Unexpected high diversity of galling insects in the Amazonian upper canopy: The savanna out there

PLoS ONE

Volumn 9, Issue 12, 2014, Pages

  Julião, Genimar R ^a,b   Venticinque, Eduardo M ^c   Fernandes, G Wilson ^d   Price, Peter W ^e  

^a INSTITUTO NACIONAL DE PESQUISAS DA AMAZÔNIA   (Brazil)

^b INSTITUTO OSWALDO CRUZ   (Brazil)

^c FEDERAL UNIVERSITY OF RIO GRANDE DO NORTE   (Brazil)

^d FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^e NORTHERN ARIZONA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BIOGEOGRAPHIC REGION; BRAZIL; CANOPY; FLOODPLAIN; GALL INSECT; HABITAT; NONHUMAN; POPULATION ABUNDANCE; SAVANNA; SOIL PROPERTY; SPECIES DIVERSITY; SPECIES RICHNESS; TREE; VEGETATION; ANIMAL; BIODIVERSITY; CLASSIFICATION; FOREST; GRASSLAND; INSECT; POPULATION DYNAMICS; SEASON; SOIL;

HEXAPODA;

SOIL;

ANIMALS; BIODIVERSITY; BRAZIL; FORESTS; GRASSLAND; INSECTS; POPULATION DYNAMICS; SEASONS; SOIL; TREES;

EID: 84938614595     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0114986     Document Type: Article

References (76)

1. Fernandes GW, Price PW (1988) Biogeographical gradients in galling species richness: test of hypotheses. Oecologia 76: 161-167.
2. Fernandes GW, Price PW (1992) The adaptive significance of insect gall distribution: survivorship of species in xeric and mesic habitats. Oecologia 90: 14-20.
3. Price PW, Fernandes GW, Lara ACF, Brawn J, Barrios H, et al. (1998) Global patterns in local number of insect galling species. J Biogeogr 25: 581-591.
4. Espírito-Santo MM, Fernandes GW (2007) How many species of gall-inducing insects are there on Earth, and where are they? Ann Entomol Soc Am 100: 95-99.
5. Tooker JF, Rohr JR, Abrahamson WG, De Moraes CM (2008) Gall insects can evade and alter indirect plant defenses. New Phytol 178: 657-671.
6. Medianero E, Ibáñez A, Nieves-Aldrey JL (2010) Importance of beta diversity in local gall-inducing arthropods communities. Neotrop Entomol 39: 365-370.
7. Sullivan LL, Johnson BL, Brudvig LA, Haddad NM (2011) Can dispersal mode predict corridor effects on plant parasites? Ecology 92: 1559-1564.
8. Fernandes GW, Gonçalves-Alvim SJ, Carneiro MAA (2005) Habitat-driven effects on the diversity of gall-inducing insects in the Brazilian cerrado. In: Raman A, Schaefer CW, Withers TM, editors.Biology, ecology, and evolution of gall-inducing arthropods.Enfield, USA: Science Publishers. pp. 693-708.
9. Fernandes GW, Price PW (1991) Comparisons of tropical and temperate galling species richness: the role of environmental harshness and plant nutrient status. In: Price PW, Lewinsohn TM, Fernandes GW, Benson WW, editors.Plant-animal interactions: evolutionary ecology in tropical and temperate regions.New York: John Wiley. pp. 91-116.
10. Fernandes GW, Lara ACF (1993) Diversity of Indonesian gall-forming herbivores along altitudinal gradients. Biodivers Letters 1: 186-192.
11. Lara ACF, Fernandes GW, Gonçalves-Alvim SJ (2002) Tests of hypotheses on patterns of gall distribution along an altitudinal gradient. Trop Zool 15: 219-232.
12. Lara ACF, Fernandes GW (1996) The highest diversity of galling insects: Serra do Cipó, Brazil. Biodivers Letters 3: 111-114.
13. Fernandes GW, Araújo RC, Araújo SC, Lombardi JA, Paula AS, et al. (1997) Insect galls from Jequitinhonha Valley, Minas Gerais, Brazil. Naturalia 22: 221-224.
14. Blanche KR (2000) Diversity of insect-induced galls along a temperature-rainfall gradient in the tropical savannah region of the northern territory, Australia. Aust Ecol 25: 311-318.
15. Cuevas-Reyes P, Quesada M, Siebe C, Oyama K (2004) Spatial patterns of herbivory by gall-forming insects: a test of the soil fertility hypothesis in a Mexican tropical dry forest. Oikos 107: 181-189.
16. Ribeiro SP, Silva Jr. MB, Tagliati MC, Chavana-Bryant C (2011) Vegetation traits and herbivory distribution in an Australian subtropical forest. Mem Queensl Mus - Nature 55: 481-493.
17. Hill RS (1998) Fossil evidence for the onset of xeromorphy and scleromorphy in Australian Proteaceae. Aust Syst Bot 11: 391-400.
18. Veldtman R, McGeoch MA (2003) Gall-forming insect species richness along a non-scleromorphic vegetation rainfall gradient in South Africa: The importance of plant community composition. Aust Ecol 28: 1-13.
19. Yukawa J, Tokuda M, Uechi N, Sato S (2001) Species richness of galling arthropods in Manaus, Amazon and surroundings of the Iguassu Falls. Esakia 41: 11-15.
20. Julião GR, Venticinque EM, Fernandes GW (2005) Richness and abundance of gall-forming insects in the Mamirauá Várzea, a flooded Amazonian forest. Uakari 1: 39-42.
21. Ribeiro SP (2003) Insect herbivores in the canopies of savannas and rainforests. In: Basset Y, Novotny V, Miller SE, Kitching RL, editors.Arthropods of Tropical Forests: spatio-temporal dynamics and resource use in the canopy.Cambridge, UK: Cambridge University Press. pp. 348-359.
22. Ribeiro SP, Basset Y (2007) Gall-forming and free-feeding herbivory along vertical gradients in a lowland tropical rainforest: the importance of leaf sclerophylly. Ecography 30: 663-672.
23. Medianero E, Barrios H (2001) Riqueza de insectos cecidógenos en el dosel y sotobosque de dos zonas ecológicas en Panamá. Scientia (Panamá) 16: 17-42.
24. Paniagua MR, Medianero E, Lewis OT (2009) Structure and vertical stratification of plant galler-parasitoid food webs in two tropical forests. Ecol Entomol 34: 310-320.
25. Turner IM (1994) Sclerophylly: primarily protective? Funct Ecol 8: 669-675.
26. Prance GT (1979) Notes on the vegetation of Amazonia III. The terminology of Amazonian forest types subject to inundation. Brittonia 31: 26-38.
27. Pires JM (1985) The vegetation types of the Brazilian Amazon. In: Prance GT, Lovejoy TE, editors.Key environments: Amazonia.Oxford, UK: Pergamon Press. pp. 83-94.
28. Junk WJ (1983) As águas da região Amazônica. In: Salati E, Junk WJ, Shubart HOR, Oliveira A, editors. Amazônia: desenvolvimento, integração e ecologia.Brazil: Editora Brasiliense/CNPq. pp.45-100.
29. Junk WJ (1989) Flood tolerance and tree distribution in central Amazonian floodplains. In: Nielsen LB, Nielsen IC, Balslev H, editors.Tropical forests: botanical dynamics, speciation and diversity.London: Academic Press. pp. 47-64.
30. Haugaasen T, Peres CA (2006) Floristic, edaphic and structural characteristics of flooded and unflooded forests in the lower Rio Purús region of central Amazonia, Brazil. Acta Amaz 36: 25-36.
31. Pereira MJR, Marques JT, Palmeirim JM (2010). Vertical stratification of bat assemblages in flooded and unflooded Amazonian forests. Curr Zool 56: 469-478.
32. Junk WJ (1984) Ecology of the várzea, floodplain of Amazonian white water rivers. In: Sioli H, editor.The Amazon: Limnology and landscape ecology of a mighty tropical river and its basin.The Netherlands, Dordrecht: W. Junk Publishers. pp. 215-243.
33. Schöngart J, Piedade MTF, Wittmann F, Junk WJ, Worbes M (2005) Wood growth patterns of Macrolobium acaciifolium (Benth.) Benth. (Fabaceae) in Amazonian black-water and white-water floodploain forests. Oecologia 145: 454-461.
34. Oliveira AA, Mori SA (1999) A central Amazonian terra firme forest. I. High tree species richness on poor soils. Biodivers conserv 8: 1219-1244.
35. Powers JS, Treseder KK, Lerdau MT (2005) Fine roots, arbuscular mycorrhizal hyphae and soil nutrients in four neotropical rain forests: patterns across large geographic distances. New Phytol 165: 913-921.
36. Blanche KR, Westoby M (1995) Gall-forming insect diversity is linked to soil fertility via host plant taxon. Ecology 76: 2334-2337.
37. Southwood TRE (1960) The abundance of Hawaiian trees and the number of their associated insect species. Proc Hawaiian Entomol Soc 17: 229-303.
38. Fernandes GW (1992) Plant historical and biogeographical effects on insular gall-forming species richness. Global Ecol Biogeogr Lett 2: 71-74.
39. Wittmann F, Anhuf D, Junk WJ (2002) Tree species distribution and community structure of Central Amazonian várzea forests by remote sensing techniques. J Trop Ecol 18: 805-820.
40. Wittmann F, Junk WJ, Piedade MTF (2004) The várzea forests in Amazonia: flooding and the highly dynamic geomorphology interact with natural forest succession. Forest Ecol Manag 196: 199-212.
41. Bell AD, Bell A, Dines TD (1999) Branch construction and bud defense status at canopy surface of a West African rainforest. Biol J Linn Soc 66: 481-499.
42. Malcolm JR (1991). Comparative abundances of Neotropical small mammals by trap height. J Mammal 72: 188-192
43. Carneiro MAA, Branco CSA, Braga CED, Almada ED, Costa MBM, et al. (2009) Are gall midge species (Diptera: Cecidomyiidae) host plant specialists? Rev Bras Entomol 53: 365-378.
44. Crawley MJ (2007) The R Book. West Sussex, England, John Wiley & Sons. 942p.
45. Price PW (1991) Patterns in communities along latitudinal gradients. In: Price PW, Lewinsohn TM, Fernandes GW, Benson WW, editors.Plant-animal interactions: Evolutionary ecology in tropical and temperate regions.New York: John Wiley. pp. 51-70.
46. Wright MG, Samways MJ (1998) Insect species richness tracking plant species richness in a diverse flora: gall-insects in the Cape Floristic Region, South Africa. Oecologia 115: 427-433.
47. Yang MM, Tung GS (1998) The diversity of insect-induced galls on vascular plants in Taiwan: a preliminary report. In Csóka G, Mattson WJ, Stone GN, Price PW, editors. The Biology of Gall-Inducing Arthropods. General Technical Report NC-199, U. S. Department of Agriculture, Washington, USA. pp. 44-53.
48. Blanche KR, Ludwig JA (2001) Species richness of gall-inducing insects and host plants along an altitudinal gradient in Big Bend National Park, Texas. Am Midl Nat 145: 219-232.
49. Medianero E, Valderrama A, Barrios H (2003) Diversidad de insectos minadores de hojas y formadores de agallas en el dosel y sotobosque del bosque tropical. Acta Zool Mex 89: 153-168.
50. Sioli H (1991) Amazônia: fundamentos da ecologia da maior região de florestas tropicais. Rio de Janeiro, Brazil: Editora Vozes. 72 p.
51. Victoria RL, Martinelli LA, Cunha HB, Richey JE (2000) The Amazon basin and its natural cycles. In: Salati E, Absy ML, Victoria RL, editors.Amazônia: um ecossistema em transformação.Manaus: INPA, Brasília: CNPq. pp.163-214.
52. Franklin EN, Adis J, Woas S (1997) The Oribatid Mites. In: Junk WJ, editor.The Central-Amazonian Floodplain: Ecology of a Pulsing System. Ecological Studies.Vol. 126.Berlin, Heidelberg, New York: Springer Verlag. pp. 331-349.
53. Höfer H (1997) The spider communities. In: Junk WJ, editor.The Central-Amazonian Floodplain: Ecology of a Pulsing System. Ecological Studies.Vol. 126.Berlin, Heidelberg, New York: Springer Verlag. pp.373-383.
54. Prance GT (1989) American tropical forests. American tropical forests. In: Lieth H, Werger MJA, editors.Tropical rain forest ecosystems - biogeographical and ecological studies.Amsterdam: Elsevier Science Publishers. p. 99-132.
55. Kubitzki K (1989) The ecogeographical differentiation of Amazonian inundation forests. Plant Syst Evol 162: 285-304.
56. Worbes M (1997) The Forest Ecosystem of the Floodplain. In: Junk WJ, editor.The Central-Amazonian Floodplain: Ecology of a Pulsing System. Ecological Studies.Vol. 126.Berlin, Heidelberg, New York: Springer Verlag. pp. 223-266.
57. Sobrado MA (2010) Leaf characteristics, wood anatomy and hydraulic properties in tree species from contrasting habitats within upper Rio Negro forests in the Amazon region. J Trop Ecol 26: 215-226.
58. Sanches MC, Ribeiro SP, Dalvi VC, Silva Júnior MB, Sousa HC, et al. (2010) Differential leaf traits of a neotropical tree Cariniana legalis (Mart.) Kuntze (Lecythidaceae): comparing saplings and emergent trees. Trees 24: 79-88.
59. Tribuzy ES (2005) Variações da temperatura foliar do dossel e o seu efeito na taxa assimilatória de CO2 na Amazônia Central. Unpublished PhD thesis, Universidade de São Paulo, Brazil.
60. Doughty CE, Goulden ML (2008) Are tropical forests near a high temperature threshold? J Geophys Res 113: G00B07, doi: 10.1029/2007JG000632.
61. Tribuzy ES, Teixeira LM, Chambers JQ, Reis TS, Trumbore S, et al. (2003) Physiological responses of tree species growing under different site conditions in the Central Amazon. In: Seventh LBA-ECO Science Team Business Meeting, Fortaleza, Brazil. LBA/INPA/NASA. p. 94
62. Marenco RA, Gonçalves JFC, Vieira G (2001) Leaf gas exchange and carbohydrates in tropical trees differing in successional status in two light environments in central Amazonia. Tree Physiol 21: 1311-1318.
63. Gonçalves JFC, Vieira G, Marenco RA, Ferraz JBS, Santos Junior UM, et al. (2005) Nutritional status and specific leaf area of mahogany and tonka bean under two light environments. Acta Amaz 35:..23-27.
64. Camargo MAB, Marenco RA (2012) Growth, leaf and stomatal traits of crabwood (Carapa guianensis Aubl.) in central Amazonia. Revista Árvore 36: 07-16.
65. Groom PK, Lamont BB (1999) Which common indices of sclerophylly best reflect differences in leaf structure? Ecoscience 6, 471-474.
66. Lima CS, Torres-Boeger MR, Carvalho LL, Pelozzo A, Soffiatti P (2013) Sclerophylly in mangrove tree species from South Brazil. Rev Mex Biodiv 84: 1159-1166.
67. Junk WJ, Piedade MTF, Parolin P, Wittmann F, Schöngart J (2010) Ecophysiology, biodiversity and sustainable management of central Amazonian floodplain forests: A synthesis. In: Junk WJ, Piedade MTF, Wittmann F, Schöngart J, Parolin P, editors.Amazonian Floodplain Forests: Ecophysiology, Biodiversity and Sustainable Management.Dordrecht, Heidelberg, London, New York: Springer. pp. 511-540.
68. Waldhoff D, Parolin P (2010) Morphology and anatomy of leaves. In: Junk WJ, Piedade MTF, Wittmann F, Schöngart J, Parolin P, editors.Amazonian Floodplain Forests: Ecophysiology, Biodiversity and Sustainable Management.Dordrecht, Heidelberg, London, New York: Springer. pp.179-202.
69. Madeira JA, Maia VC, Monteiro RF (2002) Gall makers (Cecidomyiidae, Diptera) on Calophyllum brasiliense Camb. (Clusiaceae): descriptions and biology. Arch Mus Nac (Rio de J) 61: 31-48.
70. Ribeiro KT, Madeira JA, Monteiro RF (1998) Does flooding favour galling insects? Ecol Entomol 23: 491-494.
71. Fagundes MFS, Neves FS, Fernandes GW (2005). Direct and indirect interactions involving ants, insect herbivores and parasitoids on the host plant Baccharis dracunculifolia (Asteraceae). Ecol Entomol 30: 28-35.
72. Mendonça Jr MS (2007) Plant diversity and galling arthropod diversity searching for taxonomic patterns in an animal-plant interaction in the neotropics. Bol Soc Argent Bot 42: 347-357.
73. Fernandes GW, Almada ED, Carneiro MAA (2010) Gall-Inducing Insect Species Richness as Indicators of Forest Age and Health. Environ Entomol 39: 1134-1140.
74. Wright MG, Samways MJ (1996) Gall-insect species richness in the African Fynbos and Karoo vegetation: The importance of plant species richness. Biodiv Lett 3: 151-155.
75. Ribeiro SP, Borges PAV, Gaspar C, Melo C, Serrano ARM, et al. (2005) Canopy insect herbivores in the Azorean Laurisilva forests: key host plant species in a highly generalist insect community. Ecography 28: 315-330.
76. Carvalho-Fernandes SP (2010) Insetos galhadores associados à família Burseraceae da Reserva Florestal Ducke, Manaus-AM. Unpublished MSc thesis, Instituto Nacional de Pesquisas da Amazônia, Brazil.