Oecologia (2003) 135:442-450 DOI 10. 1007/s00442-003-1212-9 Valerie Fournier * Jay A. Rosenheim a Jacques Brodeur *Lee 0. Laney *Marshall W. Johnson Herbivorousmites as ecological engineers: indirecteffects on arthropodsinhabiting papaya foliage Received: 28 October 2002 / Accepted: 4 February2003 / Published online: 11 March 2003 ? Springer-Verlag2003 Abstract We examined the potential of a leaf roller to Introduction indirectly influence a community of arthropods. Two mite species are the key herbivores on papaya leaves in Ecologists are increasingly appreciating the importance of Hawaii: a spider mite, Tetranychus cinnabarinus Boisdu- indirect interactions in structuring animal communities val, and an eriophyid mite, Calacarus flagelliseta, which (Strauss 1991; Wootton 1994; Polis and Winemiller 1996; induces upward curling of the leaf margin at the end of Janssen et al. 1998). For arthropod communities in the summer when populations reach high densities. A particular, indirect interactions can be mediated by survey and three manipulative field experiments demon- shelters created by one species and subsequently used strated that (1) leaf rolls induce a consistent shift in the by another species (Damman 1993). spatial distribution of spider mites and their predators, the Shelter building through leaf rolling, folding, or tying coccinellid Stethorus siphonulus Kapur, the predatory is a common behavior among several arthropod taxa, mites Phytoseiulus spp., and the tangle-web building including caterpillars (Lepidoptera), sawflies (Hymenop- spider Nesticodes rufipes Lucas; (2) the overall abun- tera: Pamphiliidae), weevils (Coleoptera: Attelabidae), dance of spiders increases on leaves with rolls; (3) the and herbivorous mites in the superfamily Eriophyoidea specialist predators Stethorus and Phytoseiulus inhabit the (Acari) (Frost 1959; Keifer et al. 1982; Castagnoli 1996; rolls in response to their spider mite prey; and (4) the Westphal and Manson 1996). By protecting residents spider inhabits the rolls in response to the architecture of from natural enemies, providing a suitable microenviron- the roll itself. This study shows the importance of indirect ment for development, or reducing effects of plant effects in structuring a terrestrial community of herbi- defenses, leaf shelters may have strong impacts on the vores. survivorship, abundance, distribution, and diversity of other plant-dwelling arthropods(reviewed in Fukui 2001). Keywords Herbivory Leaf rolling * Plant architecture* For example, leaf rolling by early-season lepidopterans Spider facilitates later colonization and survival by late-season lepidopterans (Cappuccino 1993). Leaf rolls made by lepidopteran larva on cottonwood trees enhance arthropod abundance sevenfold and biodiversity fourfold (Martinsen V. Foumier (X) - J. A. Rosenheim et al. 2000). Leaf rollers exemplify "bioengineers" or Departmentof Entomology, "physical ecosystem engineers," organisms that directly University of California, CA 95616 Davis, USA or indirectly control the availability of resources to other e-mail: [email protected] Fax: 1-530-7521537 organisms by causing physical state changes in biotic and abiotic materials (Jones et al. 1997). V. Foumier * L. 0. Laney * M. W. Johnson Here we report a study in which a herbivorous mite Departmentof Plant and EnvironmentalSciences, modifies the architecture of its host plant, papaya, by University of Hawaii at Manoa, HI 96822 Honolulu, USA inducing leaf rolls. We conducted a survey and three manipulative field experiments to address the following J. Brodeur questions: (1) Do leaf rolls modify the spatial distribution Departementde Phytologie, of foliar arthropods in the community? (2) Do leaf rolls Gl K 7P4, Canada Universite Laval, Ste-Foy, Quebec, change the population densities of arthropods in the Present address: community? (3) Do predators colonize leaf rolls in M. W. Johnson, Departmentof Entomology, response to the architecture of the rolled leaf itself or in University of California, response to spider mite prey? Riverside, CA 92521, USA This content downloaded from 169.237.77.249 on Thu, 4 Sep 2014 13:15:17 PM All use subject to JSTOR Terms and Conditions 443 Materialsand methods leaves (V. Fournier, unpublished data). These herbivorous mites tend to shift to the upper (adaxial) leaf surface when densities on Study system the lower surfacebecome high (>10,000 adults/leaf).When moving from the lower to the upper surface of the leaf, the mites first infest Papaya (Carica papaya L., Caricaceae) is a short-lived perennial the upper leaf margin and induce the edge to curl upward.Curling crop, native to Central America (Storey 1976). Papaya trees in may occur on some or all of the fingers of a leaf, with a heavily commercialorchards typically consist of a single erect stem with a infested leaf supportingfrom 25 to 45 rolled leaf segments. When terminalcrown of about 25-30 large leaves. The midrib of mature leaf rolling is very severe, the rolls may form complete tubes. Rolls leaves reaches 35-40 cm in length, and the total leaf area averages are about 10 cm in length and 2 cm in diameter. Usually, only the approximately 1,000 cm2. Leaves are held on long petioles (45- leaves located in the middle and lowest parts of the canopy crown 70 cm in length) that extend horizontally from the trunk. New are affected by rolling (V. Foumier, personal observation). leaves are producedyear-round, emerging from the growing point Calacarus infests papaya all year long, but leaf rolling is mostly at the tip of the trunk.They are palmatelylobed and usually possess observed in the late summer, when population densities peak (V. seven major fingers, each of which is subdivided into 3-8 minor Foumier, unpublisheddata). fingers, for a total of 40-50 fingers per leaf (Fig. 1). The life span of When papaya leaves are unrolled, the spider mite and its a papayaleaf varies from 75 to 125 days in a pesticide-freeorchard predators usually inhabit the lower leaf surfaces (Esguerra and (V. Foumier, unpublisheddata). Haramoto 1980). However, when the leaves are rolled by The community of arthropods inhabiting papaya foliage in Calacarus mites, preliminaryobservations suggested that members Hawaii includes two key herbivorous mites: the host-specific of the arthropodcommunity may colonize the upper surfaces of eriophyid mite, Calacarusflagelliseta Fletchmann,DeMoraes, and leaves within the leaf rolls and coexist there with the leaf edgeroller Barbosa (Acari: Eriophyidae),and the polyphagouscarmine spider mites. mite, Tetranychuscinnabarinus Boisduval (Acari: Tetranychidae). The most common predatorsin the system are the predatorymites Phytoseiulus macropilis Banks and P. persimilis Athias-Henriot Experimentalsite (Acari: Phytoseiidae), the beetle Stethorus siphonulus Kapur (Coleoptera: Coccinellidae), and the tangle-web building spider Our researchwas conducted at the University of Hawaii Poamoho Nesticodes rufipes Lucas (Araneae: Theridiidae) (Esguerra and Experimental Station on Oahu, Hawaii, during the summers of Haramoto 1980; Rosenheim et al., unpublisheddata). The phyto- 2001 and 2002. Trees used in this study were from pesticide-free seiid mites and the coccinellid are specialist consumers of spider papaya plots (Solo variety, cv. X77). They were 8 months old and mites (Prasad1973; Raros and Haramoto1974), whereas the spider approximately1.75 m tall in 2001 and 20 months old and 3.5 m tall Nesticodes, which spins a sparse and hardlydiscernable web at the in 2002. junction of leaf veins, is a generalistthat preys upon a wide variety of arthropods(Barreto et al. 1987; Cushing and LeBeck 1994; Fox 1998), including the carmine spider mite (Esguerraand Haramoto Survey 1980), Stethorus,and Phytoseiulus spp. (Rosenheim et al., unpub- lished data) (Fig. 2). No naturalenemies of the eriophyid mite are We measured arthropod distribution and abundance on papaya known to occur in Hawaii (V. Fournier,personal observation). leaves with and without rolls. We censused insects, mites, and The eriophyid Calacarus can colonize both the surfaces of arachnids on 13-16 August 2001, when the density of the leaf papaya leaves and the fruits (C. citrifolii in Jeppson et al. 1975; edgeroller mite population peaked and leaves began to roll. We Fletchmannet al. 2001), but it prefersthe lower (abaxial)surface of surveyed 50 mid-crown leaves, 25 with rolls and 25 without rolls, F-qb-?.to 4 1~~~~~~-14 7 11r# s' Fig. 1 Carica papaya leaf and a leaf roll. Papaya leaves are densities of Calacarusflagelliseta peak and trigger the edge of the palmately lobed and usually possess seven major fingers, each of leaves to curl upward,each one of the minor fingers can roll and which is subdivided into three to eight minor fingers. When form a complete tube This content downloaded from 169.237.77.249 on Thu, 4 Sep 2014 13:15:17 PM All use subject to JSTOR Terms and Conditions 444 were randomly assigned to one of three treatments:(1) no rolls Nesticodes (unmanipulatedcontrol); (2) presence of wires or rubberbands but no rolls (wire/rubberband control); or (3) artificial rolls. Identical numbers of rubberbands or wire rings were used in treatments2 and 3. Experiment la comprised 30 replicatesof each treatment(total of 90 leaves) distributedover 22 trees. Experimentlb comprised51 Stethorus Phytoseiulus spp. replicates of each treatment(total of 153 leaves) over 37 trees. All experimental leaves were located at the mid-crown height of the trees to standardize leaf age and reduce the effect of leaf senescence.