Evolution of plant defenses in nonindigenous environments

Annual Review of Entomology

Volumn 55, Issue , 2010, Pages 439-459

  Orians, Colin M ^a,b   Ward, David ^c  

^a TUFTS UNIVERSITY   (United States)

^b SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

^c UNIVERSITY OF KWAZULU NATAL   (South Africa)

Author keywords

Enemy release; Evolution of increased competitive ability; Exotic plants; Generalist and specialist herbivores; Invasions; Resource availability

Indexed keywords

ANIMAL; ECOSYSTEM; EVOLUTION; GENETIC SELECTION; GENETICS; GEOGRAPHY; HOST PARASITE INTERACTION; IMMUNOLOGY; INSECT; PARASITOLOGY; PHYSIOLOGY; PLANT; REVIEW;

ANIMALS; ECOSYSTEM; EVOLUTION; GEOGRAPHY; HOST-PARASITE INTERACTIONS; INSECTS; PLANTS; SELECTION, GENETIC;

EID: 77449114545     PISSN: 00664170     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev-ento-112408-085333     Document Type: Review

References (130)

1. Agrawal AA, Kotanen PM, Mitchell CE, Power AG, GodsoeW, KlironomosJ. 2005. Enemy release? An experiment with congeneric plant pairs and diverse above-and belowground enemies. Ecology 86:2979-2989
2. Alpert P, Bone E, Holzapfel C. 2000. Invasiveness, invasibility and the role of environmental stress in the spread of non-native plants. Persp. Plant Ecol. Evol. Syst. 3:52-66
3. Auerbach M, Simberloff D. 1988. Rapid leaf-miner colonization of introduced trees and shifts in sources of herbivore mortality. Oikos 52:41-50
4. Bais HP, Vepachedu R, Gilroy S, Callaway RM, Vivanco JM. 2003. Allelopathy and exotic plant invasion: from molecules and genes to species interactions. Science 301:1377-1380
5. Berenbaum MR, Zangerl AR. 2006. Parsnip webworms at home and abroad: trophic complexity in a geographic mosaic. Ecology 87:3070-3081
6. Bergelson J, Purrington CB. 1996. Surveying patterns in the cost of resistance in plants. Am. Nat. 148:536-558
7. Biggs AR, Miles NW, Bell RL. 1992. Heritability of suberin accumulation in wounded peach bark. Phytopathology 82:83-86
8. Blair AC, Wolfe LM. 2004. The evolution of an invasive plant: an experimental study with Silene latifolia. Ecology 85:3035-3042
9. Blossey B, Nötzold R. 1995. Evolution of increased competitive ability in invasive nonindigenous plants: a hypothesis. J. Ecol. 83:887-889
10. Blumenthal DM. 2006. Interactions between resource availability and enemy release in plant invasion. Ecol. Lett. 9:887-895
11. Bossdorf O, Auge H, Lafuma L, Rogers WA, Siemann E, Prati D. 2005. Phenotypic and genetic differentiation between native and introduced plant populations. Oecologia 144:1-11
12. Bossdorf O, Lipowsky A, Prati D. 2008. Selection of preadapted populations allowed Senecio inaequidens to invade Central Europe. Divers. Distrib. 14:676-685
13. Bowen L, Van Vuren D. 1997. Insular endemic plants lack defenses against herbivores. Conserv. Biol. 11:1249-1254
14. Brändle M, Kühn I, Klotz S, Belle C, Brandl R. 2008. Species richness of herbivores on exotic host plants increases with time since introduction of the host. Divers. Distrib. 14:905-912
15. Bruin J, Sabelis MW, Dicke M. 1995. Do plants tap SOS signals from their infested neighbours? Trends Ecol. Evol. 10:167-170
16. Bryant JP, Chapin FS, Klein DR. 1983. Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory. Oikos 40:357-368
17. Callaway RM, Aschehoug ET. 2000. Invasive plants versus their new and old neighbors: a mechanism for exotic invasion. Science 290:521-523
18. Callaway RM, Cipollini D, Barto K, Thelen GC, Hallett SG, et al. 2008. Novel weapons: invasive plant suppresses fungal mutualists in America but not in its native Europe. Ecology 89:1043-1055
19. Callaway RM, Maron JL. 2006. What have exotic plant invasions taught us over the past 20 years? Trends Ecol. Evol. 21:369-374
20. Caño L, Escarré J, Vrieling K, Sans FX. 2009. Palatability to a generalist herbivore, defence and growth of invasive and native Senecio species: testing the evolution of increased competitive ability hypothesis. Oecologia 159:95-106
21. Cappuccino N, Carpenter D. 2005. Invasive exotic plants suffer less herbivory than non-invasive exotic plants. Biol. Lett. 1:435-438
22. Cebrian J, Duarte CM. 1994. The dependence of herbivory on growth rate in natural plant communities. Funct. Ecol. 8:518-525
23. Chew FS, Renwick JAA. 1995. Hostplant choice in Pieris butterflies. In Chemical Ecology of Insects II, ed. RT Cardé, WJ Bell, pp. 214-238 NY: Chapman & Hall
24. Cipollini DF, Mbagwu J, Barto K, Hillstrom C, Enright S. 2005. Expression of constitutive and inducible chemical defenses in native and invasive populations of Alliaria petiolata. J. Chem. Ecol. 31:1255-1267
25. Cipollini DF, Purrington CB, Bergelson J. 2003. Costs of induced responses in plants. Basic Appl. Ecol. 4:79-89
26. Coley PD, Bryant JP, Chapin FS III. 1985. Resource availability and plant anti-herbivore defense. Science 230:895-899
27. Compton SG, Lawton JH, Rashbrook VK. 1989. Regional diversity, local community structure and vacant niches: the herbivorous arthropods of bracken in South Africa. Ecol. Entomol. 14:365-373
28. Connor EF, Faeth SH, Simberloff D, Opler PA. 1980. Taxonomic isolation and the accumulation of herbivorous insects: a comparison of introduced and native trees. Ecol. Entomol. 5:205-211
29. Cripps MG, Hinz HL, McKenney JL, Price WJ, Schwarzlander M. 2009. No evidence for an 'evolution of increased competitive ability' for the invasive Lepidium draba. Basic Appl. Ecol. 10:103-112
30. Daehler CC. 2003. Performance comparisons of co-occurring native and alien plants: implications for conservation and restoration. Annu. Rev. Ecol. Syst. 34:183-211
31. Daehler CC, Strong DR. 1997. Reduced herbivore resistance in introduced smooth cordgrass (Spartina alterniflora) after a century of herbivore-free growth. Oecologia 110:99-108
32. Dalin P, Bjö rkman C. 2006. Native insects colonizing introduced tree species\patterns and potential risks. In Invasive Forest Insects, Introduced Forest Trees, and Altered Ecosystems, ed. TD Paine, pp. 63-77. Dordrecht, Neth.: Springer
33. Davis MA, Grime JP, Thompson K. 2000. Fluctuating resources in plant communities: a general theory of invasibility. J. Ecol. 88:528-536
34. DeWalt SJ, Denslow JS, Ickes K. 2004. Natural-enemy release facilitates habitat expansion of the invasive tropical shrub Clidemia hirta. Ecology 85:471-483
35. Duke SO, Blair AC, Dayan FE, Johnson RD, Meepagala KM, et al. 2009. Is (-)-catechin a novel weapon of spotted knapweed (Centaurea stoebe). J. Chem. Ecol. 35:141-153
36. Durka W, Bossdorf O, Prati D, Auge H. 2005. Molecular evidence for multiple introductions of garlic mustard (Alliaria petiolata, Brassicaceae) to North America. Mol. Ecol. 14:1697-1706
37. Eigenbrode SD, Andreas JE, Cripps MG, Ding H, Biggam RC, Schwarzländer M. 2008. Induced chemical defenses in invasive plants: a case study with Cynoglossum officinale L. Biol. Invas. 10:1373-1379
38. Fine PVA, Miller ZJ, Mesones I, Irazuzta S, Appel HM, et al. 2006. The growth-defense trade-off and habitat specialization by plants in Amazonian forests. Ecology 87:S150-62
39. Franks SJ, Pratt PD, Dray FA, Simms EL. 2008. No evolution of increased competitive ability or decreased allocation to defense in Melaleuca quinquenervia since release from natural enemies. Biol. Invas. 10:455-466
40. Garland T, Harvey PH, Ives AR. 1992. Procedures for the analysis of comparative data using phyloge-netically independent contrasts. Syst. Biol. 41:18-32
41. Glynn C, Herms DA, Orians CM, Hansen RC, Larsson S. 2007. Testing the growth-differentiation balance hypothesis: dynamic responses of willows to nutrient availability. New Phytol. 176:623-634
42. Gurevitch J, Hedges LV. 2001. Meta-analysis: combining the results of independent experiments. In Design and Analysis of Ecological Experiments, ed. SM Scheiner, J Gurevitch, pp. 378-398 New York: Chapman and Hall
43. Hamilton JG, Zangerl AR, DeLucia EH, Berenbaum MR. 2001. The carbon-nutrient balance hypothesis: its rise and fall. Ecol. Lett. 4:86-95
44. Haugen R, Steffes L, Siemens DH. 2008. Evolution of drought tolerance and defense: dependence of tradeoffs on mechanism, environment and defense switching. Oikos 117:231-244
45. Herms DA, Mattson WJ. 1992. The dilemma of plants: to grow or defend. Q. Rev. Biol. 67:283-335
46. Hierro J, Maron JL, Callaway RM. 2005. A biogeographical approach to plant invasion biology: the importance of studying exotics in their introduced and native range. J. Ecol. 93:5-15
47. Hobbs RJ, Huenneke L. 1992. Disturbance, diversity, and invasion: implications for conservation. Conserv. Biol. 6:324-337
48. Huenneke LF, Hamburg SP, Kode R, Mooney HA, Vitousek PM. 1990. Effects of soil resources on plant invasion and community structure in Californian serpentine grassland. Ecology 71:478-491
49. Inderjit, Seastedt TR, Callaway RM, Pollock JL, Kaur J. 2008. Allelopathy and plant invasions: traditional, congeneric, and bio-geographical approaches. Biol. Invas. 10:875-890
50. Jogesh T, Carpenter D, Cappuccino N. 2008. Herbivory on invasive exotic plants and their non-invasive relatives. Biol. Invas. 10:797-804
51. Joshi J, Vrieling K. 2005. The enemy release and EICA hypothesis revisited: incorporating the fundamental difference between specialist and generalist herbivores. Ecol. Lett. 8:704-714
52. Kang M, Buckley YM, Lowe AJ. 2007. Testing the role of genetic factors across multiple independent invasions of the shrub Scotch broom (Cytisus scoparius). Mol. Ecol. 16:4662-4673
53. Kato T, Ishida K, Sato H. 2007. The evolution of nettle resistance to heavy deer browsing. Ecol. Res. 23:339-345
54. Keane RM, Crawley MJ. 2002. Exotic plant invasions and the enemy release hypothesis. Trends Ecol. Evol. 17:164-170
55. Keller SR, Taylor DR. 2008. History, chance and adaptation during biological invasion: separating stochastic phenotypic evolution from response to selection. Ecol. Lett. 11:852-866
56. Koricheva J. 2002. Meta-analysis of sources of variation in fitness costs of plant antiherbivore defenses. Ecology 83:176-190
57. Koricheva J, Nykänen H, Gianoli E. 2004. Meta-analysis of trade-offs among plant antiherbivore defenses: Are plants jacks-of-all-trades, masters of all? Am. Nat. 163:E64-75
58. Lampert EC, Zangerl AR, Berenbaum MR, Ode PJ. 2008. Tritrophic effects of xanthotoxin on the polyembryonic parasitoid Copidosoma sosares (Hymenoptera: Encyrtidae). J. Chem. Ecol. 34:783-790
59. Leger EA, Forister ML. 2005. Increased herbivore resistance in invasive populations of the California poppy (Eschsholzia californica). Divers. Distrib. 11:311-317
60. Leger EA, Rice KJ. 2003. Invasive California poppies (Eschscholzia californica Cham.) grow larger than native individuals under reduced competition. Ecol. Lett. 6:257-264
61. Levine JM, Adler PB, Yelenik SG. 2004. A meta-analysis of biotic resistance to exotic plant invasions. Ecol. Lett. 7:975-989
62. Lewis KC, Bazzaz FA, Liao Q, Orians CM. 2006. Geographic patterns of herbivory and resource allocation to defense, growth, and reproduction in an invasive biennial, Alliaria petiolata. Oecologia 148:384-395
63. Liu H, Stiling P. 2006. Testing the enemy release hypothesis: a review and meta-analysis. Biol. Invas. 8:1535-1545
64. Liu H, Stiling P, Pemberton RW. 2007. Does enemy release matter for invasive plants? Evidence from a comparison of insect herbivore damage among invasive, non-invasive and native congeners. Biol. Invas. 9:773-781
65. Løe G, Toräng P, Gaudeul M, A? gren J. 2006. Trichome production and spatiotemporal variation in herbivory in the perennial herb Arabidopsis lyrata. Oikos 116:134-142
66. Lonsdale WM. 1999. Global patterns of plant invasions and the concept of invasibility. Ecology 80:1522-1536
67. Macel M, Vrieling K. 2003. Pyrrolizidine alkaloids as oviposition stimulants for the cinnabar moth, Tyria jacobaeae. J. Chem. Ecol. 29:1435-1446
68. Mack MC, D'Antonio CM. 1998. Impacts of biological invasions on disturbance regimes. Trends Ecol. Evol. 13:195-198
69. Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M, Bazzaz FA. 2000. Biotic invasions: causes, epidemiology, global consequences and control. Ecol. Appl. 10:689-710
70. Maron JL, Vilà M, Arnason J. 2004. Loss of natural enemy resistance among introduced populations of St. John's Wort, Hypericum perforatum. Ecology 85:3243-3253
71. Maron JL, Vilà M, Bommarco R, Elmendorf S, Beardsley P. 2004. Rapid evolution of an invasive plant. Ecol. Monogr. 74:261-280
72. Massey FP, Hartley SE. 2009. Physical defences wear you down: progressive and irreversible impacts of silica on insect herbivores. J. Anim. Ecol. 78:281-291
73. McArthur C, Sanson GD, Beal AM. 1995. Salivary proline-rich proteins in mammals: roles in oral homeostasis and counteracting dietary tannin. J. Chem. Ecol. 21:663-691
74. McKey DB, Waterman PG, Mbi CN, Gartlan JS, Struhsaker TT. 1978. Phenolic content of vegetation in two African rain forests: ecological implications. Science 202:61-64
75. McNaughton SJ, Tarrants JL. 1983. Grass leaf silicification: natural selection for an inducible defense against herbivores. Proc. Natl. Acad. Sci. USA 80:790-791
76. Meyer GA, Hull-Sanders HM. 2008. Altered patterns of growth, physiology and reproduction in invasive genotypes of Solidago gigantea (Asteraceae). Biol. Invas. 10:303-317
77. Mitchell CE, Power AG. 2003. Release of invasive plants from fungal and viral pathogens. Nature 421:625-627
78. Mithen R, Raybould AF, Giomoustaris A. 1995. Divergent selection for secondary metabolites between wild populations ofBrassica oleracea and its implications for plant-herbivore interactions. Heredity 75:472-484
79. Mooney KA, Agrawal AA. 2008. Plant genotype shapes ant-aphid interactions: implications for community structure and indirect plant defense. Am. Nat. 171:E195-E205
80. Müller C, Martens N. 2005. Testing predictions of the 'Evolution of Increased Competitive Ability' hypothesis for an invasive crucifer. Evol. Ecol. 19:533-550
81. Müller-SchärerH, SchaffnerU, SteingerT. 2004. Evolution in invasive plants: implications for biological control. Trends Ecol. Evol. 9:417-422
82. Myers JH, Bazely DR. 2003. Ecology and Control of Introduced Plants. Cambridge: Cambridge Univ. Press. 313 pp.
83. Novak SJ, Mack RN. 2005. Genetic bottlenecks in alien plant species: influence of mating systems and introduction dynamics. See Ref. 88, pp. 95-122
84. Ode PJ, Berenbaum MR, Zangerl AR, Hardy ICW. 2004. Host plant, host plant chemistry, and the polyembryonic parasitoid Copidosoma sosares: indirect effects in a tritrophic interaction. Oikos 104:388-400
85. Power DM, ed. 1980. The California Islands: Proceedings of a Multidisciplinary Symposium. Santa Barbara, CA: Santa Barbara Mus. Nat. Hist. 787 pp.
86. Ridenour WM, Vivanco JM, Feng Y, Horiuchi J-I, Callaway RM. 2008. No evidence for trade-offs: Centaurea plants from America are better competitors and defenders. Ecol. Monogr. 78:369-386
87. Rose US, Tumlinson JH. 2003. Volatiles released from cotton plants inresponse to Helicoverpa zea feeding damage on flower buds. Planta 218:824-832
88. Sax DF, Stachowicz JJ, Gaines SD, eds. 2005. Species Invasions: Insights into Ecology, Evolution, and Biogeography. Sunderland, MA: Sinauer. 495 pp.
89. Scargle JD. 2000. Publication bias: the "file-drawer problem" in scientific inference. J. Sci. Explor. 14:91-106
90. Shaltiel L, Ayal Y. 1998. The use of kairomones for foraging decisions by an aphid parasitoid in small host aggregations. Ecol. Entomol. 23:319-329
91. Sher AA, Hyatt LA. 1999. The disturbed resource-flux invasion matrix: a new framework for patterns of plant invasion. Biol. Invas. 1:107-114
92. Siemann E, Rogers WE, DeWalt S. 2006. Rapid adaptation of insect herbivores to an invasive plant. Proc. R. Soc. London Sci. Ser. B 273:2763-2769
93. Silvertown J, Dodd M. 1997. Comparing plants and connecting traits. In Plant Life Histories: Ecology, Phylogeny and Evolution, ed. J Silvertown, M Franco, JL Harper, pp. 3-16. Cambridge, UK: Cambridge Univ. Press
94. Singer MC, Thomas CD, Parmesan C. 1993. Rapid human-induced evolution of insect diet. Nature 366:681-683
95. Siska EL, Pennings SC, Buck TL, Hanisak MD. 2002. Latitudinal variation in palatability of salt-marsh plants: Which traits are responsible? Ecology 83:3369-3381
96. Soler R, Bezemer TM, Van Der Putten WH, Vet LEM, Harvey JA. 2005. Root herbivore effects on aboveground herbivore, parasitoid and hyperparasitoid performance via changes in plant quality. J. Anim. Ecol. 74:1121-1130
97. Stamp N. 2003. Out of the quagmire of plant defense hypotheses. Q. Rev. Biol. 78:23-55
98. Stastny M, Schaffner U, Elle E. 2005. Do vigour of introduced populations and escape from specialist herbivores contribute to invasiveness? J. Ecol. 93:27-37
99. Strauss SY, Rudgers JA, Lau JA, Irwin RE. 2002. Direct and ecological costs of resistance to herbivory. Trends Ecol. Evol. 17:278-285
100. Strong DR, Lawton JH, Southwood TRE. 1984. Insects on Plants: Community Patterns and Mechanisms. Oxford: Blackwell Sci. 313 pp.
101. Strong DR, McCoy ED, Rey JR. 1977. Time and the number of herbivore species: the pests of sugarcane. Ecology 58:167-175
102. Swihart RK, Bryant JP, Newton L. 1994. Latitudinal patterns in consumption of woody plants by snowshoe hares in the eastern United States. Oikos 70:427-434
103. Thompson JN. 1999. Specific hypotheses on the geographic mosaic of coevolution. Am Nat. 153:S1-S14
104. Tomovic Z, Orlovic S, Guzina V, Ivanis?evic P. 1997. Comparative investigation of growth rate and length of thorns of black locust (Robinia pseudoacacia L.). Genetika 29:23-30
105. Van Dam NM, Vuister LWM, Bergshoeff C, de Vos H, Van Der Meijden ED. 1995. The "raison d'être" of pyrrolizidine alkaloids in Cynoglossum officinale: deterrent effects against generalist herbivores. J. Chem. Ecol. 21:507-523
106. Van Kleunen M, Fischer M. 2008. Adaptive rather than non-adaptive evolution of Mimulus guttatus in its invasive range. Basic Appl. Ecol. 9:213-223
107. Van Kleunen M, Schmid B. 2003. No evidence for an evolutionary increase in competitive ability in an invasive plant. Ecology 84:2816-2823
108. Van Vuren D, Coblentz BE. 1987. Some ecological effects of feral sheep on Santa Cruz Island, California, USA. Biol. Conserv. 41:253-268
109. Verhoeven KJF, Biere A, Harvey JA, Van Der Putten WH. 2009. Plant invaders and their novel natural enemies: Who is nä?ve? Ecol. Lett. 12:107-117
110. Vet LEM, Dicke M. 1992. Ecology of infochemical use by natural enemies in a tritrophic context. Annu. Rev. Entomol. 37:141-172
111. Vet LEM, Godfray HCJ. 2008. Multitrophic interactions and parasitoid behavioral ecology. In Behavioural Ecology of Insect Parasitoids: From Theoretical Approaches to Field Application, ed. E Wajnberg, C Bernstein, JJM Van Alphen, pp. 231-251 Oxford: Blackwell
112. Vicari M, Bazely DR. 1993. Do grasses fight back: the case for anti-herbivore defences. Trends Ecol. Evol. 8:137-141
113. Vilà M, Gomez A, Maron JL. 2003. Are alien plants more competitive than their native conspecifics? A test using Hypericum perforatum L. Oecologia 137:211-215
114. Vourc'h G, Martin J-L, Duncan P, Escarré J, Clausen TP. 2001. Defensive adaptations of Thuja plicata to ungulate browsing: a comparative study between mainland and island populations. Oecologia 126:84-93
115. Vourc'h G, Vila B, Gillon D, Escarré J, Guibal F, et al. 2002. Disentangling the causesofdamage variation by deer browsing on young Thuja plicata. Oikos 98:271-283
116. Vrieling K, van Wijk AM. 1994. Estimating costs and benefits of the pyrrolizidine alkaloids of Senecio jacobaea under natural conditions. Oikos 70:449-454
117. Wäckers FL, Bezemer TM. 2003. Root herbivory induces an above-ground indirect defence. Ecol. Lett. 6:9-12
118. Ward D, Spiegel M, Saltz D. 1997. Gazelle herbivory and interpopulation differences in calcium oxalate content of leaves of a desert lily. J. Chem. Ecol. 23:333-346
119. Ward D, Young TP. 2002. Effects of large mammalian herbivores and ant symbionts on condensed tannins of Acacia drepanolobium in Kenya. J. Chem. Ecol. 28:913-929
120. Willis AJ, Blossey B. 1999. Benign climates don't explain the increased vigour of non-indigenous plants: a cross-continental transplant experiment. Biocontrol Sci. Technol. 9:567-577
121. Willis AJ, Memmott J, Forrester RI. 2000. Is there evidence for the post-invasion evolution of increased size among invasive plant species? Ecol. Lett. 3:275-283
122. Wolfe LM. 2002. Why alien invaders succeed: support for the escape-from-enemy hypothesis. Am. Nat. 160:705-711
123. Wolfe LM, Elzinga JA, Biere A. 2004. Increased susceptibility to enemies following introduction in the invasive plant Silene latifolia. Ecol. Lett. 7:813-820
124. Zangerl AR, Berenbaum MR. 1997. Cost of chemically defending seeds: furanocoumarins and Pastinaca sativa. Am. Nat. 150:491-504
125. Zangerl AR, Berenbaum MR. 2003. Phenotype matching in wild parsnips and parsnip webworms: causes and consequences. Evolution 57:806-815
126. Zangerl AR, Berenbaum MR. 2005. Increase in toxicity of an invasive weed after reassociation with its coevolved herbivore. Proc. Natl. Acad. Sci. USA 102:15529-15532
127. Zangerl AR, Rutledge CE. 1996. Probability of attack and patterns of constitutive and induced defense: a test of optimal defense theory. Am. Nat. 147:599-608
128. Zangerl AR, Stanley MC, Berenbaum MR. 2008. Selection for chemical trait remixing in an invasive weed after reassociation with a coevolved specialist. Proc. Natl. Acad. Sci. USA 105:4547-4552
129. Zhang D-Y, Jiang X-H. 2006. Interactive effects of habitat productivity and herbivore pressure on the evolution of anti-herbivore defense in invasive plant populations. J. Theor. Biol. 242:935-940
130. Zou J, Rogers WE, Siemann E. 2008. Increased competitive ability and herbivory tolerance of the invasive plant Sapium sebiferum. Biol. Invas. 10:291-302