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Summer Research Fellowship Programme of India's Science Academies

CATCH ME IF YOU CAN : Conspicuous colorations and contrasting patterns as an anti-predator strategy in prey-predator interactions

Yogesh M

Department of Biotechnology, Rajalakshmi Engineering College, Chennai 602105

Gopal Murali & Ullasa Kodandaramaiah

School of Biology, Indian Institue of Scientific Education and Research, Thiruvananthapuram 695551

Abstract

Nature has a broad range of strategies developed through evolutionary processes which ensures the existence of various species capable of surviving in the continually changing ecological parameters and corresponding challenges accompanying the changes. Among the essential motives to survive, anti-predator strategies have presented itself in a spectrum of morphologically identifiable or physiologically associatable qualities such as mimicry, aposematism, decoy mechanisms and other mechanisms. The diversity in these strategies necessitates a radical understanding of the underlying principles and the effectiveness of combined strategies. The major part of this work revolves around understanding the effect of patterns, in improving the survival chances of ground dwelling prey. A variety of ground dwelling reptilian species, for instance species belonging to the suborder of Lacertilia and Serpents represent a group of highly advanced reptiles with versatile habitats across South Indian regions, suggesting the effective expression of observable anti-predator strategies developed over time. These reptiles, observed in Western Ghats of Kerala, India, exhibit a conspicuous bright eye catching coloration with contrasting sharp stripes on the dorsal or lateral side which acts as an efficient anti-predator strategy against the avian predators. The implementation of visual deception by deceiving the predators with the bright contrasting stripes, redirecting the avian attack towards the sacrificable and conspicuous colorless essential parts and thus ensuring the safety of vital organs has been studied through an interactive game designed using the software SCRATCH 2.0. The result exhibits a strong reasoning and explanation for the cooperative action of both stripes and conspicuous bright coloration leading to a successful anti-predation strategy.

Keywords: anti-predator strategy, conspicuous contrasting coloration, stripes, deception, behavioral study

Abbreviations

Abbreviation
GLMM  Generalised Linear Mixed-effects Models

INTRODUCTION

Background

The basic understanding of evolutionary adaptations that assists a species to survive in an environment by achieving a specific level of fitness or strategy to thrive with a decent population density in that particular ecology has been the main concern of evolutionary biology and ecological studies. Animal coloration has frequently been the subject to significant ontogenetic change, and these changes may often have adaptive consequences ( Booth C.L ,1990 : Garcia, et al, 2003 ). The simple aim that necessitates the evolution of a species, is to survive and ensure the continuity of the lineage.

The importance of color pattern as an anti-predator strategy to tackle the visually oriented avian predators in reptilia and other animals have been well studied over a period of time ( Cott, et al 1940 ; Endler 1978 ; King 1992 ). The recent advances have shown that more than one evolutionary adaptations might act in a harmonious manner to achieve an highly effective anti-predator strategy. The necessity to survive can be tangled with the need to ensure the continuity of the linege and thus the anti-predator strategy has been visualized as one among the paramount aspect to be stuided in the multitude of evolutionary adaptations. Earlier, studies have focused on the integration of multiple phenotypic aspects of an organism to achieve a specific function ( Irschick, et al2001; Ghalambor, et al 2003 )​.

The general consensus based on previous stuides have left some questions unanswered. Although the colorations, patterns and other strategies have been explained in other reptilians such as snakes, there occurs an opportunity in verifying the conclusions from the previous studies. The generalization of these conclusions to ground dwelling reptiles suggests more than one evolutionary adaptations and their cooperative effect. The effective mechanism of stripes and coloration that results in visual deception to redirects the visually oriented avian predator attacks ( Cooper, 1985 ). Thus this study is important in understanding the integrative function of stripes and conspicuous coloration against predators.

The purpose

The observed anti-predator reptilian features usually has a conspicuous bright conspicuous colorations and eye catching high contrasting stripes contrasting to the actual coloration of the reptilian skin. These ground dwelling reptiles have advanced adaptations in body type that facilitates the swift movement and rapid random direction changes.

  • The anti-predator strategy can be correlated logically to the foraging nature of the reptile. There exists various anti-predator strategies which differ in principle for various foragers. The slow foragers tend to exhibit the camouflage strategy while the active foragers focus on decoy mechanisms, aposematisms and others strategies that ensures the safety of essential organs ( Karine Monceau 2013 ).
  • It is necessary to understand the combined effect of multiple evolutionary adaptations as an anti-predator strategy as it reflects on possible ecological stresses that might have caused the adaptions to evolve through evloution.
  • The study aims at rational and successful description of the mechanism by which these visual deceptions function against the highly efficient tetrachromatic eyes of the avian predators that orients itself towards the prey in motion for predation.
  • The study interprets the results of predation through the results obtained from an interactive game designed to mimic actual pattern recognition, in a manner that reflects the pattern vulnerable for predation ( Khater, et al, 2016 ).
  • The game designed was taken up by naive participants to avoid any kind of bias and to deduce actual pattern vulnerable for predation. The usual reptilian anti-predator features considered from the literature studies were used for the simulation. Although the study is restricted to the general reptilian patterns from literature studies, the results are applicable to all similar foragers with resembling patterns and conspicuous coloration.
  • These reptiles often have a short stipulated foraging period as the local climatic conditions might be subjected to variations due to seasonal changes which also affects the frequency and the duration of basking sessions a necessity for these poikilothermic organisms.
  • The population density of the avian predator and distribution density of the prey for these reptiles decides the habitat and foraging grounds i.e habitat change may interact with predation rates ( Evans, 20042004 ). On threatend by the avian predators these reptiles tend to hide in between the damp braches or twings clumped together in such a way that it is impenetratable for the avian predators to catch them ( Devi M. Stuart-Fox, 200320032235 ).

Objectives of the Research

Overall objective

The overall objectives of this study are mentioned below.

  • To understand and explain the visual deception leading to mislocation of attack from avian predator by the ground dwelling prey as in motion dazzle.
  • To point out the logic behind the evolution of stripes.
  • To identify the most vulnerable patterns and easily camouflaging nature in predation process.

Scope

The scope of this work aims at providing an explation for stripes and conspicous coloration and the coordinated effect of both in visual deception during escape or foraging activity of ground dwelling reptiles. The morphological adaptations developed due to the ecological stress of predation, in relevance to the behavioral aspect and foraging nature which inturn necessitates the choice of habitat for the successful survival and reproduction of the species, describes the possiblities of various evolutionary constraints and challenges faced by the reptiles in their specific ecology. This is an important evolutionary aspect that dictates the behavioral nature of the respective species.

LITERATURE REVIEW

Information

An extraordinary feature of several animals and several other species of reptiles is the existence an extremely sharp and contrasting stripes with respect to their skin coloration which makes them quite conspicuous in their respective ecological system. There have been researches with aim of understating the importance of conspicuous colorations and patterns prey–predator signaling and predator perception or deceptions ( Caro T 2009; Wallace AR, 1867 ). Although there have been researches that supports the motion dazzle hypothesis, as an effective anti-predator strategy ( ​Hughes AE, et al​ 2014 ), this work differs in one aspect where the human perception evaluates the deception through an interactive computer game ( ​Murali Gopal​ 2016 ).

According to the motion dazzle hypothesis, the sharp contrasting patterns causes a visual deception by mis-locating prey along a particular trajectory at any given speed of prey in motion ( ​How MJ, et al​ 2014 ;​Scott-Samuel NE, et al​ 2011 ; ​Rojas B, et al​ 2014 ). Various other studies have also focussed on the presence of stripes parallel to the major axis of the reptilian body and the corresponding relevance in escape strategies ( Hughes AE, et al 2015 ). This study tests if the longitudinal contratsing stripes along with the conspicuous coloration is an effective antipredator strategy.

Summary

The image processing time lag caused by the high constrast stripe of a reptile, in motion, especially when an eye-catching conspicuous sharp coloration is taken into observation, it so happens that the avian predator which solely depends on visual orientation and tracking of the reptile trajectory ends up attacking the sacrificable posterior portion and thus enabling the reptile to have an increased survival chance. It is also possible that a reptile might escape the attack from an avian predator by attempting a rapid random change in the trajectory while the avian predator might end up locating the reptile in a spot behind the actual location.

METHODOLOGY

Concepts

The need for an innovative and interactive method.

The actual predation process involves the avian predators and ground dwelling reptile in a natural ecosystem ( Costs of reproduction, et al, 1992 ; Avian Predation on a Large Lizard 1996 ). Due to the possible difficulties and high chances of errors that might occur during the wild observation in those respective ecosystems and the limited frequency of any specific species being predated that could be recorded per day, other innovative methods to estimate and evaluate the prey predator signallling and the influence of patterns and colorations are necessary.

The following points highlights the basic concepts

  • An interactive game was designed with various prominent patterns that commonly occurs in the prey species and other close relative species that are hypothesized to follow similar strategy, using a modified program devised by Gopal Murali and Ullasa Kodandaramaiah in ( ​Murali Gopal​ 2016 ). The game was written in SCRATCH 2.0 (2014). The participats were naive and consent forms were collected from the respective volunteers.
  • The data were analyzed using a generalised linear mixed-effects models (GLMM) with the glmer function in the lme4 package (Bates et al. 2014). A Poisson GLMM model was used because the outcome was in the form of count data. To account for repeated measures from the same volunteer, participant ID was taken as the random intercept and object type as the fixed effect. Tukey post hoc pairwise comparisons among object types were done using the multicomp v.1.4-8 package (Hothorn et al. 2017)

This method basically involves a source code which directs the rectangular target with four patterns and colours taken into consideration for the study. The four targets were named uniform white, uniform black, uniform grey and parallel stripped. As directed by the program the target enters the screen with blotted background and moves in random direction with specific velocity. The game generates a result wherein the number of times when a participant touches the anterior part which corresponds to the neck and body of the prey and the total number of times when the participant catches the prey, irrespective of anterior and posterior position. The statistical analysis of the result generated shows the pattern most intimidating to the avian predator is usually seen in the target reptiles with conspicuous coloration and the study hence supports the motion dazzle hypothesis ( SangHeeLee Journal of the Korean Physical SocietyFebruary 2018 ).

Methods

The method by which the prey predator actions are studied can basically either be an wild life study as in the cases of carnivorus predator behavioral analysis. For instance, Panthera leo (​​ Emma J. Dunston 2016 Behavioral correlates between daily activity and sociality, et al ) was studied in the respective ecosystem. The frequency of attacks by the localized and densely populated predator was high and the process of predation can be observed with a clear view.

In other cases that involves avian predators of a forest ecosystem, the lack of visibilty, limited frequency of the attacks the depends indirectly on the population density of the prey, the ground dwelling reptiles, can affect the quality of results. This necessitates the use of other innovative interactive methods ( Burt Kotler, et al, 20162016 ).

The previous work has followed similar protocols with slight modifications suiting their respective aims and objectives. Among the vast variety of works previously carried out with aims related to conspicuous coloration and anti-predator strategy, most of them deal with a mathematical model or a video based analysis of the foraging activity. The reliability of the results from these methodologies are assumed to be on par with ecological study based results. This interactive method mimics the predation process and aims to observe the vulnerability of patterns in reptiles.

  • An interactive game was designed with various prominent patterns that commonly occurs in the prey species and other close relative species that are hypothesized to follow similar strategy, using a modified program devised by Gopal Murali and Ullasa Kodandaramaiah in ( ​Murali Gopal​ 2016 ). The game was written in SCRATCH 2.0 (2014). The participats were naive and consent forms were collected from the respective volunteers.
  • The data were analyzed using a generalised linear mixed-effects models (GLMM) with the glmer function in the lme4 package (Bates et al. 2014). A Poisson GLMM model was used because the outcome was in the form of count data. To account for repeated measures from the same volunteer, participant ID was taken as the random intercept and object type as the fixed effect. Tukey post hoc pairwise comparisons among object types were done using the multicomp v.1.4-8 package (Hothorn et al. 2017)

The following analysis of the results were generated by the naive participants who have completed the computerized game.


Contrasts Estimate Std. Error Z-value P-value
Uniform-grey vs Uniform-black -0.3539 0.0582 -6.080 <0.0001
Parallel-striped vs Uniform-black -0.3578 0.0576 -6.212 <0.0001
Uniform-white vs Uniform-black -0.1164 0.0538 -2.162 0.134
Parallel-striped vs Uniform-grey -0.0038 0.0630 -0.061 0.9999
Uniform-white vs Uniform-grey 0.2375 0.0596 3.983 <0.0001
Uniform-white vs Parallel-striped 0.2414 0.0590 4.089 <0.0001

The statistical analysis of the result generated shows the pattern most intimidating to the avian predator is usually seen in reptileswith conspicuous coloration and the study hence supports the motion dazzle hypothesis.

Results.png
    Mean and 95% CI estimated for the regression model for the number of successful attacks. A ‘*’ represents a significant difference p<0.05. Non-significant comparisons are not highlighted.

    The statistical analysis shows that the parallel stripped pattern although vulnerable to an attack by the predator, the predator could not attack the prey in a precise manner.

    RESULTS AND DISCUSSION

    Perspectives

    The results generated by the computerized prey-predator game, indicates that the number of times the target with parallel stripped pattern was caught actually by the anterior side. This suggests that the parallel stripes, during motion, causes a time lag in perceiving the visual perception resulting in a deception. The visual deception especially, causes the avian predator to locate the prey towards the posterior section, i.e opposite to the direction of the prey trajectory. The speed of the prey determines the extent of deception, in essence, the faster is the prey the tougher it is for the predator to locate the prey.

    The result also suggests that the evolution of anti-predator strategy can be associated to the nature of foraging activity. The fast foragers have developed themselves with the evolutionary adaptations of striking bright stripes contrasting to their skin and eye catching conspicuous sharp coloration. The adaptations emphasize that the prey has some sort of knowledge on the method by which an avian predator attacks the target. It is an unanswered question, " Is there an evolutionary memory, that enhances and facilitates the survival chances of the prey by driving the evolutionary adaptations and specializations, both morphologically and behaviorally? "

    The ecological stresses and parameters which necessitates the adaptations can be contemplated under certain conditions, over the due course of time, might suggest informations on the triggers that necessitates the adaptations. Although it might be quite difficult to analyse the ecological conditions that were prevailing during the course of evolution, a basic understanding of variation in a population caused by switching to specific adaptations or specializations can be achieved. Sometimes a logical connection between varying populations in different geographical regions can be established. Through this study, we can establish a logical connection between the behavioral aspect of different species closely related to each other and other reptilian species that has sharp high contrasting bright stripes or conspicuous bright coloration or both. Some lizard species in specific has the capability of autotomy that further launches a eye catching decoy following the motion dazzle. Although the regeneration of the tail is an energy expenditure process and thus the lizards tend to escape initially ( escape theory ) or switch to motion dazzle principle if in case the lizards have sharp contrasting stripes. After a particular juncture, the lizards switch to decoy mechanism.

    There might occur other possibilities in the prey-predation strategies that opens the vacancy for researchers to establish a correlation between evolutionary aspects that drives the specializations and the possibility of further evolutionary changes that might occur under specific constrains imposed over generations. The behavioral analysis of induced evolutionary adaptations through ecological constrains imposed on generations and the wild original race can explain the possible role of evolutionary memory in socializing and foraging activities in reptiles. However, this method might be time consuming and might be extremely dependant on the period of lifecycle, the ability to adapt swiftly and the ability to express the adaptation as an observable feature of the reptilian population.

    CONCLUSION AND RECOMMENDATIONS

    The final thoughts that from this study supports the motion dazzle hypothesis in specific. The study also establishes possible logics that associates other behavioral aspects the prey to the observed specific evolutionary adaptations. Based on the observed results, it is evident that the basic driving force behind evolution of the sharp and highly contrasting stripes and bright conspicuous colorations in are the need to survive and ensure the continuity of the reptilian lineage in thst particular ecosystem. In other words, it is an evolutionary adaptation that increases the chances of survival by avoiding predation. The visual deception by the bright conspicuous colorations and motion dazzle effect together forms a highly advanced anti-predator strategy in reptiles and other animals that faces predation.

    ACKNOWLEDGEMENTS

    I would like to express my gratitude to my guide, Dr. Ullasa Kodandaramaiah, Assistant Professor, School of Biology, Indian Institute of Science Education and Research, Thiruvananthapuram for his exemplary guidance. Without his guidance ad help, completion of this project would have not been possible.

    I would also like to express my gratitude to my co-guide Mr. Gopal Murali who has always been there to guide me and help me. Without his guidance I would have not been able to complete my summer research fellowship sucessfully. I am grateful for his patience and willingness to let me work with him. I am obliged to thank Ms. Saloni Rose, Ms Ibakordor Khyriem, Mr. Jose, Mr. Abel and Ms. Amanda Ben for helping me carry out the interactive game. I am grateful for the people at Vanasiri Lab and BEE lab for their extended support and encouragement. would like to thank the School of Biology, Indian Institute of Science Education and Research, Thiruvananthapuram, for allowing to do my summer research fellowship and for providing all the necessary infrastructure and research facilities and my institute, Rajalakshmi Engineering College for permitting me to complete my fellowship.

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