Trophic Interactions Among Insectivorous Birds, Herbivorous Insects, and Prants in Temperate Deciduous Forest
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Title Trophic Interactions among Insectivorous Birds, Herbivorous Insects, and Prants in Temperate Deciduous Forest Author(s) Murakami, Masashi Citation 北海道大学. 博士(地球環境科学) 甲第4511号 Issue Date 1998-03-25 DOI 10.11501/3137227 Doc URL http://hdl.handle.net/2115/32517 Type theses (doctoral) File Information 4511.pdf Instructions for use Hokkaido University Collection of Scholarly and Academic Papers : HUSCAP Trophic Interactions among Insectivorous Birds, Herbivorous Insects, and Plants in Temperate Deciduous Forest A Dissertation Submitted to Division of BioScience, Graduate School of Environmental Earth Science, Hokkaido University for the Degree of Doctor by Murakami Masashi 1997 CONTENTS ABSTRACT .•......•.••.•.•••.•......•••.......•••..•......•••••........•••.•.•••.........•......•.......•. 1 GENERAL INTRODUCTION .•..•....•..••.....•.....••.•.....•....••.......•..•...••.............•.... 4 I Seasonal changes in foraging behaviors of forest passerine birds: Indirect effects of plant defense through herbivorous insect Introduction ................................................................................................................................ 9 Methods ................................................................................................................................... 11 Results .................................................................................................................................... 16 Discussion ............................................................................................................................... 21 II Roles of insectivorouS' birds in forest ecosystems: Experimental approaches ..•.•....•.• 34 1 Effect of avian predation on leaf rolling lepidopterous larvae Introduction .............................................................................................................................. 35 Materials and Methods ................................................................................................................ 36 Results .................................................................................................................................... 38 Discussion ............................................................................................................................... 39 2 Canopy enclosure experiment Introduction .............................................................................................................................. 45 Methods ................................................................................................................................... 46 Results .................................................................................................................................... 48 Discussion ............................................................................................................................... 50 CONCLUSIONS ......••........•.........•.....•....•.•••...........•...........•..............•..•..•. 57 REFERENCES •........................................................•.......•........................ 62 Abstract Trophic interactions among insectivorous passerine birds, carnivorous and herbivorous insects, and plants (oak) were studied in temperate deciduous forests, focusing onJhe variability and versatility in each component. In Chapter I, indirect effects of strengthening plant defenses on bird foraging behaviors via herbivorous insects, in particular, lepidopterous larvae, were studied. I investigated seasonal changes in leaf characteristics related to the defense system against herbivorous insects, distribution of arthropod populations, and foraging behaviors of four bird species, great tit (Parus major), marsh tit (Parus palustris), narcissus flycatcher (Ficedula narcissina), and crowned willow warbler (PhyUoscopus occipitalis), in a temperate deciduous forest in northern Japan. During a relatively short period after the budbreak, leaf toughness and tannin content of oak leaves increased, while nitrogen and water contents decreased. The biomass of lepidopterous larvae in the canopy was large in early spring, three weeks after the budbreak, but decreased rapidly in mid June. In contrast, the larvae became abundant on the forest floor from early to late June. A rearing experiment showed that one of typical spring-feeding lepidopterous species, Conistra unimacula (Noctuidae), could not grow up to the 6th (last) instar if reared only on canopy leaves. However, when the food was changed from canopy leaves to seedling leaves after the 4th instar, 72% of the larvae could survive through the 5th instar, and 30% pupated. Seedling leaves were softer, fresher, and more nutritious than canopy leaves. These differences in leaf quality improved the performance of larvae reared on seedling leaves. These findings suggest that lepidopterous larvae 1 migrate from the oak canopy to the forest floor in late spring not only to pupate in the ground but also to seek alternative food resources on the forest floor. Thus, strengthening of defense traits in canopy leaves caused changes in the abundance and distribution of lepidopterous larvae. Narcissus flycatchers foraged in the canopy from late May to mid June but on the ground from late June, mostly preferring lepidopterous larvae (about 80% of the total prey items). The other species, great tit, marsh tit, and crowned willow warbler, however, did not change their foraging heights; they continued to forage in the canopy. This difference is probably due to the greater preference of the flycatcher for lepidopterous larvae compared with the other species. The other species changed their prey from lepidopterous larvae to spiders or other arthropods in mid June, when the number of lepidopterous larvae decreased in the canopy. Thus, the studied bird species showed the specific responses to the spatio-temporal variation in the , resource abundance and distribution. Foraging behaviors of insectivorous birds were indirectly affected by plants through herbivorous insects. In Chapter II, two field experiments were performed to detect effects of avian predation on the lower trophic levels. First, to assess effects of avian predation on leaf-rolling lepidopterous larvae, birds were excluded from Japanese lilac (Syringa reticulata) trees by covering them with nets. Only one species, Zelleria sp. was reduced in number by avian predation: no effect of birds was detected in pylarid species. This is probably due to the differences in the shape of leaf roll. Zelleria sp. alters the leaf form greater than the other species, so that birds can detect the rolls more easily. The shape of leaf roll or the degree of alteration of leaf arrangement may be a compromise among adaptations to different stresses, plant resistance, parasitism and/or predation by arthropods and 2 birds. Of the four predominant insectivorous species, great tit and marsh tit, intensely visited the lilac to forage on leaf rollers, but narcissus flycatcher and crowned willow warbler did not. This is probably due to the differences in their foraging methods. Next, to determine effects of foliage gleaning bird (great tit) and bark gleaning bird (nuthatch) on organisms at lower trophic levels, I manipulated their presence or absence within a large canopy enclosure. This experiment detected effects of the two bird species on lepidopterous larvae, ants, and the degree of leaf damage of oak (Quercus crispula) leaves. Great tit reduced the abundance of lepidopterous larvae and eventually the degree of leaf damage. On the other hand, nuthatch reduced the abundance of ants, but did not affect the abundance of lepidopterous larvae and the degree of leaf damage. Effects of ants on lepidopterous larvae were also convinced. These results indicate that insectivorous birds play different roles in forest ecosystems according to their species-specific natures of foraging behaviors. 3 General Introduction Ecologists have long been interested in the importance of interactions between trophic levels in determining distribution and abundance of organisms and hence community structure (Strauss 1991; Hunter and Price 1992; Wootton 1992). Recently, attention has been drawn toward the relative importance of direct effects (effects of one species on another as a consequence of a physical interaction between the two) and indirect effects (effects that are not the result of a physical interaction but are operated via a third species) of species interactions on community structure (Wootton 1992; Menge et al. 1996). However, indirect effects have been less studied than direct' effects, perhaps because indirect effects are often considered to be unimportant compared to direct interactions (cf. Strauss 1991) and difficult to detect due to the incorporation of a third species (Davidson et al. 1984; Wootton 1992). Those ecologists who agree that trophic interactions are important still debate whether primary control is by resources (bottom-up forces) or predators (top-down effects; Wiens 1989; Smith and Rotenberry 1990). According to the bottom-up view, organisms on each trophic level are regulated or limited by their resources (food limited). The top-down view holds that organisms are regulated or limited by predators (Power 1992). Hunter and Price (1992) offered a synthetic framework and sensible advice regarding this controversy. They suggested that ecologists not ask, "Do resource or predators regulate this particular population?" but rather, "What factors modulate resource limitation and