Captive breeding causes small body size in Morpho peleides limpida (Nymphalidae: Morphinae)


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Captive breeding causes small body size in Morpho peleides limpida (Nymphalidae: Morphinae)

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Captive breeding causes small body size in Morpho peleides limpida (Nymphalidae: Morphinae)
Translated Title:
La cría en cautiverio causa el tamaño corporal pequeño en Morpho peleides limpida (Nymphalidae: Morphinae)
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Goldish, Danny
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Text in English

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Morpho peleides ( lcsh )
Inbreeding ( lcsh )
Endogamia ( lcsh )
Butterflies ( lcsh )
Mariposas ( lcsh )
Costa Rica--Puntarenas--Monteverde Zone
Costa Rica--Puntarenas--Zona de Monteverde
CIEE Spring 2009
CIEE Primavera 2009
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Reports

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Abstract:
Captive breeding has many positive implications in terms of conservation, but when practiced irresponsibly, can result in harmful consequences like inbreeding. Inbreeding has been shown to result in developmental instabilities like small body size and fluctuating asymmetry. In this study, I used small body size as a proxy for inbreeding by comparing measurements of the butterfly Morpho peleides limpida from wild and captive bred populations in terms of right forewing and right antennae length. Both measures of size were found to be larger in wild populations than captive populations. The greatest variation in the means was observed in female right wing measurements, with larger mean lengths in wild populations (76.99mm ± 4.23mm) compared to captive populations (66.58mm ± 2.10mm). This shows that rearing techniques used in butterfly gardens may invoke varying amounts of inbreeding. New measures must be taken to practice more responsible breeding such as ensuring the introduction and maintenance of more genetic variation in captive populations. ( , )
Abstract:
La cría en cautiverio tiene muchas implicaciones positivas en términos de conservación, pero cuando la practican con irresponsabilidad, puede resultar en consecuencias dañinas como la endogamia. Se ha demostrado que la endogamia puede resultar en inestabilidades en el desarrollo como un cuerpo pequeño y asimetría fluctuante. En este estudio, yo usé el cuerpo pequeño como un aproximado de endogamia comparando medidas del largo del ala derecha y el largo de la antena.
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Student Affiliation: College of Biological Sciences, University of Minnesota
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M39-00110 ( USFLDC DOI )
m39.110 ( USFLDC Handle )

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1 Captive breeding causes small body size in Morpho peleides limpida Nymphalidae : Morphinae Danny Goldish College of Biological Sciences, University of Minnesota A BSTRACT Captive breeding has many positive implications in terms of conservation, but w hen practiced i rresponsibly, can result in harmful consequences like inbreeding . Inbreeding has been shown to result in developmental instabilities like small body size and fluctuating asymmetry. In this study, I use d small body size as a proxy for inbr eeding by comparing measurements of the butterfly Morpho peleides limpida from wild and captive bred populations in terms of right forewing and right antennae length . Both measures of size were found to be larger in wild populations than captive populatio ns. The greatest variation in the means was observed in female right wing measurements, with larger mean lengths in wild populations 76.99mm ð± 4.23mm compared to captive populations 66.58mm ð± 2.10mm. This shows that rearing techniques used in butterf ly gardens may invoke varying amounts of inbreeding . N ew measures must be taken to practice more responsible breeding such as ensuring the introduction and maintenance of more genetic variation in captive populations. R ESUMEN La c ría en cautiverio tiene muchas implicaciones positivas para conservacion, p ero cuando la practican con irre sponsabilidad, puede resultar en consequencias dañinas como endogamia. La e ndogamia puede resultar en inestabilidades en el desarrollo como un cuerpo pequeño y asimetría f luctuante . En esto estudio, yo usé el cuerpo pequeño como un aproximado de endogamia comparando medidas del largo del ala derecha y el largo de la antena . La s dos medidas de tamaño fueron mayores en las mariposas Morpho peleides limpida en la naturaleza. La mayor diferencias observada s fue ron en las ala s derechas de las hembra , siendo mas grandes en la naturaleza 76.99mm ð± 4.23mm comparado con las de cautiverio 66.58mm ð± 2.10mm. Esto muestra que métodos utilizados en cautiverio puede n causar endoga mia. Se necesitan técnicas má s responsables para la crianza, como la introducción y man tenimiento de la diversidad gené tica en poblaciones en cautiverio . I NTRODUCTION Captive breeding, when practiced correctly, can help to maintain fitness and divers ity in populations Balmford 1996, and has been the difference between survival and extinction in many endangered species populations Derrickson et al. 1992, Jones et al. 1995 , Snyder et al. 1996. A unique example of breeding in captivity is in the cas e of butterfly gardens, as they have different goals in mind. Butterfly gardens use poor rearing techniques to maximize profits, which often result in inbreeding. This is seen by certain gardens breeding over 100 generations of butterflies without the in troduction of new genes Lewis et al. 2001 . Inbreeding causes a magnification of homozygosis , while also making rare alleles more rare Barber 2002. Homozygotes tend to have lower fitness than heterozygotes Barber 2002, Reed et. al 2003, Saccheri 199 6 . In addition,

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2 larger population sizes and high genetic variation are correlated with higher fitness Joron and Brakefield 2003, Reed et. al 2003. Inbreeding works with genetic drift to decrease genetic diversity in a population, and usually results in inbreeding depression Barber 2002. Because butterfly gardens tend to have inbreeding and therefore greater homozygosis , small population sizes, and low genetic variation, they should also exhibit lower fitness. Evidence of this is seen by an increas ed extinction rate in inbred populations of fruit flies and mice Milius 1998. Inbreeding in captive populations has been found to cause asymmetry and reduced body size in progeny Clarke 1995 , Milius 1998. Fluctuating asymmetry is known as nondirect ional variation between left and right sides of the body, or deviations from perfect bilateral symmetry Breuker et al. 2003, Palmer et al. 1986, VanValen 1962. Deviations from bilateral symmetry and reduction in antennae and wing size are important dete rminants of butterfly fitness. Antennae size is critical for pheromone and food sensing as well as flight balance, whereas reductions in wing size are important in terms of flight aerodynamics DeVries 1987. Increases in fluctuating asymmetry are though t to be negatively correlated with heterozygosis Gomendio et al. 2000, and therefore correlated with inbreeding. It is assumed that identical genes affect bilateral symmetry Clarke 1995, but asymmetry can also result from developmental stress Breuke r et al. 2003. Lewis et al. 2001 found that captive bred populations of the butterfly Pieris brassicae had smaller wings and lower wing aspect ratios. However, in addition to inbreeding depression, food quality may also have a negative impact on butte rflies Cassel 1999. This means gardens with poor quality food may have smaller butterflies as a result. However, past studies on Drosophila populations have found great reductions in wing size solely due to inbreeding Robertson and Reeve 1952, Lewis e t al. 2001, Wright 2007, showing that small wing size can be used as a proxy for inbreeding. T he aim of this study is to compare size reduction in captive bred populations to wild populations in Morpho p eleides limpida, a large butterfly in Costa Rica D eVries 1987. Decrease in size will be used as a proxy to measure inbreeding and other developmental stresses associated with butterfly gardens. M ETHODS S TUDY S PECIES . ¾ Morpho peleides limpida is a large butterfly common on the Atlantic and Pacific slope of Costa Rica DeVries 1987. Because it is large, variations in size were greater and easily observed. There is sexual dimorphism; the female is generally larger than the male and has a wider black margin DeVries 1987. Also, males fly from early mor ning to midday, whereas females are seen flying only around midday DeVries 1987. I used these behavioral and morphological differences, along with the fact that the male€s claspers can be extruded with gentle pressure to produce a smell like vanilla De Vries 1987, to sex the butterflies. S TUDY S ITE . ¾ This study was carried out in Monteverde, Costa Rica, from April 26 th to May 6 th 2009. I captured and measured captive M. peleides butterflies at the Monteverde Butterfly Garden, and compared them to wild individuals captured near the Creativa School in Cerro Plano and the San Luis Río Bruja de Monteverde.

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3 Creativa is located at around 1500 m elevation, whereas Río Bruja is around 1100 m elevation. All wild capturing sites were along roadsides near fores t fragments. The M. peleides butterflies from the Monteverde Butterfly Garden were sampled from Garden One, which is protected from rain, but wind my affect ambient temperature. M EASUREMENT . ¾ While collecting data on butterflies in captivity, I avoid ed resampling by keeping all captive individuals in wax envelopes until all sampling was complete. Wild butterflies were marked with a red paint pen on the dorsal side of the abdomen, to allow future recognition. Right forewing measurements were taken fro m the distance of the basal area to the tip of the apex, as described by DeVries 1987 Fig. 1A, and right antennae length was measured from the head to the tip of the antennae DeVries 1987 Fig. 1B. All measurements were taken with a caliper in milli meters to the nearest tenth of a millimeter. Figure 1: Methods of measuring butterfly forewing A and antennae B, as described by DeVries 1987. S TATISTICAL A NALYSES . ¾ A two way MANOVA was used to examine the differences in both right forewing an d right antennae between wild and captive bred male and female M. peleides butterflies. A MANOVA test is more conservative than two separate two way ANOVAs, and is more accurate than univariate tests Avalos et. al 2007. I used a two way ANOVA test to c ompare right forewing differences in wild and captive populations, and the same procedure was used again for the right antennae. All statistical analyses were done using JMP IN statistical software. R ESULTS In total, 23 wild and 35 captive butterf lies were collected and measured. Captive male populations had a sampling size of 29, and captive female populations had a sampling size of 5. Populations sampled from wild sites had a sampling effort of 13 male and 10 female butterflies. Captive male and female butterflies varied in size from 54.0 to 69.5 mm and 63.5 to 68.6 mm in right forewing length respectively. Wild measurements of male and female sizes varied from 54.8 to 74.7 mm and 71.1 to 82.5 mm in right forewing lengths. Following this trend, right antennae lengths of males were 18.3 to 25.2 mm for captive and 19.6 to 27.1 mm for wild individuals. Females€ right antennae

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4 ranged in size from 19.7 to 22.5 mm and 22.6 to 27.5 mm for captive and wild populations respectively. Mean sizes of captive bred populations were shown to be smaller than wild populations in all measurements in both male and female butterflies Fig. 2. The MANOVA results for the two right forewing length and right antennae length indicated significant differences for both sex F 1,53 = 44.4503, P < .0001 and treatment type F 1,53 = 29.9577, P < .0001. No interaction was found, however, between treatment type and sex F 1,53 = 1.2825, P = 0.2625. A two way ANOVA indicated significance for right forewing lengths between ca ptive and wild populations F 3,54 = 47.1507, P < .0001; Fig. 2a, and between sexes F 3,54 = 34.4780, P < .0001; Fig. 2a, with no interaction between the treatment type and sex F 3,54 = 2.4615, P = 0.1225; Fig. 2a. A two way ANOVA for right antennae len gths signified that there was a difference between rearing environments of captive and wild populations F 3,53 = 40.4542, P < .0001; Fig. 2b, but no statistical difference is seen between male and female F 3,53 = 3.5191, P = 0.0662; Fig. 2b, nor for an i nteraction between sex and treatment environment F 3,53 = 3.2283, P = 0.0781; Fig. 2b.

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5 F IG . 2. M ean size + SE of right forewing A and rig ht antennae B of wild and captive populations of M. peleides , separated by sex, female f and male m. N values are shown in their corresponding boxes. D ISCUSSION I predict ed that wild butterflies would be larger in terms of right forewing and anten nae length. Wild butterflies are greater in size than captive butterflies Fig. 2. During my observations in the Monteverde Butterfly Garden, I witnessed that some Morpho peleides butterflies emerged from their cocoons with disfigured wings. The Garden staff informed me this is a clear sign of inbreeding. Since all of these butterflies come from the same

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6 breeder, they are all reared together, and likely to have come from the same gene pool. These trends are consistent with the idea that captive breedin g and perhaps therefore inbreeding reduces body size of individuals. Because body size can be related to fitness DeVries 1987, it can be said that inbreeding may reduce the fitness of offspring, consistent with inbreeding depression trends. Inbreedi ng depression has also been found to act with disease and genetic drift to induce extinction in wild populations New 1995. This has been previously observed by massive disease outbreaks and bottlenecks during harsh conditions in butterfly gardens DuPont 2007. Because of these negative effects correlated with inbreeding, captive breeding techniques of butterflies are in great need of improvement. S ome possible steps gardens can take to reduce the impacts of captivity would be to quantify the initial g enetic diversity, introduce wild individuals into the population to increase diversity, and make sure all individuals are contributing genetic information to the next generation Barber 2002. These would all act to reduce the effects of drift and inbreed ing depression Barber 2002. Past experiments have shown that rearing in captivity can select for female butterflies with higher ovary mass and more egg production Lewis et al. 2001. Also, butterflies that reproduce well in captivity may not necessaril y reproduce well in the wild Barber 2002, indicating the importance of retaining all genetic diversity in captive populations. It has been observed that captive breeding leads to a reduction in size, most likely from inbreeding due to poor rearing tech niques. All variables in rearing techniques have not been separated to distinguish how much each factor affects size. Future studies should focus on larval populations with the same degree of inbreeding, and feed them varying qualities of food to see the amount quality of food affects size in captive and wild butterfly populations. A CKNOWLEDG MENTS Thanks to all the staff at the Monteverde Butterfly Garden for allowing me to sample their stocks. Thanks to the CIEE students Sonia and Brian for their hel p in capturing and recording butterflies. Thanks to Pablo Allen for the knowledge of techniques to handle the butterflies and his statistically support. I would also like to thank the Creativa for allowing me to trap and measure their nearby M. peleides p opulation. L ITERATURE CITED Avalos, G., S.S. Mulkey, K. Kitajima, and S.J. Wright. 2007. Colonization Strategies of Two Liana Species in a Tropical Dry Forest Canopy. Biotropica 393: 393  399 B almford, A., G.M. Mace, and N.L. Williams. 1996. Desi gning the Ark: Setting Priorities for Captive Breeding. Conservation Biology 103: 719 727. Barber, R.C. 2002. Inbreeding and Heritable Diseases in Captive Popul a t ions. Pg: 184 189. The 2 nd International Symposium on Assisted Reproductive Technology f or the Conservation & Genetic Management of Wildlife. Breuker, C.J., and P.M. Brakefield. Lack of response to selection for lower fluctuating asymmetry of mutant eyespots in the butterfly Bicyclus anynana. Nature Publishing Group. Heredity 91: 17 27.

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7 Cassel, A., J. Windig, S. Nylin, and C. Wiklund. 1999. Effects of Population Size and Food Stress on Fitness Related Characters in the Scarce Heath, a Rare Butterfly in Western Europe. Conservation Biology 156: 1667 1673. Clarke, G.M. 1995. Relatio nships between Developmental stability and Fitness: Applications for Conservation Biology. Conservation Biology 91: 18 24. Derrickson, S.R., and N.F.R. Snyder. 1992. Potentials and limits of captive breeding in parrot conservation. In S.R. Beissinge r and N.F.R. Snyder Ed. New World parrots in crisis : solutions from conservation biology. Pg: 133 163. Smithsonian Institution Press, Washington, D. C. DeVries, P.J. 1983. Morpho peleides. In, Daniel H. Janzen. Ed. Costa Rican Natural History. pp. 74 1. University of Chicago Press, Chicago. DeVries , P.J . 1987. The Butterflies of Costa Rica and Their Natural History . Pg: 9 20, 244. Princeton University Press, New Jersey. DuPont, M. 2007. ‚Asymmetry and small body size in captive bred populations of Nymphalid butterflies. CIEE Tropical Ecology and Conservation.ƒ in CIEE, Monteverde, Costa Rica. Gomendio, M., J. Cassinello, and E.R.S. Rolan. 2000. A Comparative Study of Ejaculate Traits in Three Endangered Ungulates with Different Levels of Inbreed ing: Fluctuating Asymmetry as an Indicator of Reproductive and Genetic Stress. Proceedings: Biological Sciences 2671446: 875 882. Jones, C.G., W. Heck, R.E. Lewis, Y. Mungroo, G. Slade, and T. Cade. 1995. The restoration of the Mauritius Kestrel Falc o punctatus population. Ibis 137 Supplement 1: 173 180. Joron M, and P.M. Brakefield . 2003. Captivity masks inbreeding effects on male mating success in butterflies. Nature 424: 191 194. Lewis O.T., and C.D. Thomas . 2001. Adaptations to Captivity i n the Butterfly Pieris brassicae L. and the Implications for Ex situ Conservation. Journal of Insect Conservation, 51: 55. Milius, S. 1998. Wild Inbred Butterflies Risk Extinction. Science News, Vol. 15314:214. N EW TR. 1995. Introduction to Inv ertebrate Biology. Pg: 103 111. Oxford University Press, New York. Palmer, A.R. and C. Strobeck. 1986. Fluctuating Asymmetry: Measurement, Analysis, Patterns. Annual Reviews Inc. Ecol. Syst. 17:391 421. Reed, H.D. 2003. Correlation between Fitness a nd Genetic Diversity. Conservation Biology Vol. 17. No. 1. Pg: 6 8. Robertson, F.W., E.C.R. Reeve. 1952. Heterozygosity, Environmental Variation and Heterosis. Nature 170: 286. Saccheri, I.J., P.M. Brakefield, and R.A. Nichols. 1996. Severe Inbreeding Depression and Rapid Fitness Rebound in the Butterfly Bicyclus anynana Satyridae. Evolution, Vol. 50, No. 5: 2000 2013. Synder, N.F.R., S.R. Derrickson, S.R. Bessinger, J.W. Wiley, T.B. Smith, W.D. Toone, and B. Miller. 1996. Limitations of Captive Bre eding in Endagered Species Recovery. Conservation Biology, 102: 338 348. VanValen L. 1962. A study of fluctuating asymmetry. Evolution 6: 125 142. Wright, L.I., T. Tregenza, D.J. Hosken. 2007. Inbreeding, inbreeding depression and extinction. Conse rvation Genetics 94: 833 843.


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