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Discriminacin de la presa nueva y aposemtica por Sceloporus malachiticus
Discrimination of aposematic and novel prey by mature Sceloporus malachiticus
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.
Text in English.
Predator & prey
Warning coloration (Biology)
Depredador y presa
Lagartija de caon
Coloracin de advertencia
Tropical Ecology 2006
Ecologa Tropical 2006
t Monteverde Institute : Tropical Ecology
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 colo ration 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, avo iding 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 experim ent 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 adul ts. RESUMEN Las presas usan muchas tipos de defensas diferentes para evitar a los de predad ores, y muchas veces usan colores de advertencias en un sistema que se llama aposematismo para anunciar a los depredad ores que no son buenos para comer. Los depredadores tambiÃ©n ha n desarrollado defensas contra las presas tÃ³xicas; por ejemplo, son selectivos en los tipos de presas que eligen de comer, y evitan presas con colores de advertencias. Unos depredad ores son aÃºn mÃ¡s selectivos, y evitan todas las presas que les parecen nuevas neophobia, asÃ evitan do las presas que podrÃan ser tÃ³ xicas. Estudios previos han mostrado que Sceloporus malachiticus neonatales evitan innatamente las presas con colores de advertencias. En este experimento examinÃ© cambios en la selecciÃ³n de presas de S. malachiticus con presas aposemÃ¡ ticas o nuevas en Monteverde, Costa Rica. UsÃ© bolÃgrafos de pinturas para crear tres dibujos diferentes en grillos; negro, aposem Ã¡ tica, y nuevo. AlimentÃ© a nueve S. malachiticus con estos grillos diferentes en una orden alea toria por se is pruebas. EncontrÃ© que las la gartijas no mostraron ninguna preferencia para el tipo de color Friedman; p = 0.0970, n = 9 indicando una pÃ©rdida del conservatismo en las dietas como adultos. INTRODUCTION Predation is one of the most impor tant fitness affecting ecological factors; hence many anti predator defenses have evolved to combat this threat Riessen 1992. Organisms can be cryptic, such as phasmids which resemble twigs or leaves, or they can invest in mobility, such as flight, in o rder to escape predators Pietrewicz and Kamil 1977. Some organisms invest in mechanical defenses, such as rough surfaces or spines e.g. urticating hairs in caterpillars, and some invest in chemical defenses to make themselves distasteful. Danaus spp. for example use cardiac glycosides to confer unpalatability, inducing predators to vomit if they are eaten Duffey 1970. Organisms
2 can also use toxins to inflict serious harm on predators, such as Dendrobates spp. that produce alkaloid poisons excreted on their skin to make themselves toxic to predators Saporito 2004. Mechanical and chemical defenses are often coupled with warning coloration, also called aposematism, to advertise to predators that the prey is unrewarding to eat Sherratt 2002. In tu rn, 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 cryptic prey that do not invest in chemical or mechanica l defenses Franks 2004, Sherratt 2002. Such avoidance of aposematism can be either learned or innate Reznick et. al.1981. Prey may induce learned avoidance in predators by being distasteful and emetic, e.g. Danaus spp. requiring a predator to try th e prey item at least once before the predator learns to avoid that prey item Duffey 1970. Some predators exhibit an innate avoidance to prey items, usually exhibited in response to lethal prey. One example is Turquoise browed Motmots Eumomota supercil iosa , which have shown an innate avoidance 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 conservative strategy by avoiding a ll novel food types, a type of neophobia Thomas et. al. 2004. Often it is not cost effective for predators to risk trying a new and potentially toxic prey item, 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 novel, 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 the level of neophobia as adults, since the more exposure to novel food types, the more familiar they become. Orange winged Amazon Parrots Amazona amazonica show differences in the level of neophobia according to the amount of novel objects to which th ey 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 indi viduals to metabolize toxic compounds. Mammals, for example are able to increase the capacity of their detoxification 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 had more exposures to chemicals than young individuals, and hence have greater 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.
3 Three day old S. malach iticus 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 diff erent ages three days, 18 30 days, 45 61 days, and wild caught adults were split up into two 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 blac k. Group B were presented with dermestid beetles, one painted black and the other with 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 preference hypothesis was to see if the differences in selection were due to characteristics other than color, which was tested by comparing how readily the lizards attacked milkweed bugs versus dermestid beetles. Although the results were not sig nificant for either the color preference or insect preference test, invariably a larger number of lizards attacked the black insect first. In testing the insect preference hypotheses, they found that each of the three captive born subjects attacked t he 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 characteristics Reznick et. al 1981. Sceloporus malachiticus have exhibited innate avoidance of aposematic colored prey at an early age, but it is not known whether 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 whether the innate aposematic avoidance of S. malachiticus is maintained in adult individuals, and also whether the avoidance of these colorations is actually a more conservative and general 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 zo nes of Central America. They are heliothermic, and with high temperature or light they are seen as bright green with turquoise tails, but with lower 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 EstaciÃ³n BiolÃ³gica de Monteverde, 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.
4 Experimental Set Up The nine S. malachiticus obtained were kept in fi ve 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 d ishes 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 Est aciÃ³n BiolÃ³gica de Monteverde. No forest debris was put inside the test arena to enhance visual acuit y of the lizards. Two lamps with 100 watt bulbs were clamped to the sides 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 sides with wooden pla nks, leaving one open so lizard behavior could be viewed. For a prey source I used stock crickets ~200 from the nearby Frog Pond of Monteverde and kept them in an identical glass terrarium with cornmeal as food ground surface. I used Sharpie paint p ens to paint the crickets with patterns: unmodified, drab, classical aposematic, and novel. A control insect was an unmodified cricket. To make sure that the paint on the crickets did not affect the lizards food preference, a second control insect painte d black was tested in each trial. The two treatment insects were classically aposematic and novel, depending on the color patterns painted on them. Classical aposematic coloration is a commonly used warning display that uses red, yellow, and black s tripes used by coral snakes, milkweed bugs, tiger stripe butterflies etc.. Novel coloration was purple, green, and orange, simply because it is a coloration pattern not commonly seen, nor used by aposematic/chemically protected species. Feeding Trials The two 100 watt bulbs were turned on ten minutes before the beginning of the first trial to allow time to heat up the terrarium. Single lizards were moved to the test terrarium and remained there alone under the heat lamps for fifteen minutes so that t hey increase their body temperature. In all trials 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 hung ry throughout the trial, and any avoidance of prey was due to active discrimination. The first three color patterns were randomized using a standard die rolling a one or two = drab, three or four = aposematic, and five or six = novel. The lizard was fe d a new color pattern when it ate the insect, or after ten minutes, 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 change d 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 crickets, no matter what type was presented. I staggered the later trials to be two or three days apart. Each trial began in the morning at about 0900 hours and lasted until early afternoon. The lizards were not fed anything between trials. The frequency of each color pattern eaten or ignored was recorded.
5 RESULTS 0 5 10 15 20 25 30 35 40 Drab Aposematic Novel Control Color Patterns Total Number of Prey Eaten Drab Aposematic Novel Control 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 prey were eaten Fig.1. Although there was slightly lower preference for novel and classically aposematic prey, the results were not significant. The only discernible pattern of foraging behavior was that the majority of the lizards remained stationary and would only strike an insect if it came very close to its head. This behavior seemed to be the only 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 difference between color types. There was also no apparent hesitation by the lizards when confronting aposematic or novel prey; they were eaten in the same way as both controls, and just as quickly. 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 p rey 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 patt ern designations.
6 There was also a high amount of variability in the behavior of the lizards over all the t rials. 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 during the first trial and never again, even thou gh the lizard was not fed in between trials. There was also a large amount of variation between lizards concerning how many of each color type were eaten. Lizard # two ate only one aposematic bug, while # 3 ate five. From my observations, the lizards ex hibited foraging behavior that could be best described as lazy. In most cases the position of the insects as well as their movement in relation to the stationary lizard was the most important factor determining if or when an insect would be eaten. Becaus e lizards rarely chased and instead waited for insects to come very near, individual insect color trials often required most of the allotted ten minutes. DISCUSSION The avoidance of aposematic prey items by S. malachiticus appears to have changed with a ge. There were no observed preferences 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 pre y 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 compou nds, foraging for aposematic as well as novel organisms is less likely to harm the lizard Conney and Burns 1972. This lowered 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 pos sible prey items. It also may be possible that drab and familiar prey are not abundant enough to make choosiness profitable. Since neophobia is especially prevalent when there are both novel and familiar food types present, perhaps predators cannot afford to be so picky in the absence of abundant familiar prey Marples and Kelly 1999. Also, as 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 orange 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
7 mimicry is an important factor in anti predator defense, perhaps the abundance of aposematic but palatable prey Batesian mimics is great enough that sampling apo sematic individuals is beneficial. This would 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 individuals seems to present a paradox. Som e have argued that it is paradoxical that warning coloration could 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 si multaneously, which is unlikely, it seems as though aposematic prey items would be far more vulnerable to predators than cryptic ones. Without chemical defenses, aposematic individuals would just be palatable prey that are extremely obvious to predators, and hence their survival would be hard to understand. Both aposematism and chemical defense must be present in order for predators to either learn to associate aposematism with unapalatability, or induce an innate avoidance. However, with neophobia as a f actor any novel organism could be avoided by predators long enough for it to reach fixation in a population, and thus aposematism could evolve Thomas et. al. 2003, 2004, Sherratt 2002, LindstrÃ–m et. al. 2001, Marples and Kelly 1999. The loss of neophobi a 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 sugg est 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. Also, a thermometer inside the test terrarium to be sure the temperatu re is about the same throughout 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 t hank the Estaci Ã³ n Biol Ã³ gica Monteverde for allowing me to conduct my project in the lower lab. I would like to thank my host family, and especially Amabelis 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 I ll 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 Thompson s last kidney. I d like to thank my fellow Green Mountain Boys bluegrass b and for giving me one of the best nights I ve 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 che micals 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
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