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Leaf miner and plant galler species richness on Acacia: relative importance of plant traits and climate

  • Plant-Animal interactions - Original Paper
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Abstract

Diversity patterns of herbivores have been related to climate, host plant traits, host plant distribution and evolutionary relationships individually. However, few studies have assessed the relative contributions of a range of variables to explain these diversity patterns across large geographical and host plant species gradients. Here we assess the relative influence that climate and host plant traits have on endophagous species (leaf miners and plant gallers) diversity across a suite of host species from a genus that is widely distributed and morphologically variable. Forty-six species of Acacia were sampled to encapsulate the diversity of species across four taxonomic sections and a range of habitats along a 950 km climatic gradient: from subtropical forest habitats to semi-arid habitats. Plant traits, climatic variables, leaf miner and plant galler diversity were all quantified on each plant species. In total, 97 leaf mining species and 84 plant galling species were recorded from all host plants. Factors that best explained leaf miner richness across the climatic gradient (using AIC model selection) included specific leaf area (SLA), foliage thickness and mean annual rainfall. The factor that best explained plant galler richness across the climatic gradient was C:N ratio. In terms of the influence of plant and climatic traits on species composition, leaf miner assemblages were best explained by SLA, foliage thickness, mean minimum temperature and mean annual rainfall, whilst plant gall assemblages were explained by C:N ratio, %P, foliage thickness, mean minimum temperature and mean annual rainfall. This work is the first to assess diversity and structure across a broad environmental gradient and a wide range of potential key climatic and plant trait determinants simultaneously. Such methods provide key insights into endophage diversity and provide a solid basis for assessing their responses to a changing climate.

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References

  • Abrahamson WG, Hunter MD, Melika G, Price PW (2003) Cynipid gall-wasp communities correlate with oak chemistry. J Chem Ecol 29:208–223. doi:10.1007/s11284-008-0541-x

    Article  Google Scholar 

  • Anderson DL, Henderson LJ (1986) Sealed chamber digestion for plant nutrient analysis. Agron J 78:937–938

    Article  CAS  Google Scholar 

  • Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA+ for PRIMER: guide to software and statistical methods. PRIMER-E, Plymouth

    Google Scholar 

  • Andrew NR, Hughes L (2004) Species diversity and structure of phytophagous beetle assemblages along a latitudinal gradient: predicting the potential impacts of climate change. Ecol Entomol 29:527–542. doi:10.1111/j.0307-6946.2004.00639.x

    Article  Google Scholar 

  • Andrew NR, Hughes L (2005a) Diversity and assemblage structure of phytophagous Hemiptera along a latitudinal gradient: predicting the potential impacts of climate change. Glob Ecol Biogeogr 14:249–262. doi:10.1111/j.1466-822x.2005.00149.x

  • Andrew NR, Hughes L (2005b) Herbivore damage along a latitudinal gradient: relative impacts of different feeding guilds. Oikos 108:176–182. doi:10.1111/j.0030-1299.2005.13457.x

    Article  Google Scholar 

  • Andrew NR, Hughes L (2008) Abundance-body mass relationships among insects along a latitudinal gradient. Aust Ecol 33:253–260. doi:10.1111/j.1442-9993.2007.01804.x

    Article  Google Scholar 

  • Austin AD, Dangerfield PC (1998) Biology of Mesostoa kerri (Insecta: Hymenoptera: Braconidae: Mesostoinae), an emdemic Australian wasp that causes stem galls on Banksia marginata. Aust J Bot 46:559–569. doi:10.1071/BT97042

    Article  Google Scholar 

  • Baust JG, Grandee R, Condon G, Morrissey RE (1979) The diversity of overwintering strategies utilized by separate populations of gall insects. Physiol Zool 52:572–580

    Google Scholar 

  • Bernays EA, Graham M (1988) On the evolution of host specificity in phytophagous arthropods. Ecology 69:886–894

    Article  Google Scholar 

  • 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. doi:10.1046/j.1442-9993.2000.01040.x

    Google Scholar 

  • 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 Mid Nat 145:219–232

    Article  Google Scholar 

  • Blanche KR, Westoby M (1995) Gall-forming insect diversity is linked to soil fertility via host plant taxon. Ecology 76:2334–2337. doi:10.2307/1941706

    Article  Google Scholar 

  • Blanche KR, Westoby M (1996) The effect of the taxon and geographic range size of host eucalypt species on the species richness of gall-forming insects. Aust J Ecol 21:332–335. doi:10.1111/j.1442-9993.1996.tb00616.x

    Article  Google Scholar 

  • BOM (2008) Australian Climate Statistics, vol. 2008. Department of Environment, Water, Health and Arts, Canberra

  • Carneiro MAA, Fernandes GW, De Souza OFF (2005) Convergence in the variation of local and regional galling species richness. Neotrop Entomol 34:547–553. doi:10.1590/S1519-566X2005000400003

    Article  Google Scholar 

  • Clarke KR, Gorley RN (2006) PRIMER v6 user manual/tutorial. PRIMER-E, Plymouth

    Google Scholar 

  • Coley PD, Bryant JP, Chapin FS (1985) Resource availability and plant antiherbivore defense. Science 230:895–899. doi:10.1126/science.230.4728.895

    Article  PubMed  CAS  Google Scholar 

  • Colwell RK (2006) EstimateS: statistical estimation of species richness and shared species from samples, version 8. http://purl.oclc.org/estimates

  • Connor EF, Taverner MP (1997) The evolution and adaptive significance of the leaf-mining habit. Oikos 79:6–25

    Article  Google Scholar 

  • Connor EF, Adamsmanson RH, Carr TG, Beck MW (1994) The effects of host plant phenology on the demography and population dynamics of the leaf-mining moth, Cameraria hamadryadella (Lepidoptera: Gracillariidae). Ecol Entomol 19:111–120. doi:10.1111/j.1365-2311.1994.tb00400.x

    Article  Google Scholar 

  • Cornell HV (1985) Local and regional richness of cypine wasps on california oaks. Ecology 66:1247–1260. doi:10.2307/1939178

    Article  Google Scholar 

  • Crespi BJ, Carmean DA, Chapman T (1997) Ecology and evolution of galling thrips and their allies. Ann Rev Entomol 42:51–71. doi:10.1146/annurev.ento.42.1.51

    Article  CAS  Google Scholar 

  • Crespi BJ, Morris DC, Mound LA (2004) Evolution of behavioural and ecological diversity: Australian Acacia thrips as model organisms. ABRS, Canberra

  • CSIRO (2007) Climate change in Australia: observed changes and projections. http://www.climatechangeinaustralia.gov.au

  • Cuevas-Reyes P, Siebe C, Martínez-Ramos M, Oyama K (2003) Species richness of gall-forming insects in a tropical rain forest: correlations with plant diversity and soil fertility. Biodiv Conserv 12:411–422. doi:10.1023/A:1022415907109

    Article  Google Scholar 

  • 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. doi:10.1111/j.0030-1299.2004.13263

    Article  Google Scholar 

  • Cunningham SA, Summerhayes B, Westoby M (1999) Evolutionary divergences in leaf structure and chemistry, comparing rainfall and soil nutrient gradients. Ecol Monogr 69:569–588. doi:10.1890/0012-9615(1999)069[0569:EDILSA]2.0.CO;2

    Article  Google Scholar 

  • Dethier VG (1952) Evolution of feeding preferences in phytophagous insects. Evolution 8:33–54

    Article  Google Scholar 

  • Espirito-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

    Article  Google Scholar 

  • Faeth SH, Connor EF, Simberloff D (1981a) Early leaf abscission: a neglected source of mortality for folivores. Am Nat 117:409–415. doi:10.1086/283724

    Google Scholar 

  • Faeth SH, Mopper S, Simberloff D (1981b) Abundances and diversity of leaf-mining insects on three oak host species: effects of host-plant phenology and nitrogen content of leaves. Oikos 37:238–251

    Article  Google Scholar 

  • Feeny P (1975) Biochemical coevolution between plants and their insect herbivores. In: Gilbert LE, Raven PH (eds) Coevolution of animals and plants. University of Texas Press, Austin, pp 3–19

    Google Scholar 

  • Fernandes GW, Price PW (1988) Biogeographical gradients in galling species richness. Oecologia 76:161–167. doi:10.1007/BF00379948

    Article  Google Scholar 

  • Fernandes GW, Price PW (1991) Comparison of tropical and temperate galling species richness: the roles of environmental harshness and plant nutrient status. In: Price PW, Lewinsohn TM, Fernandes GW, Benson WW (eds) Plant–animal interaction: evolutionary ecology in tropical and temperate regions. Wiley, London, pp 91–115

    Google Scholar 

  • Fernandes GW, Price PW (1992) The adaptive significance of insect gall distribution: suvivorship of species in xeric and mesic habitats. Oecologia 90:14–20. doi:10.1007/BF00317803

    Article  Google Scholar 

  • Fernandes GW, Castro FMC, Faria ML, Marques ESA, Greco MKB (2004) Effects of hygrothermal stress, plant richness, and architecture on mining insect diversity. Biotropica 36:240–247. doi:10.1111/j.1744-7429.2004.tb00315.x

    Google Scholar 

  • Ferrier SM, Price PW (2004) Oviposition preference and larval performance of a rare bud-galling sawfly (Hymenoptera: Tenthredinidae) on willow in Northern Arizona. Environ Entomol 33:700–708

    Article  Google Scholar 

  • Fuentes-Contreras E, Gianoli E, Caballero PP, Niemeyer HM (1999) Influence of altitude and host-plant species on gall distribution in Colliguaja spp. (Euphorbiaceae) in central Chile. Rev Chile Hist Nat 72:305–313

    Google Scholar 

  • Gaston KJ, Reavey D, Valladares GR (1992) Intimacy and fidelity: internal and external feeding by the British microlepidoptera. Ecol Entomol 17:86–88. doi:10.1111/j.1365-2311.1992.tb01044.x

    Article  Google Scholar 

  • Goncalves-Alvim SJ, Fernandes GW (2001) Biodiversity of galling insects: historical, community and habitat effects in four neotropical savannas. Biodiv Conserv 10:79–98. doi:10.1023/A:1016602213305

    Article  Google Scholar 

  • Hairston NG, Smith FE, Slobodkin LB (1960) Community structure, population control, and competition. Am Nat 94:421–425. doi:10.1086/282146

    Article  Google Scholar 

  • Hartley SE, Jones CG (1997) Plant chemistry and herbivory, or why the world is green. In: Crawley MJ (ed) Plant ecology. Blackwell, London, pp 284–324

    Google Scholar 

  • Hering EM (1951) Biology of the leaf miners. Kluwer, The Hague

  • Hespenheide HA (1991) Bionomics of leaf-mining insects. Ann Rev Entomol 36:535–560. doi:0.1146/annurev.en.36.010191.002535

    Google Scholar 

  • Hnatiuk RJ, Maslin BR (1988) Phytogeography of Acacia in Australia in relation to climate and species-richness. Aust J Bot 36:361–383. doi:10.1071/BT9880361

    Google Scholar 

  • Hodkinson ID, Bird J, Miles JE, Bale JS, Lennon JJ (1999) Climatic signals in the life histories of insects: the distribution and abundance of heather psyllids (Strophingia spp.) in the UK. Funct Ecol 13:83–95

    Google Scholar 

  • Houlder DJ, Hutchinson MF, Nix HA, McMahon JP (2000) ANUCLIM user guide, version 5.1. Centre for Resource and Environmental Studies, Australian National University, Canberra

  • Landsberg J, Gillieson DS (1995) Regional and local variation in insect herbivory, vegetation and soils of eucalypt associations in contrasted landscape positions along a climatic gradient. Aust J Ecol 20:299–315. doi:10.1111/j.1442-9993.1995.tb00542.x

    Article  Google Scholar 

  • Lara ACF, Fernandes GW, Goncalves-Alvim SJ (2002) Tests of hypotheses on patterns of gall distribution along an altitudinal gradient. Trop Zool 15:219–232

    Google Scholar 

  • Lopez-Vaamonde C, Godfray HCJ, Cook JM (2003) Evolutionary dynamics of host-plant use in a genus of leaf-mining moths. Evolution 57:1804–1821. doi:10.1111/j.0014-3820.2003.tb00588.x

    PubMed  Google Scholar 

  • Majer JD, Recher HF, Ganeshanandam S (1992) Variation in foliar nutrients in Eucalyptus trees in eastern and Western Australia. Aust J Ecol 17:383–393. doi:10.1111/j.1442-9993.1992.tb00821.x

    Article  Google Scholar 

  • Marques ESD, Price PW, Cobb NS (2000) Resource abundance and insect herbivore diversity on woody fabaceous desert plants. Environ Entomol 29:696–703

    Article  Google Scholar 

  • Maslin BR (2004) Classification and phylogeny of Acacia. In: Crespi B, Morris DC, Mound LA (eds) Evolution of ecological and behavioural diversity: Australian Acacia thrips as model organisms. ABRS, Canberra, pp 97–112

    Google Scholar 

  • Matson P, Johnson L, Billow C, Miller J, Pu R (1994) Seasonal patterns and remote spectral estimation of canopy chemistry across the Oregon Transect. Ecol Appl 4:280–298. doi:10.2307/1941934

    Article  Google Scholar 

  • Mazerolle MJ (2006) Improving data analysis in herpetology: using Akaike’s information criterion (AIC) to assess the strength of biological hypotheses. Amphib Rept 27:169–180. doi:10.1163/156853806777239922

    Google Scholar 

  • McDonald PGM, Fonseca CR, Overton JM, Westoby M (2003) Leaf-size divergence along rainfall and soil-nutrient gradients: is the method of size reduction common among clades? Funct Ecol 17:50–57

    Article  Google Scholar 

  • Medina E, Garcia V, Cuevas E (1990) Sclerophylly and oligotrophic environments: relationships between leaf structure, mineral nutrient content, and drought resistance in tropical rain forests of the Upper Rio Negro region. Biotropica 22:51–64

    Google Scholar 

  • Memmott J, Godfray HCJ, Gauld ID (1994) The structure of a tropical host–parasitoid community. J Anim Ecol 63:521–540

    Google Scholar 

  • Miller JT, Bayer RJ (2001) Molecular phylogenetics of Acacia (Fabaceae: Mimosoideae) based on the chloroplast matK coding sequence and flanking trnK intron spacer regions. Am J Bot 88:697–705

    Article  CAS  PubMed  Google Scholar 

  • Mittelbach GG et al (2007) Evolution and the latitudinal diversity gradient: speciation, extinction and biogeography. Ecol Lett 10:315–331. doi:10.1111/j.1461-0248.2007.01020.x

    Article  PubMed  Google Scholar 

  • Mooney HA, Gulmon SL (1982) Constraints on leaf structure and function in reference to herbivory. Bioscience 32:198–206

    Article  CAS  Google Scholar 

  • Mooney HA, Ferrar PJ, Slatyer RO (1978) Photosynthetic capacity and carbon allocation patterns in diverse growth forms of Eucalyptus. Oecologia 36:103–111. doi:10.1007/BF00344575

    Google Scholar 

  • Morris DC, Schwarz MP, Crespi BJ (2002) Pleometrosis in phyllode-glueing thrips (Thysanoptera: Phlaeothripidae) on Australian Acacia. Biol J Linn Soc 75:467–474. doi:10.1046/j.1095-8312.2002.00033.x

    Google Scholar 

  • Novotny V, Basset Y, Miller SE, Drozd P, Cizek L (2002) Host specialization of leaf-chewing insects in a New Guinea rainforest. J Anim Ecol 71:400–412. doi:10.1046/j.1365-2656.2002.00608.x

    Article  Google Scholar 

  • Orians GH, Milewski AV (2007) Ecology of Australia: the effects of nutrient-poor soils and intense fires. Biol Rev 82:393–423. doi:10.1111/j.1469-185X.2007.00017.x

    Article  PubMed  Google Scholar 

  • Pedley L (1978) A revision of Acacia Mill. in Queensland. Austrobaileya 1:75–234

    Google Scholar 

  • Price PW (1991) Patterns in communities along latitudinal gradients. In: Price PW, Lewinsohn TM, Fernandes GW, Benson WW (eds) Plant–animal interaction: evolutionary ecology in tropical and temperate regions. Wiley, London, pp 51–69

    Google Scholar 

  • Price PW, Fernandes GW, Waring GL (1987) Adaptive nature of insect galls. Environ Entomol 16:15–24

    Google Scholar 

  • Price PW et al (1998) Global patterns in local number of insect galling species. J Biogeogr 25:581–591. doi:10.1046/j.1365-2699.1998.2530581.x

    Article  Google Scholar 

  • Rangel TFLVB, Diniz-Filho JAF, Bini LM (2006) Towards an integrated computational tool for spatial analysis in macroecology and biogeography. Glob Ecol Biogeogr 15:321–327. doi:10.1111/j.1466-822x.2006.00237.x

    Article  Google Scholar 

  • Schoonhoven LM, Loon JJA, Dicke M (2005) Insect–plant biology, 2nd edn. Oxford University Press, Oxford

  • Scriber JM (1977) Limiting effects of low leaf-water content on the nitrogen utilization, energy budget, and larval growth of Hyalophora cecropia (Lepidoptera: Saturniidae). Oecologia 28:269–287. doi:10.1007/BF00751605

  • Sinclair RJ, Hughes L (2008) Incidence of leaf mining in different vegetation types across rainfall, canopy cover and latitudinal gradients. Aust Ecol 33:353–360. doi:10.1111/j.1442-9993.2007.01825.x

    Article  Google Scholar 

  • Speight MR, Hunter MD, Watt AD (1999) Ecology of insects: concepts and applications. Blackwell, Oxford

  • Steffen W et al (2009) Australia’s biodiversity and climate change: summary for policy makers. Australian Government, Canberra

  • Strong DR, Lawton JH, Southwood TRE (1984) Insects on plants. Community patterns and mechanisms. Harvard University Press, Cambridge

  • Turner IM (1994) Sclerophylly: primarily protective? Funct Ecol 8:669–675

    Google Scholar 

  • 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. doi:10.1111/j.1442-9993.2003.tb00221.x

    Article  Google Scholar 

  • Waring GL (1986) Galls in harsh environments. Proc Entomol Soc Wash 88:376–380

    Google Scholar 

  • Whitham TG (1980) The theory of habitat selection: examined and extended using pemphigus aphids. Am Nat 115:449–466. doi:10.1086/283573

    Article  Google Scholar 

  • 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. doi:10.1007/s004420050537

    Article  Google Scholar 

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Acknowledgments

We thank National Parks and Wildlife NSW and Forests NSW for access and logistical support at field sites. We thank Matt Binns for assistance in accessing field site meteorological data and map generation. The work was funded by an Australian Research Council (ARC) Discovery Grant (DP0769961) to N.R. Andrew and M.A. McGeoch.

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  1. Centre for Behavioural and Physiological Ecology, Zoology, University of New England, Armidale, NSW, 2351, Australia

    Katy A. Bairstow, Kerri L. Clarke & Nigel R. Andrew

  2. Centre for Invasion Biology, Department of Conservation Ecology and Entomology, University of Stellenbosch, Private Bag X1, Matieland, 7602, South Africa

    Melodie A. McGeoch

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  1. Katy A. Bairstow
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  2. Kerri L. Clarke
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  3. Melodie A. McGeoch
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  4. Nigel R. Andrew
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Correspondence to Nigel R. Andrew.

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Communicated by Sven Bacher.

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Bairstow, K.A., Clarke, K.L., McGeoch, M.A. et al. Leaf miner and plant galler species richness on Acacia: relative importance of plant traits and climate. Oecologia 163, 437–448 (2010). https://doi.org/10.1007/s00442-010-1606-4

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