臺灣博碩士論文加值系統

1. 抵禦掠食者攻擊是獵物適應上重要的一環。獵物的次級防禦機制 （例如毒性） 常伴隨著警戒色的出現，並可藉由避免被捕食讓掠食者與獵物彼此獲利。因此警戒色獵物被預期具有和警戒色彩一起演化的有效次級防禦機制。
2. 早在將近一百五十年前，華萊士就已經提出球背象鼻蟲 (Pachyrhynchus) 以鮮豔的花紋來警告掠食者，並以堅硬的外骨骼作為防禦的假說；然而這項假說至今依然無實驗證據驗證。本研究檢驗球背象鼻蟲的次級防禦機制假說，並探討堅硬外骨骼在球背象鼻蟲身上所扮演的生態功能。
3. 我們以斯文豪氏攀木蜥蜴（Japalura swinhonis）作為掠食者，實驗設計四組象鼻蟲處理（軟/硬；有足鉤/無足鉤）進行操控性行為實驗測試其存活率。並以比較破壞球背象鼻蟲的外骨骼，和掠食者共域昆蟲獵物所需的力量 (牛頓)，與掠食者的咬合力大小，來了解球背象鼻蟲的硬度在生態上的重要性。
最後用氣相色譜質譜法 (GC-MS) 分析球背象鼻蟲體內是否有毒性或驅避性的化合物。
4. 所有「硬」球背象鼻蟲被蜥蜴攻擊後都立即被吐出且存活。相較之下「軟」球背象鼻蟲則在被多次咀嚼後吞下。此外不論足鉤存在與否，蜥蜴對球背象鼻蟲的捕食結果都與上述相同。
5. 「硬」球背象鼻蟲的硬度顯著高於共域昆蟲的平均硬度和當地蜥蜴族群的平均咬合力。
6. GC-MS 分析出球背象鼻蟲體內四種可能的化合物（ethyl propyl ether、diethylene glycol、butylated hydroxy toluene 以及cadalene） 均無毒性或對脊椎動物有驅避的功能。
7. 本研究指出具警戒色物種的硬度是一項有效抵禦捕食者的次級防禦機制，亦提供ㄧ個探討脊椎動物掠食者與具有警戒色獵物之間時空互動的研究模式。

1. Anti-predator strategies are significant components of adaptation for prey species. The advance of the secondary defenses like toxins have led to the evolution of warning colours that benefit both prey and predators by mutual avoidance. Therefore aposematic prey are expected to possess effective secondary defenses evolved together with their warning colours.
2. This study tested the hypothesis of secondary defensive function and ecological significance of the hard body in aposematic Pachyrhynchus weevils, which was pioneered by Alfred Russel Wallace nearly 150 years.
3. We used predation trials of Japalura tree lizards to assess the survivorship of ‘hard’ (mature) vs. ‘soft’ (teneral) and ‘claw’ (intact) vs. ‘clawless’ (surgically
removed) weevils. The ecological significance of the weevil’s hard body was
evaluated by assessing the hardness of the weevils, local insect prey, and the bite forces of lizard populations. The existence of toxins or deterrents of the weevil was examined by Gas Chromatography-Mass Spectrometry (GC-MS).
4. All ‘hard’ weevils were spat out and survived the attack by the lizards. By contrast, the ‘soft’ weevils were chewed and subsequently swallowed. The results were the same regardless of presence or absence of the weevil’s tarsal claws.
5. The hardness of ‘hard’ Pachyrhynchus weevil was significantly higher than the average hardness of insect prey in the same habitat and mean bite forces of local lizards.
6. The four candidate compounds of the weevil identified by GC-MS (ethyl propyl ether, diethylene glycol, butylated hydroxy toluene and cadalene) had no known toxic or repellent functions against the vertebrates.
7. These results reveal that the hardness of aposematic prey functions as effective secondary defense, and provide a framework for understanding spatio-temporal interactions between vertebrate predators and aposematic insect prey.

致謝 i
中文摘要 ii
Abstract iv

Introduction 1
Materials and methods 5
Ethics statement 5
Weevil and lizard 5
Colour and mobility of ‘hard’ and ‘soft’ weevils 7
Behavioral trials 9
Insect prey and hardness measurement 10
Chemical analysis 12
Statistical analyses 13
Results 13
Effects of the hardness and claws 13
Hardness of prey and lizard’s bite force 15
Biochemical compounds of P. sarcitis kotoensis 16
Discussion 17
Effective secondary defense 17
Multiple secondary defenses 19
Mechanical mechanism of hardness 20
Adaptive defense against lizard’s predation 21
References 24
Figures 31
Supplementary tables 39
Supplementary movies 56

Abrams, P.A. (2000) The evolution of predator-prey interactions: theory and evidence. Annual Review of Ecology and Systematics, 31, 79-105.
Anbutsu, H., Moriyama, M., Nikoh, N., Hosokawa, T., Futahashi, R., Tanahashi, M., Meng, X.Y., Kuriwada, T., Mori., N., Oshima., K., Hattori, M., Fujie, M., Satoh, N., Maeda, T., Shigenobu, S., Koga, R. & Fukatsu, T. (2017) Small genome symbiont underlies cuticle hardness in beetles. Proceedings of the National Academy of Sciences of the United States of America, 201712857.
Andersen, S.O. (2010) Insect cuticular sclerotization: a review. Insect Biochemistry and Molecular Biology, 40, 166-178.
Anderson, R.A., McBrayer, L.D., & Herrel, A. (2008) Bite force in vertebrates: opportunities and caveats for use of a nonpareil whole‐animal performance measure. Biological Journal of the Linnean Society, 93, 709-720.
Barševskis, A. (2013) Contribution to the knowledge of the genus Doliops Waterhouse, 1841 (Coleoptera: Cerambycidae). Baltic Journal of Coleopterology, 13, 73-89.
Bennett, A.T. & Théry, M. (2007) Avian color vision and coloration: multidisciplinary evolutionary biology. The American Naturalist, 169, S1-S6.
Blount, J.D., Rowland, H.M., Drijfhout, F.P., Endler, J.A., Inger, R., Sloggett, J.J., Hurst, G.D.D., Hodgson, D.J. & Speed, M.P. (2012) How the ladybird got its spots: Effects of resource limitation on the honesty of aposematic signals. Functional Ecology, 26, 334-342.
Blum, M. (2012) Chemical Defenses of Arthropods. Elsevier.
Caro, T. (2017) Wallace on coloration: contemporary perspective and unresolved insights. Trends in Ecology & Evolution, 32, 23-30.
Chen, P.C., Chang, M.H., Chen, S.F., Li, Z.L., Chen, S.L., Lin, H.C. & Chu, C.W. (2008) The Research of Terrestrial Vertebrate Fauna on the Green Island. Marine National Park Headquarters.
Chen, Y.T., Tseng, H.Y., Jeng, M.L., Su, Y.C., Huang, W.S. & Lin, C.P. (2017) Integrated species delimitation and conservation implications of an endangered weevil Pachyrhynchus sonani (Coleoptera: Curculionidae) in Green and Orchid Islands of Taiwan. Systematic Entomology, 42, 796-813.
Collins, J.A. (1993) Failure of materials in mechanical design: analysis, prediction, prevention. John Wiley & Sons.
Cooper Jr, W.E. (1989) Absence of prey odor discrimination by iguanid and agamid lizards in applicator tests. Copeia, 472-478.
Cox, P.G., Rayfield, E.J., Fagan, M.J., Herrel, A., Pataky, T.C. & Jeffery, N. (2012) Functional evolution of the feeding system in rodents. PLoS ONE, 7, e36299.
Dickerson, R.E., Merrill, E.D., McGregor, R.C., Schultze, W., Taylor, E.H. & Herre, A.W. (1928) Distribution of Life in the Philippines. Bureau of Printing.
Edmunds, M. (1974) Defence in Animals: A Survey of Anti-Predator Defences. Longman Publishing Group.
Eisner, T., Eisner, M., & Siegler, M. (2005) Secret weapons: defenses of insects, spiders, scorpions, and other many-legged creatures. Harvard University Press.
El-Sayed, A.M. (2014) The Pherobase: Database of pheromones and semiochemicals. The Pherobase.
Evans, A.R., & Sanson, G.D. (2005) Biomechanical properties of insects in relation to insectivory: cuticle thickness as an indicator of insect ‘hardness’ and ‘intractability’. Australian Journal of Zoology, 53, 9-19.
Fisher, R.A. (1958) The genetic theory of natural selection. Dover.
Herrel, A., Damme, R.V., Vanhooydonck, B., & Vree, F.D. (2001) The implications of bite performance for diet in two species of lacertid lizards. Canadian Journal of Zoology, 79, 662-670.
Hopkins, T.L. & Kramer, K.J. (1992) Insect cuticle sclerotization. Annual Review of Entomology, 37, 273-302.
Huang, W.S. (2007) Ecology and reproductive patterns of the agamid lizard Japalura swinhonis on an east Asian island, with comments on the small clutch sizes of island lizards. Zoological Science, 24, 181-188.
Iniesta, L.F.M., Ratton, P. & Guerra, T.J. (2017) Avian predators avoid attacking artificial aposematic millipedes in Brazilian Atlantic Forest. Journal of Tropical Ecology, 33, 89-93.
Klocke, D., & Schmitz, H. (2011) Water as a major modulator of the mechanical properties of insect cuticle. Acta Biomaterialia, 7, 2935-2942.
Li, Z.D., Su, Y., Li, Z.M., Guo, S.J., Wu, T.Y., Lin, Y.J., Yang, D.Q., Liang, Y.Z., Yu, H.Y., Qiu, B.H., Hsu, S.T., Lin, Y.Z., Liu, Z.H., Weng, R.H., Ye, R.K., Ye, C.B., Wu, Y.X., Tseng, Y.H., Pan, T.Z., Tsai, Z.H. Su, X.Q., Chen, Y.J. & Tsai, J.H. (2010) The Inventory of Natural Systems in Orchid Island. Marine National Park Headquarters.
Maan, M.E. & Cummings, M.E. (2011) Poison frog colors are honest signals of toxicity, particularly for bird predators. The American Naturalist, 179, E1-E14.
Mappes, J., Kokko, H., Ojala, K., & Lindström, L. (2014) Seasonal changes in predator community switch the direction of selection for prey defences. Nature Communications, 5, 5016.
Meyers, J.J. & Irschick, D.J. (2015) Does whole-organism performance constrain resource use? A community test with desert lizards. Biological Journal of the Linnean Society, 115, 859-868.
Pasteels, J.M., Grégoire, J.C. & Rowell-Rahier, M. (1983) The chemical ecology of defense in arthropods. Annual Review of Entomology, 28, 263-289.
R Development Core Team. (2016) R: A Language and Environment for Statistical Computing. Vienna, Austria. ISBN 3-900051-07-0. URL http://www.R-project.org.
Rajabi, H., Darvizeh, A., Shafiei, A., Eshghi, S. & Khaheshi, A. (2014) Experimental and numerical investigations of Otala lactea’s shell–I. Quasi-static analysis. Journal of the Mechanical Behavior of Biomedical Materials, 32, 8-16.
Riedel, A., Sagata, K., Surbakti, S., Tänzler, R., & Balke, M. (2013) One hundred and one new species of Trigonopterus weevils from New Guinea. ZooKeys, 280, 1.
Robinson, M.H. (1969) Defenses against visually hunting predators. Evolutionary Biology, 3, 5-59.
Roslin, T., Hardwick, B., Novotny, V., Petry, W.K., Andrew, N.R., Asmus, A., ... & Cameron, E.K. (2017) Higher predation risk for insect prey at low latitudes and elevations. Science, 356, 742-744.
Ruxton, G.D., Sherratt, T.N. & Speed, M.P. (2004) Avoiding Attack: The Evolutionary Ecology of Crypsis, Warning Signals and Mimicry. Oxford University Press.
Schofield, R.M.S., Nesson, M.H. & Richardson, K.A. (2002) Tooth hardness increases with zinc-content in mandibles of young adult leaf-cutter ants. Naturwissenschaften, 89, 579-583.
Schultze, W. (1923) A monograph of the pachyrrhynchid group of the Brachyderinae, Curculionidae: Part I. The genus Pachyrhynchus Germar. The Philippine Journal of Science, 23, 609-673.
Seago, A.E., Brady, P., Vigneron, J.P., & Schultz, T.D. (2009) Gold bugs and beyond: a review of iridescence and structural colour mechanisms in beetles (Coleoptera). Journal of the Royal Society Interface, 6, S165-S184.
Severinghaus, L.L., Ding, T.S., Fang, W.H., Lin, W.H., Tsai, M.C., & Yen, C.W. (2012) The avifauna of Taiwan 2nd edition. Taipei, Taiwan: Forestry Bureau of Council of Agriculture of Executive Yuan.
Sherratt, T.N. & Beatty, C.D. (2003) The evolution of warning signals as reliable indicators of prey defense. The American Naturalist, 162, 377-389.
da Silva Souza, E. & Willemart, R.H. (2011) Harvest-ironman: heavy armature, and not its defensive secretions, protects a harvestman against a spider. Animal Behaviour, 81, 127-133.
Starr, C.K. & Wang, H.Y. (1992) Pachyrhynchine weevils (Coleoptera: Curculionidae) of the islands fringing Taiwan. Journal of Taiwan Museum, 45, 5-14.
Stevens, M. (2013) Sensory Ecology, Behaviour, and Evolution. Oxford University Press.
Summers, K. & Clough, M.E. (2001) The evolution of coloration and toxicity in the poison frog family (Dendrobatidae). Proceedings of the National Academy of Sciences of the USA, 98, 6227-6232.
Tian, H., Zhan, P., Deng, Z., Yan, H. & Zhu, X. (2014) Development of a flavour fingerprint by GC‐MS and GC‐O combined with chemometric methods for the quality control of Korla pear (Pyrus serotina Reld). International Journal of Food Science & Technology, 49, 2546-2552.
Tseng, H.Y., Lin, C.P., Hsu, J.Y., Pike, D.A. & Huang, W.S. (2014) The functional significance of aposematic signals: geographic variation in the responses of widespread lizard predators to colourful invertebrate prey. PLoS ONE, 9, e91777.
Tseng, H.Y., W.S. Huang, M.L. Jeng, R.J.T. Villanueva, O.M. Nuñeza & Lin, C.P. (2017) Complex inter-island colonization and peripatric founder speciation promote diversification of flightless Pachyrhynchus weevils in the Taiwan-Luzon volcanic belt. Journal of Biogeography, in press.
Van De Kamp, T., dos Santos Rolo, T., Vagovič, P., Baumbach, T., & Riedel, A. (2014) Three-dimensional reconstructions come to life-interactive 3D PDF animations in functional morphology. PLoS ONE, 9, e102355.
Van de Kamp, T., Riedel, A. & Greven, H. (2016) Micromorphology of the elytral cuticle of beetles, with an emphasis on weevils (Coleoptera: Curculionoidea). Arthropod Structure and Development, 45, 14-22.
Van der Meij, M.A.A., & Bout, R.G. (2006) Seed husking time and maximal bite force in finches. Journal of Experimental Biology, 209, 3329-3335.
Verwaijen, D., Van Damme, R., & Herrel, A. (2002) Relationships between head size, bite force, prey handling efficiency and diet in two sympatric lacertid lizards. Functional Ecology, 16, 842-850.
Wallace, A.R. (1867) Mimicry and other protective resemblance among animals. Westminster and Foreign Quarterly Review, 32, 1-43.
Wallace, A.R. (1895) Natural Selection and Tropical Nature: Essays on Descriptive and Theoretical Biology. Macmillan, London, UK.
Willink, B., Garcia-Rodriguez, A., Bolaños, F., & Pröhl, H. (2014). The interplay between multiple predators and prey colour divergence. Biological Journal of the Linnean Society, 113, 580-589.
Yewers, M.S., McLean, C.A., Moussalli, A., Stuart-Fox, D., Bennett, A.T.D. & Knott, B. (2015) Spectral sensitivity of cone photoreceptors and opsin expression in two colour-divergent lineages of the lizard Ctenophorus decresii. Journal of Experimental Biology, 218, 1556-1563.