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Comportamiento defensivo maternal de los salta hojas Ataliba Umbonia
Maternal defensive behavior of Umbonia ataliba Treehoppers
A population of Umbonia ataliba (Homoptera: Membracidae) located between 1300 and 1500 m in Monteverde, Costa Rica was studied from October to November 2006. The maternal defensive behavior exhibited by these subsocial insects toward nymphs of different developmental stages was experimentally investigated. The purpose of my study was to determine how the defensive behavior changed from eggs to adults and in response to two different predator types. I attached dead wasps to long wooden sticks and then simulated predator approaches toward family groups of eggs, second instar and fourth instars nymphs. I found that the defensive behavior by females guarding nymphs of different ages differed from random in type and frequency. I determined that female parents with second instars were the most aggressive, and that the most common behavior type among all groups proved to be kicking. In regards to the behavior changes exhibited against predator types, females were generally more aggressive when approached with the black wasp, but there was no significant change in the frequency of behaviors.
Estudie de octubre a noviembre del 2006 una poblacin de Umbonia ataliba (Homoptera: Membracidae), ubicado entre los 1300 y 1500m en Monteverde, Costa Rica. Estudie la conducta defensiva maternal en las diferentes etapas de desarrollo de las ninfas. El propsito de mi estudio fue determinar como la conducta defensiva cambia de los huevos a adultos y en respuesta a dos tipos diferentes de depredadores.
Text in English.
Tropical Ecology 2006
Maternal defensive behavior
Ecologia Tropical 2006
Comportamiento defensivo maternal
t Monteverde Institute : Tropical Ecology
1 Maternal Defensive Behavior of Umbonia ataliba Treehoppers Sarah Anvik Department of Environmental Studies College of Arts and Sciences University of Colorado, Boulder ABSTRACT A population of Umbonia ataliba Homoptera: Membracidae located between 1300 and 1500 m in Monteverde, Costa Rica was studied from October to November 2006. The maternal defensive behavior exhibited by these subsocial insects toward nymphs of different developmental stages was experimentall y investigated. The purpose of my study was to determine how the defensive behavior changed from eggs to adults and in response to two different predator types. I attached dead wasps to long wooden sticks and then simulated predator approaches toward fam ily groups of eggs, second instar and fourth instar nymphs. I found that the defensive behavior by females guarding nymphs of different ages differed from random in type and frequency. I determined that female parents with second instars were the most a ggressive, and that the most common behavior type among all groups proved to be kicking. In regards to the behavior changes exhibited against predator types, females were generally more aggressive when approached with the black wasp, but there was no sign ificant change in the frequency of behaviors. RESUMEN Estudie un poblaciÃ³n de Umbonia ataliba Homoptera : Membracidae localizada entre de 1300 y 1500 m en Monteverde, Costa Rica de Octubre a Noviembre 2006. Estudie la conducta defensiva maternal en las diferentes etapas de desarrollo de las nintas. El propÃ³sito de mi estudio fue a determinar como la conducta defensiva cambia de huevos a adultos y en respuesta a dos diferentes depredadores. ConcretÃ© avispas muertas a palos de madera y simulÃ© el acercamiento del depredador en grupos familiares de la madre con huevos y nintas a diferentes edades. EncontrÃ© que la conducta defensiva de las hembras al proteger las ninfas, difiere de aleatoria en tipo y frecuencia . Determin Ã© que madres con ninfas en segundo estado de desarrollo son las mÃ¡s agresivas, y el tipo de conducta mÃ¡s comÃºn entre todos grupos fue patear. ConsiderÃ³ que la conducta exhibida contra los de predadores difiriÃ³ porque las hembras estaban mÃ¡s agresiva se ac ercÃ³ una avispa negra, pero con el cambio en la conducta no fue significativo.
2 INTRODUCTION Females of the genus Umbonia are semelparous, with the ability to produce only one brood of young in their lifetime. Different types of maternal behavior make them subsocial insects. According to Tallamy and Wood 1986 subsocial behavior is the most primitive level of social interaction involving parents and offspring. Subsocial behavior of treehoppers, including Umbonia , is restricted to maternal care of eg gs and nymphs Chung Ping et al. 2004. Egg guarding is the most common form and is defined as the female remaining on top of the egg mass for a period of time after oviposition. In this case the body of the female is used as a shield to protect her youn g from predation and parasitism Chung Ping et al. 2004. According to Zink 2003, guarding behaviors are important for the protection and survival of eggs. In U. ataliba sibling s are reared together under the care of the mother who embeds 50 100 eggs into the branch tip of the host plant Mimosaceae and then tends the offspring throughout development Masters 2000. The development stages include eggs, nymphs and adults. Egg development is lengthy and usually lasts about 40 days Masters 1994. Nym ph development, in which the young mature from first to fourth instars, lasts approximately 44 days Masters 1994. The mother will remain with her young until they reach adulthood. Since the female is semelparous, her investment in the brood is extremely high and thus she exhibits several types of parental care. Tallamy 1983 describes parental care as any parent offspring interactions that promote the survival, growth, and development of immature insects. Two types of parental care exhibited by female s of this species include behaviors that physically protect the young from danger and those that facilitate offspring feeding. Following egg guarding the mother drills a series of slits in a spiral around the branch tip using her ovipositor Wood 1973. When the nymphs hatch they cluster around the slits, which facilitate access to the plants vascular tissue. The nymphs remain in this aggregation around the plantÂ€s host stem with the mother positioned below Cocroft 1999. The placement of the mother a nd the nymphs are essential in allowing the mother to provide another type of parental care, physical. Maternal defensive behavior in Umbonia is crucial for the survival of the brood as they are vulnerable to a number of invertebrates and are highly preye d upon. Their most common predators are wasps, and in Monteverde, assassin bugs Reduuvidae are common as well. In the case of Umbonia crassicornis wasps approach family groups from the air and land on or near the aggregation, attempting to remove nymph s through biting and then pulling them from the branch Cocoroft 2002. In order to protect the brood, the femaleÂ€s defenses have become extremely specialized and include behaviors such as kicking, wing fanning and running towards the predators. These ac tions are often effective in deterring predators and therefore increase the survival of the brood. Visual and chemical stimuli are both important in allowing the mother to sense predators and actively defend her young Wood 1975. A study by Wood 1973 on U. crassicornis showed that when a brood was left without the mother, 100% of them died within ten days. Maternal defense is therefore important for both eggs and developing nymphs. The purpose of my project was to observe and compare the motherÂ€s pro tective behavior from eggs to adults in U. ataliba . As the nymphs age, they occupy more space on the branch, making it increasingly difficult for the mother to defend them. At the
3 same time, the nymphs become better suited to defend themselves. My hypot hesis is that the mother will defend her brood through all developmental stages but that the effectiveness of the behaviors will vary. My prediction is that the frequency of defensive behavior types will differ as the nymphs age. METHODS AND MATERIALS S tudy site My study was conducted on a fallow pasture at approximately 1500 m in Monteverde, Costa Rica from October to November 2006. Ten years ago, trees of family Mimosaceae known host were planted on this land and occupy much of the property. Many o f the tree species, such as Inga punctata are clumped, with up to four individuals in close proximity of each other, while others are solitary, such as Zygia palmanum . Tree species suitable for examination included Zygia palmanum, Inga punctata, Inga sierra e and Cojoba costaricensis . Group location Umbonia ataliba groups were located on branch tips of Mimosaceae trees and covered with mesh bags. This ensured that the groups would be safe from predation. Groups were monitored for nymph maturation. Defens ive behavior experiment Mothers with eggs, second instars and fourth instars were tested for defensive behaviors against simulated black and yellow wasps, both known predators. In order to test the maternal defensive behaviors, it was necessary to imitate incoming predators. To accomplish this, I first collected a dozen dead wasps, half of them black and half of them yellow. I then carefully attached each of the wasps to the pointed end of a long wooden sticks using super glue. I always glued the stick to the underside of the abdomen, leaving the wasps unaltered on the top to create a more realistic appearance. In order to test the femaleÂ€s behavior, certain abiotic factors were necessary including warm temperatures without direct precipitation; these c onditions increased the likelihood of the female displaying active responses. A good indicator of a favorable testing day was the presence of active butterflies. As I approached the group with the wasp, I would gently wiggle the stick in order to simulat e the appearance of a flying wasp. The group was approached from both the front and the rear, and the wasp was moved up and down the branch. The wasp was brought close enough to the female and the group for direct contact to take place. I tested each gr oup for two minutes; making tallies next to the demonstrated behaviors. In order to give the female a chance to respond, I allowed her to show a behavior at least five times before stopping to record the data. After two minutes had passed, I made final t allies and re covered the group. In order to minimize infection, I removed any dead leaves or debris from the mesh bag before placing it over the branch, being careful not to disturb the mother or the young. With each group I ran tests in a similar fash ion, noting environmental conditions and predator type before I began. The five types of behavior I tested for were kicking, fanning, running, covering and tilting by nymphs Table 1. Each family group was tested for these behaviors on two separate occas ions, once with the black and once with the
4 yellow wasp. The order of testing varied; some groups were approached with the black wasp first and others with the yellow. Statistical Analysis A 3x6 contingency table was constructed and examined with a Goodn ess of fit test; used to analyze maternal defensive behavior against two predator types. Running behavior was not included in the analysis because it never occurred more than once for any developmental age and for some groups it never occurred at all. Th e tilting behavior is mainly a defense of the nymphs and not of the mother, and hence it was analyzed separately. A Goodness of fit test was then used to analyze the frequency of demonstrated maternal behaviors. A Chi squared test of independence was als o run to determine if females are more aggressive overall towards a particular wasp color morph. RESULTS Among the four species of the family Mimosaceae examined for this project, individual females were found on Z. palmanum and I. sierrae , but family gr oups were only present on I. punctata . I studied 33 different females and their families. The difference in observed versus expected values was significant as it differed from random Goodness of fit test, Ã°c 2 = 131.696, p < 0. 0001, df=10 Fig.1. This indicates that the frequency of the motherÂ€s behavior deviates from random. Defense of eggs, second instars and fourth instars For females with eggs, the most common type of behavior was kicking with 97 yellow and 106 black occurrences, followed by f anning 4 and 3 respectively. Mothers with eggs more often than expected by random, whereas the frequency of fanning is lower than expected by random Figure 2 Next, mothers with second instar nymphs also favored kicking, exhibiting this behavior 134 y ellow and 154 black times. However, the expected value for kicking was less than actually observed. By contrast, mothers with second instars fanned and covered more than expected, showing more occurrences of covering 43 and 56 than fanning 26 and 3 6 Fig.2. Finally, mothers with fourth instar nymphs also demonstrated kicking more than any other defensive behavior, demonstrating it 98 times with the yellow and 121 times with the black wasp. Covering was rare for mothers with this age, who showed t his type of behavior only once for both predator types. Similarly, the mothers did not choose to fan very often, although the numbers are significantly higher for fanning than expected by chance Fig. 1. Also interesting to note is the high number of ti lting behavior examined by the nymphs of this age Table 2. Although tilting is a behavior of the nymphs rather than adults, I compared its frequencies and found that it too differed in frequency from one developmental stage to the next. Defensive beh avior The defensive behavior most common among all group ages was kicking Fig. 3. Kicking behavior occurred at the highest frequency with second instar groups, followed by mothers with fourth instars and lastly individuals with eggs. Covering was the next
5 most common behavior and was only used with seconds, followed by fanning, also used mainly for seconds Fig. 3. These examinations allowed for the conclusion that mothers with second instar nymphs are the most aggressive of all mothers tested. The t otal number of defensive behaviors exhibited by the mothers for eggs, second instars and fourth instars were 212, 449, and 256 respectively. Responses to Black versus Yellow Wasp Females respond to black and yellow wasps with the same frequency of defense behaviors. However, the Chi squared test of independence revealed that mothers are overall more aggressive toward black wasps than they are toward yellow wasps showing significance at the .05 level Ã°c 2 =8.27, df=1 Figure 4. DISCUSSION My hypothesis f or this study was that the mother would defend her brood through all developmental stages but that the effectiveness of different defense behaviors would vary. Thus my prediction was that the frequency of defensive behavior types would differ as the nymph s aged. My prediction was confirmed in this experiment, thus supporting my hypothesis. As predicted, female parents guarded their brood through all stages of development. This is explained by the fact that the mother is semelparous and the survival of t he young depends on her. In treehopper species that lay only one clutch, the cost of remaining with the brood are expected to be so minimal that the female should always display extended care Zink 2003. I also found that the mothersÂ€ behaviors varied t hroughout nymphal developmental stages because some behaviors were more effective than others in deterring predators. For example, covering is not as effective of a behavior for fourth instars as it is for seconds because the nymphs at this age are too la rge, making it difficult and time consuming for the mother to carry out this behavior. Although the frequency of different behaviors changed with the age of the nymphs, kicking was the most common behavior overall. In this study, I found that females wit h eggs showed the least amount of response and movement when approached by a predator. In the case of U. crassicornis , Wood 1983 believes that lack of movement enhances cryptic coloration and reduces the vulnerability of parent females while guarding eg gs. The main behavior exhibited by mothers with eggs proved to be kicking, with some fanning. The frequency of behaviors shown in this age group is likely due to their position on the branch. In the later stage, mothers with second instars proved to be very aggressive. They favored kicking over other behaviors followed by covering and then fanning. Mothers with second instars were the only groups to exhibit covering behavior multiple times during a single test. This change in frequency can be attribute d to the effectiveness of behaviors used. Although kicking is the most effective when the predator is nearby, when the predator is not within reach, other behaviors must be used. Due to the size and vulnerability of nymphs at this age, covering appears t o be a quite effective and easily accomplished way of protecting the brood from predator invasion. The final groups, fourth instars are unique in that they too act to defend themselves against predators, mostly by tilting. However, when looking solely a t maternal defensive behavior, I found that as with other groups, mothers chose to kick
6 more than anything else. The next highest frequency of behavior observed was fanning. This can be explained using a study on U. crassicornis , which found direct movem ent to be the most effective, followed by fanning, which provides defense without movement toward the predator Wood 1974. Based on this evidence, it can be concluded that mothers show varied defensive behaviors to be effective at deterring predators. M y study is unique in that is the first to compare behavior between developmental stages in Umbonia . Similarly, it is the first to test for different responses toward predators of different types. Although significant results were not found for a change i n frequency of behavior between predators, the females prove to be more aggressive toward the black wasp; although it is unknown exactly why. Some types of black wasps in Monteverde are known to be parasites, though the ones used in the study are not. It is possible that the females act more aggressively because they perceive these wasps as being parasitic; however, this proposal is extremely difficult to prove. In future studies, it would be interesting to include reduuvid bugs as predators. Unlike was ps, which approach from the air, these insects approach the group by walking toward them on the branch. Also, if time allowed, it would be helpful to track the same groups throughout developmental stages to see how behavior changed for that specific femal e. These kind of data would allow for a more detailed analysis, although similar results would likely be obtained. ACKNOWLEDGEMENTS I would like to first of all thank Karen Masters for suggesting this idea for a project. Her assistance, encouragement, motivation and common love for this unique insect have helped to guide me through the research process and allowed me to be successful with my project. At times when I was frustrated and ready to give up, she pushed me to keep going and try harder. Witho ut this I would not have made the progress I did in this short span of time. I also want to thank Alan Masters for supporting my ideas and talking me through my frustrations. Next, I would like to thank Tom and especially Camryn for being awesome TAÂ€s an d helping me work through issues with research, proposals and figures. Your help is extremely appreciated and without it I would have lost endless hours of my life attempting to sort through the inter workings of Excel and Stat View. Finally, I want to t hank my best friend Katie Korus for always being supportive. Without her constant willingness to listen and lend a hand or a hug, I never would have made it through all of this. LITERATURE CITED Chung Ping, Lin, Danfourth, Bryan N. & Wood, Thomas K. 200 4. Molecular phylogenetics and evolution of maternal care in membracid treehoppers. Systematic Biology 53:400 426. Cocroft, Reginald B. 1998. Offspring parent communication in a subsocial treehopper Hemiptera: Membracidae: Umbonia crassicornis. Behavior 136:1 21. Cocroft, Reginald B. 2002. Antipredator defense as a limited resource: unequal predation risk in broods of an insect with maternal care. Behavioral Ecology 13:125 133.
7 Hernick, Charles A. 2001. ÂDistribution of Host Species Ranges of Umbonia ata liba and Umbonia crassicornis and the Potential for Interspecific Competition.Â‚ In CIEE Fall 2001 Tropical Ecology and Conservation , pp. 25 33. Masters, Karen L., Masters, Alan R. & Forsyth, A. 1994: Female biased sex ratios in the neotropical treehopper U mbonia ataliba Homoptera: Membracidae. Ethology 96: 353 366. Masters. Karen L. 2000. Sex and Social Life of Umbonia Treehoppers. In: Monteverde: Ecology and Conservation of a Tropical Cloud Forest . Nadkarni, N.M. and N.T. Wheelwright eds. Oxford Univers ity Press, New York, New York, pp. 103 104. Tallamy, Douglas W. 1983. Insect Parental Care. BioScience 34:20 24. Tallamy, Douglas W. and Wood, Thomas K. 1986. Convergence patterns in subsocial insects. Annual Reviews of Entomology 31:361 390. Wood, T.K. 1973. Aggregating Behavior of Umbonia crassicornis Homoptera: Memracidae. Canadian Entomologist 106:169 173. Wood, T.K. 1974. Alarm Behavior of Brooding Female Umbonia crassicornis Homoptera: Memracidae. Annals of the Entomological Society of America 69:340 344. Wood, T.K. 1983. Umbonia crassicornis Bicho Espino, Thorn Bug, Treehopper. In: Costa Rican Natural History , D.H. Janzen, ed. The University of Chicago Press. Chicago, Illinois, pp. 773 775. Zink, Andrew G. 2003. Quantifying the costs and ben efits of parental care in female treehoppers. Behavioral Ecology 14:687 69
8 0 20 40 60 80 100 120 140 160 180 kicking fanning covering Behavior Types Frequency of Occurences Mom with eggs Mom with 2nd Mom with 4th 0 20 40 60 80 100 120 140 160 kicking fanning covering Behavior Types Frequency of Occurences Mom with eggs Mom with 2nd Mom with 4th Figure 1: The frequency of defensive behaviors kicking, fanning and covering exhibited by the moth er in response to the black wasp A and the yellow wasp B across three developmental stages. Asterisks indicate an observed behavior which deviated from random A B * * * * * * * * * * * *
9 Figure 2: The frequency of behavioral occurrences between developmental stages. This grap h demonstrates the aggressiveness of mothers with second instar nymphs compared to other developmental age groups. 0 100 200 300 400 500 600 700 800 kicking fanning covering Defensive Behaviors Number of Occurences Mom w/4th Mom w/2nd Mom w/eggs Figure 3: The frequency of observed behaviors occurring across developmental stages. This graph demonstrates that the most common observed behavior is kickin 0 50 100 150 200 250 300 350 400 450 500 Mom w/eggs Mom w/2nd Mom w/4th Developmental Stages Number of Occurences covering fanning kicking
10 0 100 200 300 400 500 600 Black wasp Yellow wasp Predator type Total number of defensive behaviors # of defensive behaviors Figure 4: The total number of observed maternal defensive behaviors exhibited in response to black and yellow wasps. Females showed more aggressive behaviors toward the black wasps than the yellow wasps. Table 1: Descriptions of defensive behavior types Behavior Description Kicking Fanning Running Covering Took place when the mother was close enough to the predator to touch the wasp with one of her hind legs Took place at various proximities, consisted of mother aggressively fluttering her wings Took place when the wasp was to on the opposite side of mother, and she quickly move from the terminal end of the branch toward it Took place when predator was out of range for physical contact, consisted of her inching along the branch, positioning herself on top of the nymphs Took place when nymphs attempted to defend themselves by lifting their abdomens in a synchronized wave Tilting
11 Table 2: Tilting behavior examined over three developmental stages with two predator types Yellow and Bl ack wasps. Eggs Black Seconds Black Fourths Black Eggs Yellow Seconds Yellow Fourths Yellow Tilting 0 2 58 0 4 62