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Birds using honeydew reduce herbivory
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Birds using honeydew reduce leaf herbivory on scale insects’ host plant—tritrophic
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interactions in Mexican forests
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Heather A. Gamper1 and Suzanne Koptur
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Department of Biological Sciences, Florida International University, Miami, FL 33199
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USA
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Tallahassee, FL 32306-1100, USA. E-mail: gamper@bio.fsu.edu
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Present address: Department of Biological Science, Florida State University,
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ABSTRACT
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Honeydew, a sugar solution produced as waste by phloem-feeding insects, is commonly a
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prized food for ants, which may serve to protect the insects’ host plant by reducing the
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number of other herbivorous insects. A wide variety of birds both eat arthropods and use
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the honeydew produced by the scale insect Stigmacoccus garmilleri (family
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Margarodidae), which is associated with oak trees (Quercus spp.) in Mexican forests. By
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removing potential leaf-chewing insects, birds may aid the plant by reducing the amount
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of leaf area lost, as do the ants in ant-honeydew systems. We used bird exclosures to
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examine experimentally the indirect effects of birds on leaf damage on oak trees
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harboring scale insects. Leaves on the branches from which birds were excluded
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sustained substantially more damage than those on control branches, a result that suggests
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that birds may decrease herbivory on trees harboring both scale insects and other
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herbivorous insects.
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Keywords: honeydew, herbivory, birds, Margarodidae, Quercus spp., exclosures
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INTRODUCTION
Herbivores can put strong selective pressure on plants by removing plant biomass
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that might have been used for growth or reproduction (Coley et al. 1985). An extensive
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literature addresses ants and the negative impact they often have on herbivorous insect
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populations, which results in protection of the plant on which they live (reviewed in
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Hölldobler & Wilson 1990). Ants that forage on scale-insect honeydew have been shown
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to reduce the number of herbivorous insects and protect the host plant (e.g. Bach 1991,
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Gaume et al. 1998). Previous studies (e.g. Holmes et al. 1979, Gradwohl & Greenberg
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1982, Loyn et al. 1983, Fowler et al. 1991, Bock et al. 1992, Gunnarsson 1996) have
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shown that birds also significantly reduce the number of herbivorous insects on plants.
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Several experiments, in addition, demonstrated a decrease in plant damage by
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herbivorous insects in the presence of insectivorous vertebrates (Atlegrim 1989; Spiller &
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Schoener 1990a, b; Marquis & Whelan 1994; Dial & Roughgarden 1995; Greenberg et
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al. 2000; Sanz 2001).
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A honeydew-producing scale insect, Stigmacoccus garmilleri (family
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Margarodidae, tribe Xylococcini), is associated with the trunk and branches of Quercus
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spp. in highland forests of Mexico. This relationship was first described from San
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Cristobal, Chiapas (Greenberg et al. 1993); Quercus spp. in forests of Chiconquiaco,
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Veracruz, were found to have the same scale insects, and this interaction probably occurs
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in other highland areas of Mexico. Migratory birds were found to compete aggressively
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for scale-insect honeydew during winter months in Chiapas (Greenberg et al. 1993) and
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in this system in Chiconquiaco. Trees with scale insects have a characteristic appearance,
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visible even from a distance: their trunks and branches are covered with a black sooty
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mold growing on the copious accumulated honeydew.
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The study site is located in humid, montane forests between 1950 and 2100 m in
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elevation. Most studies have found that the highest ant species richness and abundance
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occur at low or intermediate elevations (Koptur 1985, Samson et al. 1997, Sanders et al.
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2003). Fifty km east of the study area, at sea level, 30 species of ants associated with
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plants were documented in coastal habitat (Rico-Gray 1993). Sanders et al. (2003) found
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that, over the approximate elevation range of 900–2300 m in the tropics, ant species
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richness decreased with increasing elevation. A study conducted at elevations and in
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forests similar to those in our study area in Mexico found the same tendency in the
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number of ant species (Diaz-Castelazo & Rico-Gray 1998).
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The members of the Margarodidae are unique in that the immature instars bear
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long anal tubes, and honeydew is presented at a distance from the body (Gullan and
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Kosztarab 1997). The immature instars of S. garmilleri position themselves within the
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bark of the tree in small cracks and fissures, and each releases honeydew at the tip of a
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long anal filament (averaging 10 cm in length), a substantial distance from the plant
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surface (Fig. 1). In addition to possible geographical constraints on their distribution,
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ants may therefore find access to the honeydew droplets difficult.
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The effect of insectivory by vertebrates has been evaluated through both
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exclosure experiments (e.g. Holmes et al. 1979, Atlegrim 1989, Spiller & Schoener
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1990b, Bock et al. 1992, Marquis & Whelan 1994, Murakami & Nakano 2000) and
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vertebrate-removal experiments (Loyn et al. 1983, Dial & Roughgarden 1995, Jäntti et al.
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2001). Many experiments (with the exception of Forkner & Hunter 2000 and Wiens et
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al. 1991) have demonstrated a significant impact on arthropods by foraging birds or
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lizards. Many avian exclosure experiments have been conducted in grasslands, temperate
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forests, or marine systems, but few have been conducted in tropical systems. Gradwohl
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& Greenberg (1982) and Greenberg et al. (2000) found that avian exclosures increased
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the number of herbivorous insects in moist tropical understory in Panama and in
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Guatemalan coffee plantations.
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Our study explored the impact of birds on arthropod-caused leaf damage on trees
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with scale-insect colonies in high-elevation oak forests of mainland Mexico. We used
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field experiments to test the hypothesis that, like ants, birds protect plants against insect
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herbivores. We hypothesized that leaf damage would be greater on branches from which
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birds were excluded than on control branches, that is, that birds (the third trophic level)
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would modify the interaction between the first and second trophic levels (plant and
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herbivorous insects, respectively).
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METHODS
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Our study was conducted in the township of Chiconquiaco, Veracruz, Mexico
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(19°43’60 N, 96°46’0 W; 15ºC mean annual temperature; 1532 mm mean annual
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precipitation). This area has three seasons: a somewhat dry and cool season from
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October to March, a dry warm season from April to May, and a wet warm season from
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June to September (Williams-Linera et al. 2000). The area is covered by heavy fog on
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most days. The forest in this area is approximately 2010 m in elevation, and the habitat is
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a mosaic of mature forest patches, cow pastures, and small corn fields. The experimental
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trees were located within a forest remnant (ca. 25 ha) on a west-facing slope with a
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canopy of Quercus spp. Several species of oaks have been identified from the study area
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(Q. laurina, Q. germana, Q. salicifolia, Q. corrugata, Q. affinis, and Q. xalapensis) and
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they are all apparently capable of hosting the scale insects.
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A total of 40 trees were chosen for intense study. All trees chosen had colonies of
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scale insects producing honeydew, though not all trees at each site had scale-insect
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colonies. The number and species of birds visiting the tree, the total time spent in the tree
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by each individual bird, and food items taken were recorded during hour-long
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observation periods at focal trees. All individual trees were observed on four occasions
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(distributed evenly within morning and afternoon hours) between March 2002 and May
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2002, for a total of 160 hours of bird observation.
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On two occasions, 31 May 2003 and 5 June 2003, we placed ant baits to examine
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the ant species composition in the area. Petri dishes, baited alternately with tuna and
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honey, were placed in line transects of 16 baits at 4-m intervals. Baits were then checked
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at 30-min intervals for 90 min. Two transects were run simultaneously in different
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habitat types, and ant numbers and morphospecies were recorded. Forest, pasture, and
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edge habitat types were sampled. Time to discovery was calculated for each bait (120
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min was used for undiscovered baits, resulting in a somewhat exaggerated picture of ant
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activity on the transects). Specimens of ants were preserved in alcohol and later pointed
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and sent for identification (to W. P. MacKay, University of Texas, El Paso). Analysis-of-
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variance tests evaluated the effects of habitat type, food type, date of sampling, and
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sampling area on the number of baits discovered and the average number of ants
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encountered in each Petri dish.
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We chose the most isolated forest area for the exclosure experiments to decrease
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the possibility that the netting would be removed by humans. Although scale insects are
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found on pasture and forest-edge trees, we chose trees in the forest interior to minimize
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human interference. Branches of oak trees on which the majority of leaves were new
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(and nearly fully expanded) were selected. On four experimental trees, four branches of
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similar size were selected, for a total of 16 branches. Two branches in each tree were
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covered by bird exclosures, and two, approximately equal size and similar foliage
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density, were marked as controls. Treatments were assigned to branches randomly. On
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each branch, 25 new, undamaged leaves were individually labeled with numbered tags
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(colored pigeon bands, National Band & Tag Co., Newport, KY, USA) and their areas
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estimated with the aid of a clear plastic ruler marked with 5-mm squares.
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The exclosures were left in place from 5 April 2003 to 1 July 2003. Leaf damage,
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the response variable, was expressed as the proportion of the originally measured leaf
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area missing or affected (the number of 5-mm squares of which at least 50% of the area
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was missing or affected) at the end of the exclosure period. Missing parts of leaves, leaf-
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mining, and insect galls were all included as insect damage; leaf browning exhibited by
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some leaves in both treatment types was not.
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Exclosures were made of black, plastic netting with 1.5-cm openings and 1.5-mm-
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wide threads (plastic hardware cloth). We constructed them by attaching the ends of the
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netting to the tree branch, surrounding the desired vegetation, and closing the top and
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bottom with 16-gauge copper wire. The wire also suspended the netting away from the
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enclosed vegetation. The net openings were too small for birds to enter the exclosures
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but openings were large enough to allow movement of most arthropods. Relative
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humidity was measured inside exclosures and on control branches, and differences were
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only about 1%. Because some exclosures were more and others less humid than controls,
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we attributed the differences to natural variability within the habitat rather than to effects
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of the netting. Neither the treatment nor the control braches received direct sunlight, and
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the netting was unlikely to have contributed to light interference.
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The most common organisms excluded by the netting that were found feeding on
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leaf-dwelling insects were birds. Lizards were not found in forested areas, although they
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were present in pasture areas and on the edges of the forest patches in low abundance.
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Bats or small nocturnal rodents might remove insects in the study area, but neither these
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organisms nor evidence of them was encountered in the study area.
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A data transformation suggested by Zar (1984) was used because the data did not
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meet the homogeneity-of-variances assumption of analysis of variance (ANOVA). The
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following transformation lead to a value X’ with an expected variance of 0.25 over all
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values of X and n: X’ = 0.5 (arcsin √(x/n + 1) + arcsin √(x + 1/n + 1)). After data
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transformation, Levene’s test for homogeneity of variances confirmed (P > 0.14) that the
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assumption of equality of variances was met, but even after transformation data were not
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normally distributed, so non-parametric tests were used. Equivalent parametric tests
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yielded the same results, so the latter are reported.
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A 4  2 ANOVA was also used to evaluate the effects of tree and treatment
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(control and exclosure) on leaf loss. Trees and treatment were treated as fixed factors. A
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plot of the residuals against predicted values showed no obvious pattern, suggesting that
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the assumption of independence was reasonable.
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RESULTS
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The diverse bird community in the study area includes many Neotropical migrant
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species. Approximately 55 species were observed visiting oak trees in the vicinity of the
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experimental trees between 15 March and 17 April 2002 (Gamper pers. obs.).
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We collected 5 species belonging to 5 ant genera: Formica argentea,
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Crematogaster cerasi, Tapinoma sessile, Pheidole sp., Monomorium marjoriae. Of
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these, only F. argentea and C. cerasi were observed using honeydew. These
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observations were made on pasture trees where scale-insect anal tubes had been blown by
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the wind and stuck to the trunk, where the honeydew pooled and was accessible to ants.
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Baits in pasture were most frequently discovered (59.37%), followed by edge transects
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(14.06%); baits in forest habitat were never discovered. Although different ant species
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visit tuna and honey baits (Koptur 1992), we combined the results because we were
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simply measuring overall ant activity and abundance. Clearly no ants were detected in
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the forest habitat, so use of scale-insect honeydew in the forest habitat is left for other
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organisms.
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Although ant foraging on S. garmilleri honeydew was uncommon, bird foraging
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on this carbohydrate-rich resource was very common. Birds were also observed, on
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occasion, to supplement their diet with insects. Species observed visiting focal trees to
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feed on honeydew on more than two occasions are presented in Table 1. Audubon’s
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warblers were observed most frequently at focal trees (n = 272), followed by Nashville
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warblers (n = 214), Black-throated green warblers (n = 145), and Wilson’s warblers (n =
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126). Migratory warblers were found to forage more on honeydew than did resident
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breeding birds during these observation periods. The relationship between time spent
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feeding on honeydew and time spent feeding on insects was positive and significant
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(Spearman’s rank correlation = 0.612, n = 24, P < 0.001).
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Protected leaves suffered a 12.1% loss of area and control leaves a 7.3% loss. A
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Mann-Whitney U test on transformed values showed that the results were in the expected
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direction and significant (z = –3.934, P < 0.001) and therefore that exclusion of birds did
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increase leaf damage. Exclosures had an average rank of 189.86 and control branches
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148.25. Leaf loss is plotted against treatment effect on the four trees used in the study in
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Figure 2. The ANOVA results showed significant main effects for treatment (F(1,327) =
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20.11, P < 0.001) and tree (F(3,327) = 26.37, P < 0.001), but the interactions were not
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significant (F(3,337) = 0.536, P = 0.658). Post-hoc analyses consisted of all pairwise
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comparisons among the four trees. The results of a Tukey Honestly Significant
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Difference test indicated that leaves on tree 1 sustained significantly more damage than
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did those on trees 2–4 (P < 0.001), which did not differ significantly from each other
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(Fig. 2). Our results indicate substantially greater leaf loss for the bird exclosures
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branches than control branches.
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DISCUSSION
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Leaves often sustain the most damage early in their lives, and results of exclusion
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experiments are most dramatic on young leaves (Koptur 1984). In our experiment, using
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young oak leaves allowed us to measure the significant effects on damage of excluding
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birds. Our results concur with those of several other studies in which exclosure
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treatments produced significant increases in amount of leaf damage (Atlegrim 1989,
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Spiller & Schoener 1990a, b, Marquis & Whelan 1994, Dial & Roughgarden 1995,
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Greenberg et al. 2000). These studies demonstrate that insectivorous birds can reduce
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herbivory and potentially increase the fitness of the plants on which they forage by
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reducing leaf loss to herbivory. Although we did not measure fitness effects, reduction of
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damage to the oak trees might increase their competitive abilities and might also lessen
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demand on the plant to synthesize secondary compounds to deter herbivores (Coley et al.
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1985). Increasing the health of the host species may support larger scale-insect colonies,
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dense populations of which could in turn attract more birds that remove leaf-damaging
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insects. Even though trees with dense colonies of scale insects appear healthy, the effect
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of varying scale-insect densities on the host plant and the way the insects affect the
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overall health of the trees should be examined.
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Insect numbers on experimental and control branches were not recorded during
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our study. If the insects are very mobile and the number of leaves monitored is relatively
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few, measurement of insect numbers could be extremely subjective. Murakami &
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Nakano (2000) found that differences in the degree of leaf damage between treatments in
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an exclosure study mimicked the trends observed for Lepidoptera larvae. Insect counts
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may introduce error based on time of day of counting or on disturbance if the exclosures
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have to be opened for insect counts. Even though direct interactions may be important to
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species populations, the indirect interactions that arise from them can be equally
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important. The direct interactions that affect a species may be weaker than those that
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make up an indirect effect (Spiller & Schoener 1990b), but direct measurements of the
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abundance of arthropods can strengthen the argument for the capability of predators to
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exhaust their food resources (Jäntti et al. 2001). Lictenberg & Lictenberg (2003)
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recorded direct observations of predation events (vespid wasp and ant predation on
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lepidopteran larvae), but for some organisms that are sensitive presence of an observer,
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such results could be misleading.
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Changes in the abundances of birds may affect the rate of insect removal from the
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plant (Marquis & Whelan 1994). Holmes et al. (1979) estimated removal rates of
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caterpillars from plants in the understory of temperate forests to be higher during June
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and mid-July, when birds were feeding nestlings. The effects of temporal differences in
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the bird community on our results should be examined. In addition, placing our
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exclosures higher in the canopy might be critical to understanding of the within-forest-
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area effects of bird predation. Many of the birds in our study area forage at specific
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heights, and our experiment included only those that forage in the understory/lower
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canopy. The effects of bird predation on leaf-feeding insects might be higher in the mid-
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canopy, where many bird foraging guilds overlap.
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Our data cannot entirely rule out the possibility that improved microclimate
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within our exclosures attracted herbivorous insects and increased herbivory in that way.
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This effect seems unlikely, however, because the differences in microclimate between the
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exclosures and the control branches were similar to those within exclosures and within
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controls. Experiments designed to assess the importance of these factors directly would
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strengthen our results. Finally, results from more than a single season are necessary
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before we can conclude that birds normally regulate leaf damage.
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The study reported here is the first to investigate the role of birds in protection of
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the plants hosting honeydew-producing insects. Our results suggest the third trophic
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level (birds) can modify interactions between the first trophic level (oak trees) and the
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second level (herbivorous insects), as ants do in many other systems. This increased
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knowledge of trophic-level interactions can shed light on issues such as the indirect
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benefits of scale insects to their host plant and the importance of insectivorous birds in
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forest ecosystems.
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ACKNOWLEDGEMENTS
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The authors thank R. Greenberg, J. García-Franco, and G. Williams-Linera for help with
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field logistics; P. Gullan (scale), W. P. MacKay (ant), and M. Peralta Méndez (oak) for
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species determination; V. Ruiz Mandoval, M. Ferrer, M.Cuautle, and A. Plata for field
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assistance; and EPA Fellowship (U916078) for funding.
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Table 1 The resident (R) or migratory (M) status, number of visits to focal trees, and total time (in seconds) spent feeding on
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honeydew (Honeydew time) and insects (Insect time) during those visits. Data were gathered during hour-long observations at 40
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focal trees totaling 160 hours. Species with less than three visits to focal trees are omitted from the table.
Species
Status
No. visits
Honeydew time
Insect time
Audubon's warbler (Dendroica coronata auduboni)
M
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53930
1387
Nashville warbler (Vermivora ruficapilla)
M
230
44600
1002
Black-throated green warbler (Dendroica virens)
M
160
22935
1069
Wilson's warbler (Wilsonia pusilla)
M
156
19674
2168
Townsend's warbler (Dendroica townsendi)
M
70
13831
397
Yellow-eyed junco (Junco phaeonotus)
R
53
5827
165
Ruby-crowned kinglet (Regulus calendula)
M
44
3510
630
Bumblebee hummingbird (Selasphorus heloisa)
R
23
2212
0
Chipping sparrow (Spizella passerina)
R
20
3668
30
Painted redstart (Myioborus pictus)
R
18
1213
180
White-eared hummingbird (Basilinna leucotis)
R
15
578
0
Common bush-tanager (Chlorospingus ophthalmicus)
R
14
1485
878
Gamper & Koptur
366
367
19
Crescent-chested warbler (Parula superciliosa)
R
9
151
116
Black and white warbler (Mniotilta varia)
M
8
818
100
Flame-colored tanager (Piranga bidentata)
R
8
762
165
Hermit warbler (Dendroica occidentalis)
M
5
1781
0
Golden-browed warbler (Basileuterus belli)
R
5
300
38
Violet sabrewing (Campylopterus h. hemileucurus)
R
5
144
0
American robin (Turdus migratorius)
M
3
938
0
House finch (Carpodacus mexicanus)
R
3
520
0
Ivory-billed woodcreeper (Xiphorhynchus flavigaster)
R
3
60
960
Gamper & Koptur 20
368
FIGURE LEGEND
369
Figure 1 Hair-like anal filaments of the scale insect Stigmacoccus garmilleri bearing
370
371
drops of honeydew (Chiconquiaco, Veracruz, Mexico).
Figure 2 Effects of treatments on amount of leaf damage on the four trees measured in
372
2003. Each mean is the average of leaves from two branches on the same tree.
373
Error bars represent 95% confidence intervals around the mean. Damage was
374
significantly higher where birds were excluded on all four trees (P < 0.001), and
375
tree 1 was significantly different from trees 2, 3, and 4 (P < 0.001), which did not
376
differ significantly from each other.
377
378
Gamper & Koptur 21
379
380
Gamper & Koptur 22
Tre a tm e n t
Co nt ro l
Bird s e xc lu d e d
Percentage leaf damage
30
20
10
0
1
2
3
Tre e
381
4