effects of nitrogen fertilization on tritrophic interactions

REVIEW PAPER

Effects of nitrogen fertilization on tritrophic interactions

Yigen Chen • Dawn M. Olson • John R. Ruberson

Received: 29 September 2009 / Accepted: 14 April 2010 / Published online: 29 April 2010

� Springer Science+Business Media B.V. 2010

Abstract Tritrophic interactions (plant—herbivore—

natural enemy) are basic components of nearly all eco-

systems, and are often heavily shaped by bottom-up forces.

Numerous factors influence plants’ growth, defense,

reproduction, and survival. One critical factor in plant life

histories and subsequent trophic levels is nitrogen (N).

Because of its importance to plant productivity, N is one of

the most frequently used anthropogenic fertilizers in agri-

cultural production and can exert a variety of bottom-up

effects and potentially significantly alter tritrophic inter-

actions through various mechanisms. In this paper, the

potential effects of N on tritrophic interactions are

reviewed. First, in plant-herbivore interactions, N avail-

ability can alter quality of the plant (from the herbivore’s

nutritional perspective) as food by various means. Second,

nitrogen effects can extend directly to natural enemies

through herbivores by changes in herbivore quality vis-a-

vis the natural enemy, and may even provide herbivores

with a defense against natural enemies. Nitrogen also may

affect the plant’s indirect defenses, namely the efficacy of

natural enemies that kill herbivores attacking the plant. The

effects may be expressed via (1) quantitatively and/or

qualitatively changing herbivore-induced plant volatiles or

other plant features that are crucial for foraging and attack

success of natural enemies, (2) modifying plant architec-

ture that might affect natural enemy function, and (3)

altering the quality of plant-associated food and shelter for

natural enemies. These effects, and their interactive top–

down and bottom-up influences, have received limited

attention to date, but are of growing significance with the

need for expanding global food production (with accom-

panying use of fertilizer amendments), the widening risks

of fertilizer pollution, and the continued increase in

atmospheric CO2.

Keywords Nutrients � Tritrophic interactions �Herbivore � Predator � Parasitoid � Pathogen

Introduction

Tritrophic interactions (plant—herbivore—natural enemy)

are basic components of nearly all ecosystems, and are

often heavily shaped by bottom-up forces (McNeill and

Southwood 1978; Mattson 1980; Hunter and Price 1992;

Hunter 2001). Numerous factors influence plants’ growth,

defense, reproduction, and survival, exerting effects on

higher trophic levels. One critical factor in plant life his-

tories and subsequent trophic levels is nitrogen (N).

Because of its importance in plant life histories, N is one of

the most frequently used anthropogenic fertilizers in agri-

cultural production and can exert a variety of bottom-up

effects and potentially significantly alter tritrophic inter-

actions through various mechanisms (McNeill and South-

wood 1978; White 1978; Stiling and Moon 2005). The

potential effects of N on tritrophic interactions are complex

and are outlined in Fig. 1. First, in plant-herbivore

Handling Editor: Robert Glinwood.

Y. Chen � J. R. Ruberson (&)

Department of Entomology, University of Georgia, Tifton,

GA 31793, USA

e-mail: [email protected]

Present Address:Y. Chen

Department of Entomology, Michigan State University,

East Lansing, MI 48824, USA

D. M. Olson

USDA-ARS, CPMRU, Tifton, GA 31794, USA

123

Arthropod-Plant Interactions (2010) 4:81–94

DOI 10.1007/s11829-010-9092-5

interactions, N availability can alter quality of the plant

(from the herbivore’s nutritional perspective) as food by

various means. For example, plant’s direct defenses to

herbivorous insects can be changed by N fertilization

through qualitative and quantitative alterations of defensive

compounds such as digestibility reducers and toxins. The

importance of these defenses to the plant will likely depend

on whether the benefits derived from antagonizing her-

bivory outweigh the nutritional profitability of the

increased N in the plant. However, direct plant defensive

compounds can extend to natural enemies (i.e., predators,

parasitoids and pathogens) through herbivores by changes

in herbivore quality vis-a-vis the natural enemy (Krips

et al. 1999; Francis et al. 2001), and may even provide

herbivores with a direct defense against natural enemies

(Thurston and Fox 1972; Campbell and Duffey 1979;

Turlings and Benrey 1998). The plant’s investment in

toxins and digestibility reducers may therefore depend on

the cost of production of defensive compounds in relation

to the plant’s metabolic demands and the action of herbi-

vores and their natural enemies. Nitrogen also may affect

the plant’s indirect defenses, namely the efficacy of natural

enemies that kill herbivores attacking the plant. The effects

may be expressed via (1) quantitatively and/or qualitatively

changing herbivore-induced plant volatiles that are crucial

for foraging success of natural enemies, (2) modifying

plant architecture that might affect natural enemy foraging

efficiency, and (3) altering the quality of plant-associated

food and shelter for natural enemies. All of these interac-

tions are diagramed in Fig. 1.

Studies on the impacts of nitrogen on tritrophic inter-

actions have basic and applied implications, and yield

information to help: (1) enhance the understanding of

bottom-up forces in shaping tritrophic interactions; (2)

maximize bottom-up effects on management of insect pests

by increasing compatibility of plant resistance and natural

enemies; and (3) indirectly predict the impact of elevated

atmospheric CO2 concentration on tritrophic interactions.

Relative to the third point, it is evident that global CO2

levels are rising. The global concentration of atmospheric

CO2 has increased to a present level of 386 ppm (National

Oceanic & Atmospheric Administration (NOAA) 2009)

from 270 to 280 ppm at the beginning of the industrial

revolution (Houghton et al. 1996). Although the accurate

prediction of future atmospheric CO2 concentrations is

difficult and the predictions vary greatly, most analyses

anticipate levels will rise to over 700 ppm (Sundquist

1993). Short-term elevation of atmospheric CO2 increases

the photosynthetic rates of C3 plants (Lee et al. 2001 and

references therein) and carbon-based secondary com-

pounds (Koricheva et al. 1998), but also affects the ability

of plants to acquire nitrogen. Plants grown under enriched

CO2 typically have a lower percentage of total nitrogen in

their dry mass, and higher carbon (C) to N ratios (Rogers

et al. 1996; Lawler et al. 1997). Therefore, bottom-up

effects of nitrogen may become increasingly important as

atmospheric CO2 rises. However, how plants will respond

to increases in CO2 and N availability over the long term is

not clear. For example, Lee et al. (2001) found that 13

perennial species representing 4 functional groups (C3

grasses, C4 grasses, legumes and non-leguminous forbs)

showed pronounced photosynthetic acclimation over

2 years resulting in minimal stimulation of photosynthesis,

and this did not depend on the level of nitrogen supplied.

Other studies involving various species found neutral or

greater photosynthetic responses at higher N under

Fig. 1 Schematic

representation of tritrophic

effects of nitrogen. Solid linesrepresent positive effects and

dashed lines signify negative

ones

82 Y. Chen et al.

123

elevated CO2, and still other species have greater photo-

synthetic responses at lower N (reviewed in Lee et al.

2001). Thus, predicting plant species community responses

to elevated CO2 and N over the long term will require an

understanding of the extent that species acclimate photo-

synthesis and how N availability affects this response under

prolonged elevated CO2 conditions.

This review considers the various direct and indirect

effects on tritrophic interactions of altering N available to

plants in hopes of generating greater interest in this important

area. Anthropogenic N is becoming increasingly abundant in

managed and natural systems, and it has the potential to

significantly modify ecosystem structure and function. Thus,

understanding these interactions has important implications

for agriculture and conservation biology.

N alters suitability of plants as herbivore hosts

Nutritional quality of a food plant

The nutritional quality of plant tissue varies with spatial

location within the plant, plant developmental stage

(ontogenetic variation), species and genotype (between

plant variation), and external factors associated with geo-

graphic location and season. Within an individual plant the

N levels can vary from 0.03 to 7.0% of dry weight, with

higher N content in young and expanding plant parts or

reproductive structures (e.g., seeds; Mattson 1980). For

example, in the early developmental stages, cotton leaf

tissue contains ca. 4% N, but it decreases to less than 3%

shortly after flowering (Bassett et al. 1970). N also varies

between plant species. Many plants have evolved under N-

limited conditions, but may differ in their growth strategy

depending on their habitats. For example, Grime (1977)

categorized plants that typically have rapid growth, higher

non-sequestered N content, and occur in habitats with

higher resource availability as C- and R-selected strategist,

in comparison to S-selected plants that experience slower

growth and were characterized as occurring in habitats with

more limited resources. Grime (1977) suggested that plants

that exhibit more vigorous growth and are not so readily

limited by resources would be generally more palatable for

herbivores than S-selected plants. C-selected plants mini-

mize herbivory through selective spatial and temporal

herbivore resistance factors. R-selected plants compensate

for herbivory through rapid completion of their life cycle

and maximization of seed production. S-selected plants, on

the contrary, are predicted to be less palatable overall,

presumably in response to slower growth rates and inten-

sive natural selection for resistance to herbivores. These

strategies can also differentially affect the responses of

herbivores.

Phytophagous insects that feed on diets or host plants of

lower nutritional quality typically exhibit lower growth

rates, lower efficiency of conversion of ingested food, and

lower fecundity (Dixon 1970; Mattson 1980; Weibull 1987;

Karowe and Martin 1989; Lindroth et al. 1995; Awmack and

Leather 2002; Chen et al. 2004), although the degree of

response to N variation can be dependent on herbivore

feeding guild and specific herbivore-plant interactions. For

example, addition of N to white sagebrush, Artemisia lu-

doyiciana Nutt. (Asteraceae), increases performance of

seed- and phloem-feeding insects but not leaf chewing

insects (Strauss 1987). The abundance of the leaf feeding

cereal aphid Metopolophium dirhodum (Walker) (Hemip-

tera: Aphididae) is greater on fertilized wheat Triticum

aestivum L. (Gramineae) and barley Hordeum vulgare L.

(Gramineae) compared to unfertilized wheat and barley,

whereas the performance of the ear-feeding grain aphid Si-

tobion avenae F. is unaffected by fertilization (Honek 1991).

Given choices, many insect herbivores can distinguish

host plants of high nutritional quality from those of low

quality. Females of two Pieris butterflies, Pieris rapae

crucivora and P. canidia canidia (Lepidoptera: Pieridae)

(Chen et al. 2004) and buckeye butterfly, Junonia coenia

Hubner (Lepidoptera: Nymphalidae) (Prudic et al. 2005)

prefer fertilized over unfertilized host plants for oviposi-

tion. Similarly, Chen et al. (2008a) found that female

Spodoptera exigua (Hubner) preferentially oviposited on

cotton plants receiving higher levels of N. In a small-scale

field study, the diamondback moth, Plutella xylostella (L.)

(Lepidoptera: Plutellidae), was more abundant in high N

plots than in low N plots (Fox et al. 1990).

To compensate for low N availability in N-stressed plants,

insects tend to adjust their total food consumption by

increasing consumption rates, prolonging feeding periods, or

a combination of the two, or by adjusting their nutrient

processing efficiency, for example through changes in food

residence time or digestive enzyme levels (Mattson 1980;

Barbehenn et al. 2004). Paper birch, Betula papyrifera

(Betulaceae), grown under elevated CO2 environments had

decreased N content (Lindroth et al. 1995). Fourth-instar

saturniid caterpillars, Hyalophora cecropia L., Actias luna

L., and Antheraea polyphemus Cramer (Lepidoptera: Sat-

urniidae), grown on these birch plants consumed more plant

material than on those grown under ambient atmospheric

CO2 (Lindroth et al. 1995). Insect herbivores typically need

to reach a certain size before molting to the next stage of

development, and N availability will influence this process.

Furthermore, the nutritional indices, such as approximate

digestibility index (AD), efficiency of conversion of ingested

food (ECI) and/or efficiency of conversion of assimilated or

digested food (ECD) of insects feeding on low N food are

typically decreased (Mattson 1980; Chen et al. 2004; but see

Barbehenn et al. 2004). This means more low-N food is

Effects of nitrogen fertilization on tritrophic interactions 83

123

needed by many insects to complete their development,

which may be exacerbated by the general increase in

induction of anti-feedants and toxins in lower N plants.

Population densities will likely decrease for these herbivore

species, especially in temperate regions where delayed

growth rates in nutritionally challenged herbivores may

hamper escape in time from environmental exigencies; for

example, they may not reach their critical stage for winter

diapause. Delays in attainment of reproductive age also slow

population growth.

Both increased consumption rates and prolonged feed-

ing periods may also increase exposure and/or suscepti-

bility of herbivores to potential predators, parasitoids, and

pathogens, and result in greater herbivore mortality, as

predicted by the slow-growth-high-mortality (SG-HM)

hypothesis. The SG-HM hypothesis states that slower

developing herbivores would be expected to suffer higher

mortality from enemies (Feeny 1976; Augner 1995;

Haggstrom and Larsson 1995; Benrey and Denno 1997;

Fordyce and Shapiro 2003), although the validity of the

hypothesis might depend on the system of study and the

underlying assumptions (Clancy and Price 1987; Williams

1999). Outcomes also may vary with the life history of

herbivorous insects and their natural enemies, and the

extent to which plant characteristics that impair herbivore

growth also interfere with the foraging efficiency of, or

host/prey suitability for the natural enemies (Benrey and

Denno 1997), because plant traits that confer resistance to

herbivores are not always compatible with the functioning

of natural enemies of the herbivores (Cortesero et al. 2000;

see Hare 2002 for a review). For example, adverse effects

of plant morphological traits, such as glandular trichomes

and trichome density, on parasitic insect foraging have

been noted in tobacco (Nicotiana tabacum L.) (Rabb and

Bradley 1968; Kantanyukul and Thurston 1973; Elsey and

Chaplin 1978), cotton (Gossypium hirsutum L.) (Treacy

et al. 1986), wild potato (Solanum berthaultii Hawkes)

(Obrycki and Tauber 1984; Obrycki 1986), alfalfa (Medi-

cago sativa L.) (Lovinger et al. 2000), and soybean (Gly-

cine max L.) (McAuslane et al. 1995). However, in relation

to plant nitrogen levels, reduced food quality and resulting

developmental delays and impaired vigor of herbivores

would be generally expected to lead to greater herbivore

mortality and dampening of population growth. Williams

(1999) pointed out that the SG-HM hypothesis appears to

apply consistently to generalist natural enemies, which are

less likely to be adversely affected by suboptimal prey/

hosts because of their capacity to switch food types.

Direct resistance traits of food plants

Instead of being helpless, plants have innate capacities for

resistance to herbivores, with traits that can be broadly

grouped into direct and indirect resistance. Indirect resis-

tance includes any plant traits that increase fitness through

interactions with organisms other than herbivores, for

example, attracting entomophagous enemies of herbivores.

In contrast, direct resistance refers to morphological (e.g.,

glandular trichomes) and chemical traits (e.g., terpenes)

that directly exert negative effects on herbivores. Direct

resistance can be further divided into constitutive and

induced. Besides maintaining diverse constitutive mor-

phological structures and plant secondary metabolites

independent of herbivory, plants can be induced to manu-

facture a larger array of defensive compounds and struc-

tures in response to herbivory. These nitrogen-containing

(e.g., alkaloids, non-protein amino acids) and non-nitrogen-

containing (e.g., flavonoids, phenolics, tannins, and terp-

enes) plant secondary metabolites had previously been

considered waste products because they were thought to

have no clear functions in plant survival (Seigler and Price

1976). However, more evidence is emerging of diverse

ecological, physiological and biochemical roles of these

chemicals (Seigler and Price 1976; Bennett and Wallsgrove

1994; Constabel and Ryan 1996; Zangerl and Rutledge

1996; Simmonds 2003; Wink 2003; Zagrobelny et al.

2004), although, the distribution of these compounds

among plants appears highly idiosyncratic (Berenbaum and

Zangerl 2008), and there is as yet no unifying theory to

explain how and why plants produce, transport, and store

such a diverse array of chemicals (see Firn and Jones 2000;

Dudareva et al. 2004; Penuelas and Llusia 2004; Owen and

Penuelas 2005, 2006a, b; Firn and Jones 2006a, b; Pi-

chersky et al. 2006 for discussion). Furthermore, there are

several well-studied examples of herbivores that have

developed detoxification mechanisms, and these mecha-

nisms are highly idiosyncratic in distribution among her-

bivore taxa even for those feeding on the same plant

(Berenbaum and Zangerl 2008). Berenbaum and Zangerl

(2008) suggest that using genomic tools that have been

developed in studies of the relatively few plant families

used as models over the last several decades may clarify

our understanding of the ecologically idiosyncratic nature

of production and detoxification of plant defense com-

pounds. Given the breadth of secondary compounds, the

range of possible functions, and the inconsistent pattern of

responses to secondary compounds by herbivores, predic-

tions of ecosystem- and community-level outcomes for N

changes are difficult.

Expression of constitutive and induced allelochemicals

in a wide range of plant species is significantly influenced

by soil nutrient availability (Dudt and Shure 1994; Kori-

cheva et al. 1998; Stout et al. 1998; Darrow and Bowers

1999; Cipollini and Bergelson 2001; Coviella et al. 2002;

Hol et al. 2003; Orians et al. 2003; Wall et al. 2005),

although the magnitude of their expression may increase,

84 Y. Chen et al.

123

remain neutral, or decline depending on the study systems.

For example, total concentration of the carbon-based irid-

oid glycoside from Plantago lanceolata L. (Plantagina-

ceae) was decreased by fertilization (Darrow and Bowers

1999; Prudic et al. 2005). Nitrogen addition also lowered

constitutive phenolics in tomato plants, Lycopersicon es-

culentum Mill. (Solanaceae) (Stout et al. 1998), polyphe-

nols in Solanum carolinense L. (Solanaceae) (Wall et al.

2005), and condensed tannins in quaking aspen Populus

tremuloides (Salicaceae) (Hemming and Lindroth 1999).

However, fertilization had no effect on the phenolics of

tulip poplar, Liriodendron tulipifera L., and dogwood,

Cornus florida L. (Dudt and Shure 1994). Proteinaceous

trypsin inhibitor concentrations in Brassica napus L.

(Brassicaceae) seedlings (Cipollini and Bergelson 2001)

and in tobacco Nicotiana attenuata Torr. ex S. Watson

(Solanaceae) (Lou and Baldwin 2004), and nicotine content

in tobacco (Lou and Baldwin 2004) were enhanced by

nutrient fertilization. Proteinase inhibitor levels of tomato

(L. esculentum) plants grown under low, medium, and high

N conditions remained at the same levels, although leaflet

total protein concentrations increased as N availability

went from low to high (Stout et al. 1998). In stinking

willie, Senecio jacobaea L. (Asteraceae), the total amount

of the N-based defensive compound pyrrolizidine alkaloid

was not affected by addition of nutrients, although con-

centrations were decreased because of higher plant mass

due to more rapid growth (Hol et al. 2003). These authors

suggest that there is no need for additional defense as long

as plant growth is faster than biomass removal by herbiv-

ory. Plants may, therefore, invest in more rapid growth

when this strategy allows them to escape herbivory in time.

A growth-escape strategy would be expected to have little

or no adverse effect on herbivores, but may be beneficial to

individual and population growth of herbivores.

Besides the effects on C- and N-based constitutive

chemicals discussed above, N may also affect plants’

induced defense at the time of herbivory. For example, N

fertilization increased the degree of induced resistance in

poplar (Populus nigra L.) after continuous feeding of

gypsy moth (Lymantria dispar L.) for 72 h (Glynn et al.

2003). Similarly, the magnitude of induced trypsin inhibi-

tor in the high nutrient treatment was greater than in the

low nutrient treatment in Brassica napus L. following

mechanical damage (Cipollini and Bergelson 2001).

However, there appear to be upper thresholds of N quantity

above which induced responses of plants to herbivory are

reduced. For example, Olson et al. (2009) found that cotton

(G. hirsutum) plants that were grown with twice the rec-

ommended N levels and those plants grown with no

nitrogen had increased feeding damage on leaf tissue by

Spodoptera exigua when compared to plants grown with

recommended levels of nitrogen, presumably because of

reduced induction of terpenoid aldehydes (Olson et al.

2009). Conversely, Chen et al. (2008b) found that terpe-

noid aldehyde induction was increased in low-N (42 ppm)

cotton plants experiencing herbivory by S. exigua relative

to plants receiving more N. Therefore, there is likely a

range of nitrogen concentrations that is optimal for pro-

duction of N-responsive defensive secondary compounds.

Above this range the plant may be at greater risk for her-

bivory, but in a nutrient-rich environment the plant may be

able to outgrow herbivory with minimal investment in

chemical defense.

N alters herbivore suitability as prey/host of natural

enemies

Nutritional quality of prey/host

The development time of immature parasitoids is typically

positively related to host size, although the relationship can

be neutral and negative in some cases (e.g., King 1987;

Sequeira and Mackauer 1992). The dependency of devel-

opment time upon host size differs between idiobiont

(parasitoids that terminate host development at the time of

oviposition) and koinobiont parasitoids (parasitoids that

allow hosts to continue developing after oviposition) (Salt

1941; Vinson and Iwantsch 1980; Kouame and Mackauer

1991; Godfray 1994). Size of herbivore hosts is, in turn,

closely and directly related to the nutritional quality of

their host plants, and herbivore size can be used as a proxy

for plant quality.

Adult parasitoids also may be affected by differences in

host quality. Host-feeding parasitoid adults are restricted to

the insect order Hymenoptera and 140 species from 17

families were noted to have this behavior (Jervis and Kidd

1986). The fecundity of host-feeding parasitoids is affected

by the hosts on which they feed (Jervis and Kidd 1986;

Thompson 1999). For example, fecundity of hymenopteran

parasitoids, such as Bracon hebetor Say (Braconidae),

Aphytis lingnanensis Compere (Aphelinidae), and Pimpla

turionellae (L.) (Ichneumonidae) was greatest when sup-

plied with hemolymph of their hosts, compared to those

starved or provided only water (Edwards 1954; Debach and

White 1960; Benson 1973; Lum 1977), because they obtain

amino-nitrogen for egg development (Jervis and Kidd

1986). Therefore, qualitative changes in herbivores due to

plant N may directly affect parasitoid reproduction.

The fitness of predators can also be affected by their

diets (Jervis and Kidd 1986; Li and Jackson 1997;

Thompson 1999; Mayntz and Toft 2001). For example,

when jumping spiders, Portia fimbriata (Araneae: Saltici-

dae), were provided with prey composed of intraguild

spiders, they had greater survival, in comparison to those


123

supplied with N-poor phytophagous insects (Li and Jack-

son 1997). Compared to predaceous stink bugs (Podisus

maculiventris) reared on caterpillars fed on diets made of

mature-leaf powder, their conspecifics reared on caterpil-

lars fed on diets made of new-leaf powder grew faster

(Strohmeyer et al. 1998). The higher growth rate of P.

maculiventris when feeding on caterpillars reared on a

young leaf diet was attributed to higher nutrients in the

caterpillars, even in the presence of higher amounts of

iridoid glycosides, which are known feeding deterrents to

generalist herbivores (Strohmeyer et al. 1998). Thus, the

fitness of predators may depend on the quality of the

predator’s prey, which in turn may depend on the quality of

the prey’s host.

It is likely that entomopathogens are also affected by N

changes in plants. As noted above, reduced plant quality

often leads to increased consumption by herbivores. Some

entomopathogens (bacteria, fungi, and viruses) can persist

on the phylloplane as infective units (e.g., spores), and

some of these (bacteria and viruses) must be ingested to

infect the host. Thus, increased consumption by herbivores

may increase the probability of consuming infective

propagules (Cory and Hoover 2006). Increased movement

also may expose the herbivore to more fungal spores,

thereby increasing the risk of infection. Host herbivores

also may be weakened as a result of inappropriate plant N

levels, leading to reduced resistance to infection. Indeed,

Lee et al. (2006) observed that dietary protein levels were

highly influential in determining success of nuclear poly-

hedrosis virus infection in the caterpillar Spodoptera lit-

toralis (Boisduval), and infected caterpillars actively

modified their N intake to address the infection. Changes in

plant architecture resulting from N availability also may

indirectly affect entomopathogen survival and infection

success by altering the microhabitat (most notably

humidity and UV irradiation).

Herbivore defense against natural enemies

Lower nutritional quality of host plants may lower an

herbivore’s encapsulation ability. The herbivore’s chances

of encapsulating invading parasites or pathogens is gener-

ally correlated with the herbivore’s developmental stage

(instar), physiological condition, and capacity for defensive

behavior (Salt 1968; Smith and Smilowitz 1976; Blumberg

and Debach 1981; van Driesche and Bellows 1988), which,

in turn, may be influenced by N availability (Chen et al.

2008a).

Many plant allelochemicals that function as defensive

compounds are sequestered by various herbivorous insects

in the hemolymph. The predators and host-feeding para-

sitoids that feed on those insects, and larval offspring of

parasitic wasps that live part of their life time inside such

insects will in many cases suffer in terms of developmental

time and survivorship (Campbell and Duffey 1979; Duffey

et al. 1986; van Emden 1995; Kester and Barbosa 1991; for

a review, see Turlings and Benrey 1998; but see Schuler

et al. 1999). The adverse effect of the antibiotic tobacco

compound nicotine absorbed in tobacco hornworm, M.

sexta, hemolymph on parasitism and survival of the gre-

garious parasitoid Cotesia congregata (Say) is a good

example (Morgan 1910; Gilmore 1938; Thurston and Fox

1972). Manduca sexta is a specialist herbivore in tobacco

and can process nicotine effectively mostly through

excretion. However, some amount of nicotine is seques-

tered in the M. sexta hemolymph without any ill-effect to

the herbivore (Self et al. 1964). The parasitic wasp C.

congregata, on the other hand, is more sensitive to nico-

tine, which reduces their survival (Parr and Thurston 1972;

Thorpe and Barbosa 1986; Barbosa et al. 1991).

The effects of N on herbivore defense, and natural

enemies may vary with the plant species or the type of

allelochemical produced. For example, Lou and Baldwin

(2004) noted that N addition increased tobacco nicotine

production, however, Baldwin (1999) found that M. sexta

is resistant to nicotine. In separate studies, Thorpe and

Barbosa (1986), and Parr and Thurston (1972) found lower

survival of C. congregata on M. sexta larvae that had fed

on tobacco plants with nicotine and artificial diets con-

taining nicotine compared to cotton plants and artificial

diets without nicotine. Therefore, addition of N to tobacco

plants may adversely affect the performance of C. con-

gregata. In contrast, as shown previously, the quantities of

many constitutive defensive plant secondary metabolites

are negatively related to N levels. Consequently, in such

cases predators and parasitoids that consume herbivores

that are grown on host plants of higher N levels may per-

form better.

N affects plant indirect resistance/defense incurred

through natural enemies

The attraction of entomophagous natural enemies by plants

is referred to as plant indirect defense. Because the rela-

tionship can appear mutualistic, these natural antagonists of

herbivores are sometimes called ‘plant bodyguards’ (Dicke

and Sabelis 1988; Whitman 1994; Cortesero et al. 2000).

Herbivore-induced volatile organic compounds (VOCs)

that natural enemies rely on when foraging, as well as food

and shelter of natural enemies, may be altered by plant N

status. In the study by Olson et al. (2009), cotton plants

grown in zero nitrogen that were induced by feeding of

Spodoptera exigua (Hubner) were significantly less

attractive to Microplits croceipes (Hymenoptera: Braconi-

dae) in flight choice bioassays than damaged plants grown

86 Y. Chen et al.

123

in recommended N levels. Interestingly, parasitoids were

also more favorably responsive to damaged plants receiv-

ing recommended N rates than to plants grown in twice the

recommended N similarly damaged by S. exigua. This

indicates the potential for decreased attraction of this and

likely other natural enemy species in cotton fields that have

too little or too much N. Therefore, fluctuations in N due to

resource availability or acquisition capacity may contribute

to significant changes in population dynamics of herbivores

and their natural enemies.

N changes volatile release pattern (orienting cues)

Plants release a blend of volatile chemicals following

wounding by herbivores. Some of these induced volatiles

are released around the actual feeding site, while others are

systemically released from plant tissue distal to and above

the wounded site. Green leaf volatiles (GLVs) (e.g., (Z)-3-

hexenal, (Z)-3-hexenol, and (Z)-3-hexenyl acetate), some

acyclic monoterpenes, sesquiterpenes, homoterpenes, and

indole are among the typical locally induced volatile

organic compounds (VOCs) in cotton (Loughrin et al.

1994; McCall et al. 1994; Turlings et al. 1995; Pare and

Tumlinson 1997, 1998). (Z)-3-hexenyl acetate, some acy-

clic monoterpenes, sesquiterpenes and homeoterpenes can

be systemically induced (Loughrin et al. 1994; Rose et al.

1996; Pare and Tumlinson 1997, 1998). Many of these

herbivore-induced plant-originated VOCs provide foraging

natural enemies essential cues to locate potential hosts/

prey. Both parasitoids and predators have been observed to

respond actively to VOCs. For example, the parasitoids

Cotesia marginiventris (Cresson) (Rose et al. 1998), Mi-

croplitis croceipes (Cresson) (Rose et al. 1998) and Car-

diochiles nigriceps Viereck (De Moraes et al. 1998) fly

more frequently to host-damaged plants. The predatory

mite Phytoseiulus persimilis (Acari: Phytoseiidae) and two

insect predators, Scolothrips takahashii (Thysanoptera:

Thripidae) and Oligota kashmirica benefica (Coleoptera:

Staphylinidae), were attracted to spider mite (Tetranychus

urticae)-infested lima bean plants (Dicke et al. 1990; Shi-

moda et al. 2002; Choh et al. 2004). These VOCs also have

repellent effects on ovipositing conspecific herbivores (De

Moraes et al. 2001), which would appear to benefit both the

plant by reducing herbivore load and the herbivore by

reducing intra-specific competition.

Nitrogen levels can alter the production and release of

these volatiles. Depending upon the plant, positive,

negative and no effects have been observed. In corn (Zea

mays var Delprim), the peak of volatile release was

detected when N concentration in the nutrient solution

was the lowest, both after mechanical wounding and

addition of volicitin (an elicitor isolated from oral

secretion of beet army worm, Spodoptera exigua

(Hubner) (Schmelz et al. 2003). Low N availability also

increased production of the main sesquiterpenes ((E)-a-

bergamotene, b-caryophyllene and (E)-b-farnesene) to a

greater extent after volicitin application, compared with

mechanical damage. In addition, reduced N levels made

the concentration of jasmonic acid (a chemical messen-

ger thought to be crucial to the induction of volatiles)

wane at a slower rate when compared to those levels in

higher N level plants. Jang et al. (2008) found decreased

levels of jasmonic acid in rice plants receiving higher

rates on N fertilization in all three of the cultivars tested.

Likewise, in a second system studied, celery with addi-

tional N had a lower quantity of volatile compounds

(Van Wassenhove et al. 1990). Nevertheless, Gouinguene

and Turlings (2002) found that unfertilized corn plants

(Zea mays var Delprim) emanated less volatiles when

compared with those that had received a complete

nutrient solution. The role of N was not implied in this

study as all the nutrients were varied (Schmelz et al.

2003). In tobacco (Nicotiana attenuata), oral secretion

from tobacco hornworm Manduca sexta (L.) and methyl

jasmonate (MeJA) induced volatile release was not

affected by N, though low N availability attenuated the

jasmonate and salicylate levels and reduced two N-con-

taining anti-herbivore defense compounds, nicotine and

trypsin proteinase inhibitors (Lou and Baldwin 2004).

Chen et al. (2008b) found that cotton plants with the

lowest N had substantially higher induced VOC’s than

those plants with higher N. GC–MS analyses indicated

that nitrogen affected the amount and/or rate of volatiles

released, not the induction per se, in cotton plants grown

with no nitrogen and those grown with twice the rec-

ommended nitrogen, compared with those grown in

recommended nitrogen (Olson et al. 2009). No other

studies on VOC release patterns are available to date.

However, the studies to date suggest that the effects of N

on the release pattern of VOCs might be system- or

species-specific. Plants generally increase VOC emission

under stress from low nitrogen, unless the plant has

evolved more plastic responses to herbivory and defen-

ses, such as found in tobacco plants; these plants have

VOC production that is independent of nutrient avail-

ability, and have a major herbivore, Manduca sexta,

which has developed resistance to nicotine (Baldwin

1999). Placing more emphasis on VOC emission than

secondary compound production would be advantageous

to the plant when herbivores are less affected by the

secondary metabolites, or if the fitness costs of nicotine

production are too high as a result of N limitation

(Baldwin 1999). This underscores the need to understand

how plants and their herbivores have co-evolved (e.g.,

Berenbaum and Zangerl 2008). It would be of interest to

determine if plants in the families Brassicaceae and


123

Apiaceae that have herbivores that have evolved detox-

ification methods (Berenbaum 2001; Li et al. 2007), also

exhibit VOC production that is independent of nutrient

availability.

Plants as food and shelter of natural enemies

Many insect predators feed on pollen as supplemental food,

whereas the prevalence of pollen-feeding in parasitoids

seems to be rather uncommon (reviews in Wackers 2005).

Pollen is primarily a source of nitrogenous compounds

(proteins and amino acids), but also contains starch, lipids

and some sterols. It is likely that with increasing N this

food source will increase in value and/or abundance to

those species that feed upon it.

Both predators and parasitoids feed on floral and extra-

floral nectar and various fitness correlates of many natural

enemies such as longevity, movement and fecundity are

increased by feeding on these plant foods (Hagley and

Barber 1992; Wackers and Swaans 1993; Olson and Nec-

hols 1995; Morales-Ramos et al. 1996; Baggen and Gurr

1998; Eijs et al. 1998; Jervis and Kidd 1999; Irvin and

Hoddle 2007). Male and female parasitoids Diachasmi-

morpha longicaudata (Ashmead) (Hymenoptera: Braconi-

dae), of the tephritid fruit fly for example, lived up to 15

and 28 days, respectively, when cotton extrafloral nectaries

were available (Sivinski et al. 2006). Conversely, with

provision of only water male and female parasitoids lived a

maximum of 7 days. Trissolcus basalis (Wollaston)

(Hymenoptera: Scelionidae), an important egg parasitoid of

southern green stink bug (Nezara viridula (L.)) (Hemip-

tera: Pentatomidae), lives longer when floral nectars are

available (Rahat et al. 2005). Provision of food sources can

attract more natural enemies and increase the mortality of

herbivorous insects. For instance, parasitism of the gypsy

moth, Lymantria dispar L. (Lepidoptera: Lymantriidae),

was higher on plants with extrafloral nectaries, although the

parasitoid species richness between nectaried and nectari-

less plants was not different (Pemberton and Lee 1996).

More bollworm, H. zea, eggs were parasitized by Tricho-

gramma pretiosum Riley (Hymenoptera: Trichogrammati-

dae) in cotton plants with extrafloral nectaries than those

without nectar (Treacy et al. 1987).

Overall N effects on nectar production appear to vary

among plant species. Burkle and Irwin (2009) found that

increasing N fertilization increased nectar production of

Ipomopsis aggregata (Pursh) V.E. Grant (Polemoniaceae),

but had no effect on nectar production by Linum lewisii

Pursh (Linaceae). Similarly, Ryle (1954a, 1954b) reported

that increasing N (as nitrates) fertilization led to decreased

nectar production in apple trees and mustard plants, but

enhanced nectar production in buckwheat and had no effect

on clover. However, she also noted that there was an

interaction between N and the other nutrients relative to

nectar production, underscoring the need to consider mul-

tiple variables. Nitrogen changes may also affect the amino

acid content of nectar, which may affect herbivore quality

(Mevi-Schutz and Erhardt 2005) for natural enemies, or N

availability may alter the abundance of nectar through

influencing changes in numbers of available nectaries (e.g.,

through changes in flower abundance), possibly reducing

or increasing competition for resources among natural

enemies. Studies of reduced N in conjunction with

increased CO2 levels also noted increased carbohydrates

(Koricheva et al. 1998), and one study (Fischer et al. 1997)

found that the concentration of sugars, but not their com-

position in floral nectar of Gentianella germanica

increased by 36% under elevated CO2. Thus, over the

longer term as CO2 levels rise, plant carbohydrate avail-

ability may increase and ameliorate any possible short-term

negative effects of reduced N accessibility.

Plants not only provide natural enemies with food, but

also shelter. Many plant structures such as leaf domatia and

leaf veins can provide shelter and overwintering sites to

various natural enemies (Karban et al. 1995; Walter 1996;

Hance and Boivin 1993; Whitman 1994; Corbett and Ro-

senheim 1996; Elkassabany et al. 1996; Maschwitz et al.

1996; Agrawal and Karban 1997). Despite the importance

of these plant structures, there are no studies of the effects

of N availability on their growth and development and

ultimately, their ability to provide shelter to natural ene-

mies. However, at the plant community scale, increased

nitrogen availability substantially increases the density and

changes the composition of plant communities (e.g.,

Manning et al. 2009). This is likely to extend over the long-

term as atmospheric N levels continue to rise in response to

increased N from fertilization and combustion of fossil

fuels (Vitousek et al. 1997). Plant communities with

increased N have increased net primary productivity and

decreased plant biodiversity (Gough et al. 2000; Suding

et al. 2005). Increases in plant biomass and reduced plant

diversity may profoundly affect plant species’ ability to

acquire nutrients or to evade attack. For example, increases

in plant density (biomass) means more plant surface area

and higher edge to surface area ratios for natural enemies to

forage and this could have negative effects on predators

and parasitoids in locating their hosts and prey (e.g.,

reviews in Olson and Andow 2006 for parasitoids and

Rutledge and O’Neil 2005 for predators). Beckerman et al.

(1997) found that the generalist leaf-chewing grasshopper

Melanoplus femurrubrum shifted habitat from grasses to

more complex herbaceous species as predation risks from

the hunting spider, Pisaurina mira increased. Reductions in

plant community biodiversity could also remove needed

refuge habitats for herbivore species, making them more

vulnerable to predation. Therefore, increased plant density

88 Y. Chen et al.

123

and biomass, along with the previously discussed reduction

in VOCs in higher N plants is expected to negatively affect

the foraging efficacy of natural enemies. Decreased plant

diversity in higher N plant communities is expected to have

a negative effect on herbivores that are unable to switch

habitats while feeding on a particular plant species, but this

would depend on how complex the structure of the vege-

tation becomes in the original habitat by increased N. In the

latter case, N increases with concomitant increases in

complexity would likely decrease predation rates overall,

and increase herbivory on the plants.

Predation/parasitism rates changed by N

Natural enemies (predators, parasitoids, and pathogens) of

herbivores employ chemical, visual, and vibrational cues

(both from hosts/prey and food plants of hosts/prey) to

search for and/or attack potential preys/hosts. Chemical

cues (also called semiochemicals) are, in most cases, the

most important cues used by predators and parasitoids to

locate hosts/prey (Mattiacci et al. 2001; Wackers and

Lewis 1994; Rose et al. 1998; Olson et al. 2000; Dicke

et al. 1990; Shimoda et al. 2002; Choh et al. 2004).

Nitrogen has been shown to affect chemical attractiveness

of plants for foraging enemies of herbivores.

In small-plot studies, parasitoids were more attracted to

plots with higher N plants and exerted greater control on

herbivores on such plants. Encarsia formosa Gahan

(Hymenoptera: Aphelinidae), a parasitoid of the whitefly

Bemisia argentifolii Bellows and Perring (Hemiptera:

Aleyrodidae), was more frequently observed on N-fertil-

ized and whitefly-infested poinsettia plants, Euphorbia

pulcherrima Willd. ex Klotzsch, than on whitefly-infested

but unfertilized plants in choice-tests (Bentz et al. 1996).

Significantly more whiteflies were parasitized per leaf in

the higher N treatment than in the lower N treatment. The

mean counts of whitefly per leaf (sum of parasitized, fed

upon and unparasitized) were about the same across the

treatments (see Table 1 of Bentz et al. 1996), so the pos-

sibility that the parasitoids were responding to greater

sucking damage or host density alone could be excluded. In

a study of the impact of collard plant (B. oleracea) quality

on parasitism rate and sex ratio of the diamondback moth

parasitoid Diadegma insulare (Cresson) (Hymenoptera:

Ichneumonidae), Fox et al. (1990) found more parasitoids

in the well-fertilized treatment and parasitism rates were

lowest under regimes without application of fertilizer,

although foliar N level and protein concentration were

marginally positively correlated with parasitism rate.

Additionally, parasitoids that had emerged from high N

treatments were more female-biased. Loader and Damman

(1991) also found that parasitism rates were higher on

cabbage butterfly, Pieris rapae (L.) (Lepidoptera:

Pieridae), developing on collards with higher N. All of

these studies were carried out with potted plants where

differences in plant density in the plot stands were con-

trolled. Small parasitoids that are weaker fliers and more

wind-borne may not rely on chemical and visual cues to the

extent that stronger fliers can. With no apparent increased

plant surface area or increased edge to surface area ratios in

these plots, the parasitoids may have located hosts equally

well on high and low N plants, even though they had higher

success developing in herbivores that had fed on higher N

plants. Larger parasitoids, with the exception of D. insu-

lare, responded as predicted; higher parasitism was found

on low N plants. Diadegma insulare are known to have

variable sex ratios, but also produce more females on high

N plants and within larger hosts (Fox et al. 1990) which

may explain its higher success on high N plants. Therefore,

parasitioids and predators may increase their overall fitness

developing in higher N hosts due to increased suitability.

However, their ability to locate hosts will likely be reduced

in higher N plant communities because of reduced phyto-

chemical cues and greater foraging areas in foliage.

The cues that natural enemies respond to in the studies

discussed remains unknown. The crop systems utilized to

investigate VOC release patterns differ from those selected

to examine natural enemy effects. Based on limited infor-

mation available at this point, it is hard to draw conclusions

on whether or not the observed parasitism/predation pat-

terns are consistent with variable rates of VOC release.

Other orienting cues such as visual cues may also play a

role in some of the cases because plants with low and high

N availability not only often differ in height, but also in

color, architecture, density, and community composition.

Plant morphological traits also interact with foraging effi-

ciency of natural enemies, and mutualistic, antagonistic,

and neutral relationships between plant trichomes, and

other structural features, and natural enemies of herbivores

have been documented (e.g., Elsey and Chaplin 1978; Price

et al. 1980; Obrycki 1986; Treacy et al. 1986; Kauffman

and Kennedy 1989; McAuslane et al. 1995; Sutterlin and

van Lenteren 1997; Bottrell et al. 1998; Cortesero et al.

2000; Lovinger et al. 2000; Gassmann and Hare 2005;

Simmons and Gurr 2005; Olson and Andow 2006; Styrsky

et al. 2006).

Summary

N fertilization may exert profound bottom-up influences on

ecosystems— interactively extending across trophic levels

and influencing outcomes at the individual, population, and

community levels. These influences, and their interactive

top–down and bottom-up effects, have received limited

attention to date, but are of growing significance with the


123

need for expanding global food production (with accom-

panying use of fertilizer amendments), the widening risks

of fertilizer pollution, and the continued increase in

atmospheric CO2. The biomass loss of low N plants due to

reduced growth and compensatory consumption of herbi-

vores appears to be compensated for at least in part by

increased direct plant defenses, and by greater indirect

defenses through enhanced natural enemy recruitment and

reduced foraging areas due to decreased plant size and

complexity. On the other hand, high N availability to plants

promotes plant biomass production and the increased bio-

mass might be offset by increased herbivory resulting from

greater recruitment of herbivores to a more nutritious plant,

and reduced natural enemy recruitment because of reduced

chemical cues. However, plants may respond by providing

increased food (e.g., nectar and pollen) and shelter

resources for natural enemies. Further, plant life history

(e.g., perennial vs. annual) may alter the relative contri-

butions of induced defensive and volatile compounds in

response to herbivory and N availability such that the low

N/high defense and volatile pattern observed in the few

examples studied may not hold true. Ultimately, plants

must balance N utilization against the action of herbivores

and their natural enemies, as well as the metabolic

requirements of constitutive and induced defenses, in their

management of herbivory. Maintaining this balance will

likely become more complicated with increasing environ-

mental contamination by anthropogenic N and CO2.

Acknowledgments We appreciate funding support from the Geor-

gia Cotton Commission and Cotton Incorporated. We also appreciate

the valuable comments of the anonymous reviewers and editor on the

manuscript.

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