Plants are intelligent, here's how.

HYPOTHESES: The drive to survive is a biological universal. Intelligent behaviour is usually recognized when individual organisms including plants, in the face of fiercely competitive or adverse, real-world circumstances, change their behaviour to improve their probability of survival. SCOPE: This article explains the potential relationship of intelligence to adaptability and emphasizes the need to recognize individual variation in intelligence showing it to be goal directed and thus being purposeful. Intelligent behaviour in single cells and microbes is frequently reported. Individual variation might be underpinned by a novel learning mechanism, described here in detail. The requirements for real-world circumstances are outlined, and the relationship to organic selection is indicated together with niche construction as a good example of intentional behaviour that should improve survival. Adaptability is important in crop development but the term may be complex incorporating numerous behavioural traits some of which are indicated. CONCLUSION: There is real biological benefit to regarding plants as intelligent both from the fundamental issue of understanding plant life but also from providing a direction for fundamental future research and in crop breeding.

Tuned in: plant roots use sound to locate water.

Because water is essential to life, organisms have evolved a wide range of strategies to cope with water limitations, including actively searching for their preferred moisture levels to avoid dehydration. Plants use moisture gradients to direct their roots through the soil once a water source is detected, but how they first detect the source is unknown. We used the model plant Pisum sativum to investigate the mechanism by which roots sense and locate water. We found that roots were able to locate a water source by sensing the vibrations generated by water moving inside pipes, even in the absence of substrate moisture. When both moisture and acoustic cues were available, roots preferentially used moisture in the soil over acoustic vibrations, suggesting that acoustic gradients enable roots to broadly detect a water source at a distance, while moisture gradients help them to reach their target more accurately. Our results also showed that the presence of noise affected the abilities of roots to perceive and respond correctly to the surrounding soundscape. These findings highlight the urgent need to better understand the ecological role of sound and the consequences of acoustic pollution for plant as well as animal populations.

Experience teaches plants to learn faster and forget slower in environments where it matters.

The nervous system of animals serves the acquisition, memorization and recollection of information. Like animals, plants also acquire a huge amount of information from their environment, yet their capacity to memorize and organize learned behavioral responses has not been demonstrated. In Mimosa pudica-the sensitive plant-the defensive leaf-folding behaviour in response to repeated physical disturbance exhibits clear habituation, suggesting some elementary form of learning. Applying the theory and the analytical methods usually employed in animal learning research, we show that leaf-folding habituation is more pronounced and persistent for plants growing in energetically costly environments. Astonishingly, Mimosa can display the learned response even when left undisturbed in a more favourable environment for a month. This relatively long-lasting learned behavioural change as a result of previous experience matches the persistence of habituation effects observed in many animals.

Love thy neighbour: facilitation through an alternative signalling modality in plants.

BACKGROUND: Both competitive and facilitative interactions between species play a fundamental role in shaping natural communities. A recent study showed that competitive interactions between plants can be mediated by some alternative signalling channel, extending beyond those channels studied so far (i.e. chemicals, contact and light). Here, we tested whether such alternative pathway also enables facilitative interactions between neighbouring plant species. Specifically, we examined whether the presence of a 'good' neighbouring plant like basil positively influenced the germination of chilli seeds when all known signals were blocked. For this purpose, we used a custom-designed experimental set-up that prevented above- and below-ground contact and blocked chemical and light-mediated signals normally exchange by plants. RESULTS: We found that seed germination was positively enhanced by the presence of a 'good' neighbour, even when the known signalling modalities were blocked, indicating that light, touch or chemical signals may not be indispensible for different plant species to sense each other's presence. CONCLUSIONS: We propose that this alternative signalling modality operates as a general indicator of the presence of heterospecifics, enabling seeds to detect and identify a neighbour prior to engaging in a more finely-tuned, but potentially more costly, response.

Mimicking orchids lure bees from afar with exaggerated ultraviolet signals.

Flowers have many traits to appeal to pollinators, including ultraviolet (UV) absorbing markings, which are well-known for attracting bees at close proximity (e.g., <1 m). While striking UV signals have been thought to attract pollinators also from far away, if these signals impact the plant pollinia removal over distance remains unknown. Here, we report the case of the Australian orchid Diuris brumalis, a nonrewarding species, pollinated by bees via mimicry of the rewarding pea plant Daviesia decurrens. When distant from the pea plant, Diuris was hypothesized to enhance pollinator attraction by exaggeratedly mimicking the floral ultraviolet (UV) reflecting patterns of its model. By experimentally modulating floral UV reflectance with a UV screening solution, we quantified the orchid pollinia removal at a variable distance from the model pea plants. We demonstrate that the deceptive orchid Diuris attracts bee pollinators by emphasizing the visual stimuli, which mimic the floral UV signaling of the rewarding model Daviesia. Moreover, the exaggerated UV reflectance of Diuris flowers impacted pollinators' visitation at an optimal distance from Da. decurrens, and the effect decreased when orchids were too close or too far away from the model. Our findings support the hypothesis that salient UV flower signaling plays a functional role in visual floral mimicry, likely exploiting perceptual gaps in bee neural coding, and mediates the plant pollinia removal at much greater spatial scales than previously expected. The ruse works most effectively at an optimal distance of several meters revealing the importance of salient visual stimuli when mimicry is imperfect.

Do plants pay attention? A possible phenomenological-empirical approach.

Attention is the important ability of flexibly controlling limited cognitive resources. It ensures that organisms engage with the activities and stimuli that are relevant to their survival. Despite the cognitive capabilities of plants and their complex behavioural repertoire, the study of attention in plants has been largely neglected. In this article, we advance the hypothesis that plants are endowed with the ability of attaining attentive states. We depart from a transdisciplinary basis of philosophy, psychology, physics and plant ecophysiology to propose a framework that seeks to explain how plant attention might operate and how it could be studied empirically. In particular, the phenomenological approach seems particularly important to explain plant attention theoretically, and plant electrophysiology seems particularly suited to study it empirically. We propose the use of electrophysiological techniques as a viable way for studying it, and we revisit previous work to support our hypothesis. We conclude this essay with some remarks on future directions for the study of plant attention and its implications to botany.

Ocean acidification erodes crucial auditory behaviour in a marine fish.

Ocean acidification is predicted to affect marine ecosystems in many ways, including modification of fish behaviour. Previous studies have identified effects of CO(2)-enriched conditions on the sensory behaviour of fishes, including the loss of natural responses to odours resulting in ecologically deleterious decisions. Many fishes also rely on hearing for orientation, habitat selection, predator avoidance and communication. We used an auditory choice chamber to study the influence of CO(2)-enriched conditions on directional responses of juvenile clownfish (Amphiprion percula) to daytime reef noise. Rearing and test conditions were based on Intergovernmental Panel on Climate Change predictions for the twenty-first century: current-day ambient, 600, 700 and 900 µatm pCO(2). Juveniles from ambient CO(2)-conditions significantly avoided the reef noise, as expected, but this behaviour was absent in juveniles from CO(2)-enriched conditions. This study provides, to our knowledge, the first evidence that ocean acidification affects the auditory response of fishes, with potentially detrimental impacts on early survival.

Extended cognition in plants: is it possible?

Plants do not possess brains or neurons. However, they present astonishingly complex behaviors such as information acquisition, memory, learning, decision making, etc., which helps these sessile organisms deal with their ever-changing environments. As a consequence, they have been proposed to be cognitive and intelligent, an idea which is becoming increasingly accepted. However, how plant cognition could operate without a nervous central system remains poorly understood and new insights on this topic are urgently needed. According to the Extended Cognition hypothesis, cognition may also occur beyond the limits of the body, encompassing objects from the environment. This was shown possible in humans and spiders, who actively manipulate their external environment to extend their cognitive capacity. Here, we propose that extended cognition may also be found in plants and could partly explain the complexity of plant behavior. We suggest that plants can extend their cognitive abilities to the environment they manipulate through the root influence zone and the mycorrhizal fungi that associate with them. The possibility of a cognitive process involving organisms from different kingdoms is exciting and worthwhile exploring as it may provide key insights into the origin and evolution of cognition.

Comment on 'Lack of evidence for associative learning in pea plants'.

In 2016 we reported evidence for associative learning in plants (Gagliano et al., 2016). In view of the far-reaching implications of this finding we welcome the attempt made by Markel to replicate our study (Markel, 2020). However, as we discuss here, the protocol employed by Markel was unsuitable for testing for associative learning.

Hormonally mediated maternal effects shape offspring survival potential in stressful environments.

In most egg-laying vertebrates, maternal responses to stressful conditions are translated into the release of glucocorticoid hormones such as cortisol, which are then transmitted to their developing embryos. Although such maternally transmitted hormonal resources have been shown to influence or even interfere with the optimal developmental trajectories of offspring in many taxa, their influence on the dynamics of wild fish populations remains largely unexplored. Here, we examined the extent to which simulated hormonally mediated maternal effects influence the development and early survival of the coral reef damselfish, Pomacentrus amboinensis. Concentrations of cortisol in the eggs were manipulated within naturally occurring limits by immersion. We found that the proportion of embryos that delayed hatching when exposed to high levels of cortisol was considerably lower than in the other two treatments (low cortisol dose and control). High cortisol levels in P. amboinensis eggs resulted in increased egg mortality and greater asymmetry in hatchlings. For embryos that successfully hatched, individuals from the elevated cortisol treatments (especially low dose) survived longer after hatching. Although individuals that originated from eggs with elevated cortisol levels survived longer after hatching, they may not gain an overall survival advantage. Our results suggest that subtle increases in the allocation of maternally derived hormones, such as cortisol, to offspring are a direct way for stressed mothers to endow their young with an immediate survival advantage. We propose that this immediate benefit outweighs the developmental costs which may be expressed as reduced fitness at later life stages.

Dispersal without errors: symmetrical ears tune into the right frequency for survival.

Vertebrate animals localize sounds by comparing differences in the acoustic signal between the two ears and, accordingly, ear structures such as the otoliths of fishes are expected to develop symmetrically. Sound recently emerged as a leading candidate cue for reef fish larvae navigating from open waters back to the reef. Clearly, the integrity of the auditory organ has a direct bearing on what and how fish larvae hear. Yet, the link between otolith symmetry and effective navigation has never been investigated in fishes. We tested whether otolith asymmetry influenced the ability of returning larvae to detect and successfully recruit to favourable reef habitats. Our results suggest that larvae with asymmetrical otoliths not only encountered greater difficulties in detecting suitable settlement habitats, but may also suffer significantly higher rates of mortality. Further, we found that otolith asymmetries arising early in the embryonic stage were not corrected by any compensational growth mechanism during the larval stage. Because these errors persist and phenotypic selection penalizes asymmetrical individuals, asymmetry is likely to play an important role in shaping wild fish populations.

Survival against the odds: ontogenetic changes in selective pressure mediate growth-mortality trade-offs in a marine fish.

For organisms with complex life cycles, variation among individuals in traits associated with survival in one life-history stage can strongly affect the performance in subsequent stages with important repercussions on population dynamics. To identify which individual attributes are the most influential in determining patterns of survival in a cohort of reef fish, we compared the characteristics of Pomacentrus amboinensis surviving early juvenile stages on the reef with those of the cohort from which they originated. Individuals were collected at hatching, the end of the planktonic phase, and two, three, four, six and eight weeks post-settlement. Information stored in the otoliths of individual fish revealed strong carry-over effects of larval condition at hatching on juvenile survival, weeks after settlement (i.e. smaller-is-better). Among the traits examined, planktonic growth history was, by far, the most influential and long-lasting trait associated with juvenile persistence in reef habitats. However, otolith increments suggested that larval growth rate may not be maintained during early juvenile life, when selective mortality swiftly reverses its direction. These changes in selective pressure may mediate growth-mortality trade-offs between predation and starvation risks during early juvenile life. Ontogenetic changes in the shape of selectivity may be a mechanism maintaining phenotypic variation in growth rate and size within a population.

Learning by Association in Plants.

In complex and ever-changing environments, resources such as food are often scarce and unevenly distributed in space and time. Therefore, utilizing external cues to locate and remember high-quality sources allows more efficient foraging, thus increasing chances for survival. Associations between environmental cues and food are readily formed because of the tangible benefits they confer. While examples of the key role they play in shaping foraging behaviours are widespread in the animal world, the possibility that plants are also able to acquire learned associations to guide their foraging behaviour has never been demonstrated. Here we show that this type of learning occurs in the garden pea, Pisum sativum. By using a Y-maze task, we show that the position of a neutral cue, predicting the location of a light source, affected the direction of plant growth. This learned behaviour prevailed over innate phototropism. Notably, learning was successful only when it occurred during the subjective day, suggesting that behavioural performance is regulated by metabolic demands. Our results show that associative learning is an essential component of plant behaviour. We conclude that associative learning represents a universal adaptive mechanism shared by both animals and plants.

Facing the environment: onset and development of UV markings in young fish.

Most colour patterns in animals represent an elegant compromise between conspicuousness to ensure effective communication with preferred receivers and camouflage to avoid attracting the attention of unwanted predators. Many species, including several coral reef fishes, overcome this conflict by using ultraviolet (UV) colouration and signalling, as these colours are visible only over short distances and are often invisible to their predators. Despite a great interest in their behavioural significance and ecological influence on survival, little is known about when these colours first develop on the bodies of free-living animals. Here we show for the first time that the UV facial patterns of a coral reef fish do not develop in captivity but only when juveniles experience the socio-behavioural conditions of their natural environment. Using field and laboratory experiments, we determined that the onset and early development of these UV facial markings did not occur at metamorphosis. Instead, juveniles developed the UV markings during their first two weeks on the reef. Exposure to different reef environments revealed significant plasticity in the development of these markings. The direct or indirect (through intraspecific interactions) exposure to predators is a likely candidate trigger for the plastic development of these UV markings in the wild.

In a green frame of mind: perspectives on the behavioural ecology and cognitive nature of plants.

It is increasingly recognized that plants are highly sensitive organisms that perceive, assess, learn, remember, resolve problems, make decisions and communicate with each other by actively acquiring information from their environment. However, the fact that many of the sophisticated behaviours plants exhibit reveal cognitive competences, which are generally attributed to humans and some non-human animals, has remained unappreciated. Here, I will outline the theoretical barriers that have precluded the opportunity to experimentally test such behavioural/cognitive phenomena in plants. I will then suggest concrete alternative approaches to cognition by highlighting how (i) the environment offers a multitude of opportunities for decision-making and action and makes behaviours possible, rather than causing them; (ii) perception in itself is action in the form of a continuous flow of information; (iii) all living organisms viewed within this context become agents endowed with autonomy rather than objects in a mechanistically conceived world. These viewpoints, combined with recent evidence, may contribute to move the entire field towards an integrated study of cognitive biology.

Green symphonies: a call for studies on acoustic communication in plants.

Sound and its use in communication have significantly contributed to shaping the ecology, evolution, behavior, and ultimately the success of many animal species. Yet, the ability to use sound is not a prerogative of animals. Plants may also use sound, but we have been unable to effectively research what the ecological and evolutionary implications might be in a plant's life. Why should plants emit and receive sound and is there information contained in those sounds? I hypothesize that it would be particularly advantageous for plants to learn about the surrounding environment using sound, as acoustic signals propagate rapidly and with minimal energetic or fitness costs. In fact, both emission and detection of sound may have adaptive value in plants by affecting responses in other organisms, plants, and animals alike. The systematic exploration of the functional, ecological, and evolutionary significance of sound in the life of plants is expected to prompt a reinterpretation of our understanding of these organisms and galvanize the emergence of novel concepts and perspectives on their communicative complexity.

Spot the difference: mimicry in a coral reef fish.

Eyespots on the body of many animals have long been assumed to confer protection against predators, but empirical evidence has recently demonstrated that this may not always be the case and suggested that such markings may also serve other purposes. Clearly, this raises the unresolved question of what functions do these markings have and do they contribute to an individual's evolutionary fitness in the wild. Here, we examined the occurrence of eyespots on the dorsal fin of a coral reef damselfish (Pomacentrus amboinensis), where these markings are typical of the juvenile stage and fade away as the fish approaches sexual maturation to then disappear completely in the vast majority of, but not all, adult individuals. By exploring differences in body shape among age and gender groups, we found that individuals retaining the eyespot into adulthood are all sexually mature males, suggesting that these eyespots may be an adult deceptive signal. Interestingly, the body shape of these individuals resembled more closely that of immature females than mature dominant males. These results suggest that eyespots have multiple roles and their functional significance changes within the lifetime of an animal from being a juvenile advertisement to a deceptive adult signal. Male removal experiments or colour manipulations may be necessary to establish specific functions.

Natural-born con artists and counterfeiters: Who is being deceived here?

Deception is ubiquitous in plant and animal kingdoms and is widely thought to provide selective advantages to the individual and evolutionary success to the species. Mimicry, a form of deception whereby an individual imitates their model to advantage by closely resembling their behavior or appearance, is particularly well documented and represented by the peripheral eyespots seen on the wings of many butterfly species. The significance of butterfly eyespots has been convincingly demonstrated to serve as an anti-predatory function either by imitation of a predator's own dangerous enemies (intimidation hypothesis) or by deflecting predator strikes toward less-vital parts of the body (deflection hypothesis). A convincing and compelling explanation in butterflies, the functional role of eyespots as anti-predatory devices has become a widely held and firmly entrenched belief that has been freely adopted into other systems. Here we comment on a recent paper that demonstrates a vastly different role for eyespots, that of intra-specific male-male competition, and make the point that even long-held beliefs need to be tested and challenged under different contexts if we are not to be deceived ourselves.