral apparency, is that plants can potentially avoid herbivory through visual crypsis. Although crypsis is widely reported in animals as an anti-predation strategy, it is not frequently reported in plants (but see Klooster, Clark, & Culley, 2009;Lev-Yadun, 2016;Niu, Sun, & Stevens, 2018;Strauss & Cacho, 2013). While visual crypsis in flowers as anti-herbivory defence may seem counterintuitive, visual signalling is not always the primary mechanism plants use to attract pollinators (Johnson, 1995). ...
... Interestingly, the plant species that close at night had upper petal surfaces that are more apparent to pollinators than those that do not close. This suggests that the reduction in herbivory that results from cryptic lower petal surface coloration might mitigate the herbivory costs associated with brightly coloured upper petal surfaces, allowing upper petal surfaces of closing daisies to become more conspicuous to pollinators.Cryptic coloration as anti-herbivore defence in plant vegetative tissue is increasingly being recognized(Lev-Yadun, 2016;Niu et al., 2018). Various studies have shown local adaptation of leaf colour to match the background colour, particularly in sparse vegetation or in rocky areas, leading to reduced herbivory(Niu et al., 2014;Strauss & Cacho, 2013;Strauss, Cacho, Schwartz, Schwartz, & Burns, 2015).For instance, some palatable plant species on scree slopes match the colour of the scree, and the lower apparency reduces herbivory rates(Niu et al., 2014;Strauss & Cacho, 2013). ...
Article
Floral apparency is shaped by both mutualistic and antagonistic interactions that can act in opposing ways. Pollinators are expected to select for more visually apparent flowers, but this likely trades off against the potentially severe fitness costs of damage to apparent flowers by floral herbivores. One way in which flowers that close during parts of the day might circumvent this trade‐off is by evolving less visible lower petal surfaces that are inconspicuous to herbivores when flowers are closed. Here, we used visual system modelling and herbivory experiments to test whether petal surfaces that are exposed when flowers are closed are cryptically coloured. We collected lower and upper petal surface spectra for 77 Asteraceae species from Namaqualand, South Africa. This included closing species that expose their lower petal surfaces for 5–6 daylight hours and non‐closing species that do not expose their lower surfaces. We used these contrasting groups to test the expectation of reduced conspicuousness of lower petal surfaces in closing, but not non‐closing species. By modelling reflectance spectra of petal surfaces against a green leaf background in various visual systems, we showed (a) that conspicuousness of upper petal surfaces to pollinators and various herbivores was strongly correlated, suggesting the potential for fitness trade‐offs between attracting mutualists and antagonists to open flowers, (b) that closing species' lower petal surfaces were less visible to herbivores against a leaf background than those of non‐closing species and (c) that closing species had larger differences between upper and lower petal surface coloration than non‐closing species. Behavioural experiments with tortoise herbivores demonstrated that flowers are easily detected when upper surfaces are exposed, but that tortoises were unable to distinguish lower petal surfaces against a leaf background, resulting in reduced flower herbivory. These results are consistent with selection by herbivores for cryptic coloration of lower petal surfaces, and divergence of coloration between lower and upper petal surfaces in species with closing flowers. Visual crypsis of flowers may be an effective anti‐herbivory strategy during times when pollinators are inactive, and provides an alternative to chemical defence, which often involves costs to pollination. A free Plain Language Summary can be found within the Supporting Information of this article. A free Plain Language Summary can be found within the Supporting Information of this article.
... Camouflage in plants is well documented and can take many forms (Niu et al., 2018). For example, different coloured Pinus seeds undergo different rates of predation by birds on the mosaic of soil types in post-fire landscapes (Nystrand and Granstr€ om, 1997;Saracino et al., 1997Saracino et al., , 2004Lev-Yadun and Ne'eman, 2013). ...
... not oval or round) and many of the lights morphs of these species produce seeds with mottled colouration, producing an obvious patterning. This type of patterning is known to reduce detectability in many animals (Stevens et al., 2006;Stoddard and Osorio, 2019) and some plants (Lev-Yadun, 2016;Niu et al., 2018) and would be an interesting avenue of future research in fynbos plants. ...
Article
Plant species with large seeds are susceptible to high levels of seed predation. Seeds of serotinous Proteaceae plants display what appears to be background matching, with polymorphic colours or ornamented surfaces reducing their detectability on certain soil types. We investigated whether seed crypsis (background matching) in Proteaceae seeds can reduce seed predation by visually-cued bird granivores using field observations, seed removal trials and spectrophotometry data. We found no difference in seed predation of winged seeds on different substrates by a diurnal rodent granivore. We therefore ruled out rodent granivores as selective agents driving visual seed crypsis in Cape Proteaceae. Light seeds of most polymorphic Leucadendron seeds showed background matching with their native soils, with granivorous birds predicted to have difficulty distinguishing them apart. Monomorphic Protea seeds with hairs generally do not background match with no reduction in detectability from visually cued predators. This is the first widescale documentation of seed colours and first description of crypsis in the seeds of Cape plants. We suggest that seed colour polymorphisms are adaptations to substrate-specific seed predation biases, with visually-cued bird granivores the likely selective agent driving the visual crypsis of Cape fynbos seeds.
... It has long been appreciated that these associations are a product of natural selection 3,4 , with individuals camouflaged against the prevailing visual environment 5 . Indeed, selection has driven correlations in appearance between individual phenotypes and backgrounds in a wide range of animals, from rodents and lizards in terrestrial habitats 6,7 to crabs in marine habitats 2,8,9 , and even in plants 10 . These examples of phenotype-environment associations are highly suggestive of a camouflage function, but past work has rarely demonstrated or quantified the actual camouflage resulting from any match to the local environment; that is, phenotype-environment matching (but see 1 ). ...
Article
Full-text available
Camouflage is a key defence across taxa and frequently critical to survival. A common strategy is background matching, resembling the colour and pattern of the environment. This approach, however, may be ineffective in complex habitats where matching one patch may lead to increased visibility in other patches. In contrast, disruptive coloration, which disguises body outlines, may be effective against complex backgrounds. These ideas have rarely been tested and previous work focuses on artificial systems. Here, we test the camouflage strategies of the shore crab (Carcinus maenas) in two habitats, being a species that is highly variable, capable of plastic changes in appearance, and lives in multiple environments. Using predator (bird and fish) vision modelling and image analysis, we quantified background matching and disruption in crabs from rock pools and mudflats, predicting that disruption would dominate in visually complex rock pools but background matching in more uniform mudflats. As expected, rock pool individuals had significantly higher edge disruption than mudflat crabs, whereas mudflat crabs more closely matched the substrate than rock pool crabs for colour, luminance, and pattern. Our study demonstrates facultative expression of camouflage strategies dependent on the visual environment, with implications for the evolution and interrelatedness of defensive strategies.
... Plant scientists suggested several non-exclusive explanations to non-green plant coloration patterns (Jiang et al., 2004). These possible mechanisms can be sorted to three different groups: (1) Chlorophyll deficiency (Aluru et al., 2001;Sheue et al., 2012); (2) defense from enemies including by aposematic coloration, undermining the camouflage of herbivorous insects, mimicry of dead or infested plants, masquerade and camouflage (Lev-Yadun et al., 2004;Lev-Yadun, 2016, 2017Niu et al., 2018); ...
Article
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Leaves of the spiny winter annual Silybum marianum express white patches (variegation) that can cover significant surface areas, the outcome of air spaces formed between the epidermis and the green chlorenchyma. We asked: (1) what characterizes the white patches in S. marianum and what differs them from green patches? (2) Do white patches differ from green patches in photosynthetic efficiency under lower temperatures? We predicted that the air spaces in white patches have physiological benefits, elevating photosynthetic rates under low temperatures. To test our hypotheses we used both a variegated wild type and entirely green mutants. We grew the plants under moderate temperatures (20◦C/10◦C d/n) and compared them to plants grown under lower temperatures (15◦C/5◦C d/n). The developed plants were exposed to different temperatures for 1 h and their photosynthetic activity was measured. In addition, we compared in green vs. white patches, the reflectance spectra, patch structure, chlorophyll and dehydrin content, stomatal structure, plant growth, and leaf temperature. White patches were not significantly different from green patches in their biochemistry and photosynthesis. However, under lower temperatures, variegated wildtype leaves were significantly warmer than all-green mutants – possible explanations for that are discussed These findings support our hypothesis, that white variegation of S. marianum leaves has a physiological role, elevating leaf temperature during cold winter days.
... The lighter their color becomes because of their white bark, the more they will be invisible, with the white bark probably also serving under such lighting conditions as white countershading, a character found on the ventral side of many aquatic and terrestrial animals (e.g., Cott 1940;Ruxton et al. 2004;Caro 2005;Penacchio et al. 2015). In their review of plant camouflage, Niu et al. (2018) posited that countershading was never demonstrated in plants. However, additional measurements under relevant lighting conditions are needed in order to be sure that countershading indeed operates in plants. ...
... C ryptic coloration allowing visual camouflage is a cosmopolitan antipredator strategy in nature and provides classic examples of evolution by natural selection [1][2][3][4][5] . Crypsis works by reducing the chance of prey detection or recognition by the visual system of potential predators 1,6,7 , often through background matching 1,5,[8][9][10] . ...
Article
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Camouflage is driven by matching the visual environment, yet natural habitats are rarely uniform and comprise many backgrounds. Therefore, species often exhibit adaptive traits to maintain crypsis, including colour change and behavioural choice of substrates. However, previous work largely considered these solutions in isolation, whereas many species may use a combination of behaviour and appearance to facilitate concealment. Here we show that green and red chameleon prawns (Hippolyte varians) closely resemble their associated seaweed substrates to the vision of predatory fish, and that they can change colour to effectively match new backgrounds. Prawns also select colour-matching substrates when offered a choice. However, colour change occurs over weeks, consistent with seasonal changes in algal cover, whereas behavioural choice of matching substrates occurs in the short-term, facilitating matches within heterogeneous environments. We demonstrate how colour change and behaviour combine to facilitate camouflage against different substrates in environments varying spatially and temporally.
... 垂头植物 钟花垂头菊(Cremanthodium campanulatum)特殊的垂头 结构具有吸收地面辐射, 升高花序温度以及降低紫外 辐射对花粉萌发率的不利影响的功能 [16] . 垫状植物团 状福禄草(Arenaria polytrichoides), 关节委陵菜(Poten- [20,21] . ...
... Plant scientists suggested several non-exclusive explanations to non-green plant coloration patterns (Jiang et al., 2004). These possible mechanisms can be sorted to three different groups: (1) Chlorophyll deficiency (Aluru et al., 2001;Sheue et al., 2012); (2) defense from enemies including by aposematic coloration, undermining the camouflage of herbivorous insects, mimicry of dead or infested plants, masquerade and camouflage (Lev-Yadun et al., 2004;Lev-Yadun, 2016Niu et al., 2018); ...
Chapter
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Leaves of the spiny winter annual Silybum marianum express white patches (variegation) that can cover significant surface areas, the outcome of air spaces formed between the epidermis and the green chlorenchyma. We asked: (1) what characterizes the white patches in S. marianum and what differs them from green patches? (2) Do white patches differ from green patches in photosynthetic efficiency under lower temperatures? We predicted that the air spaces in white patches have physiological benefits, elevating photosynthetic rates under low temperatures. To test our hypotheses we used both a variegated wild type and entirely green mutants. We grew the plants under moderate temperatures (20�C/10�C d/n) and compared them to plants grown under lower temperatures (15�C/5�C d/n). The developed plants were exposed to different temperatures for 1 h and their photosynthetic activity was measured. In addition, we compared in green vs. white patches, the reflectance spectra, patch structure, chlorophyll and dehydrin content, stomatal structure, plant growth, and leaf temperature. White patches were not significantly different from green patches in their biochemistry and photosynthesis. However, under lower temperatures, variegated wildtype leaves were significantly warmer than all-green mutants – possible explanations for that are discussed These findings support our hypothesis, that white variegation of S. marianum leaves has a physiological role, elevating leaf temperature during cold winter days
... Generally, there are two types of camouflage strategies, namely, natural camouflage and artificial camouflage. Natural camouflage is exhibited by living creatures that act in a passive or active mode [5][6][7] . By contrast, artificial camouflage is designed by humans to disguise soldiers and weapons by masking artificial textures or coloration [8][9][10] . ...
Article
Unveiling the cheating mask of camouflage is of great significance in scientific and military research, but the acquisition of detailed information about camouflaged objects remains extremely difficult. This paper presents a fringe projection decamouflaging (FPDC) approach that can provide the position, outer rim profile, and shadow information about well-camouflaged objects in a complex scenario. FPDC requires no expensive instruments, just one camera and one projector for monitoring. A bionic detection field, namely, a phase-jump field, is established to detect the intrusion of camouflaged objects. Based on local variations in this field, multiple-parameter decamouflaging is achieved for the first time. Simulations and experiments show the superiority of this technique, which has potential applications in counterespionage, discovery of wild animals, and search-and-rescue.
... In contrast, the use of visual cues by plants for protection from phytophagous arthropods has received significant attention only in recent years (e.g. Lev-Yadun, 2006, 2016Archetti et al., 2009;Klooster et al., 2009;Burns, 2010;Schaefer and Ruxton, 2011;Lev-Yadun and Ne'eman, 2013;Farmer, 2014;Niu et al., 2014Niu et al., , 2018Strauss et al., 2015;Fadzly et al., 2016;Quicke, 2017). Most studies of plants' protective visual signals and cues have been carried out in natural habitats and usually do not include controlled experiments. ...
Chapter
This book presents the current knowledge on arthropod vision and the results of successful manipulations of arthropods. It also suggests new methods for using optical manipulation to protect against arthropod pests and to improve the performance of beneficial arthropods. Due to the applied nature of this book, only brief overviews of the knowledge about light, vision and behavior are included (Chapters 2 and 3). The main applied information is presented in Chapters 6-9. The information in Chapters 3 and 7 is classified by the orders and families of the arthropods. It is hoped that this book will enhance the use of optical manipulation as a component of integrated pest management.
... In certain groups of ferns, gymnosperms and angiosperms, flavonoids can be further metabolised into anthocyanidins or condensed tannins (CTs; also known as proanthocyanidins; Popper & Fry, 2004;Weng, 2014). The former play a photoprotective role as leaf pigments and signalling components (Costa et al., 2015;Niu et al., 2018), whereas the latter can be found in high concentrations in leaves, bark, roots or developing seeds of some plants (Dixon et al., 2005). Due to their large size and high number of reactive phenolic groups, CTs interact with organic nitrogen compounds, which contributes to their antiherbivore properties (Hagerman, 2012). ...
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Plants accumulate a wide array of phenolic compounds, including flavonoids and condensed tannins, which are suggested to have important functions in plant defence. Sequestration of these highly bioactive compounds into vacuoles or specialised storage structures (such as glandular trichomes, located on the shoot epidermis) can enhance their defensive capacities or reduce their potential autotoxic effects. To investigate the roles of flavonoids and condensed tannins in the resilience of Betula pendula (silver birch) against herbivory and ultraviolet B radiation (UVB), two experiments were performed with control and genetically modified plants, in which specific enzymes of the flavonoid-tannin pathway were partially silenced using RNA interference (RNAi). Silencing of dihydroflavonol reductase (DFR), anthocyanidin synthase (ANS) or anthocyanidin reductase (ANR) should block the production of one or both types of condensed tannin monomers and lead to reduced accumulation or altered structure of condensed tannins. A third experiment with native B. pendula genotypes (originating from a natural population) focused in the potential roles of glandular trichomes in relation to heating and altered soil moisture. As expected, flavonoid intermediates or alternative products that were located upstream of each partially blocked enzyme accumulated in modified plants. Silencing of DFR reduced the accumulation of condensed tannins in leaves and stems, while silencing of ANS or ANR reduced tannin accumulation in stems only. DFRi resulted in strongly reduced photosynthesis and growth, and ANRi decreased growth compared to the unmodified control plants. In the herbivory experiment, accumulation of certain flavonoids or increased glandular trichome density seemed to deter feeding by late-instar Epirrita autumnata (autumnal moth) larvae, while condensed tannins, trans-flavan-3-ols or certain phenolic acids reduced the growth efficiency of the larvae. In the UVB experiment, altered phenolic composition did not affect the resilience of B. pendula to UVB enhancement. In addition to flavonol glycosides, which are generally responsive to UVB in B. pendula, UVB had accumulating effects throughout the whole flavonoid-tannin pathway, including on condensed tannins. The leaf surface affected the responses of glandular trichomes to different combinations of heating and watering or to UVB enhancement. On the upper leaf surface, the density of foliar glands increased in response to UVB enhancement (in control and modified plants) but decreased in response to separately applied heating, drought or excess watering in native genotypes. On the lower leaf surface, the density of foliar glands did not respond to environmental treatments, but it was higher in native genotypes in late compared to mid-season. The available evidence suggests that foliar flavonoids of B. pendula play roles in both herbivore and UVB resistance. Foliar condensed tannins may have some antinutritive or toxic effects against insect herbivores. Glandular trichomes on the upper leaf surface could contribute to the herbivore deterrence and/or UVB resilience of B. pendula, while their ecological roles on the lower leaf surface remain unclear. Partial silencing of the flavonoid tannin pathway in a way that greatly increased the ratio of flavonoids to condensed tannins strongly reduced the growth of B. pendula. Further studies are required to pinpoint the physiological mechanisms and to determine whether these phenolic metabolites can modify the morphological responses of B. pendula and other plants to various environmental conditions.
... In the last decade, camouflage through background matching has been verified as a defensive strategy in a number of plants, functioning to reduce herbivory, [6][7][8] with the degree of background matching linked to the level of selection pressure. 9 Fritillaria delavayi is a perennial herb distributed in the alpine screes from the Hengduan mountains. ...
Article
Color in nature mediates numerous among and within species interactions,¹ and anthropogenic impacts have long had major influences on the color evolution of wild animals.² An under-explored area is commercial harvesting, which in animals can exert a strong selection pressure on various traits, sometimes greater even than natural selection or other human activities.³,⁴ Natural populations of plants that are used by humans have likely also suffered strong pressure from harvesting, yet the potential for evolutionary change induced by humans has received surprisingly little attention.⁵ Here, we show that the leaf coloration of a herb used in traditional Chinese medicine (Fritillaria delavayi) varies among populations, with leaves matching their local backgrounds most closely. The degree of background matching correlates with estimates of harvest pressure, with plants being more cryptic in heavily collected populations. In a human search experiment, the time it took participants to find plants was greatly influenced by target concealment. These results point to humans as driving the evolution of camouflage in populations of this species through commercial harvesting, changing the phenotype of wild plants in an unexpected and dramatic way.
... Other plants hide in temporal refuges, which consists of growing or flowering when herbivores are not active (Mortensen, 2013). With regard to the second strategy, some plants can camouflage themselves (crypsis) among other similar colored plants, which is known as background matching (Niu et al., 2018). And some other plants resemble natural elements, e.g., stones, for avoiding recognition (Mortensen, 2013). ...
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Plant blindness or the inability to notice plants in one’s everyday life is a complex phenomenon in the field of science education. Although plant blindness is well documented in the literature, the underlying factors, whether biological or cultural, are still under research. Here I focus on its biological basis. That is, I review and discuss how plants’ own inherent characteristics cause effects on human visual and cognitive processes. Animals versus plant differences in human attention and memory are also addressed. Grounded on that knowledge, some recommendations for effective practice in plant science education emerge. I conclude that only when we understand human-plant relationships will we know how to enhance teaching and learning about plants.
... colour pattern) matches the appearance of its background (Endler 1978(Endler , 1984Merilaita and Lind 2005;Michalis et al. 2017). Numerous studies have found support for this strategy in a variety of taxa ranging from insects (Feltmate and Williams 1989), amphibians and reptiles (Norris and Lowe 1964), fishes (Armbruster and Page 1996;Clarke and Schluter 2011), mammals (Vignieri et al. 2010), and also plants (Niu et al. 2017(Niu et al. , 2018. However, unlike plants, most animals are not sedentary and need to move in search of food, mates and shelter (Merilaita et al. 1999). ...
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Camouflage through background matching is a widespread antipredator strategy in which animals blend in with their background to avoid detection. To maximise survival in a variable natural environment, animals can have colourations that either match one of the backgrounds maximally (i.e. specialist strategy) or match multiple backgrounds partially (i.e. generalist strategy). Theoretical work indicates that the optimal strategy depends on the extent of visual difference between the backgrounds (i.e. heterogeneity) or how commonly the animal will encounter the background types. However, the role of another critical determinant of detection, the visual complexity of the background, on optimal camouflage strategy (specialist versus generalist) in the face of background heterogeneity, remains unknown. Here, we performed a virtual predation experiment employing humans as surrogate ‘predators’ and explored how background complexity influences camouflage in heterogeneous backgrounds. Under low heterogeneity, we found the latency to attack generalists was higher than that for specialists on a complex background, but there was no difference between specialists and generalists on a simple background. At intermediate heterogeneity, both specialist and generalist targets took a similar time to be attacked irrespective of complexity, suggesting that both the strategies may co-exist. In contrast, at high levels of heterogeneity, we found generalists were attacked sooner when compared to specialists irrespective of whether the background was simple or complex. Our results thus suggest that complex backgrounds favour the evolution of a generalist background matching strategy that maximises fitness in multiple backgrounds but only when the visual difference between the backgrounds is low. Overall, our study provides key insights highlighting the underappreciated role of background complexity on the optimization and evolution of camouflage colouration in a heterogeneous environment. Significance statement Many animals often face the challenge of encountering multiple visually distinct backgrounds due to variation in their environment, i.e. background heterogeneity. How should animals optimise camouflage when there is background heterogeneity? Theoretical studies have proposed that animals may match one of the many backgrounds (specialise) or match multiple backgrounds partially (generalise) as an optimal solution. However, cognitive constraints from the predator’s perspective may also have a role to play in this optimization problem, but this has not been examined. Our experiments involving humans as ‘predators’ show that when background complexity renders the search task more difficult, generalist targets took a longer time to be attacked than specialist targets, but only in less heterogeneous backgrounds. However, irrespective of complexity, specialist targets are better than generalists at avoiding attack in highly heterogeneous backgrounds. Cognitive constraints of predators may, therefore, play a significant role in the optimization of camouflage colouration in heterogeneous environments.
... Background matching Blending in with the background vegetation and/or substrate may increase the likelihood that a plant could escape its herbivores (Strauss and Cacho 2013;Strauss et al. 2015;Niu et al. 2018;Cacho and McIntyre 2020, and references therein). Blending in (or crypsis) could come about chemically by reducing volatile emissions, or visually. ...
Chapter
Plant traits that lead to escape of plants from their herbivores have not been formerly considered as part of plant resistance theory. We review the evidence that plant stature, phenology, mimicry, background matching, adaptation to ephemeral habitats, and dispersal contribute to the likelihood that plants will escape from their herbivores in space and time. We outline how researchers can determine the relevant importance of three components of resistance (escape, defense, and tolerance), through either interspecific comparisons, or manipulation all three components within a single plant species. Evidence suggests that escape can be used effectively to reduce herbivore pressure in agricultural systems, and that escape also contributes to biodiversity maintenance in less human disturbed ecosystems.
... Mimicry refers to the adaptive similarity or resemblance between a mimic organism and its model. Whereas mimicry is a well-known phenomenon in the animal kingdom, examples of true plant mimicry are less frequent (Niu et al., 2018;Williamson, 1982), with documented cases in the plant literature being scarce (Lev-Yadun, 2016). An illustration nonetheless is provided by Gianoli and Carrasco-Urra (2014), who report that the leaves of Boquila trifoliolata can mimic the leaves of its supporting host, including size, shape, orientation, color, and petiole length, among other features. ...
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Unlike animal behavior, behavior in plants is traditionally assumed to be completely determined either genetically or environmentally. Under this assumption, plants are usually considered to be noncognitive organisms. This view nonetheless clashes with a growing body of empirical research that shows that many sophisticated cognitive capabilities traditionally assumed to be exclusive to animals are exhibited by plants too. Yet, if plants can be considered cognitive, even in a minimal sense, can they also be considered conscious? Some authors defend that the quest for plant consciousness is worth pursuing, under the premise that sentience can play a role in facilitating plant's sophisticated behavior. The goal of this article is not to provide a positive argument for plant cognition and consciousness, but to invite a constructive, empirically informed debate about it. After reviewing the empirical literature concerning plant cognition, we introduce the reader to the emerging field of plant neurobiology. Research on plant electrical and chemical signaling can help shed light into the biological bases for plant sentience. To conclude, we shall present a series of approaches to scientifically investigate plant consciousness. In sum, we invite the reader to consider the idea that if consciousness boils down to some form of biological adaptation, we should not exclude a priori the possibility that plants have evolved their own phenomenal experience of the world. Cognitive Biology > Evolutionary Roots of Cognition Philosophy > Consciousness Neuroscience > Cognition A climbing bean (Phaseolus vulgaris) with needle electrodes inserted into its main stem aimed to reveal the underpinnings at work as it responds to the environment. At the Minimal Intelligence Laboratory, we seek to correlate the behavior of plants and phytoneural activity in order to study plant cognition and sentience.
... (Castro et al., 2018). Studies have shown that variegation in plants is not just a color mutation but has some adaptive functions that may benefit the plants, such as: defense from enemies including aposematic coloration, mimicry of dead or infested plants, masquerade and camouflage, improved water or gas transport, mitigation of UV radiation and thermoregulation (Fooshee & Henny, 1990;Lev-Yadun, 2016;Lev-Yadun, 2017;Lev-Yadun et al., 2004;Niu et al., 2018;Roelfsema et al., 2006;Shelef et al., 2019 (Elias, 1980;Paiva & Machado, 2006). In addition to P. organensis, Passiflora contracta, P. ferruginea, and P. misera also have glands that occur on abaxial surface and margin of leaf blade with a circular shape forming an ocellus (Lemos et al., 2017 (Cardoso-Gustavson et al., 2013;Durkee, 1982). ...
Article
Passiflora organensis is a small herbaceous vine with characteristic morphological variations throughout its development. The plant bears button‐shaped extrafloral nectaries exclusively in adult leaves. Extrafloral nectaries are structures that secrete nectar and play an important role in plant–animal interactions as a strategy for protecting plants against herbivory. In this work, we performed anatomical and ultrastructural studies to characterize P. organensis extrafloral nectaries during their secretory phase. We showed extrafloral nectaries in Passiflora organensis are composed of three distinct regions: nectary epidermis, nectariferous parenchyma, and subnectariferous parenchyma. Our data suggests that all nectary regions constitute a functional unit involved in nectar production and release. The high metabolic activity in the nectary cells is characterized by the juxtaposition of organelles such as mitochondria and plastids together plasmalemma. In addition, calcium oxalate crystals are frequently associated to the nectaries. An increasing concentration of calcium during leaf development and nectary differentiation was observed, corresponding to the calcium deposition as calcium oxalate crystals. This is the first description of extrafloral nectaries in Passiflora organensis that is a promising tropical model species for several studies. The anatomical and ultrastructural characteristics and the presence of calcium oxalate crystals in the nectary tissue suggest novel strategies against herbivory in the genus Passiflora.
... Therefore, FDiv logically increases with increasing latitude. When resource availability at high latitudes becomes a limiting factor, due to the temperature declining, species must develop extreme functional traits to adapt to the external environment for survival (Niu et al., 2018;Ottaviani et al., 2020). ...
Article
Functional trait diversity is an integrative plant trait index that represents an emerging and promising approach for exploring gross primary productivity (GPP); however, it is necessary to determine how these indices vary at large scales in natural forests to establish their linkage to GPP. Here, we explored spatial variation in functional diversity and underlying linkages to GPP in the natural forests of China. Specifically, we consistently measured 10 leaf traits related to the GPP of 366 tree species in nine typical forests along the North-South Transect of Eastern China and calculated three functional diversity indices (functional richness, FRic; functional evenness, FEve; and functional divergence, FDiv) for each community. All three indices consistently varied in different directions along the transect, due to the impact of climate (temperature and precipitation). FRic increased with temperature and precipitation, whereas FDiv decreased. FRic and FDiv (but not FEve) were identified as important metrics influencing GPP at large scales. Functional diversity, climate, and soil combined explained 90.4% of total variation in GPP from cold-temperate to tropical forests. The results confirmed that there is spatial variation in functional trait diversity, and that functional diversity is important for determining spatial variation in GPP in natural forests at large scales and should be integrated into ecological models.
... This kind of heterogeneity can model reversible changes of phenotypes, i.e., trait changes that affect the prey's interaction with predators but are not permanent. For example, changes in coat color or camouflage [11,12,13], physiological changes such as defense [14], and biomass allocation among tissues [15,16]. One could also think of the prey types as subpopulations within different spatial patches, if each predator hunts at a preferred patch and the prey migrate between the patches [17,18]. ...
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Ecosystems are formed by networks of species and their interactions. Traditional models of such interactions assume a constant interaction strength between a given pair of species. However, there is often significant trait variation among individual organisms even within the same species, causing heterogeneity in their interaction strengths with other species. The consequences of such heterogeneous interactions for the ecosystem have not been studied systematically. As a theoretical exploration, we analyze a simple ecosystem with trophic interactions between two predators and a shared prey, which would exhibit competitive exclusion in models with homogeneous interactions. We consider several scenarios where individuals of the prey species differentiate into subpopulations with different interaction strengths. We show that in all these cases, whether the heterogeneity is inherent, reversible, or adaptive, the ecosystem can stabilize at a new equilibrium where all three species coexist. Moreover, the prey population that has heterogeneous interactions with its predators reaches a higher density than it would without heterogeneity, and can even reach a higher density in the presence of two predators than with just one. Our results suggest that heterogeneity may be a naturally selected feature of ecological interactions that have important consequences for the stability and diversity of ecosystems.
... For example, some coastal and dune plants get covered by sand because of their sticky glandular trichomes, making them less conspicuous. This intelligent behavior requires the ability to acquire external information, process complex information, and flexibly adapt in order to successfully achieve its goal [66] 18.9 30.6 30.6 19.8 111 2.5 ...
Article
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Background Evidence suggests that plants can behave intelligently by exhibiting the ability to learn, make associations between environmental cues, engage in complex decisions about resource acquisition, memorize, and adapt in flexible ways. However, plant intelligence is a disputed concept in the scientific community. Reasons for lack of consensus can be traced back to the history of Western philosophy, interpretation of terminology, and due to plants lacking neurons and a central nervous system. Plant intelligence thus constitutes a novel paradigm in the plant sciences. Therefore, the perspectives of scientists in plant-related disciplines need to be investigated in order to gain insight into the current state and future development of this concept. Methods This study analyzed opinions of plant intelligence held by scientists from different plant-related disciplines, including ethnobiology and other biological sciences, through an online questionnaire. Results Our findings show that respondents’ personal belief systems and the frequency of taking into account other types of knowledge, such as traditional knowledge, in their own field(s) of study, were associated with their opinions of plant intelligence. Meanwhile, respondents’ professional expertise, background (discipline), or familiarity with evidence provided on plant intelligence did not affect their opinions. Conclusions This study emphasizes the influential role of scientists’ own subjective beliefs. In response, two approaches could facilitate transdisciplinary understanding among scientists: (1) effective communication designed to foster change in agreement based on presented information; and (2) holding space for an interdisciplinary dialogue where scientists can express their own subjectivities and open new opportunities for collaboration.
... One of the most widespread defensive strategies to avoid predation in nature is camouflage [1], which is defined as the use of colour patterns and other morphological adaptations by an organism to reduce the probability of being detected or recognized by an observer [2]. This anti-predatory strategy is found in many taxa with reports including from dinosaurs to plants and used both from prey and predators [2][3][4][5][6]. Even studied over a century, including observations and seminal studies made by Wallace & Poulton [7,8], camouflage is frequently defined as the simple association between the colour patterns of the organisms and their backgrounds [9]. ...
Article
Although numerous studies about camouflage have been conducted in the last few decades, there is still a significant gap in our knowledge about the magnitude of protective value of different camouflage strategies in prey detection and survival. Furthermore, the functional significance of several camouflage strategies remains controversial. Here we carried out a comprehensive meta-analysis including comparisons of different camouflage strategies as well as predator and prey types, considering two response variables: mean predator search time (ST) (63 studies) and predator attack rate (AR) of camouflaged prey (28 studies). Overall, camouflage increased the predator ST by 62.56% and decreased the AR of prey by 27.34%. Masquerade was the camouflage strategy that most increased predator ST (295.43%). Background matching and disruptive coloration did not differ from each other. Motion camouflage did not increase ST but decreases AR on prey. We found no evidence that eyespot increases ST and decreases AR by predators. The different types of predators did not differ from each other, but caterpillars were the type of prey that most influenced the magnitude of camouflage's effect. We highlight the potential evolutionary mechanisms that led camouflage to be a highly effective anti-predatory adaptation, as well as potential discrepancies or redundancies among strategies, predator and prey types.
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The risk of consumption is a pervasive aspect of ecology and recent work has focused on synthesis of consumer–resource interactions (e.g., enemy–victim ecology). Despite this, theories pertaining to the timing and magnitude of defenses in animals and plants have largely developed independently. However, both animals and plants share the common dilemma of uncertainty of attack, can gather information from the environment to predict future attacks and alter their defensive investment accordingly. Here, we present a novel, unifying framework based on the way an organism’s ability to defend itself during an attack can shape their pre-attack investment in defense. This framework provides a useful perspective on the nature of information use and variation in defensive investment across the sequence of attack-related events, both within and among species. It predicts that organisms with greater proportional fitness loss if attacked will gather and respond to risk information earlier in the attack sequence, while those that have lower proportional fitness loss may wait until attack is underway. This framework offers a common platform to compare and discuss consumer effects and provides novel insights into the way risk information can propagate through populations, communities, and ecosystems.
Article
Animal camouflage has long been used to illustrate the power of natural selection, and provides an excellent testbed for investigating the trade‐offs affecting the adaptive value of colour. However, the contemporary study of camouflage extends beyond evolutionary biology, co‐opting knowledge, theory and methods from sensory biology, perceptual and cognitive psychology, computational neuroscience and engineering. This is because camouflage is an adaptation to the perception and cognition of the species (one or more) from which concealment is sought. I review the different ways in which camouflage manipulates and deceives perceptual and cognitive mechanisms, identifying how, and where in the sequence of signal processing, strategies such as transparency, background matching, disruptive coloration, distraction marks, countershading and masquerade have their effects. As such, understanding how camouflage evolves and functions not only requires an understanding of animal sensation and cognition, it sheds light on perception in other species. Camouflage provides an excellent testbed for investigating the trade‐offs affecting the adaptive value of colour. However, because camouflage is an adaptation to the perception and cognition of the species (one or more) from which concealment is sought, the study of camouflage sheds light on visual processing and decision‐making in other species. This review charts the rapid recent progress in understanding the different methods by which camouflage is achieved, within a framework of minimizing the signal‐to‐noise ratio. Photo credit: Gerard Cheshire
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Insects typically forage in complex habitats in which their resources are surrounded by non-resources. For herbivores, pollinators, parasitoids, and higher level predators research has focused on how specific trophic levels filter and integrate information from cues in their habitat to locate resources. However, these insights frequently build specific theory per trophic level and seldom across trophic levels. Here, we synthesize advances in understanding of insect foraging behavior in complex habitats by comparing trophic levels in specialist host-parasitoid-hyperparasitoid systems. We argue that resources may become less apparent to foraging insects when they are member of higher trophic levels and hypothesize that higher trophic level organisms require a larger number of steps in their foraging decisions. We identify important knowledge gaps of information integration strategies by insects that belong to higher trophic levels.
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The efficacy of camouflage through background matching is highly environment-dependent, often resulting in intraspecific colour divergence in animals to optimize crypsis in different visual environments. This phenomenon is largely unexplored in plants, although several lines of evidence suggest they do use crypsis to avoid damage by herbivores. Using Corydalis hemidicentra, an alpine plant with cryptic leaf colour, we quantified background matching between leaves and surrounding rocks in five populations based on an approximate model of their butterfly enemy’s colour perception. We also investigated the pigment basis of leaf colour variation and the association between feeding risk and camouflage efficacy. We show that plants exhibit remarkable colour divergence between populations, consistent with differences in rock appearances. Leaf colour varies because of a different quantitative combination of two basic pigments-chlorophyll and anthocyanin-plus different air spaces. As expected, leaf colours are better matched against their native backgrounds than against foreign ones in the eyes of the butterfly. Furthermore, improved crypsis tends to be associated with a higher level of feeding risk. These results suggest that divergent cryptic leaf colour may have evolved to optimize local camouflage in various visual environments, extending our understanding of colour evolution and intraspecific phenotype diversity in plants. © 2017 The Author(s) Published by the Royal Society. All rights reserved.
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In living color Animals live in a colorful world, but we rarely stop to think about how this color is produced and perceived, or how it evolved. Cuthill et al. review how color is used for social signals between individual animals and how it affects interactions with parasites, predators, and the physical environment. New approaches are elucidating aspects of animal coloration, from the requirements for complex cognition and perception mechanisms to the evolutionary dynamics surrounding its development and diversification. Science , this issue p. eaan0221
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Animal camouflage is a longstanding example of adaptation. Much research has tested how camouflage prevents detection and recognition, largely focusing on changes to an animal’s own appearance over evolution. However, animals could also substantially alter their camouflage by behaviourally choosing appropriate substrates. Recent studies suggest that individuals from several animal taxa could select backgrounds or positions to improve concealment. Here, we test whether individual wild animals choose backgrounds in complex environments, and whether this improves camouflage against predator vision. We studied nest site selection by nine species of ground-nesting birds (nightjars, plovers and coursers) in Zambia, and used image analysis and vision modelling to quantify egg and plumage camouflage to predator vision. Individual birds chose backgrounds that enhanced their camouflage, being better matched to their chosen backgrounds than to other potential backgrounds with respect to multiple aspects of camouflage. This occurred at all three spatial scales tested (a few centimetres and 5 m from the nest, and compared with other sites chosen by conspecifics) and was the case for the eggs of all bird groups studied, and for adult nightjar plumage. Thus, individual wild animals improve their camouflage through active background choice, with choices highly refined across multiple spatial scales. Ground-nesting birds actively choose backgrounds for their nests that enhance their camouflage, refining this choice across spatial scales.
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There are two main factors explaining variation among species and the evolution of characters along phylogeny: adaptive change, including phenotypic and genetic responses to selective pressures, and phylogenetic inertia, or the resemblance between species due to shared phylogenetic history. Phenotype-habitat colour match, a classic Darwinian example of the evolution of camouflage (crypsis), offers the opportunity to test the importance of historical versus ecological mechanisms in shaping phenotypes among phylogenetically closely related taxa. To assess it, we investigated fur (phenotypic data) and habitat (remote sensing data) colourations, along with phylogenetic information, in the species-rich Gerbillus genus. Overall, we found a strong phenotype-habitat match, once the phylogenetic signal is taken into account. We found that camouflage has been acquired and lost repeatedly in the course of the evolutionary history of Gerbillus. Our results suggest that fur colouration and its covariation with habitat is a relatively labile character in mammals, potentially responding quickly to selection. Relatively unconstrained and substantial genetic basis, as well as structural and functional independence from other fitness traits of mammalian colouration might be responsible for that observation.
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Background Quantifying the conspicuousness of objects against particular backgrounds is key to understanding the evolution and adaptive value of animal coloration, and in designing effective camouflage. Quantifying detectability can reveal how colour patterns affect survival, how animals’ appearances influence habitat preferences, and how receiver visual systems work. Advances in calibrated digital imaging are enabling the capture of objective visual information, but it remains unclear which methods are best for measuring detectability. Numerous descriptions and models of appearance have been used to infer the detectability of animals, but these models are rarely empirically validated or directly compared to one another. We compared the performance of human ‘predators’ to a bank of contemporary methods for quantifying the appearance of camouflaged prey. Background matching was assessed using several established methods, including sophisticated feature-based pattern analysis, granularity approaches and a range of luminance and contrast difference measures. Disruptive coloration is a further camouflage strategy where high contrast patterns disrupt they prey’s tell-tale outline, making it more difficult to detect. Disruptive camouflage has been studied intensely over the past decade, yet defining and measuring it have proven far more problematic. We assessed how well existing disruptive coloration measures predicted capture times. Additionally, we developed a new method for measuring edge disruption based on an understanding of sensory processing and the way in which false edges are thought to interfere with animal outlines. Results Our novel measure of disruptive coloration was the best predictor of capture times overall, highlighting the importance of false edges in concealment over and above pattern or luminance matching. Conclusions The efficacy of our new method for measuring disruptive camouflage together with its biological plausibility and computational efficiency represents a substantial advance in our understanding of the measurement, mechanism and definition of disruptive camouflage. Our study also provides the first test of the efficacy of many established methods for quantifying how conspicuous animals are against particular backgrounds. The validation of these methods opens up new lines of investigation surrounding the form and function of different types of camouflage, and may apply more broadly to the evolution of any visual signal. Electronic supplementary material The online version of this article (doi:10.1186/s12862-016-0854-2) contains supplementary material, which is available to authorized users.
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Commercial and recreational harvests create selection pressures for fitness-related phenotypic traits that are partly under genetic control. Consequently, harvesting can drive evolution in targeted traits. However, the quantification of harvest-induced evolutionary life history and phenotypic changes is challenging, because both density-dependent feedback and environmental changes may also affect these changes through phenotypic plasticity. Here, we synthesize current knowledge and uncertainties on six key points: (i) whether or not harvest-induced evolution is happening, (ii) whether or not it is beneficial, (iii) how it shapes biological systems, (iv) how it could be avoided, (v) its importance relative to other drivers of phenotypic changes, and (vi) whether or not it should be explicitly accounted for in management. We do this by reviewing findings from aquatic systems exposed to fishing and terrestrial systems targeted by hunting. Evidence from aquatic systems emphasizes evolutionary effects on age and size at maturity, while in terrestrial systems changes are seen in weapon size and date of parturition. We suggest that while harvest-induced evolution is likely to occur and negatively affect populations, the rate of evolutionary changes and their ecological implications can be managed efficiently by simply reducing harvest intensity. This article is part of the themed issue ‘Human influences on evolution, and the ecological and societal consequences'.
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Remaining undetected is often key to survival, and camouflage is a widespread solution. However, extrinsic to the animal itself, the complexity of the background may be important. This has been shown in laboratory experiments using artificially patterned prey and backgrounds, but the mechanism remains obscure (not least because 'complexity' is a multifaceted concept). In this study, we determined the best predictors of detection by wild birds and human participants searching for the same cryptic targets on trees in the field. We compared detection success to metrics of background complexity and 'visual clutter' adapted from the human visual salience literature. For both birds and humans, the factor that explained most of the variation in detectability was the textural complexity of the tree bark as measured by a metric of feature congestion (specifically, many nearby edges in the background). For birds, this swamped any effects of colour match to the local surroundings, although for humans, local luminance disparities between the target and tree became important. For both taxa, a more abstract measure of complexity, entropy, was a poorer predictor. Our results point to the common features of background complexity that affect visual search in birds and humans, and how to quantify them.
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Anthropogenic climate change has created myriad stressors that threaten to cause local extinctions if wild populations fail to adapt to novel conditions. We studied individual and population-level fitness costs of a climate change-induced stressor: camouflage mismatch in seasonally colour molting species confronting decreasing snow cover duration. Based on field measurements of radiocollared snowshoe hares, we found strong selection on coat colour molt phenology, such that animals mismatched with the colour of their background experienced weekly survival decreases up to 7%. In the absence of adaptive response, we show that these mortality costs would result in strong population-level declines by the end of the century. However, natural selection acting on wide individual variation in molt phenology might enable evolutionary adaptation to camouflage mismatch. We conclude that evolutionary rescue will be critical for hares and other colour molting species to keep up with climate change.
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The recognition that animals sense the world in a different way than we do has unlocked important lines of research in ecology and evolutionary biology. In practice, the subjective study of natural stimuli has been permitted by perceptual spaces, which are graphical models of how stimuli are perceived by a given animal. Because colour vision is arguably the best-known sensory modality in most animals, a diversity of colour spaces are now available to visual ecologists, ranging from generalist and basic models allowing rough but robust predictions on colour perception, to species-specific, more complex models giving accurate but context-dependent predictions. Selecting among these models is most often influenced by historical contingencies that have associated models to specific questions and organisms; however, these associations are not always optimal. The aim of this review is to provide visual ecologists with a critical perspective on how models of colour space are built, how well they perform and where their main limitations are with regard to their most frequent uses in ecology and evolutionary biology. We propose a classification of models based on their complexity, defined as whether and how they model the mechanisms of chromatic adaptation and receptor opponency, the nonlinear association between the stimulus and its perception, and whether or not models have been fitted to experimental data. Then, we review the effect of modelling these mechanisms on predictions of colour detection and discrimination, colour conspicuousness, colour diversity and diversification, and for comparing the perception of colour traits between distinct perceivers. While a few rules emerge (e.g. opponent log-linear models should be preferred when analysing very distinct colours), in general model parameters still have poorly known effects. Colour spaces have nonetheless permitted significant advances in ecology and evolutionary biology, and more progress is expected if ecologists compare results between models and perform behavioural experiments more routinely. Such an approach would further contribute to a better understanding of colour vision and its links to the behavioural ecology of animals. While visual ecology is essentially a transfer of knowledge from visual sciences to evolutionary ecology, we hope that the discipline will benefit both fields more evenly in the future.
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How easy a plant is to find, or its apparency, is thought to shape plant defenses. Recent meta-analyses suggest that the types of plant defenses employed are not well-predicted by apparency, or apparency can be confounded with life history traits like woodiness and stature. Here, we suggest that the searching environments in which plants grow also influence plant apparency and should thus affect investment in plant defense. Specifically, bare, unvegetated environments may result in greater apparency of inhabitants of all statures to enemies, as a result of loss of associational resistance. We make several predictions about plant defenses in simple searching environments. (1) Plants living in simple searching environments should be more highly defended than plants living in more vegetated, complex searching environments. (2) Plant defenses involving signals—both, signals serving to hide plants and aposematic signals—should be favored in simple searching environments. (3) Levels of damage from enemies in simple searching environments should be related to defensive strategy (resistance, aposematism, mimicry, or crypsis); apparent plants should have low damage, because, as they are easily found, they should be well-defended though physical or chemical defense. In contrast, predictions about damage levels in cryptic plants are harder to make, as damage reflects both whether plants are encountered or not, as well as overall palatability. If crypsis is favored in more palatable species, as has been suggested previously, we predict that cryptic plants should have greater variance in damage and greater maximum damage, if, once found, plants are palatable. (4) Organisms from diverse evolutionary lineages inhabiting the same simple searching environments should adapt to selection from apparency by converging on similar background matching or aposematic defenses. We then test some of these predictions with descriptive data collections in two simple searching environments: largely unvegetated graywacke scree mountaintops of New Zealand and serpentine barrens of northern California (USA). We find that plants that are more apparent (i.e., do not match local rock color as measured across 300–700 nm wavelengths) are more defended, as inferred from mean damage received. In contrast, cryptic species in the same habitats get 7× more heavily damaged, once found, suggesting overall greater palatability. There was no evidence of greater variation in damage, as measured by coefficient of variation, but maximum damage was much greater on cryptic species in both habitats. Convergence on gray substrate is found in diverse species of plants in New Zealand, as well as by scree-living grasshoppers; in California, grasshoppers have also converged on substrate color, and seed color of a non-cryptic plant also matches local outcrops. Considering searching environment and enemy searching abilities when evaluating plant apparency to enemies may shed more light on this challenge to plants.
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Camouflage is perhaps the most widespread anti-predator strategy in nature, found in numerous animal groups. A long-standing prediction is that individuals should have camouflage tuned to the visual backgrounds where they live. However, while several studies have demonstrated phenotype-environment associations, few have directly shown that this confers an improvement in camouflage, particularly with respect to predator vision. Here, we show that an intertidal crustacean, the sand flea (Hippa testudinaria), has coloration tuned to the different substrates on which it occurs when viewed by potential avian predators. Individual sand fleas from a small, oceanic island (Ascension) matched the colour and luminance of their own beaches more closely than neighbouring beaches to a model of avian vision. Based on past work, this phenotype-environment matching is likely to be driven through ontogenetic changes rather than genetic adaptation. Our work provides some of the first direct evidence that animal coloration is tuned to provide camouflage to prospective predators against a range of visual backgrounds, in a population of animals occurring over a small geographical range. © 2015 The Authors.
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Many animals decorate themselves through the accumulation of environmental material on their exterior. Decoration has been studied across a range of different taxa, but there are substantial limits to current understanding. Decoration in non-humans appears to function predominantly in defence against predators and parasites, although an adaptive function is often assumed rather than comprehensively demonstrated. It seems predominantly an aquatic phenomenon-presumably because buoyancy helps reduce energetic costs associated with carrying the decorative material. In terrestrial examples, decorating is relatively common in the larval stages of insects. Insects are small and thus able to generate the power to carry a greater mass of material relative to their own body weight. In adult forms, the need to be lightweight for flight probably rules out decoration. We emphasize that both benefits and costs to decoration are rarely quantified, and that costs should include those associated with collecting as well as carrying the material. © 2015 The Author(s) Published by the Royal Society. All rights reserved.
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A longstanding hypothesis in evolutionary biology is that trade-offs between natural and sexual selection often underlie the diversification of sexual signals in the wild. A classic example of this “selection trade-off hypothesis” proposes that males evolve elaborate and conspicuous ornamentation in low-risk environments where female preferences dominate selection on sexual traits, but they evolve muted and relatively cryptic sexual traits in high-risk environments where selection from predators acts against conspicuous sexual traits and female preferences potentially weaken or reverse. However, little direct empirical evidence supports this notion. Using the model system of Bahamas mosquitofish (Gambusia hubbsi)—where males have recently evolved greater orange coloration in their dorsal fins in blue holes lacking predatory fish relative to populations with fish predators—we tested this hypothesis using fish replicas differing only in dorsal-fin color. Specifically, we employed plastic fish models in a combination of field and lab experiments to directly examine conspicuity to predators and female preferences for dorsal-fin color. We found that orange-shifted dorsal fins resembling the color exhibited in predator-free populations appeared more conspicuous to predatory bigmouth sleepers (Gobiomorus dormitor) that are evolutionarily naive to mosquitofish. Wild-caught female mosquitofish preferred the orange-shifted dorsal-fin model during dichotomous choice tests; evolutionary history with predators did not affect female preferences. Similar mate-choice trials with lab-born virgin females also found preferences for the orange-shifted dorsal-fin model and revealed significant genetic variation for female preferences. Our study provides direct empirical evidence documenting a trade-off between natural and sexual selection in a colorful sexual signal.
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1.Mistletoes use far more water per unit carbon fixed during photosynthesis than their hosts (i.e., they have lower ‘water use efficiency’, WUE). The widely-cited “nitrogen-parasitism hypothesis” posits that N is the most limiting resource for mistletoes, and that they use their faster transpiration rates to acquire sufficient N from the host xylem. In a rather different context, the “mimicry hypothesis” arose in the literature suggesting that some mistletoes mimic the morphology of host leaves in order to deploy higher-N leaves without suffering higher levels of herbivory. These two non-exclusive hypotheses share the common goal of trying to explain patterns of mistletoe leaf N concentration.2.We set out to test the generality of both hypotheses at broad geographic scale using data for 168 mistletoes-host pairs, from 39 sites, encompassing all continents except Antarctica. We drew together data from published literature and our own field data on two key plant functional traits, leaf N concentration (Nmass) and leaf carbon isotopic composition, δ13C (representing long-term WUE and degree of stomatal control over photosynthesis).3.Key findings included (1) Little or no support for the N-parasitism hypothesis: differences in mistletoe and host Nmass explained only 3% variation in differences in leaf δ13C; and, mistletoe-host differences in leaf δ13C were unrelated to whether or not the hosts were N-fixers (presumed to have higher N concentration in xylem sap); (2) Partial support for the mimicry hypothesis: mimic mistletoes generally had higher Nmass when associated with N-fixing hosts (but, on non-N-fixing hosts there was no such pattern); and (3) More broadly, mistletoes showed similar trait-responses as their hosts to environmental drivers, for example, they showed similar-magnitude shifts in Nmass and δ13C in relation to site aridity.4.Contrary to current belief, our findings suggest that nitrogen is not the limiting nutrient for mistletoes, at least not the main component driving the faster transpiration rates. Our results also give insight into the evolution of mimicry in mistletoes and show, for the first time, that mistletoes are also constrained by local water availability, exhibiting clear trait adaptations to environmental gradients. By reconsidering these issues at broad geographic scale and across a large number of species, our findings substantially modify current knowledge on the ecology and physiology of mistletoes and their hosts.This article is protected by copyright. All rights reserved.
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Camouflage is widespread throughout the natural world and conceals animals from predators in a vast range of habitats. Because successful camouflage usually involves matching aspects of the background environment, species and populations should evolve appearances tuned to their local habitat, termed phenotype-environment associations. However, although this has been studied in various species, little work has objectively quantified the appearances of camouflaged animals from different habitats, or related this to factors such as ontogeny and individual variation. Here, we tested for phenotype-environment associations in the common shore crab (Carcinus maenas), a species highly variable in appearance and found in a wide range of habitats. We used field surveys and digital image analysis of the colors and patterns of crabs found in four locations around Cornwall in the UK to quantify how individuals vary with habitat (predominantly rockpool, mussel bed, and mudflat). We find that individuals from sites comprising different backgrounds show substantial differences in several aspects of color and pattern, and that this is also dependent on life stage (adult or juvenile). Furthermore, the level of individual variation is dependent on site and life stage, with juvenile crabs often more variable than adults, and individuals from more homogenous habitats less diverse. Ours is the most comprehensive study to date exploring phenotype-environment associations for camouflage and individual variation in a species, and we discuss the implications of our results in terms of the mechanisms and selection pressures that may drive this.
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The maximum quantum yield for photosynthetic O2 evolution in red leaf coleus varieties having anthocyanin in their upper epidermis is much lower in green light and slightly lower in white light than in a green leaf variety lacking anthocyanin. A similar degree of photoinhibition occurred under excess visible light in the red versus green varieties; whereas, the red leaf varieties were less damaged by UV-B and UV-C radiation suggesting protection by anthocyanin in their epidermal tissue.
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The defensive strategy known as masquerade, or camouflage without crypsis (a type of deception that partly overlaps mimicry) has received little scientific attention in animals, and concerning plants even less. Moreover, when cases of masquerade were described in plants, they were considered as camouflage or other types of defence through mimicry. Masquerade (including in plants) may operate not only through vision, but also via other senses. Here I review several types of published cases of masquerade in plants, although they were not defined as such when published, and propose that there are two different types of masquerade in plants: (1) non-plant-mimicking defensive masquerade, in which they look (or smell) like uninteresting objects to herbivores (look like a stone or an animal, or smell like droppings or carrion, etc.), and (2) plant-mimicking defensive masquerade, in which plants or plant parts do not look appealing for herbivores, not being green, looking dead or old, harbouring insects, already attacked, less nutritious, etc. Defensive masquerade by plants may in many cases be non-exclusive, but serve additional physiological and defensive functions or operate simultaneously with other defences. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, ●●, ●●–●●.
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Variation in seed traits is a well‐known phenomenon affecting plant ecology and evolution. Here we describe, for the first time, a bimodal colour pattern of individual seeds, proposing an adaptive explanation, using Pinus halepensis as a model. Pinus halepensis disperses its seeds either by wind on hot dry days, from regular cones, or after fires, mainly from serotinous cones. Post‐dispersal seeds are exposed to strong predation by passerine birds, making crypsis important for seed survival. Individual seeds from non‐serotinous cones have a bimodal colour pattern: one side is light brown and the other black, exposing only one colour when lying on the ground. Serotinous cones from most trees have seeds with similar bimodal colour patterns, whereas seeds from serotinous cones of some trees are light brown on both sides. The dark side provides the seed with better crypsis on dark soils, whereas the light‐brown side is better adapted to light‐coloured soils, and mainly to light‐grey ash‐covered soil, which is the natural post‐fire regeneration niche of P. halepensis. The relative reflection curves of the black and brown seed colours differ, and their calculated relative chromatic distance is 5: meaning that seed‐predating passerine birds see them differently, and probably prefer seeds that present a higher contrast against the soil background. We propose that such a bimodal colour pattern of individual seeds is probably an overlooked general phenomenon mainly linked to seed dispersal in post‐fire and other heterogeneous environments. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109, 271–278.
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Communication in plant–animal mutualisms frequently involves multiple perceivers. A fundamental uncertainty is whether and how species adapt to communicate with groups of mutualists having distinct sensory abilities. � We quantified the colour conspicuousness of flowers and fruits originating from one Euro- pean and two South American plant communities, using visual models of pollinators (bee and fly) and seed dispersers (bird, primate and marten). � We show that flowers are more conspicuous than fruits to pollinators, and the reverse to seed dispersers. In addition, flowers are more conspicuous to pollinators than to seed dispers- ers and the reverse for fruits. Thus, despite marked differences in the visual systems of mutual- ists, flower and fruit colours have evolved to attract multiple, distinct mutualists but not unintended perceivers. We show that this adaptation is facilitated by a limited correlation between flower and fruit colours, and by the fact that colour signals as coded at the photore- ceptor level are more similar within than between functional groups (pollinators and seed dispersers). � Overall, these results provide the first quantitative demonstration that flower and fruit col- ours are adaptations allowing plants to communicate simultaneously with distinct groups of mutualists.
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Distractive marks have been suggested to prevent predator detection or recognition of a prey, by drawing the attention away from recognizable traits of the bearer. The white ‘comma’ on the wings of comma butterflies, Polygonia c-album, has been suggested to represent such a distractive mark. In a laboratory experiment using blue tits, Cyanistes caeruleus, as predators, we show that the comma increased survival, since the blue tits attacked butterflies with overpainted commas more often than sham-painted butterflies with intact commas. In a field experiment we placed hibernating, similarly manipulated, comma butterflies on tree trunks of two different species and noted their survival. Although survival was higher on birch trees than on oak trees, there was no effect of treatment, probably because the butterflies were preyed on by both diurnal and nocturnal predators and the latter are unlikely to attend to small conspicuous markings.
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In their article, Merilaita et al. (2013) discuss what distractive markings are and how they may work as a potential camouflage type. They raise a number of issues, with a key debate being how to test the theory of distractive markings and what constitutes appropriate scientific experiments. Merilaita et al. argue that “because distractive markings are by definition a camouflage strategy, it is necessary to show that a marking actually decreases the risk of predation before one can argue it has anything to do with a distractive effect. Because the spots in Stevens et al. (2013) did not facilitate concealment, they were inevitably not distractive.” However, one cannot claim that distractive camouflage does by its own definition reduce predation risk because that makes it an untestable, self-affirming hypothesis. Distractive markings are not automatically “by definition a camouflage strategy,” but rather a theory for how one type of concealment might potentially work. Furthermore, the experiments of Dimitrova et al. (2009) that claim to support the distractive theory, showing high contrast prey were detected more slowly than low contrast prey, do not demonstrate why they obtained detection differences. There is no evidence from their article that differences in detection rates of prey were due to any distractive mechanism. Thus, by their own logic, their experiments do not show distraction either.
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Trichomes are known to have many functions, including protecting plants from excess sunlight, improving water economy, salt secretion, defense from herbivores, and signaling to animals. Additional anti-herbivore functions of trichomes, especially in coastal and desert habitats, are reviewed and proposed. Many sand-dune and sandy shore plants are white, whitish, or silver-colored because of white trichomes, because of sticky glandular trichomes to which sand grains and clay adhere, or because of light-colored waxes. The common explanation for this coloration is that it protects from irradiation, and that in addition, the glued sand defends them from abrasion by moving sand. This coloration was also proposed to camouflage the plants from herbivores. Similar coloration in animals that live in white, snow-covered habitats or light-colored sand or other soil substrates is commonly referred to as camouflage, and the same logic may also apply to plants. It has also been proposed that white plant surfaces undermine the camouflage of herbivorous insects that have other colors and expose them to predation. Three novel defensive mechanisms are proposed here: (1) because dust is a strong insect repellent and is lethal to insects, attached soil particles (especially clays) may defend plants with sticky glandular trichomes from insect herbivory; (2) in dicotyledonous plants that have sticky glandular trichomes, the attached sand may defend from herbivory by mammals by causing teeth wear as do phytoliths (silica bodies) of grasses; and (3) white coloration of leaves and branches may mimic fungal infestation. Direct experimental data for the functionality of these defensive mechanisms are missing for many of the old and all new hypotheses, but there are many indirect supporting indications.
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Abstract Bare, simplified searching environments, often associated with sparsely vegetated harsh soils, may cause both plant and animal inhabitants to be apparent and conspicuous. "Apparency" has been a key concept to explain the diversity of plant defensive chemistry but has been difficult to test. In animals, there is extensive work on camouflage and crypsis, adaptations to apparency that reduce detection by predators. Here, we explore apparency as a challenge in bare soil habitats characterized by sparse vegetative cover for both plants and animals. Using experiment and observation, we show that attack rates from enemies on vulnerable plants and undefended caterpillar models are greater in barer serpentine habitats than in adjacent more vegetated ones. Palatable Streptanthus species (Brassicaceae) may have adapted to apparency with a crypsis defense, typically considered the purview of animals. In Streptanthus breweri, leaf color is locally matched to soil outcrop color, and experimental mismatching of leaf and substrate color increases damage to plants, suggesting adaptation to apparency per se. Herbivore coloration may, too, have been influenced by greater enemy pressure and apparency in these sites. Adaptation to increased enemy pressure and apparency, with concomitant trade-offs in competitive ability, may be an underappreciated aspect of specialization to harsh soils, especially in plants. Apparency may be a useful framework for understanding trade-offs driving soil specialization and global biodiversity patterns.
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The color of many animals matches that of their preferred habitats, making them difficult for predators to locate. However, quantitative examples of crypsis in plants are comparatively rare. We conducted morphometric and spectrographic analyses of a heteroblastic tree species that is endemic to New Zealand (Elaeocarpus hookerianus Raoul) to test whether it is cryptic in appearance from the perspective of birds, who were once dominant browsers in New Zealand. The leaves of smaller, juvenile plants are highly variable in size and shape and are mottled brown in color from the perspective of birds, which would make them difficult for herbivorous birds to locate against a background of leaf litter. However, once plants grow to above 3 m in height, beyond the reach of the largest herbivorous bird known to inhabit New Zealand, plants suddenly produce leaves that are ordinary in size, shape, and color. Results provide quantitative support for the hypothesis that E. hookerianus is cryptically colored when within reach of flightless browsing birds.
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Abstract For 150 years mistletoe host-resemblance has been an unsolved puzzle. Mimicry, camouflage, host protection and shape modification by the host tree have all been advanced as possible solutions. No extended examination of herbivory of host-parasite pairs has ever been done, however, to put these explanations to the test. The study was carried out in northeastern Australia from March to July 1994. Rates of leaf herbivory were estimated for seven individuals of Amyema biniflora Barlow (a cryptic mistletoe species), Dendrophthoe glabrescens (Blakely) Barlow (a non-cryptic mistletoe species) and their host trees (Eucalyptus tessellaris F. Muell. and Eucalyptus platyphylla F. Muell., respectively). In addition three measures of leaf palatability–nitrogen content, moisture content and toughness–were also assessed. Variability in mistletoe leaf shape was quantified by measuring the leaf widths of mistletoes on a variety of host tree species. Mistletoes sustained greater levels of herbivory compared to their host trees, but herbivory did not differ between mistletoe species. The non-cryptic mistletoe had lower levels of nitrogen compared to its host tree, but there was no difference in nitrogen levels between the cryptic mistletoe and its host. The moisture content of mistletoe leaves was greater than that of their hosts but not between mistletoe or host species. The mistletoe species had tougher leaves than their host trees. Leaf shape was different for one species of mistletoe growing on different host trees, but constant for another species of mistletoe. The results contradict, in some crucial aspect, all of the mimicry hypotheses currently on offer.
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Floral evolution has often been associated with differences in pollina-tion syndromes. Recently, this conceptual structure has been criticized on the grounds that flowers attract a broader spectrum of visitors than one might expect based on their syndromes and that flowers often diverge without excluding one type of pollinator in favor of another. Despite these criticisms, we show that pollination syndromes provide great utility in understanding the mechanisms of floral diversification. Our conclusions are based on the importance of organizing pollinators into functional groups according to presumed similarities in the selection pressures they exert. Furthermore, functional groups vary widely in their effectiveness as pollinators for particular plant species. Thus, although a plant may be visited by several functional groups, the relative se-lective pressures they exert will likely be very different. We discuss various methods of documenting selection on floral traits. Our review of the literature indicates over-whelming evidence that functional groups exert different selection pressures on floral traits. We also discuss the gaps in our knowledge of the mechanisms that underlie the evolution of pollination syndromes. In particular, we need more information about the relative importance of specific traits in pollination shifts, about what selective factors favor shifts between functional groups, about whether selection acts on traits inde-pendently or in combination, and about the role of history in pollination-syndrome evolution.
Article
1.Being able to quantify the conspicuousness of animal and plant colouration is key to understanding its evolutionary and adaptive significance. Camouflaged animals, for example, are under strong selection pressure to minimise their conspicuousness to potential predators. However, successful camouflage is not an intrinsic characteristic of an animal, but rather an interaction between that animal's phenotype and the visual environment that it is viewed against. Moreover, the efficacy of any given camouflage strategy is determined not by the signaller's phenotype per se, but by the perceptual and cognitive capabilities of potential predators. Any attempts to quantify camouflage must therefore take both predator perception and the visual background into account. 2.Here I describe the use of species‐relevant saliency maps, which combine the different visual features that contribute to selective attention (in this case the luminance, colour and orientation contrasts of features in the visual environment) into a single holistic measure of target conspicuousness. These can be tuned to the specific perceptual capabilities of the receiver, and used to derive a quantitative measure of target conspicuousness. Furthermore, I provide experimental evidence that these computed measures of conspicuousness significantly predict the performance of both captive and wild birds when searching for camouflaged artificial prey. 3.By allowing the quantification of prey conspicuousness, saliency maps provide a useful tool for understanding the evolution of animal signals. However, this is not limited to inconspicuous visual signals, and the same approach could be readily used for quantifying conspicuous visual signals in a wide variety of contexts, including, for example, signals involved in mate choice and warning colouration. This article is protected by copyright. All rights reserved.
Article
There is strong empirical evidence that foliar anthocyanins assist in protecting chloroplasts from potentially damaging effects of supernumerary photons. Nevertheless, around 30% of published reports failed to uncover any photoprotective advantage of red pigmentation. To understand why anthocyanins are evidently more useful in some situations than in others, we compared the stress responses of wild type (Col-0) Arabidopsis thaliana, which had only trace amounts of foliar anthocyanins, with those of the anthocyanin-rich pap1-D mutant, and, in some experiments, the anthocyanin-deficient ttg1-1. We recorded effects of light quality, light intensity, air temperature, and duration of exposure on quantum yields of photosystem II (ΦPSII) in leaves of different ages, and compared pigment profiles before and after treatment. Although similar in anatomy, chlorophyll content, and xanthophyll cycle activity, pap1-D was photoinactivated less than Col-0, but only when given at least 2 h exposure to saturating light at 10 °C. Differences between the responses of red and green leaves were greatest in older plants that were given protracted exposures to high fluxes of cool-white light (5600 K) at chilling temperatures, the decline in ΦPSII being inversely proportional to foliar anthocyanin concentration. Anthocyanins were more abundant in Col-0 and pap1-D after treatment, especially acylated forms for which the absorption spectrum matched the action spectrum for photoinhibition. The quality, intensity and duration of light stress profoundly influence the degree of photoprotection afforded by foliar anthocyanins. Photoabatement by anthocyanins provides a functional advantage only when the capacity for thermal energy dissipation is exceeded by the need to quench excess light.
Article
Significance Because the sun and sky are above us, natural illumination is directional and the cues from shading reveal shape and depth. However, many animals are darker on their backs and, over 100 years ago, it was proposed that this phenomenon was camouflage: countering the cues to shape that directional illumination creates. However, does this camouflage work in practice? We predicted the optimal countershading for different lighting conditions and tested this possibility with correspondingly patterned model “caterpillars” predated by birds in the wild. Predation rates varied with coloration and lighting in exactly the manner predicted. Such subtlety in the effects of countershading vindicates conclusions from prior evidence demonstrating stronger countershading in animals in more brightly lit habitats.
Book
This book presents visual plant defenses (camouflage, mimicry and aposematism via coloration, morphology and even movement) against herbivores. It is mainly an ideological monograph, a manifesto representing my current understanding on defensive plant coloration and related issues. The book is not the final word in anything, but rather the beginning of many things. It aims to establish visual anti-herbivory defense as an integral organ of botany, or plant science as it is commonly called today. I think that like in animals, many types of plant coloration can be explained by selection associated with the sensory/cognitive systems of herbivores and predators to reduce herbivory. It is intended to intrigue and stimulate students of botany/plant science and plant/animal interactions for a very long time. This book is tailored to a readership of biologists and naturalists of all kinds and levels, and more specifically for botanists, ecologists, evolutionists and to those interested in plant/animal interactions. It is written from the point of view of a naturalist, ecologist and evolutionary biologist that I hold, considering natural selection as the main although not the only drive for evolution. According to this perspective, factors such as chance, founder effects, genetic drift and various stochastic processes that may and do influence characters found in specific genotypes, are not comparable in their power and influence to the common outcomes of natural selection, especially manifested when very many species belonging to different plant families, with very different and separate evolutionary histories, arrive at the same adaptation, something that characterizes many of the visual patterns and proposed adaptations described and discussed in this book. Many of the discussed visual defensive mechanisms are aimed at operating before the plants are damaged, i.e., to be their first line of defense. In this respect, I think that the name of the book by Ruxton et al. (2004) "Avoiding Attack" is an excellent phrase for the assembly of the best types of defensive tactics. While discussing anti-herbivory, I do remember, study and teach physiological/developmental aspects of some of the discussed coloration patterns, and I am fully aware of the simultaneous and diverse functions of many plant characters in addition to defense.
Article
Macaranga bancana is considered as a successful pioneer plant species. Usually found in disturbed and open areas, most of the current research focused on its relations with ants. One of the unique feature of the plants is that the seedling leaves are red, resembling and almost matching the background. Using a portable spectrometer, we measured the color reflectance of M. bancana seedlings (less than 20 cm in height). We also measured the leaf litter reflectance, adult M. bancana leaves and also seedlings of several other species found in the vicinity of M. bancana seedlings. The reflectances of M. bancana seedlings are very similar to that of the leaf litter background. We suggest that this cryptic coloration is crucial during the early stages of the plant when it still cannot rely on the protection of ants.
Article
Many organisms appear to mimic inanimate objects such as twigs, leaves, stones, and bird droppings. Such adaptations are considered to have evolved because their bearers are misidentified as either inedible objects by their predators, or as innocuous objects by their prey. In the past, this phenomenon has been classified by some as Batesian mimicry and by others as crypsis, but now is considered to be conceptually different from both, and has been termed 'masquerade'. Despite the debate over how to classify masquerade, this phenomenon has received little attention from evolutionary biologists. Here, we discuss the limited empirical evidence supporting the idea that masquerade functions to cause misidentification of organisms, provide a testable definition of masquerade, and suggest how masquerade evolved and under what ecological conditions. (C) 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 99, 1-8.
Chapter
Mimetic phenomena have played a central role in many evolutionary questions and today provide some of the best examples of natural selection. Since its discovery by Bates (1862) in Amazonian Heliconiid butterflies many hundreds of papers have been written on the subject and today it is recognized as a major feature of animal evolution, especially in insects.
Article
Some forest plants adapt to shade by mixotrophy, i.e., they obtain carbon both from photosynthesis and from their root mycorrhizal fungi. Fully achlorophyllous species using exclusively fungal carbon (the so-called mycoheterotrophic plants) have repeatedly evolved from such mixotrophic ancestors. However, adaptations for this evolutionary transition, and the reasons why it has happened a limited number of times, remain unknown. We investigated this using achlorophyllous variants (i.e., albinos) spontaneously occurring in Cephalanthera damasonium, a mixotrophic orchid. In two populations, we compared albinos with co-occurring green individuals in situ. We investigated vegetative traits, namely, shoot phenology, dormancy, CO2 and H2O leaf exchange, mycorrhizal colonization, degree of mycoheterotrophy (using C-13 abundance as a proxy), and susceptibility to pathogens and herbivores. We monitored seed production (in natural or experimental crosses) and seed germination. Albinos displayed (1) more frequent shoot drying at fruiting, possibly due to stomatal dysfunctions, (2) lower basal metabolism, (3) increased sensitivity to pathogens and herbivores, (4) higher dormancy and maladapted sprouting, and, probably due to the previous differences, (5) fewer seeds, with lower germination capacity. Over the growing season, green shoots shifted from using fungal carbon to an increasingly efficient photosynthesis at time of fruiting, when fungal colonization reached its minimum. Conversely, the lack of photosynthesis in fruiting albinos may contribute to carbon limitation, and to the above-mentioned trends. With a 10(3) x fitness reduction, albinos failed a successful transition to mycoheterotrophy because some traits inherited from their green ancestors are maladaptive. Conversely, mycoheterotrophy requires at least degeneration of leaves and stomata, optimization of the temporal pattern of fungal colonization and shoot sprouting, and new defenses against pathogens and herbivores. Transition to mycoheterotrophy likely requires progressive, joint evolution of these traits, while a sudden loss of photosynthesis leads to unfit plants. We provide explanations for the evolutionary stability of mixotrophic nutrition and for the rarity of emergence of carbon sinks in mycorrhizal networks. More broadly, this may explain what prevents the emergence of fully heterotrophic taxa in the numerous other mixotrophic plant or algal lineages recently described.
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Cryptic colouration is a common predation-avoidance strategy in animals that is postulated to occur in plants, but few experimental studies have rigorously tested this hypothesis.We investigated the colouration of Corydalis benecincta, an alpine plant with remarkably dimorphic leaf colours (grey and green), based on a cost–benefit analysis. First we tested the premise that herbivores (Parnassius butterflies) cannot distinguish grey leaves from a scree background by spectrographic measurements and by estimating discriminability between leaves and scree using a butterfly colour vision model. Then we estimated the potential costs of inconspicuousness by comparing the photosynthetic performance and visual attractiveness to flower visitors of the two colour morphs. Finally, we examined the potential benefits of inconspicuousness by comparing damage, survivorship and female reproductive success.It is difficult for herbivores to distinguish grey-coloured morphs against the background. This grey colour originates in a combination of anthocyanins and chlorophylls. The two colour morphs had similar photosynthetic performance, visual attractiveness and female reproductive success. However, grey morphs had significantly lower herbivore damage and higher survivorship.Grey leaves benefit C. benecincta by reducing herbivory with low investment in anthocyanin synthesis, and little cost on photosynthesis and mating opportunity. This cryptic colouration may have evolved through selection pressure imposed by visually foraging herbivores.
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Considering its widespread occurrence and importance in the animal kingdom, background matching is clearly one of the most under-studied means of concealment. Background matching means that to decrease the risk of being detected by its predators or prey an animal possesses body colours or patterns that resemble those in the surrounding environment (Figure 2.1). The principle has long been acknowledged (e.g. Darwin 1794), and because of the apparent obviousness of its function, it was used as an example to promote the idea of adaptation in many early evolutionary texts. For instance, Wallace (1889) presented numerous examples of what we today call background matching, and described various cases in which animals ‘blended into’ their backgrounds or had colours ‘assimilated’ to or to ‘harmonise’ with it.
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Why do leaves have such varied sizes and shapes? Part of the answer lies in physiological and biomechanical demands imposed by different habitats; selective forces that are now reasonably well understood. In contrast, the impact of herbivores on the evolution of leaf size and shape has rarely been investigated and is poorly understood. There are at least six ways in which herbivores, particularly vertebrates and insects, may have influenced the evolution of leaf size and shape, favouring leaf morphologies that differ from those dictated by physiological and biomechanical constraints acting on plants. They are mimicry, not only of leaves of other plant species but also grazed leaves and inanimate objects; crypsis; physical barriers to being eaten; interspecific differences in leaf morphology to reduce recognition by herbivores; very small or highly divided and dissected leaves that reduce feeding efficiency; and different adult and juvenile foliages. There is an urgent need for studies specifically designed to investigate the impact of herbivores on leaf size and shape.
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Proposes that mottling may serve to camouflage the foliage of certain groups of short-statured forest herbs, by disrupting their outline as perceived by colour-blind vertebrate herbivores in sun-dappled understoreys. Certain phenological groups are likely to be particularly vulnerable to herbivores, based on their high leaf N content (spring ephemerals, spring leaves of summer-active species), leaf activity when few other species possess foliage (evergreen species, wintergreen species, winter leaves of dimorphic species) and/or relative cost of replacing consumed foliage (evergreen species on sterile soils). These groups are also exposed to relatively high irradiance and so are less likely to suffer photosynthetic losses as a result of the reduced leaf absorptance that accompanies mottling. A survey of the incidence of leaf mottling in the native flora of the NE USA supports these ideas: mottled leaves occur almost exclusively among forest herbs and are substantially over-represented among evergreen, wintergreen, and spring ephemeral species, and among the winter leaves of dimorphic species and the spring leaves of summer-active species. -from Author
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Examines the evolutionary history of plants and insects; the visual properties of natural illuminants and plants, and properties of insect vision; the plant selection process of insects, emphasizing visual detection of plants or plant structures from a distance, from nearby and from within a plant canopy; intraspecific variation in plants and insects; and generalist versus specialist insects. Inherent physiological constraints on the insect's visual capabilities together with natural illuminant characteristics of plants prescribe the boundaries within which visual plant discrimination by insect herbivores.-from Authors
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Although adaptive plant population divergence across contrasting soil conditions is often driven by abiotic soil factors, natural enemies may also contribute. Cryptic matching to the native soil color is a form of defensive camouflage that seeds can use to avoid detection by seed predators. The legume Acmispon wrangelianus occurs across a variety of gray-green serpentine soils and brown nonserpentine soils. Quantitative digital image analysis of seed and soil colors was used to test whether genetically based seed color is a closer match to the color of the native soil than to the color of other nearby soils. Lineages bear seeds that more closely match the color of their native serpentine or nonserpentine soil type than the opposing soil type. Further, even within a soil type, lineages bear seeds with a closer color match to the soil at their native site than to other sites. The striking concordance between seed and native soil color suggests that natural selection for locally camouflaged seed color morphs, probably driven by seed predators, may maintain adaptive divergence in pigmentation, despite the opportunity for migration between soil environments.
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Because plants are sessile and their flowers and fruits are aggregated, plant mimics are less likely to be mistaken for their models than animal mimics which are mobile and dispersed among their models. Therefore, operator species are more likely to be deceived by animal mimics than plant mimics. In addition, the autonomy of plant appendages implies that warning mimicry provides less advantage to plants than to animals because plants suffer less from sampling by naive operators. Therefore, the advantage of warning mimicry is much greater for animals than plants. These reasons may explain why plant mimicry is less common than animal mimicry, based on attraction of rather than avoidance by operator species, and limited to the class of aggressive mimicry.
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Colour patterns and their visual backgrounds consist of a mosaic of patches that vary in colour, brightness, size, shape and position. Most studies of crypsis, aposematism, sexual selection, or other forms of signalling concentrate on one or two patch classes (colours), either ignoring the rest of the colour pattern, or analysing the patches sepa-rately. We summarize methods of comparing colour patterns making use of known properties of bird eyes. The meth-ods are easily modifiable for other animal visual systems. We present a new statistical method to compare entire colour patterns rather than comparing multiple pairs of patches. Unlike previous methods, the new method detects differences in the relationships among the colours, not just differences in colours. We present tests of the method's ability to detect a variety of kinds of differences between natural colour patterns and provide suggestions for analysis.
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Network analysis provides a unified framework for investigating different types of species interactions at the community level. Network analysis is typically based on null models that test for specific patterns in network topology. Here we use a novel predictive approach to investigate the topology of a mistletoe–host network. It has been hypothesised that Australian mistletoes mimic the phenotype of their preferred hosts to avoid herbivory. We developed a deterministic model based on phenotypic similarity to predict the topology of a quantitative network between Lauranthaceaous mistletoes and their hosts. We quantified mistletoe–host interactions in a semi-arid woodland central Australia, along with the size, shape and colour of leaves produced by both players in the interaction. Traditional null model analyses showed support for negative co-occurrence patterns, web specialisation and strong links between species pairs. However, our deterministic model showed that the observed network topology could not be predicted by phenotypic similarity, suggesting that Australian mistletoes do not mimic their hosts.