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Discrimination of aposematic and novel prey by mature Sceloporus malachiticus

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Title:
Discrimination of aposematic and novel prey by mature Sceloporus malachiticus
Translated Title:
Discriminación de la presa nueva y aposemática por Sceloporus malachiticus ( )
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English
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Masterson, Jeff
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Predator & prey   ( lcsh )
Canyon lizard   ( lcsh )
Warning coloration (Biology)   ( lcsh )
Depredador y presa
Lagartija de cañon
Coloración de advertencia
Tropical Ecology 2006
Aposematic prey
Ecología Tropical 2006
Presa aposemática
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Reports   ( lcsh )
Reports

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Abstract:
Prey use a variety of defenses against predators in order to avoid predation and often use warning coloration known as aposematism to advertise unpalatability to predators. Predators have accordingly evolved defenses against possibly unpalatable prey by being selective, and avoiding aposematically colored prey items. Some predators are more selective, avoiding anything appearing novel (neophobia), thus lowering the risk of unprofitable foraging by restricting their diet to familiar items. Previous studies have shown that neonatal Sceloporus malachiticus will innately avoid aposematic prey. In this experiment I examined any potential changes in prey selection concerning aposematic or novel prey items in S. malachiticus in Monteverde, Costa Rica. I used paint pens to create three different color patterns on crickets; drab, aposematic, and novel. I fed nine S. malachiticus these different treatments in random order over the course of six trials. I found that the lizards showed no apparent preference for any color type (Friedman test, p = 0.0970, n = 9), indicating a loss of dietary conservatism as mature adults.
Abstract:
Las presas utilizan una variedad de defensas contra los depredadores con el fin de evitar la depredación y a menudo el uso de coloración de advertencia conocido como aposematism para advertir inapetencia a los depredadores. Los depredadores por consiguiente han desarrollado posibles defensas contra las presas desagradables siendo selectivos, y evitando el color aposematic de las presas. Algunos depredadores son más selectivos, evitando todo lo que parece nuevo (neofobia), reduciendo así el riesgo del forrajeo no rentable restringiendo su dieta a solo las cosas conocidas. Estudios previos han demostrado que neonatal Sceloporus malachiticus evitará innatamente a la presa aposematic. En este experimento, examiné cualquier cambio potencial en la selección de presas referente a las presas aposematic o nuevas presas en S. malachiticus en Monteverde, Costa Rica.
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Text in English.
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Born Digital

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Discrimination of aposematic and novel prey by mature Sceloporus malachiticus Jeff Masterson Department of Biology, University of Oregon ABSTRACT Prey use a variety of defenses against predators in order to avoid predation and often use warning coloration known as aposematism to advertise unpalatability to predators. Pred ators have accordingly evolved defenses against possibly unpalatable prey by being selective, and avoiding aposematically colored prey items. Some predators are more selective, avoiding anything appearing novel (neophobia), thus lowering the risk of unprofitable foraging by restrictin g their diet to familiar items. Previous studies have shown that neonatal Sceloporus malachiticus will innately avoid aposematic prey. In this experiment I examined any potential changes in prey selection concerning aposematic or novel prey items in S. malachiticus in Monteverde, Costa Rica. I used paint pe ns to create three different color patterns on crickets; drab, aposematic, and novel. I fed nine S. malachiticus these different treatments in random order over the course of six trials. I found that the lizards showed no apparent pref erence for any color type (Friedman test, p = 0.0970, n = 9), indicating a loss of dietary conservatism as mature adults. RESUMEN Las presas usan muchas tipos de defensas difere ntes para evitar predatores, y muchas veces usan colores advertencias en un sistema que se llama a posematismo para anunciar a predatores que no son buenos para comer. Predatores tambin se han desarrollado defensas contra las presas txicas; por ejemplo, son selectivos en los tipos de presas que eligen de comer, y evitan presas con colores advertencias. Unos predatores son an ms selectivos, y evitan todas las presas que les parecen nuevas (neophobia), as evitando las presas que podran ser toxicas. Estudios previos han mostrado que Sceloporus malachiticus neonatales evitan innatamente las presas con colores advertencias. En este experimento examin cambios en la seleccin de presas de S. malachiticus con presas aposematicas o nuevas en Monteverde, Costa Rica. Us boligrafos de pinturas para crear tres dibujos di ferentes en grillos; negro, aposematica, y nuevo. Aliment a nueve S. malachiticus con estos grillos diferentes en una orden aleatoria por seis pruebas. Encontr que las ligartijas no mostraron ninguna preferencia para el tipo de color (Friedman; p = 0.0970, n = 9) indicando una prdida del conserva tismo en las dietas como adultos. INTRODUCTION Predation is one of the most important f itness-affecting ecological factors, hence many anti-predator defenses have evolved to combat this th reat (Riessen 1992). Organisms can be cryptic, such as phasmids wh ich resemble twigs or leaves, or they can invest in mobility, such as flight, in order to escape pr edators (Pietrewicz and Kamil 1977). Some organisms invest in mechanical defenses, such as rough surfaces or spines (e.g. urticating hairs in caterp illars), and some invest in chemical defenses to make themselves distasteful. Danaus spp. for example use cardiac glycosides to confer unpalatability, inducing predator s to vomit if they are ea ten (Duffey 1970). Organisms

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can also use toxins to inflict se rious harm on predators, such as Dendrobates spp. that produce alkaloid poisons excreted on their sk in to make themselves toxic to predators (Saporito 2004). Mechanical and chemical defenses are often coupled with warning coloration, also called aposematism, to advertis e to predators that the prey is unrewarding to eat (Sherratt 2002). In turn, predators avoid prey that may have either chemical or mechanical defenses, and do so in a variety of ways. Predators may avoid aposematically colored individuals and instead forage primarily for crypt ic prey that do not i nvest in chemical or mechanical defenses (Franks 2004, Sherratt 200 2). Such avoidance of aposematism can be either learned or innate (Reznick et. al.1981). Prey may induce learned avoidance in predators by being dist asteful and emetic, (e.g. Danaus spp.) requiring a predator to try the prey item at least once before the predator learns to avoid that prey item (Duffey 1970). Some predators exhibit an innate avoi dance to prey items, usually exhibited in response to lethal prey. One exam ple is Turquoise-browed Motmots ( Eumomota superciliosa ), which have shown an innate avoida nce to coral snake coloration (Smith 1975). Coral snakes could be lethal the first time the predator attempts to eat it, so innate avoidance evolves. Some predators exhibit a more conser vative strategy by avoiding all novel food types, a type of neophobia (Thomas et. al. 2004). Often it is not cost effective for predators to risk trying a ne w and potentially toxic prey it em, especially if there are ample palatable and familiar prey present (Marples and Kelly 1999). This has been exhibited in Common Ravens ( Corvus corax ), wild Common Blackbirds ( Terdus merula ) and European Robin ( Erithacus rubecula ) populations after the introduction of novel prey, and although there was variation in the level of the avoidance, some individuals required more than 18 months and 200 exposures to eat the nove l, palatable prey (Heinrich 1988, Thomas et. al. 2003). The cost benefit for predators foraging on either novel or aposematically colored prey may change with age and experience. Marmoset ( Callithrix jacchus) juveniles have been shown to have much stronger aversion to novel food types than adults in the same family group (Yamamoto and Lopes 2003). The predators amount of experience with novel prey as a young individual may affect th e level of neophobia as adults, since the more exposure to novel food types, the mo re familiar they become. Orange-winged Amazon Parrots ( Amazona amazonica) show differences in the level of neophobia according to the amount of novel objects to wh ich they had previously been exposed. The differences in neophobia also disappear as when the birds reach about one year of age, suggesting that maturity influences neophobic behavior. (Fox and Millan 2004) This could be due to a greater ability in mature individuals to metabolize toxic compounds. Mammals, for example are able to increase th e capacity of their de toxification system through repeated exposures to toxic compounds (Freeland and Janzen 1974). Experience with different chemicals induces enzyme synt hesis, and metabolism of one chemical can produce enzymes helpful in degrading other chemicals (Conney and Burns 1972). Mature individuals have most likely ha d more exposures to chemicals than young individuals, and hence have gr eater detoxifying capacity as well as a more enzymes that allow them to break down more chemicals. Neonate and inexperienced S. malachiticus have shown innate avoidance of aposematic milkweed bug ( Oncopeltus fasciatus ) color patterns (Reznick et. al 1981). 2

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Three-day-old S. malachiticus with no previous foraging experience were presented with cricket nymph and an adult milkweed bug at the same time. Only one trial was conducted, but all 12 lizards ate the cricket nymph first. In a follow up experiment, S. malachiticus of four different ages (three days, 18-30 days, 45-61 days, and wild caught adults) were split up into tw o trial groups both composed of about 17-23 individuals. Group A was presented with two milkweed bugs, one unmodified (black and orange bands) and one dusted black. Group B were presented with dermestid beetles, one painted black and the other w ith the characteristic black and orange bands. Two hypotheses were tested, the color preference hypothesis was that the lizards would eat all black insects first. The insect preferen ce hypothesis was to see if the differences in selection were due to character istics other than color, which was tested by comparing how readily the lizards attack ed milkweed bugs versus derm estid beetles. Although the results were not significant for either the co lor preference or ins ect preference test, invariably a larger number of liz ards attacked the black insect first. In testing the insect preference hypotheses, they found that each of the three captive born subjects attacked the dermestid beetles significantly more frequently than milkweed bugs, and that characteristic was not present in wild caught adults, showing a loss of avoidance based on non-color prey characteristic s (Reznick et. al 1981). Sceloporus malachiticus have exhibited innate avoi dance of aposematic colored prey at an early age, but it is not known whet her this avoidance is retained into their adult years. Also, inexperienced S. malachiticus may have actually been responding to the novelty of the milkweed bug, and not necessarily its aposematic coloration. The purpose of this experiment is to test whethe r the innate aposematic avoidance of S. malachiticus is maintained in adult individuals, and also wh ether the avoidance of these colorations is actually a more conservative and gene ral avoidance of novel coloration. MATERIALS AND METHODS Study Organism Sceloporus malachiticus (Squamata: Iguanidae) is a diurnal, primarily insectivorous spiny lizard found in premontane, lower montane, montane, and subalpine zones of Central America. They are heliothermic, and with high temperature or light they are seen as bright green with turquoise tails, but with lo wer body temperature their color may change to dark grey or black. Home ranges are only a few square meters, centered around perches and/or hiding spots. Within these small ranges they forage by ambushing prey. (Savage 2002) Collection Areas Sceloporus malachiticus lizards were collected from Monteverde, Costa Rica. Five individuals were obtained near the Estacion Biologica de M onteverde, three were obtained on the Arguedas-Ramirez property in el Cementerio near Santa Elena, and one individual was obtained near the Ranario in Santa Elena. 3

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Experimental Set-Up The nine S. malachiticus obtained were kept in five glass terrariums measuring 42cm X 32cm X 32cm. The lizards were kept in pairs and one trio between feeding trials. Soil from the forest floor (including dead leaves and sticks) was placed on the bottom of each terrarium (about 6 cm thick) and water dishes were placed in each terrarium. A sixth terrarium was set up as a testing arena with nothing but finely textured soil from a roadside near the Estacion Biologica de Mont everde. No forest debris was put inside the test arena to enha nce visual acuity of the lizards. Two lamps with 100-watt bulbs were clamped to the si des of the testing arena and metal hoods were used to direct heat and light down into the terrarium. To diminish outside distractions, I covered three terrarium side s with wooden planks, leaving one open so lizard behavior could be viewe d. For a prey source I used stock crickets (~200) from the nearby Frog Pond of Monteverde and kept them in an iden tical glass terrarium with cornmeal as food (ground surface). I used Sharpie paint pens to paint the crickets with patterns: unmodified, drab, classical aposematic, and novel. A control in sect was an unmodified cricket. To make sure that the paint on the crickets did not affect the lizards food preference, a second control insect painted black was tested in each trial. The two tr eatment insects were classically aposematic and novel, dependi ng on the color pattern s painted on them. Classical aposematic coloration is a commonl y used warning display that uses red, yellow, and black stripes (use d by coral snakes, milkweed bugs, tiger stripe butterflies etc.). Novel coloration was purple, green, a nd orange, simply because it is a coloration pattern not commonly seen, nor used by a posematic/chemically-protected species. Feeding Trials The two 100-watt bulbs were turned on te n minutes before the beginning of the first trial to allow time to heat up the terrar ium. Single lizards were moved to the test terrarium and remained there alone under the heat lamps for fifteen minutes so that they increase their body temperature. In all tria ls each lizard was presented with the drab, classical aposematic, and novel insects in random order. The unmodified control insect followed these insects to ensure that the lizard being tested was hungry throughout the trial, and any avoidance of prey was due to active discrimination. The first three color patterns were randomized us ing a standard die (rolling a one or two = drab, three or four = aposematic, and five or six = novel). The lizard was fed a new color pattern when it ate the insect, or after ten mi nutes, whichever came first. Six trials per individual were performed and in each of the six trial days all nine lizards were tested. The first three trial days were back to back, I soon changed this because the lizards appeared to be too satiated to participate in trials that frequently. In these trials a large portion of the lizards showed no interest whatsoever in the cric kets, no matter what type was presented. I staggered the later trials to be two or three da ys apart. Each trial began in the morning at about 0900 hours and lasted until early afternoo n. The lizards were not fed anything between trials. The frequency of each colo r pattern eaten or ignored was recorded. RESULTS 4

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0 5 10 15 20 25 30 35 40 DrabAposematicNovel Control Color Patterns Drab Aposematic Novel Control Fig. 1. The number of insects of each color pattern eaten by Sceloporus malachiticus throughout six trials. Crickets were treated with paint pens to create three different color patterns, and each lizard was presented with all three prey types in random order. Lizards were finally presented with an unmodified control insect to ensure lizards were hungry throughout the trial. There were no significant color pattern preferences (Friedman test, p = 0.0970, n = 9). See text for color pattern desi g nations. The S. malachiticus showed no significant preference in insect color patterns (Friedman test, p=0.0970, n = 9). In total, 34 drab prey were eaten, 31 classically aposematic prey were eaten, and 27 novel pr ey were eaten (Fig.1). Although there was slightly lower preference for novel and classi cally aposematic prey, the results were not significant. The only discernibl e pattern of foraging behavior was that the majority of the lizards remained stationary and would only stri ke an insect if it came very close to its head. This behavior seemed to be the onl y pattern governing when an insect would be eaten. The lizards would occasionally tilt their heads to take a closer look at prey, but there was no apparent behavioral differen ce between color types. There was also no apparent hesitation by the lizards when confr onting aposematic or novel prey; they were eaten in the same way as both c ontrols, and just as quickly. 5

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Lizard # Drab Aposematic Novel Control 1 3/6 5/6 2/6 5/6 2 5/6 1/6 3/6 4/6 3 5/6 5/6 6/6 6/6 4 4/6 4/6 3/6 4/6 5 5/6 5/6 4/6 5/6 6 1/6 0/6 0/6 1/6 7 6/6 4/6 4/6 5/6 8 4/6 4/6 3/6 4/6 9 3/6 3/6 2/6 3/6 Table1. Responses of individual lizards to crickets painted black (Drab) red-yellow-black (Aposematic), green-purple-orang e (Novel), and unmodified (Control). Unmodified Control insects were presented at the end of each trial to ensure the lizards were hungry throughout the trial. Values = (Number of insects eaten/Number of insects offered) There was also a high amount of variability in the behavior of the lizards over all the trials. Certain individuals ate a large amount of every color type (such as lizard # three) while some lizards, such as lizard # six, ate comparatively little (Table 1). Lizard # six in particular only ate duri ng the first trial and never agai n, even though the lizard was not fed in between trials. There was also a large amount of vari ation between lizards concerning how many of each color type we re eaten. Lizard # two ate only one aposematic bug, while # 3 ate five. From my observations, the lizards exhibited foraging behavior that could be best de scribed as lazy. In most cases the position of the insects as well as their movement in relation to the sta tionary lizard was the mo st important factor determining if or when an insect would be eaten. Because lizard s rarely chased and instead waited for insects to come very near individual insect colo r trials often required most of the allotted ten minutes. DISCUSSION The avoidance of aposematic prey items by S. malachiticus appears to have changed with age. There were no observed pr eferences in regard to aposematic prey, and there was also no observed neophobia. Perhaps the cost-benefit of avoidance behavior has changed with increased maturity, and the same prey defenses that drove innate aposematic prey avoidance in neonatal S. malachiticus no longer pose as much of a threat (Reznick et. al. 1981). Perhaps with maturity the lizards have eaten many prey items with defensive compounds, and due to an increased metabolic capacity to break down these compounds, foraging for aposematic as well as novel organisms is less likely to harm the lizard (Conney and Burns 1972). This lo wered risk allows the lizards to be less picky in what prey they choose to eat and in turn they benefit from a wider selection of possible prey items. It also may be possible that drab and familiar prey are not abundant enough to make choosiness profitable. Sin ce neophobia is especially prevalent when there is both novel and familiar food types presen t, perhaps predators cannot afford to be so picky in the absence of abundant familiar prey (Marples and Kelly 1999). Also, as 6

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mimicry is an important factor in anti-p redator defense, perhaps the abundance of aposematic but palatable prey (Batesia n mimics) is great enough that sampling aposematic individuals is beneficial. This woul d be especially true if the risks associated with sampling were lessened due to increased metabolic ability to break down chemicals. The loss of neophobia in mature individua ls seems to present a paradox. Some have argued that it is paradoxi cal that warning coloration c ould have evolved, when it is necessary that aposematism and a chemical defense must evolve at the same time in order for brightly colored individuals to survive. Unless those traits evolved simultaneously, which is unlikely, it seems as though apos ematic prey items would be far more vulnerable to predators than cryptic ones. Without chemical defenses, aposematic individuals would just be pa latable prey that are extrem ely obvious to predators, and hence their survival would be hard to understand. Both aposematism and chemical defense must be present in order for predator s to either learn to associate aposematism with unapalatability, or induce an innate avoida nce. However, with neophobia as a factor any novel organism could be avoided by predat ors long enough for it to reach fixation in a population, and thus aposematism could evolve (Thomas et. al. 2003, 2004, Sherratt 2002, Lindstrm et. al. 2001, Marples and Ke lly 1999). The loss of neophobia with age seems to provide some evidence against such an idea, and perhaps further study is necessary to examine the implications of age related changes in predator neophobia on the persistence of aposematic populations. For future studies I would suggest that the size of the test terrarium be smaller because normally the lizard and insect have to be very close to each other in order for the lizard to be interested enough to strike. Als o, a thermometer inside the test terrarium to be sure the temperature is about the same th roughout the trials. I do not believe that the results of the study would change with these additions, but they would help to make a more standardized testing procedure for the feeding trials. ACKNOWLEDGEMENTS I would like to thank the Estacion Biologica Monteverde for allowing me to conduct my project in the lower lab. I would like to thank my host fami ly, and especially Amabel is and Fabian Arguedas Ramirez for allowing me to take lizards off their property, and for just being really nice in general. I would especially like to thank TA Cam for feeding the lizards moths at times when I was unable to do so, and I would like to thank TA Tom McFarland for being such a badass, helping me make a thirty foot net, and helping me make a complete fool of myself catching lizards on the side of the biological station. I would like to thank Tania Pizarra for offering to kill me when my project was driving me crazy, I promise Ill repeat the favor someday. I would like to thank Alan Masters for helping me develop this project idea, playing the gut-bass, and singing I Wish I Was a Mole in the Ground very loudly and with much vigor. In thanks I offer Ellen Thompsons last kidney. Id like to thank my fellow Green Mountain Boys bluegrass band for giving me one of the best nights Ive ever had. Finally, I have all my CIEE amigos to thank for keeping me sane long enough to finish this project. LITERATURE CITED CONNEY, A.H. and J.J. Burns. 1972. Metabolic interactions among environmental chemicals and drugs. Science 178 4061:576-586 DUFFEY, S.S. 1970. Cardiac glycosides and distastefulness: Some observations on the palatability spectrum of butterflies. Science. Vol. 1690, 3940:78-79 7

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8FOX, R.A. and J.R. Millam. 2004. The effect of ear ly environment on neophobia in orange-winged amazon parrots ( Amazona amazonica). Applied Animal Behaviour Science 89 (1-2):117-129 FRANKS, DW. 2004. Warning signals and predator-prey coevolution Ed. J. Noble. Proceedings of the Royal Society of London Series B-Biological Sciences 271 1550: 1859-1865 FREELAND. W.J. and D.H. Janzen 1974. Strategies in herbivory by mammals: The role of plant secondary compounds. The American Naturalist 108 961:269-289 HEINRICH, B. 1988. Foodsharing in the raven, Corvus corax p. 285-311. In C.N. Slobodchikoff [ed.], The Ecology of Social Behavior Academic Press, New York LINDSTRM L., Rauno V. Alatalo, Anne Lyytinen and Johanna Mappes 2001. Predator experience on cryptic prey affects the survival of conspicuous aposematic prey. The Royal Society 357-361 MARPLES, N.M. and D.J. Kelly 1999. Neophobia and dietary conservatism: two distinct processes? Evolutionary Ecology 13:641-653 NELSON, A.L. 1934. Some early summer food preferen ces of the american raven in southeastern Oregon. Condor 35:10-15 PIETREWICZ, A.T. and Alan C. Kamil 1977. Visual detection of cryptic prey by blue jays ( Cyanocitta cristata ) Science Vol 195, 4278:580-582 REZNICK, D., O.J. Sexton, C. Mantis. 19 81. Initial prey preferences in the lizard Sceloporus malachiticus. Copeia, 3:681-686 RIESSEN, H.P. 1992. Cost-benefit model for the induction of an antipredator defense. The American Naturalist 140:349-362 SAPORITO, RA. 2004. Formicine ants: an arthropod source for the pumiliotoxin alkaloids of dendrobatid poison frogs Proceedings of the National Academy of Sciences of the United States of America .101 (21): 8045-8050 SAVAGE, J.M. 2002. The Amphibians and Reptiles of Costa Rica:A Herpetofauna between Two Continents, between Two Seas University of Chicago Press. SHERRATT, T.N. 2002 The coevolution of warning signals. The Royal Society. 13:741-746 SMITH, S. M. 1975. Innate recognition of coral snake pattern by a possible avian predator. Science 187:759-60 THOMAS R.J., Laura A. Barlett, Nicola M. Marples, David J. Kelly and Innes C. Cuthill 2004. Prey selection by wild birds can allow novel and conspicuous colour morphs to spread in prey populations. OIKOS 106: 285-294 ______, N. M. Marples, L.C. Cuthill, M. Takahash i and E. A. Gibson 2003. Dietary conservatism may facilitate the initial evolution of aposematism. OIKOS 101:458-466 YAMAMOTO M. E. and Fivia de Araujo Lopes 2004. Effect of removal from the family group of feeding behavior by captive Callithrix jacchus International Journal of Primatology, 25:489-500


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Prey use a variety of defenses against predators in order to avoid predation and often use warning coloration known as aposematism to advertise unpalatability to predators. Predators have accordingly evolved defenses against possibly unpalatable prey by being selective, and avoiding aposematically colored prey items. Some predators are more selective, avoiding anything appearing novel (neophobia), thus lowering the risk of unprofitable foraging by restricting their diet to familiar items. Previous studies have shown that neonatal Sceloporus malachiticus will innately avoid aposematic prey. In this experiment I examined any potential changes in prey selection concerning aposematic or novel prey items in S. malachiticus in Monteverde, Costa Rica. I used paint pens to create three different color patterns on crickets; drab, aposematic, and novel. I fed nine S. malachiticus these different treatments in random order over the course of six trials. I found that the lizards showed no apparent preference for any color type (Friedman test, p = 0.0970, n = 9), indicating a loss of dietary conservatism as mature adults.
Las presas utilizan una variedad de defensas contra los depredadores con el fin de evitar la depredacin y a menudo el uso de coloracin de advertencia conocido como aposematism para advertir inapetencia a los depredadores. Los depredadores por consiguiente han desarrollado posibles defensas contra las presas desagradables siendo selectivos, y evitando el color aposematic de las presas. Algunos depredadores son ms selectivos, evitando todo lo que parece nuevo (neofobia), reduciendo as el riesgo del forrajeo no rentable restringiendo su dieta a solo las cosas conocidas. Estudios previos han demostrado que neonatal Sceloporus malachiticus evitar innatamente a la presa aposematic. En este experimento, examin cualquier cambio potencial en la seleccin de presas referente a las presas aposematic o nuevas presas en S. malachiticus en Monteverde, Costa Rica.
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