Insect Defoliation and Nitrogen Cycling in Forests
Outbreaks of defoliating insects can have dramatic effects on forest ecosystems. Studies have shown that defoliation can decrease transpiration and tree growth and increase tree mortality, light penetration to the forest floor, and water drainage (Stephens et al. 1972, Campbell and Sloan 1977, Houston 1981). The allocation of carbon to various parts of the tree may be altered, production of defensive compounds in foliage may increase (Schultz and Baldwin 1982), and seed production may decline for many years after defoliation (McConnell 1988, Gottschalk 1990). Shifts in tree species composition (Doane and McManus 1981, Glitzenstein et al. 1990) and changes in the population size of insectivorous birds and other wildlife may also occur (Holmes et al. 1986, USDA Forest Service 1994). Several studies of insect outbreaks have also indicated an increased loss of nitrogen (N) from forest ecosystems in drainage water following defoliation, suggesting an increase in soil-available nitrogen that is subject to leaching (Swank et al. 1981, McDonald et al. 1992, Webb et al. 1995, Eshleman et al. 1998, Reynolds et al. 2000). Large losses of nitrogen via leaching would reduce long-term forest production in N-limited ecosystems. In addition, the export of nitrate (NO−3) to stream water can acidify downstream waters (Webb et al. 1995) and contribute to eutrophication of coastal waters and estuaries (Fisher and Oppenheimer 1991). At first glance, the view held by many investigators that forest ecosystems leak N in large quantities after defoliation fits the general notion of nitrogen behavior in disturbed ecosystems. Significant nitrogen losses have been observed in response to disturbances such as intensive harvesting (Likens et al. 1970), fire (Bayley and Schindler 1991), and severe windstorms (Schaefer et al. 1996). However, defoliation differs qualitatively from these other disturbances in three ways. First, most of the trees usually remain alive with their woody structure intact after defoliation by insects. (Exceptions are the high mortality rates caused by repeated severe defoliations of hardwood trees or by severe defoliation of conifers.) Second, physical disturbance of the soil is minimal and significant erosion is therefore unlikely to occur. And third, if the trees are not killed, the time for substantial canopy recovery is often measured in weeks rather than years. In this article we examine the mechanisms and magnitudes of N-cycle perturbations by defoliation, drawing heavily on the considerable body of research on the gypsy moth (Lymantria dispar L.), an introduced lepidopteran that has been the major defoliator of hardwood forests in the northeastern United States during the last 5 or 6 decades (Doane and McManus 1981). We attempt to establish a more coherent view of the likely consequences of defoliation for N cycling, and we make the case that, contrary to the commonly held view, the response of forest ecosystems to defoliation is primarily one of redistribution, rather than loss, of nitrogen. The most direct and obvious consequence of the defoliation of forests is a change in the fate of leaf-derived (foliar) nitrogen. Consider, for example, the upland mixed-oak forests at our research site in southeastern New York State, which contain about 85 kilograms of N per hectare (ha) in foliage during the growing season. (This is typical of deciduous forests in eastern North America [Johnson and Lindberg 1992].) The fate of that nitrogen is shown in Figure 1. In a normal year, small amounts of nitrogen are lost from the canopy as a result of throughfall (precipitation passing through the canopy), insect herbivory, and premature leaf fall during the growing season, but trees resorb the bulk of nitrogen before leaf abscission in the autumn. Resorption and storage of N in plant tissues ensures the availability of N to support growth of new foliage the following spring and creates a relatively tight internal N cycle in trees. If the forest is defoliated, however, much of the foliar N is diverted to insect feces (frass), green leaf fall, and insect biomass (Figure 1; Grace 1986, Hollinger 1986, Risley and Crossley 1993). Throughfall N also may increase (Stachurski and Zimka 1984, Hollinger 1986, Schowalter 1999). After a summer defoliation, some autumn litterfall and resorption of N from unconsumed leaves or from new leaves flushed after defoliation can still occur. (The N in reflushed leaves may represent an additional subsidy of N to the foliage from the tree's reserves, rather than part of the initial pool of canopy N, as implied by Figure 1.) The diversion of canopy N to green litterfall, insect biomass, frass, and throughfall comes primarily at the expense of resorption (Figure 1; May and Killingbeck 1995). This breaks the tight internal N cycle of the tree and, together with the allocation of stored N to reflushed foliage, will deplete the tree's N reserves. From the point of view of N availability, the key question is, what is the fate of the foliar N consumed by insects and deposited to the forest floor as frass, greenfall, and insect biomass? If trees can readily take up this N, the nutritional consequences of defoliation may not be too severe, although the energetic consequences of having to produce new foliage could still be substantial. Our research on oak saplings suggests that severe defoliation does not diminish a tree's ability to take up N from the soil to support compensatory photosynthesis and production of new foliage (Lovett and Tobiessen 1993). However, if N is lost from the system or otherwise becomes unavailable, the trees could suffer a severe N shortage during recovery. Low N availability has been shown to limit the ability of trees to tolerate or compensate for defoliation damage (Waring et al. 1992, Wickman et al. 1992, Lovett and Tobiessen 1993). The responses are complex, however, because low N supply can also slow the population growth of defoliating insects (Mason et al. 1992) and enhance the induction of a tree's chemical defenses against insects (Hunter and Schultz 1995). One possible mechanism of ecosystem N loss during defoliation is gaseous N loss from the insect itself. This mechanism seems especially plausible in lepidopterans, many of which use an extremely alkaline gut pH to digest their food. The midgut of a gypsy moth caterpillar has pH 11–12, one of the highest pH levels known in biological systems (Schultz and Lechowicz 1986). Adding plant N to such an alkaline environment is likely to volatilize ammonia (NH3) vapor, which could escape from the insect's digestive tract. However, in a laboratory experiment, we measured volatilization of NH3 from gypsy moth caterpillars feeding on oak leaves and found that less than 0.1% of the N consumed was volatilized (Figure 2). The reason for this apparently tight N retention by the gypsy moth became clear during our research. Although the midgut of the moth is highly alkaline, the frass pellet that emerges from the hindgut is moderately acidic (pH approximately 4 to 4.5; Lovett et al. 1998). Gypsy moths accomplish this remarkable feat of gut alkalization and reacidification through a powerful ion pumping system (Dow 1984). Acidification of the hindgut presumably recaptures any NH3 vapor generated in the midgut, making the insect relatively leakproof with regard to gaseous N emissions. This does not mean that the insect efficiently assimilates most of the N it consumes. In our laboratory experiments, approximately 84% of the N consumed by gypsy moth larvae was egested in frass (Figure 2). The amounts of N egested and volatilized indicate that the larvae assimilated only about 16% of the N they ingested (Figure 2), a remarkably low N utilization efficiency compared with other insects (Montgomery 1982). Although over their entire life cycle gypsy moths would very likely use N more efficiently, late-instar caterpillars such as those used in our experiment are known to have low efficiency of N use (Montgomery 1982). These late-instar caterpillars are very important for N cycling because they are responsible for most of the canopy defoliation (Leonard 1981). In fact, in a real defoliation the insects use the available foliar N even less efficiently because their sloppy eating habits allow a substantial amount of green leaf material to fall to the ground unconsumed (Figure 1). Our scatological research team has investigated the chemistry and fate of gypsy moth frass pellets. We found that the concentration of N in frass from gypsy moth larvae feeding on oak foliage is about 2.4% (dry mass basis) and the ratio of carbon (C) to nitrogen is about 20, similar to levels in green oak foliage but more enriched in N than is oak litter (Lovett and Ruesink 1995). About 9% of the N in frass is chemically extractable as inorganic forms (NH4+ and NO3−). The other 91% is presumably in organic forms such as uric acid. The carbon in gypsy moth frass appears to be highly labile and readily consumed by soil microbes, because adding frass to soil in laboratory experiments produces a rapid increase in microbial respiration that can last for several months (Figure 3a; Lovett and Ruesink 1995). The labile carbon fuels rapid microbial growth and results in a significant immobilization of N in microbial tissues, thereby reducing the potential for N mineralization (conversion of organic nitrogen to bioavailable forms of inorganic nitrogen) (Figure 3b). There are few other studies of the immobilization of N in insect frass with which to compare our findings. Frass additions had no effect on availability of NO−3 or phosphate (PO3−4) in the soil in small experimental enclosures in a forest in North Carolina (Reynolds and Hunter 2001). However, Lewis (1998) showed that the frass of elm spanworm (Ennomos subsignarius Hubner) larvae immobilized inorganic N when incubated in stream water. Other types of invertebrate excreta may also stimulate microbial N immobilization. Grier and Vogt (1990) showed that aphid honeydew (a carbo hydrate-rich secretion produced by aphids during phloem feeding) reduced N mineralization rates in an alder forest in western Washington. They concluded that the labile carbon in the honeydew stimulated N immobilization by microbes. Similarly, feces from herbivorous snails were shown to reduce N mineralization in a desert ecosystem (Zaady et al. 1996). When water was added to the soil, there was an immediate flush of extractable N from the snail feces, followed by a period of N immobilization. A similar pattern of release and immobilization may be occurring in gypsy moth frass. Our results indicate that lepidopteran frass, at least for the first few months after defoliation, is a strongly N-immobilizing substrate rather than a N-mineralizing one. Because gypsy moth defoliations occur in early summer (June and July), the months immediately following defoliation are critical to a tree's ability to counteract some of the damage by increasing photosynthetic rates in any remaining leaves (termed compensatory photosynthesis; Hodgkinson 1974, Heichel and Turner 1983), flushing new foliage, and replenishing reserves of N. However, all of these recovery responses require available N. For example, low N availability inhibits the compensatory photosynthetic response of oak seedlings after defoliation (Lovett and Tobiessen 1993). Immobilization of frass N in microbial biomass during this critical response period probably hinders a tree's recovery. What is the fate of this immobilized N over the longer term? We addressed this question in a field study of small plots to which we added frass and oak litter labeled with the stable isotope 15N. By using a small amount of 15N as a tracer, we were able to examine the fate of N in the soil without substantially altering the N cycle. We labeled the leaves with 15N by infusing an oak tree with a solution containing 15N during the period in the spring when the leaves were expanding. We fed some of the green leaves to gypsy moths in captivity, which produced isotopically labeled frass, and collected the remaining leaves during normal autumnal litterfall, producing labeled litter. We added the labeled frass and litter to small trenched plots in a forest in which we planted an oak seedling to act as a bioassay of N availability to plants. We sampled the plots repeatedly over 2 years to determine the fate of the applied 15N (Christenson et al. forthcoming) and measured the distribution of 15N in soil, microbial, and plant pools and its loss via leaching. Not all of the applied 15N was recovered, despite our intensive sampling of these plots. Recovery averaged 81% for plots that received leaf litter and only 40% for plots that received frass, raising the possibility of additional ecosystem losses of N that we did not measure, such as organic N leaching or gaseous N loss. Ammonia volatilization is unlikely because the pH of the soils was acidic. Denitrification is unlikely because the soils were well drained, although it may have been occurring in the frass pellets themselves. However, gaseous N oxides could have been produced through other processes, such as nitric oxide production associated with nitrification (Firestone and Davidson 1989). The fate of the recovered 15N was in the litter plots compared with the frass plots (Christenson et al. In the litter most of the recovered 15N in the only a small amount was the soil (Figure In the frass and the soil, producing a of 15N that found its all measured soil and plant pools of N. The concentration of 15N in all measured pools was in the frass than in the litter plots. than of the 15N recovered in the frass plots was in the soil, and only about of that soil 15N was in microbial, or measured in a laboratory N pools (Christenson et al. The was in a less available of soil organic but its chemical and mechanism of the soil organic are not The mechanisms microbial and of N or N and et al. 2000). leaching of inorganic N in the frass or litter than of the applied 15N in Our also that the 15N from litter in the litter plots was less likely to be recovered than the 15N in the frass but the that was recovered was more likely to be in the soils to and may have been more available to than was frass N (Christenson et al. The results of this experiment indicate that defoliation the normal cycling of N through the N is during the frass N to it is in soil organic forms of N are the but by very mechanisms and with consequences for N our laboratory and studies three important mechanisms for N in a forest First, at least in the case of gypsy moth defoliation, the ecosystem very N by volatilization from the insects themselves. Second, N that the ground in frass pellets is subject to rapid immobilization by microbes, and in the longer by soil organic if the trees not from the defoliation, their are of up available N in the soil even their foliage has been Although this has been primarily through with gypsy moths and oak of the mechanisms to that the mechanisms will in and of forest defoliation by insects. The tight of N in microbes, and soils and the of N leaching in our experiments at first glance, to be at with several studies of that in stream water export of N from forests after however, we that this can be if we that the amount of N lost from the is small compared to rates or to the amount of N by At the in western North in NO−3 in stream water were observed after a defoliation by the fall in (Swank et al. and by a in (Reynolds et al. 2000). After the stream water NO−3 concentration increased approximately but N export very at less than N Although N to the forest floor was not measured during this defoliation, we have that less than of the N was lost via leaching (Lovett and Ruesink 1995). Forest in New the site of the ecosystem study in North was by the caterpillar in and that this defoliation had no effect on stream water N Lewis (1998) that the of a stream water NO−3 response was to the that the of the defoliation loss of leaf over only about of the the of the less damage or at Eshleman and (1998) that the relatively high N observed in stream water at most of the could have from this However, showed that N in stream water were the of New during that even in that were by In any the from the study not or of N export after defoliation by the gypsy moth in many forests in and in the early with some more than of the leaf This defoliation in N in in this which had before defoliation (Webb et al. 1995, Eshleman et al. 1998). of NO−3 from these after the defoliation was also the of 4 N This of NO−3 export can have a on and eutrophication of 4 N is only of the N of about N in this even after this severe defoliation, the still had a retention of N. the that the green foliage of these forests N per before defoliation and that of the canopy was by the gypsy we that leaching losses for or less of the N from the canopy by Lewis (1998) measured the N in stream water and in by elm of the leaf of the in and NO−3 in stream water their in Lewis (1998) that the defoliation caused N export to increase by N compared with This N loss was of the N in insect frass green litterfall during the defoliation, which is than the of N loss in the other studies Lewis (1998) suggests that the high levels of N availability in soils may have to this these studies that most of the N as a result of insect defoliations is in the which is qualitatively with the laboratory and experiments However, the that in some a increase in stream N loss was observed after defoliation for In some even a small increase in N leaching can have significant consequences for stream and because NO−3 can as and from the soil and soil and to and our laboratory and experiments that N retention are that we not any N to from the it is important to what result in N losses from a forest ecosystem after This question be the subject of but on the of what we we several that could a tree mortality, and low N retention in If defoliation were severe and to a significant of N losses could Although our 15N studies indicate that most of the frass N is in soil organic rather than in our studies that tree can for that N even after defoliation if the trees are still of trees would reduce of the N from frass, reduce the for the large pool of N by mineralization from organic and large of N from a severe in the of N and in the system could soil retention mechanisms and result in leaching suggests that high rates of tree mortality in some of after the gypsy moth in the early which may the relatively high N export observed from those In the longer of the forest after such a mortality would produce a N in the that would be to reduce N losses during forest recovery and If the forest ecosystem large amounts of during or immediately after defoliation, the could decrease of frass N with soil and reduce the for N Similarly, N retention could be low in soils or soils with a large amount of that inhibits frass N and the soil our of the mechanisms by which N retention in soil, it is to about that this However, soil obvious to soils and soils with low organic would produce a pool of the soil organic that appears to be the site of most retention of frass N. In addition, or of the ecosystem with N, from N or of N may also reduce the ability to N. This may have been the case for the by Lewis in which high levels of N and export before defoliation N defoliation a major to the internal N cycle of the but this primarily a of N the ecosystem rather than a large loss of N. defoliation, nitrogen from the canopy is diverted to green leaf fall, frass, and insect autumnal resorption of N from foliage is the internal of N. the chemical of the frass, with its highly labile appears to soil a over trees for the N deposited in frass. In one study in an oak N deposited to the forest floor as gypsy moth frass was primarily in the soil organic and studies all indicate retention of N in forest ecosystems after insect in the of N loss, forest ecosystems retention of N stream water after Although the of N loss is not N losses important about the mechanisms of N retention in forest ecosystems. few studies of forest N cycling and defoliation have been and studies have primarily the gypsy studies in systems would more and because in such as digestive of defoliation, and plant all of which can have important effects on N Because of the in defoliation in the in this will most likely from a of and laboratory studies and studies of real defoliation at long-term ecosystem research the that research are studies of the mechanisms of N retention and loss after forest effects on of the that is in forests and Crossley 1984, Schowalter et al. as to the severe defoliation in this and the of insect defoliation with other such as change and N For example, of N in ecosystems could insect by altering foliar et al. 1992, et al. and altering the to N et al. 1989). the of these will require experimental studies and long-term with We are to the and the and the for support for this This is a to the of the of Figure 1. of nitrogen in foliage in years of high and low defoliation in an oak forest in the eastern United for the case are from upland mixed-oak forests of the of Studies in New for the case are from a study of oak forests in by Grace Figure of foliar nitrogen (N) consumed by gypsy moths feeding on oak from foliar frass and ammonia (NH3) volatilization in the experiment by Lovett et al. (1998) Figure of carbon release and nitrogen (N) mineralization from laboratory of soil and from the frass of a N mineralization rates indicate immobilization of inorganic N. are from Lovett and Ruesink Figure of the 15N added to small trenched plots as oak litter or gypsy moth frass. are of the applied 15N that was recovered in the pools from et al.