- Email: [email protected]
Using plant nutrient landscapes to assess Anthropocene effects on insect herbivores
Accepted Manuscript Title: Using Plant nutrient landscapes to assess Anthropocene effects on insect herbivores Author: Paul A. Lenhart PII: DOI: Reference:
S2214-5745(16)30131-6 http://dx.doi.org/doi:10.1016/j.cois.2017.07.007 COIS 368
To appear in: Received date: Revised date: Accepted date:
17-4-2017 30-6-2017 19-7-2017
Please cite this article as: Paul A. Lenhart Using Plant nutrient landscapes to assess Anthropocene effects on insect herbivores (2017), http://dx.doi.org/10.1016/j.cois.2017.07.007 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
1
USING PLANT NUTRIENT LANDSCAPES TO ASSESS ANTHROPOCENE
2
EFFECTS ON INSECT HERBIVORES
PAUL A. LENHART*1,
4
1
S-225 Agricultural Science Center N, Department of Entomology, University of
us
6
cr
5
7
Kentucky, Lexington, Kentucky.
*To whom correspondence should be addressed. email: [email protected]
M
10
an
8 9
te Ac ce p
13
d
11 12
ip t
3
1
Page 1 of 24
13 Abstract- Global climate change will dramatically affect insect herbivores in a large part
15
through changes in plant quality. Linking how multiple climate factors affect plant
16
macronutrient content may be the most accurate way to understand the response of insect
17
herbivores. Studies should embrace the complexity of interacting climate factors in
18
natural systems and characterize shifts in multidimensional plant nutrient landscapes.
19
This nutrient landscape simplifies interpretation of climate effects although selection of
20
appropriate currencies, scale, and interactions with allelochemicals present challenges.
21
By assessing climate change through the filter of nutrient landscapes we could gain an
22
understanding of how complex interacting climate change drivers affect the ‘buffet’
23
available to different insect herbivores.
Ac ce p
te
d
24
M
an
us
cr
ip t
14
2
Page 2 of 24
24 25
INTRODUCTION Global climate change will dramatically affect the distribution and abundance of
27
insect herbivores in natural and managed systems, but our understanding of these effects
28
is hindered by the complex nature of plant and insect responses. Changing climate has
29
direct effects on insect herbivore physiology but arguably more important are indirect
30
effects via changes in host plant quality. Global climate change in the newest geologic
31
epoch, the Anthropocene [1,2], is characterized by rising CO2, warming temperatures,
32
and altered precipitation, all of which can dramatically affect plant nutrient content [3].
33
Investigating these factors individually can be mechanistically useful [4], but to inform
34
practical predictions, relevant combinations of factors need to be considered as they
35
interact idiosyncratically [3,5].
d
M
an
us
cr
ip t
26
Investigators often do not adequately characterize changes in plant quality. Plant
37
nutrient quality is often incorrectly considered along a single axis [6] despite decades of
38
research showing that insect herbivores feed to simultaneously satisfy requirements for
39
many nutrients (for an in depth background see [7-9]). Nutritional imbalances reduce
40
herbivore performance [10]. To prevent imbalances, insect herbivores taste and regulate
41
intake of plant macronutrients, mainly soluble protein (Prot) and digestible carbohydrates
42
(Carb), in order to meet a specific ratio, termed the intake target, rather than an absolute
43
quantity of either nutrient alone [9]. A third macronutrient class, lipids, often makes up a
44
small fraction of plant nutrient content but may be critical for certain herbivores [11].
45
Required micronutrients (fatty acids, sterols, vitamins, lipogenic compounds, and various
46
inorganic compounds) are generally needed in such small amounts that normal feeding
Ac ce p
te
36
3
Page 3 of 24
47
satisfies demand without the need for active regulation by the insect [12]. Climate change
48
studies need to incorporate this multidimensional aspect of plant nutrient quality. Linking how multiple climate factors affect plant macronutrient content may be
50
the most accurate way to understand the response of insect herbivores to global climate
51
change. However, investigators rarely measure plant nutrient content in a manner
52
relevant to insect herbivores, i.e. as regulated, digestible nutrients in a multidimensional
53
context. The distribution of consumer-relevant nutrient concentrations across different
54
foods, in this case plant tissue, can be termed the ‘nutrient landscape’. The nutrient
55
landscape is the ‘buffet’ of food options a foraging animal can choose from. Studies
56
should embrace the complexity of interacting climate change drivers in natural systems
57
and incorporate a modern understanding of nutritional ecology to characterize shifts in
58
plant nutrient landscapes. Understanding how climate change affects herbivores via
59
nutrient landscapes could allow better predictions of pest population dynamics in agro-
60
ecosystems [13] and feedbacks to nutrient cycling [14].
62 63
cr
us
an
M
d
te
Ac ce p
61
ip t
49
ANTHROPOCENE EFFECTS ON PLANT MACRONUTRIENT CONTENT The effects of the Anthropocene on plants are complex. Numerous climate change
64
drivers co-occur and vary both temporally and spatially. Herbivores face significant
65
changes in host plant abundance and morphology [15] and superimposed on these
66
changes are shifts in macronutrient content within each plant. The most common
67
approach for predicting consequences of climate change has been to study the effects of
68
climate change drivers individually on trophic interactions [5]. While this approach has
69
provided many insights, we should move forward from this foundation by performing
4
Page 4 of 24
large-scale field surveys and experiments to understand how multiple climate change
71
drivers simultaneously shift plant macronutrient content. Changes in plant quality can be
72
quantified as a multidimensional nutrient landscape for comparison with changes in
73
herbivore performance and population dynamics.
74
ip t
70
Experiments manipulating CO2, temperature, and water individually have found a number of strong effects on plant macronutrient content that can be reasonably
76
generalized (reviewed by [3,16,17]). Rising CO2 tends to increase Carb and decrease Prot
77
[17-21]. Rising temperature increases plant photosynthetic rates which may increase Prot
78
but decrease Carb [17]. Rising drought risk is also associated with the Anthropocene [22]
79
and the effects are variable [23,24]. The best-characterized response is that intermediate
80
levels of water stress increase soluble nutrients benefiting fluid-feeding insects [23,24].
81
These mechanistic responses become more difficult to generalize once we take into
82
account differences across plant functional groups [25-27]. Even more importantly
83
multiple climate change drivers can interact in additive, antagonistic, or synergistic ways
84
that are difficult to predict [3,5].
us
an
M
d
te
Ac ce p
85
cr
75
Herbivores do not just respond to abiotic-induced changes in plants, they can, in
86
turn, alter plant macronutrient content, defenses, architecture, biomass, and community
87
structure via their feeding activity. A critical herbivore-mediated ecosystem process is
88
deposition of frass that substantially affects nutrient cycling [28-30]. These herbivore
89
feedbacks to primary production and nutrient cycling likely play a role in Anthropocene-
90
related changes in terrestrial ecosystems.
91
Experimenting on climate drivers individually, without a real world context,
92
provides a fundamental understanding of the physiological responses of plants but is
5
Page 5 of 24
unlikely to accurately translate to predictions in the field. To this end, investigators
94
should quantify changes that occur in natural or semi-natural systems, then work
95
backwards to understand the most relevant mechanisms at play. By using natural
96
experiments [26,29] and correlative surveys [31], complex global change drivers can be
97
reduced to their relevant effects on plant nutrient landscapes.
NUTRIENT LANDSCAPES
us
99
cr
98
ip t
93
To quantify a nutrient landscape, it is first necessary to determine the appropriate
101
currencies, i.e. the primary nutrients an herbivore uses to make foraging decisions. While
102
deficiencies in any essential nutrient can reduce insect performance, only actively
103
regulated nutrients determine feeding behavior [7]. Adequate knowledge of regulated and
104
limiting nutrients for the focal herbivore must be determined so that relevant nutrients
105
can be assessed in the field [32]. Among most insect herbivores, especially folivores, this
106
will largely be Prot and Carb [7], however certain insect may also regulate lipids, sterol,
107
water intake, and salt [7,33-35]. Literature on plant traits is full of quantifications of plant
108
nutrients, largely elemental content, but translating these values to relevant
109
concentrations for herbivores can be challenging.
M
d
te
Ac ce p
110
an
100
Protein has received the most attention as a plant macronutrient, yet most data
111
continues to focus on N content which does not necessarily equate to Prot. Nitrogen can
112
range from 5-30% of plant dry weight [36] and can be allocated very differently between
113
plant functional groups [37]. Consequently, the generalized conversion factor used to
114
translate N to crude protein is inaccurate [38-40]. The largest pool of Prot in plants is
115
RuBisCO, which is critical for photosynthesis [41]. Using a global plant dataset, Ghimire
6
Page 6 of 24
et al. [37] estimate that the % of total leaf N allocated for photosynthesis, including
117
RuBisCo, is as low as 25% in tropical broadleaf evergreen trees but as much as 57% in
118
cultivated crops. Cultivated crops have the lowest residual pool of N (not allocated to
119
photosynthesis or respiratory functions) and are the only plant functional group to
120
increase allocation to RuBisCO with increasing leaf N [37]. Importantly, residual N
121
includes N-based defenses such as alkaloids and protease inhibitors [42,43]. Despite a
122
general correlation, caution should be taken when using N or crude protein as a surrogate
123
for Prot.
cr
us
Carbohydrates, in contrast with N, have often been ignored by plant insect studies
an
124
ip t
116
[44], despite having a demonstrated role in foraging decisions [7], and being highly
126
variable across plants [45]. Carb for insect herbivores include starches, simple sugars, and
127
fructans [46,47]. Starches are used primarily for carbon storage in plant reserve organs,
128
while soluble sugars serve a variety of intermediate functions in leaves [45]. Fructans
129
serve as carbon storage in 15% of angiosperms [48]. Digestion of structural
130
carbohydrates such as cellulose, hemicellulose, pectin, and lignin by insects requires the
131
use of microbial symbionts and may be an important way chewing herbivores degrade
132
cell walls to access digestible cell contents [49,50]. No elemental surrogate can estimate
133
Carb [51]. Although often invoked, C is present in all organic compounds and significant
134
correlations with insect performance could be due to any number of compounds. A recent
135
global comparison of plants highlights how Carb can differ across plant tissues, functional
136
types, biomes, and seasons [45]. Herbaceous plants and conifers have the highest leaf
137
concentrations, averaging between 14-20% of dry mass with some species containing
138
over 30% [45]. Strong seasonal fluctuations in starches and simple sugars reflect different
Ac ce p
te
d
M
125
7
Page 7 of 24
139
functions [45]. More studies of plant quality should explicitly measure Carb as it probably
140
has an important effect on insect herbivores, especially as a component of the Prot:Carb
141
ratio. Lipid regulation by herbivores is often ignored because of its scarcity in plants but
ip t
142
may be important for insect feeding guilds that target plant tissues with high lipid
144
content. Pollen, fruit, and seeds are often naturally high in lipids [52-54] and lipid
145
concentrations are often increased in the nutritive tissues that form within galls [55].
146
Caterpillars have demonstrated the ability to regulate for lipids in artificial diets [56,57].
147
Given that pollinators such as bumblebees will actively adjust their foraging to collect a
148
specific protein:lipid ratio in pollen [54] it is likely that florivores, frugivores, and seed
149
predators conduct similar regulation.
us
an
M
The scale at which an herbivore makes feeding decisions must be taken into
d
150
cr
143
account as well. Figure 1a is an example of Prot and Carb nutrient landscapes quantified in
152
plant tissue that a corresponding herbivore (Figure 1b-c) would feed from. The grassland
153
plants from central Texas, serve as host plants for a diverse community of grasshoppers
154
[26]. These mobile generalist herbivores move between plants frequently as they feed. In
155
contrast, many insects, such as the caterpillar in Figure 2b complete their development on
156
a single host plant. Tissues can vary widely in their Prot:Carb content within a single plant
157
providing a broad nutrient landscape as demonstrated by Deans et al. [44] in cultivated
158
cotton plants, Gossypium spp. (Figure 1a). Detailed observations of the tissues that are
159
actually consumed by insects will prevent uneaten tissues from biasing the quantification.
160
For example, Deans et al. [44] found that entire cotton bolls (fruit) had a Prot:Carb ratio of
161
1:3, however developing seeds within bolls could be over 3:1. Measuring Prot and Carb in
Ac ce p
te
151
8
Page 8 of 24
162
the specific plant tissues consumed by an herbivore increases the accuracy of nutrient
163
landscape quantification. It is tempting to superimpose an herbivores’ intake target onto the nutrient
165
landscape to evaluate what choices the herbivore will make, however this is not so
166
simple. By comparing what herbivores consume and excrete, it is evident that not all
167
digestible nutrients are accessible or digested. A portion of digestible nutrient content
168
may be trapped behind indigestible cell walls [58]. Herbivores can also adjust what is
169
digested through a range of behavioral, physiological, and morphological responses
170
(reviewed by [8]). Herbivores can use these post-ingestive responses to correct for
171
shortfalls in the balance of nutrients ingested. A thorough understanding of post-ingestive
172
regulation would be required to link a nutrient landscape directly to the requirements of
173
an herbivore. At the ecological scale necessary to understand the effects of global climate
174
change via plant quality, we should first look for relationships between shifts in the
175
nutrient landscape and herbivore performance. While herbivores may use these plastic
176
responses to mitigate the effect of plant quality differences, they still show strong diet
177
selection and the nutrient landscape should therefore strongly correlate with feeding
178
behavior and subsequent performance.
cr
us
an
M
d
te
Ac ce p
179
ip t
164
While the focus in this paper has been on plant nutrient content, plant quality is
180
often dictated by interactions between nutrient content and plant defenses, especially
181
plant secondary metabolites (PSM’s). While theoretically PSM’s could be incorporated
182
as additional axes influencing the plant nutrient landscape, they are highly diverse with
183
varying modes of action and toxicities [59]. Plant chemical defenses may actually
184
increase the importance of accurate nutrient regulation by the herbivore rather than
9
Page 9 of 24
diminish it. Artificial diet experiments have shown that the deleterious effects of
186
defensive chemicals are reduced when diets match the herbivore’s intake target [60,61].
187
Along the same lines, susceptibility to the biopesticide Bt toxin was lowest in
188
Helicoverpa zea caterpillars reared on diets closest to their intake target [62,63].
189
However, plant defenses can make herbivores reluctant to consume foods that would
190
otherwise satisfy their nutrient demands [60]. The interactions of plant defenses and plant
191
macronutrient content will continue to be an exciting frontier for plant-herbivore
192
interactions.
193
LINKING CLIMATE AND HERBIVORES VIA PLANT NUTRIENT SHIFTS
194
While interacting Anthropocene drivers can be complex, their combined
195
outcomes on plant macronutrient content can be characterized and related to herbivore
196
feeding behavior, performance, and abundance. Three different fundamental shifts may
197
occur, either individually or in some combination (Figure 2). These include changes in
198
nutrient concentration, ratio, and variation. In many cases it is likely that climate change
199
will cause simultaneous shifts, especially in ratio and concentration [64,65].
cr
us
an
M
d
te
Ac ce p
200
ip t
185
Nutrient concentrations may change, becoming more nutrient concentrated or
201
dilute (Figure 2a). If the ratio of Prot:Carb remains constant but total macronutrient content
202
(calorie content) increases or decreases, the rate of herbivore consumption could change
203
to meet requirements [10,66]. In the case of nutrient dilution (Figure 2a), compensatory
204
feeding can be costly [7]. Consumers may also employ a range of post-ingestive
205
mechanisms to increase nutrient absorption rather than consumption [8]. In the case of
206
increasing nutrient concentration, herbivore performance and population density may
10
Page 10 of 24
207
increase. For example, elevated CO2 and temperature affected concentrations of multiple
208
limiting amino acids in alfalfa which strongly correlated with aphid fecundity [67]. Macronutrient ratios could shift due to changes along a single macronutrient axis
210
(Figure 2b). To maintain nutrient homeostasis, herbivores may respond in a multitude of
211
ways including switching host plants, feeding on different plant tissue, and employing
212
post-ingestive corrections for nutritional imbalances [9,68]. For example, severe seasonal
213
drought has been shown to induce this sort of shift in a grassland, decreasing forb Prot but
214
not Carb resulting in a more Carb -biased Prot:Carb ratio [26]. Polyphagous grasshoppers
215
responded to the shift along a single nutrient axis and their numbers in open drought plots
216
decreased compared to watered plots [26].
cr
us
an
The breadth or variation of a nutrient landscape may also shift either increasing or
M
217
ip t
209
decreasing the different nutrient ratios the herbivore can choose from (Figure 2c). The
219
response of consumers to variation in food nutrient content, rather than just the mean is a
220
largely ignored aspect of nutritional ecology [69]. Many studies show that insect
221
herbivores can tightly regulate their macronutrient intake by switching among foods with
222
complementary nutrient profiles, i.e. diet mixing [7,8]. While this phenomenon is likely
223
more important for mobile polyphagous species, even specialist species that feed on a
224
single plant for their development could select among tissues to reach their intake target
225
[44]. Because there are costs to over- or under-ingesting macronutrients, herbivores
226
generally benefit from diet mixing [70]. Even when consumers have similar or greater
227
mean fitness on a single optimal food, inter-individual variation in fitness is significantly
228
lower when diet mixing is possible [71].
Ac ce p
te
d
218
11
Page 11 of 24
229
Contrarily, Wetzel et al. [69] proposed that heterogeneity in plant nutrient content may be a way plants suppress herbivore populations and that pest outbreaks in agro-
231
ecosystems could be linked to homogeneity of plant nutrient content. An analysis of 76
232
studies found evidence that variation in nutrient content, either above or below a mean,
233
decreases insect herbivore performance both in terms of growth and survival [69]. The
234
study evaluated performance data from herbivores restricted to different nutrient
235
concentration levels (no-choice tests) and ‘nutrient’ was a broad category treated uni-
236
dimensionally. Considering how insects respond to nutrient regulation challenges, these
237
findings may reflect general performance costs when herbivores are restricted to foods
238
which force under- or over- ingestion of nutrients [69]. These are subject to the ‘rules of
239
compromise’ that herbivores make on imbalanced foods [9]. If plant nutrient variation
240
did reduce insect herbivore performance, we would hypothesize that herbivores given
241
food with an optimal Prot:Carb ratio would out-perform herbivores that could choose
242
between foods with complementary Prot:Carb concentrations. Diet mixing experiments
243
generally do not support this idea [70]. This hypothesis could also be evaluated using a
244
correlative approach in the field comparing variation in the multidimensional plant
245
nutrient landscape with herbivore performance and density.
cr
us
an
M
d
te
Ac ce p
246
ip t
230
247
FUTURE DIRECTIONS
248
Focusing on Anthropocene-related shifts in the plant nutrient landscape has the potential
249
to improve predictions of how insect herbivory responds to complex global climate
250
change drivers. Similar approaches in mammalian herbivore systems have already proved
251
insightful [31,32,72]. Despite decades of work teasing apart how insect herbivores
12
Page 12 of 24
regulate multiple macronutrients simultaneously, studies are still assessing plant nutrient
253
quality in a manner inconsistent with how insect herbivores forage. Specifically I
254
encourage studies of climate change and insect herbivores to 1) quantify plant nutrient
255
content using currencies and scale relevant to herbivores, 2) analyze them in a
256
multidimensional context, and 3) investigate the role of variation in nutrient landscapes.
257
In addition, insect-plant biologist must continue to study the interactions of nutrients and
258
secondary metabolites. A truly integrative approach will need to consider direct effects of
259
global climate change drivers on herbivores [3,4,73,74], and top-down effects of other
260
trophic levels [3,74,75], but a basic understanding of how complex interacting climate
261
change drivers affect the ‘buffet’ available to different insect herbivores may go a long
262
way to predicting their responses to this changing world.
M
an
us
cr
ip t
252
d
263
Acknowledgements- I thank Carrie Deans, Blanka Angyal, Jen White, and the
265
anonymous reviewers for their valuable feedback. This material is based on work
266
supported by a Texas A&M Diversity Fellowship, as well as grants from the
267
Orthopterist’s society, Texas Ecolab, and USDA NIFA AFRI (2012-67011-19930).
268 269
Annotated references:
270 271 272
[3] Rosenblatt AE, Schmitz OJ: Climate Change, Nutrition, and Bottom-Up and TopDown Food Web Processes. Trends in Ecology & Evolution 2016, 31:965-975. **This review presents a framework for understanding the responses of food webs to
273
climate change by incorporating nutritional ecology as well as the effects of top-down
274
and bottom-up processes. The authors argue that studies on a subset of climate change
275
drivers with subsets of food webs will not produce accurate predictions of climate change
276
effects.
Ac ce p
te
264
13
Page 13 of 24
277 [4] Clissold FJ, Simpson SJ: Temperature, food quality and life history traits of herbivorous insects. Current Opinion in Insect Science 2015, 11:63-70. *This review focuses on the integrative role temperature has in macronutrient regulation
281
by insect herbivores. Amounts of macronutrients digested depends on many factors,
282
notable plant cell structure, microclimate selection, gut physiology.
cr
283
ip t
278 279 280
[8] Simpson SJ, Clissold FJ, Lihoreau M, Ponton F, Wilder SM, Raubenheimer D: Recent advances in the integrative nutrition of arthropods. Annual Review of Entomology 2015, 60:293-311. *This review addresses the latest approaches to understanding multidimensional nutrient
288
regulation using the geometric framework. The authors cover nutrient relationships for
289
plant-herbivore, host-microbe, inter-individual, and food web interactions.
291 292 293 294 295
43. Deans CA, Behmer ST, Fiene J, Sword GA: Spatio-Temporal, Genotypic, and Environmental Effects on Plant Soluble Protein and Digestible Carbohydrate Content: Implications for Insect Herbivores with Cotton as an Exemplar. Journal of chemical ecology 2016, 42:1151-1163. *Quantification of the plant nutrient landscape available within one host plant, cultivated
296
cotton. Even an agricultural monoculture can provide a broad range of macronutrient
297
contents that varies with tissue type, age, environment, and to a lesser extent genotype.
te
Ac ce p
298
d
290
M
an
us
284 285 286 287
299 300 301
50. Lenhart PA, Eubanks MD, Behmer ST: Water stress in grasslands: dynamic responses of plants and insect herbivores. Oikos 2015, 124:381-390. *Quantification of the plant nutrient landscape within a herbaceous plant community fed
302
on by a diverse community of generalist grasshoppers. A seasonal drought manipulation
303
in this natural community revealed significant seasonal variation in both grasses and
304
forbs macronutrient content, and a water stress-related shift in forbs protein. These shifts
305
are compared to changes in grasshopper functional groups counts in open plots.
14
Page 14 of 24
306 [60] Couture J, Mason C, Habeck C, Lindroth R: Behavioral and morphological responses of an insect herbivore to low nutrient quality are inhibited by plant chemical defenses. Arthropod-Plant Interactions 2016, 10:341-349. *Variation in nutritional quality (along one dimension: N) induces compensatory feeding
311
in the generalist caterpillar Lymantria dispar but also interacts with plant defense.
312
Presence of salicinoids in diet had negative effects on larval performance but these were
313
most pronounced on nutritionally suboptimal foods.
us
cr
ip t
307 308 309 310
314
64. Wetzel WC, Kharouba HM, Robinson M, Holyoak M, Karban R: Variability in plant nutrients reduces insect herbivore performance. Nature 2016, 539:425427. *An analysis of 457 performance datasets from 53 insect herbivore species showing that
319
variance in plant nutritive traits around a mean reduce herbivore performance while
320
relationships with plant defense are linear. The authors conclude that this relationship
321
could play a role in suppression of herbivore populations in natural and agro-ecosystems.
324 325 326 327 328 329 330 331 332 333 334 335 336 337
M
d
te
323
Ac ce p
322
an
315 316 317 318
REFERENCES
1. Scherber C: Insect responses to interacting global change drivers in managed ecosystems. Current Opinion in Insect Science 2015, 11:56-62. 2. Waters CN, Zalasiewicz J, Summerhayes C, Barnosky AD, Poirier C, Gałuszka A, Cearreta A, Edgeworth M, Ellis EC, Ellis M: The Anthropocene is functionally and stratigraphically distinct from the Holocene. Science 2016, 351:aad2622. 3. Rosenblatt AE, Schmitz OJ: Climate Change, Nutrition, and Bottom-Up and TopDown Food Web Processes. Trends in Ecology & Evolution 2016, 31:965-975. 4. Clissold FJ, Simpson SJ: Temperature, food quality and life history traits of herbivorous insects. Current Opinion in Insect Science 2015, 11:63-70. 5. Rosenblatt AE, Schmitz OJ: Interactive effects of multiple climate change variables on trophic interactions: a meta-analysis. Climate Change Responses 2014, 1:8. 6. Houston AI, Higginson AD, McNamara JM: Optimal foraging for multiple nutrients in an unpredictable environment. Ecology letters 2011, 14:1101-1107.
15
Page 15 of 24
te
d
M
an
us
cr
ip t
7. Behmer ST: Insect herbivore nutrient regulation. Annual Review of Entomology 2009, 54:165-187. 8. Simpson SJ, Clissold FJ, Lihoreau M, Ponton F, Wilder SM, Raubenheimer D: Recent advances in the integrative nutrition of arthropods. Annual Review of Entomology 2015, 60:293-311. 9. Simpson SJ, Raubenheimer D: The nature of nutrition: a unifying framework from animal adaptation to human obesity: Princeton University Press; 2012. 10. Le Gall M, Behmer ST: Effects of protein and carbohydrate on an insect herbivore: the vista from a fitness landscape. Integrative and comparative biology 2014, 54:942-954. 11. Awmack CS, Leather SR: Host plant quality and fecundity in herbivorous insects. Annual review of entomology 2002, 47:817-844. 12. Chapman RF: The Insects: Structure and Function edn 5th edition. Cambridge, UK: Cambridge University Press; 2013. 13. Lamichhane JR, Barzman M, Booij K, Boonekamp P, Desneux N, Huber L, Kudsk P, Langrell SR, Ratnadass A, Ricci P: Robust cropping systems to tackle pests under climate change. A review. Agronomy for Sustainable Development 2015, 35:443-459. 14. Metcalfe DB, Asner GP, Martin RE, Silva Espejo JE, Huasco WH, Farfán Amézquita FF, Carranza Jimenez L, Galiano Cabrera DF, Baca LD, Sinca F: Herbivory makes major contributions to ecosystem carbon and nutrient cycling in tropical forests. Ecology Letters 2014, 17:324-332. 15. Dwyer JM, Hobbs RJ, Wainwright CE, Mayfield MM: Climate moderates release from nutrient limitation in natural annual plant communities. Global Ecology and Biogeography 2015, 24:549-561. 16. Barnett KL, Facey SL: Grasslands, invertebrates, and precipitation: a review of the effects of climate change. Frontiers in Plant Science 2016, 7. 17. Mundim FM, Bruna EM, Zuk M: Is there a temperate bias in our understanding of how climate change will alter plant-herbivore interactions? A metaanalysis of experimental studies. The American Naturalist 2016, 188:S74-S89. 18. Myers SS, Zanobetti A, Kloog I, Huybers P, Leakey AD, Bloom AJ, Carlisle E, Dietterich LH, Fitzgerald G, Hasegawa T: Increasing CO2 threatens human nutrition. Nature 2014, 510:139-142. 19. Stiling P, Cornelissen T: How does elevated carbon dioxide (CO2) affect plant– herbivore interactions? A field experiment and meta-analysis of CO2mediated changes on plant chemistry and herbivore performance. Global Change Biology 2007, 13:1823-1842. 20. Robinson EA, Ryan GD, Newman JA: A meta analytical review of the effects of elevated CO2 on plant–arthropod interactions highlights the importance of interacting environmental and biological variables. New Phytologist 2012, 194:321-336. 21. Ainsworth EA, Long SP: What have we learned from 15 years of free air CO2 enrichment (FACE)? A meta analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2. New Phytologist 2005, 165:351-372.
Ac ce p
338 339 340 341 342 343 344 345 346 347 348 349 350 351 352 353 354 355 356 357 358 359 360 361 362 363 364 365 366 367 368 369 370 371 372 373 374 375 376 377 378 379 380 381 382
16
Page 16 of 24
te
d
M
an
us
cr
ip t
22. Dai A: Increasing drought under global warming in observations and models. Nature Climate Change 2013, 3:52-58. 23. Sconiers WB, Eubanks MD: Not all droughts are created equal? The effects of stress severity on insect herbivore abundance. Arthropod-Plant Interactions 2017, 11:45-60. 24. Huberty AF, Denno RF: Plant water stress and its consequences for herbivorous insects: a new synthesis. Ecology 2004, 85:1383-1398. 25. Yamori W, Hikosaka K, Way DA: Temperature response of photosynthesis in C3, C4, and CAM plants: temperature acclimation and temperature adaptation. Photosynthesis research 2014, 119:101-117. 26. Lenhart PA, Eubanks MD, Behmer ST: Water stress in grasslands: dynamic responses of plants and insect herbivores. Oikos 2015, 124:381-390. 27. Sardans J, Grau O, Chen HY, Janssens IA, Ciais P, Piao S, Peñuelas J: Changes in nutrient concentrations of leaves and roots in response to Global Change factors. Global Change Biology 2017. 28. Gherlenda AN, Esveld JL, Hall AA, Duursma RA, Riegler M: Boom and bust: rapid feedback responses between insect outbreak dynamics and canopy leaf area impacted by rainfall and CO2. Global change biology 2016, 22:36323641. 29. Gherlenda AN, Crous KY, Moore BD, Haigh AM, Johnson SN, Riegler M: Precipitation, not CO2 enrichment, drives insect herbivore frass deposition and subsequent nutrient dynamics in a mature Eucalyptus woodland. Plant and soil 2016, 399:29-39. 30. Birkemoe T, Bergmann S, Hasle TE, Klanderud K: Experimental warming increases herbivory by leaf chewing insects in an alpine plant community. Ecology and Evolution 2016, 6:6955-6962. 31. Rothman JM, Chapman CA, Struhsaker TT, Raubenheimer D, Twinomugisha D, Waterman PG: Long term declines in nutritional quality of tropical leaves. Ecology 2015, 96:873-878. 32. DeGabriel JL, Moore BD, Felton AM, Ganzhorn JU, Stolter C, Wallis IR, Johnson CN, Foley WJ: Translating nutritional ecology from the laboratory to the field: milestones in linking plant chemistry to population regulation in mammalian browsers. Oikos 2014, 123:298-308. 33. Clissold FJ, Kertesz H, Saul AM, Sheehan JL, Simpson SJ: Regulation of water and macronutrients by the Australian plague locust, Chortoicetes terminifera. Journal of insect physiology 2014, 69:35-40. 34. Trumper S, Simpson S: Regulation of salt intake by nymphs of Locusta migratoria. Journal of Insect Physiology 1993, 39:857-864. 35. Simpson SJ, Sword GA, Lorch PD, Couzin ID: Cannibal crickets on a forced march for protein and salt. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:4152-4156. 36. Schoonhoven LM, Van Loon JJA, Dicke M: Insect-plant biology: Oxford University Press, USA; 2005. 37. Ghimire B, Riley WJ, Koven CD, Kattge J, Rogers A, Reich PB, Wright IJ: A global trait based approach to estimate leaf nitrogen functional allocation from observations. Ecological Applications 2017.
Ac ce p
383 384 385 386 387 388 389 390 391 392 393 394 395 396 397 398 399 400 401 402 403 404 405 406 407 408 409 410 411 412 413 414 415 416 417 418 419 420 421 422 423 424 425 426 427 428
17
Page 17 of 24
te
d
M
an
us
cr
ip t
38. Mariotti F, Tomé D, Mirand PP: Converting nitrogen into protein—beyond 6.25 and Jones' factors. Critical reviews in food science and nutrition 2008, 48:177184. 39. Boisen S, Bech-Andersen S, Eggum BrO: A critical view on the conversion factor 6.25 from total nitrogen to protein. Acta Agriculturae Scandinavica 1987, 37:299-304. 40. Mosse J: Nitrogen to protein conversion factor for ten cereals and six legumes or oilseeds. A reappraisal of its definition and determination. Variation according to species and to seed protein content. J. Agric. Food Chem 1990, 38:18-24. 41. Bhardwaj U, Bhardwaj A, Kumar R, Leelavathi S, Reddy VS, Mazumdar Leighton S: Revisiting Rubisco as a protein substrate for insect midgut proteases. Archives of insect biochemistry and physiology 2014, 85:13-35. 42. Mattson WJ: Herbivory in relation to plant nitrogen-content. Annual Review of Ecology and Systematics 1980, 11:119-161. 43. Zhu-Salzman K, Zeng R: Insect response to plant defensive protease inhibitors. Annual review of entomology 2015, 60:233-252. 44. Deans CA, Behmer ST, Fiene J, Sword GA: Spatio-Temporal, Genotypic, and Environmental Effects on Plant Soluble Protein and Digestible Carbohydrate Content: Implications for Insect Herbivores with Cotton as an Exemplar. Journal of chemical ecology 2016, 42:1151-1163. 45. Martínez Vilalta J, Sala A, Asensio D, Galiano L, Hoch G, Palacio S, Piper FI, Lloret F: Dynamics of non structural carbohydrates in terrestrial plants: a global synthesis. Ecological Monographs 2016, 86:495-516. 46. Barbehenn R, Karowe D, Chen Z: Performance of a generalist grasshopper on a C3 and a C4 grass: compensation for the effects of elevated CO2 on plant nutritional quality. Oecologia 2004, 140:96-103. 47. Cohen AC: Insect diets: science and technology: CRC press; 2015. 48. Hendry GA: Evolutionary origins and natural functions of fructans–a climatological, biogeographic and mechanistic appraisal. New phytologist 1993, 123:3-14. 49. Calderón-Cortés N, Quesada M, Watanabe H, Cano-Camacho H, Oyama K: Endogenous plant cell wall digestion: a key mechanism in insect evolution. Annual Review of Ecology, Evolution, and Systematics 2012, 43:45-71. 50. Watanabe H, Tokuda G: Cellulolytic systems in insects. Annual review of entomology 2010, 55:609-632. 51. Joern A, Provin T, Behmer ST: Not just the usual suspects: insect herbivore populations and communities are associated with multiple plant nutrients. Ecology 2012, 93:1002-1015. 52. Do Bae S, Kim HJ, Mainali BP: Changes in nutritional composition of soybean seed caused by feeding of pentatomid (Hemiptera: Pentatomidae) and alydid bugs (Hemiptera: Alydidae). Journal of economic entomology 2014, 107:10551060. 53. Stournaras KE, Prum RO, Schaefer HM: Fruit advertisement strategies in two Neotropical plant–seed disperser markets. Evolutionary Ecology 2015, 29:489509.
Ac ce p
429 430 431 432 433 434 435 436 437 438 439 440 441 442 443 444 445 446 447 448 449 450 451 452 453 454 455 456 457 458 459 460 461 462 463 464 465 466 467 468 469 470 471 472 473 474
18
Page 18 of 24
te
d
M
an
us
cr
ip t
54. Vaudo AD, Patch HM, Mortensen DA, Tooker JF, Grozinger CM: Macronutrient ratios in pollen shape bumble bee (Bombus impatiens) foraging strategies and floral preferences. Proceedings of the National Academy of Sciences 2016, 113:E4035-E4042. 55. Giron D, Huguet E, Stone GN, Body M: Insect-induced effects on plants and possible effectors used by galling and leaf-mining insects to manipulate their host-plant. Journal of insect physiology 2016, 84:70-89. 56. Stockhoff BA: Ontogenic Change in Dietary Selection for Protein and Lipid by Gypsy-Moth Larvae. Journal of Insect Physiology 1993, 39:677-686. 57. Schiff N, Waldbauer G, Friedman S: Dietary self selection for vitamins and lipid by larvae of the corn earworm, Heliothis zea. Entomologia experimentalis et applicata 1988, 46:249-256. 58. Clissold FJ, Sanson GD, Read J, Simpson SJ: Gross vs. net income: how plant toughness affects performance of an insect herbivore. Ecology 2009, 90:33933405. 59. Moore BD, Andrew RL, Külheim C, Foley WJ: Explaining intraspecific diversity in plant secondary metabolites in an ecological context. New Phytologist 2014, 201:733-750. 60. Couture J, Mason C, Habeck C, Lindroth R: Behavioral and morphological responses of an insect herbivore to low nutrient quality are inhibited by plant chemical defenses. Arthropod-Plant Interactions 2016, 10:341-349. 61. Behmer ST, Simpson SJ, Raubenheimer D: Herbivore foraging in chemically heterogeneous environments: Nutrients and secondary metabolites. Ecology 2002, 83:2489-2501. 62. Deans C, Sword G, Behmer S: Nutrition as a neglected factor in insect herbivore susceptibility to Bt toxins. Current Opinion in Insect Science 2016, 15:97-103. 63. Deans CA, Behmer ST, Tessnow AE, Tamez-Guerra P, Pusztai-Carey M, Sword GA: Nutrition affects insect susceptibility to Bt toxins. Scientific Reports 2017, 7. 64. Chen F, Wu G, Ge F, Parajulee MN, Shrestha RB: Effects of elevated CO2 and transgenic Bt cotton on plant chemistry, performance, and feeding of an insect herbivore, the cotton bollworm. Entomologia Experimentalis et Applicata 2005, 115:341-350. 65. Gherlenda AN, Haigh AM, Moore BD, Johnson SN, Riegler M: Responses of leaf beetle larvae to elevated [CO2] and temperature depend on Eucalyptus species. Oecologia 2015, 177:607. 66. Lee KP, Raubenheimer D, Simpson SJ: The effects of nutritional imbalance on compensatory feeding for cellulose mediated dietary dilution in a generalist caterpillar. Physiological Entomology 2004, 29:108-117. 67. Ryalls JM, Moore BD, Riegler M, Bromfield LM, Hall AA, Johnson SN: Climate and atmospheric change impacts on sap feeding herbivores: a mechanistic explanation based on functional groups of primary metabolites. Functional Ecology 2017, 31:161-171. 68. Clissold FJ, Coggan N, Simpson SJ: Insect herbivores can choose microclimates to achieve nutritional homeostasis. The Journal of experimental biology 2013, 216:2089-2096.
Ac ce p
475 476 477 478 479 480 481 482 483 484 485 486 487 488 489 490 491 492 493 494 495 496 497 498 499 500 501 502 503 504 505 506 507 508 509 510 511 512 513 514 515 516 517 518 519
19
Page 19 of 24
te
d
M
an
us
cr
ip t
69. Wetzel WC, Kharouba HM, Robinson M, Holyoak M, Karban R: Variability in plant nutrients reduces insect herbivore performance. Nature 2016, 539:425427. 70. Lefcheck JS, Whalen MA, Davenport TM, Stone JP, Duffy JE: Physiological effects of diet mixing on consumer fitness: a meta analysis. Ecology 2013, 94:565572. 71. Senior AM, Nakagawa S, Lihoreau M, Simpson SJ, Raubenheimer D: An overlooked consequence of dietary mixing: a varied diet reduces interindividual variance in fitness. The American Naturalist 2015, 186:649-659. 72. Craine JM, Elmore AJ, Olson K, Tolleson D: Climate change and cattle nutritional stress. Global Change Biology 2010, 16:2901-2911. 73. Lemoine NP, Shantz AA: Increased temperature causes protein limitation by reducing the efficiency of nitrogen digestion in the ectothermic herbivore Spodoptera exigua. Physiological Entomology 2016, 41:143-151. 74. Schmitz OJ, Rosenblatt AE, Smylie M: Temperature dependence of predation stress and the nutritional ecology of a generalist herbivore. Ecology 2016, 97:3119-3130. 75. Barton BT, Beckerman AP, Schmitz OJ: Climate warming strengthens indirect interactions in an old field food web. Ecology 2009, 90:2346-2351.
Ac ce p
520 521 522 523 524 525 526 527 528 529 530 531 532 533 534 535 536 537 538 539 540
20
Page 20 of 24
540 Figure 1. (a) The nutrient landscapes of cultivated cotton and native grassland plants.
542
Digestible protein (Prot) and carbohydrates (Carb) were quantified from bulk samples of
543
grass and forbs in a diverse community of mixed grassland plants in Texas, USA [26].
544
Grasses in this habitat mainly used the C4 photosynthetic pathway while forbs use the C3
545
pathway. Individual cultivated cotton plants (Gossypium spp.) from Texas provide an
546
even greater nutrient space based on plant tissue type [44]. Seeds were included as part of
547
the boll (cotton fruit) Prot:Carb, but separately their Prot:Carb can be over 60:20 (not shown).
548
(b) An acridid grasshopper (Melanoplus differentialis), one of 56 species in the grassland
549
[26], here selectively feeding on an aster flower. (c) A lycaenid caterpillar (Strymon
550
melinus) boring into a cotton boll.
M
d
551
an
us
cr
ip t
541
Figure 2. Various possible shifts in nutrient landscapes as a result of changing
553
environmental conditions. (a) Nutrient concentrations can change, affecting overall
554
calorie content. For example, here plant tissue (green ellipse) could become nutrient
555
dilute (orange ellipse) in both nutrient X and Y while maintaining the same X:Y ratio
556
(dashed line). (b) Absolute amounts of one nutrient can shift. In this case amounts of X
557
have decreased while Y remains constant. This shift has caused the plant tissue to have a
558
more Y-biased X:Y ratio (orange dashed line). (c) The breadth or variation in nutrient
559
space can change. Here a broad nutrient space (green ellipse) has contracted drastically
560
(orange ellipse), although the mean amounts of X and Y are only slightly reduced.
Ac ce p
te
552
561 562
21
Page 21 of 24
563 564
Highlights •
Insect herbivores selectively feed to balance intake of plant macronutrients.
566
•
Overlapping global change variables shift plant nutrient content idiosyncratically.
567
•
Shifts in the nutrient landscape may clarify climate change impacts on herbivores.
cr
ip t
565
us
568
Ac ce p
te
d
M
an
569 570
22
Page 22 of 24
i cr
(b)
(c)
Ac
ce
pt
ed
M
an
us
(a)
Page 23 of 24
ip t cr
Ac ce p
te
d
M
an
us
(b)
(c)
Page 24 of 24
S2214-5745(16)30131-6 http://dx.doi.org/doi:10.1016/j.cois.2017.07.007 COIS 368
To appear in: Received date: Revised date: Accepted date:
17-4-2017 30-6-2017 19-7-2017
Please cite this article as: Paul A. Lenhart Using Plant nutrient landscapes to assess Anthropocene effects on insect herbivores (2017), http://dx.doi.org/10.1016/j.cois.2017.07.007 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
1
USING PLANT NUTRIENT LANDSCAPES TO ASSESS ANTHROPOCENE
2
EFFECTS ON INSECT HERBIVORES
PAUL A. LENHART*1,
4
1
S-225 Agricultural Science Center N, Department of Entomology, University of
us
6
cr
5
7
Kentucky, Lexington, Kentucky.
*To whom correspondence should be addressed. email: [email protected]
M
10
an
8 9
te Ac ce p
13
d
11 12
ip t
3
1
Page 1 of 24
13 Abstract- Global climate change will dramatically affect insect herbivores in a large part
15
through changes in plant quality. Linking how multiple climate factors affect plant
16
macronutrient content may be the most accurate way to understand the response of insect
17
herbivores. Studies should embrace the complexity of interacting climate factors in
18
natural systems and characterize shifts in multidimensional plant nutrient landscapes.
19
This nutrient landscape simplifies interpretation of climate effects although selection of
20
appropriate currencies, scale, and interactions with allelochemicals present challenges.
21
By assessing climate change through the filter of nutrient landscapes we could gain an
22
understanding of how complex interacting climate change drivers affect the ‘buffet’
23
available to different insect herbivores.
Ac ce p
te
d
24
M
an
us
cr
ip t
14
2
Page 2 of 24
24 25
INTRODUCTION Global climate change will dramatically affect the distribution and abundance of
27
insect herbivores in natural and managed systems, but our understanding of these effects
28
is hindered by the complex nature of plant and insect responses. Changing climate has
29
direct effects on insect herbivore physiology but arguably more important are indirect
30
effects via changes in host plant quality. Global climate change in the newest geologic
31
epoch, the Anthropocene [1,2], is characterized by rising CO2, warming temperatures,
32
and altered precipitation, all of which can dramatically affect plant nutrient content [3].
33
Investigating these factors individually can be mechanistically useful [4], but to inform
34
practical predictions, relevant combinations of factors need to be considered as they
35
interact idiosyncratically [3,5].
d
M
an
us
cr
ip t
26
Investigators often do not adequately characterize changes in plant quality. Plant
37
nutrient quality is often incorrectly considered along a single axis [6] despite decades of
38
research showing that insect herbivores feed to simultaneously satisfy requirements for
39
many nutrients (for an in depth background see [7-9]). Nutritional imbalances reduce
40
herbivore performance [10]. To prevent imbalances, insect herbivores taste and regulate
41
intake of plant macronutrients, mainly soluble protein (Prot) and digestible carbohydrates
42
(Carb), in order to meet a specific ratio, termed the intake target, rather than an absolute
43
quantity of either nutrient alone [9]. A third macronutrient class, lipids, often makes up a
44
small fraction of plant nutrient content but may be critical for certain herbivores [11].
45
Required micronutrients (fatty acids, sterols, vitamins, lipogenic compounds, and various
46
inorganic compounds) are generally needed in such small amounts that normal feeding
Ac ce p
te
36
3
Page 3 of 24
47
satisfies demand without the need for active regulation by the insect [12]. Climate change
48
studies need to incorporate this multidimensional aspect of plant nutrient quality. Linking how multiple climate factors affect plant macronutrient content may be
50
the most accurate way to understand the response of insect herbivores to global climate
51
change. However, investigators rarely measure plant nutrient content in a manner
52
relevant to insect herbivores, i.e. as regulated, digestible nutrients in a multidimensional
53
context. The distribution of consumer-relevant nutrient concentrations across different
54
foods, in this case plant tissue, can be termed the ‘nutrient landscape’. The nutrient
55
landscape is the ‘buffet’ of food options a foraging animal can choose from. Studies
56
should embrace the complexity of interacting climate change drivers in natural systems
57
and incorporate a modern understanding of nutritional ecology to characterize shifts in
58
plant nutrient landscapes. Understanding how climate change affects herbivores via
59
nutrient landscapes could allow better predictions of pest population dynamics in agro-
60
ecosystems [13] and feedbacks to nutrient cycling [14].
62 63
cr
us
an
M
d
te
Ac ce p
61
ip t
49
ANTHROPOCENE EFFECTS ON PLANT MACRONUTRIENT CONTENT The effects of the Anthropocene on plants are complex. Numerous climate change
64
drivers co-occur and vary both temporally and spatially. Herbivores face significant
65
changes in host plant abundance and morphology [15] and superimposed on these
66
changes are shifts in macronutrient content within each plant. The most common
67
approach for predicting consequences of climate change has been to study the effects of
68
climate change drivers individually on trophic interactions [5]. While this approach has
69
provided many insights, we should move forward from this foundation by performing
4
Page 4 of 24
large-scale field surveys and experiments to understand how multiple climate change
71
drivers simultaneously shift plant macronutrient content. Changes in plant quality can be
72
quantified as a multidimensional nutrient landscape for comparison with changes in
73
herbivore performance and population dynamics.
74
ip t
70
Experiments manipulating CO2, temperature, and water individually have found a number of strong effects on plant macronutrient content that can be reasonably
76
generalized (reviewed by [3,16,17]). Rising CO2 tends to increase Carb and decrease Prot
77
[17-21]. Rising temperature increases plant photosynthetic rates which may increase Prot
78
but decrease Carb [17]. Rising drought risk is also associated with the Anthropocene [22]
79
and the effects are variable [23,24]. The best-characterized response is that intermediate
80
levels of water stress increase soluble nutrients benefiting fluid-feeding insects [23,24].
81
These mechanistic responses become more difficult to generalize once we take into
82
account differences across plant functional groups [25-27]. Even more importantly
83
multiple climate change drivers can interact in additive, antagonistic, or synergistic ways
84
that are difficult to predict [3,5].
us
an
M
d
te
Ac ce p
85
cr
75
Herbivores do not just respond to abiotic-induced changes in plants, they can, in
86
turn, alter plant macronutrient content, defenses, architecture, biomass, and community
87
structure via their feeding activity. A critical herbivore-mediated ecosystem process is
88
deposition of frass that substantially affects nutrient cycling [28-30]. These herbivore
89
feedbacks to primary production and nutrient cycling likely play a role in Anthropocene-
90
related changes in terrestrial ecosystems.
91
Experimenting on climate drivers individually, without a real world context,
92
provides a fundamental understanding of the physiological responses of plants but is
5
Page 5 of 24
unlikely to accurately translate to predictions in the field. To this end, investigators
94
should quantify changes that occur in natural or semi-natural systems, then work
95
backwards to understand the most relevant mechanisms at play. By using natural
96
experiments [26,29] and correlative surveys [31], complex global change drivers can be
97
reduced to their relevant effects on plant nutrient landscapes.
NUTRIENT LANDSCAPES
us
99
cr
98
ip t
93
To quantify a nutrient landscape, it is first necessary to determine the appropriate
101
currencies, i.e. the primary nutrients an herbivore uses to make foraging decisions. While
102
deficiencies in any essential nutrient can reduce insect performance, only actively
103
regulated nutrients determine feeding behavior [7]. Adequate knowledge of regulated and
104
limiting nutrients for the focal herbivore must be determined so that relevant nutrients
105
can be assessed in the field [32]. Among most insect herbivores, especially folivores, this
106
will largely be Prot and Carb [7], however certain insect may also regulate lipids, sterol,
107
water intake, and salt [7,33-35]. Literature on plant traits is full of quantifications of plant
108
nutrients, largely elemental content, but translating these values to relevant
109
concentrations for herbivores can be challenging.
M
d
te
Ac ce p
110
an
100
Protein has received the most attention as a plant macronutrient, yet most data
111
continues to focus on N content which does not necessarily equate to Prot. Nitrogen can
112
range from 5-30% of plant dry weight [36] and can be allocated very differently between
113
plant functional groups [37]. Consequently, the generalized conversion factor used to
114
translate N to crude protein is inaccurate [38-40]. The largest pool of Prot in plants is
115
RuBisCO, which is critical for photosynthesis [41]. Using a global plant dataset, Ghimire
6
Page 6 of 24
et al. [37] estimate that the % of total leaf N allocated for photosynthesis, including
117
RuBisCo, is as low as 25% in tropical broadleaf evergreen trees but as much as 57% in
118
cultivated crops. Cultivated crops have the lowest residual pool of N (not allocated to
119
photosynthesis or respiratory functions) and are the only plant functional group to
120
increase allocation to RuBisCO with increasing leaf N [37]. Importantly, residual N
121
includes N-based defenses such as alkaloids and protease inhibitors [42,43]. Despite a
122
general correlation, caution should be taken when using N or crude protein as a surrogate
123
for Prot.
cr
us
Carbohydrates, in contrast with N, have often been ignored by plant insect studies
an
124
ip t
116
[44], despite having a demonstrated role in foraging decisions [7], and being highly
126
variable across plants [45]. Carb for insect herbivores include starches, simple sugars, and
127
fructans [46,47]. Starches are used primarily for carbon storage in plant reserve organs,
128
while soluble sugars serve a variety of intermediate functions in leaves [45]. Fructans
129
serve as carbon storage in 15% of angiosperms [48]. Digestion of structural
130
carbohydrates such as cellulose, hemicellulose, pectin, and lignin by insects requires the
131
use of microbial symbionts and may be an important way chewing herbivores degrade
132
cell walls to access digestible cell contents [49,50]. No elemental surrogate can estimate
133
Carb [51]. Although often invoked, C is present in all organic compounds and significant
134
correlations with insect performance could be due to any number of compounds. A recent
135
global comparison of plants highlights how Carb can differ across plant tissues, functional
136
types, biomes, and seasons [45]. Herbaceous plants and conifers have the highest leaf
137
concentrations, averaging between 14-20% of dry mass with some species containing
138
over 30% [45]. Strong seasonal fluctuations in starches and simple sugars reflect different
Ac ce p
te
d
M
125
7
Page 7 of 24
139
functions [45]. More studies of plant quality should explicitly measure Carb as it probably
140
has an important effect on insect herbivores, especially as a component of the Prot:Carb
141
ratio. Lipid regulation by herbivores is often ignored because of its scarcity in plants but
ip t
142
may be important for insect feeding guilds that target plant tissues with high lipid
144
content. Pollen, fruit, and seeds are often naturally high in lipids [52-54] and lipid
145
concentrations are often increased in the nutritive tissues that form within galls [55].
146
Caterpillars have demonstrated the ability to regulate for lipids in artificial diets [56,57].
147
Given that pollinators such as bumblebees will actively adjust their foraging to collect a
148
specific protein:lipid ratio in pollen [54] it is likely that florivores, frugivores, and seed
149
predators conduct similar regulation.
us
an
M
The scale at which an herbivore makes feeding decisions must be taken into
d
150
cr
143
account as well. Figure 1a is an example of Prot and Carb nutrient landscapes quantified in
152
plant tissue that a corresponding herbivore (Figure 1b-c) would feed from. The grassland
153
plants from central Texas, serve as host plants for a diverse community of grasshoppers
154
[26]. These mobile generalist herbivores move between plants frequently as they feed. In
155
contrast, many insects, such as the caterpillar in Figure 2b complete their development on
156
a single host plant. Tissues can vary widely in their Prot:Carb content within a single plant
157
providing a broad nutrient landscape as demonstrated by Deans et al. [44] in cultivated
158
cotton plants, Gossypium spp. (Figure 1a). Detailed observations of the tissues that are
159
actually consumed by insects will prevent uneaten tissues from biasing the quantification.
160
For example, Deans et al. [44] found that entire cotton bolls (fruit) had a Prot:Carb ratio of
161
1:3, however developing seeds within bolls could be over 3:1. Measuring Prot and Carb in
Ac ce p
te
151
8
Page 8 of 24
162
the specific plant tissues consumed by an herbivore increases the accuracy of nutrient
163
landscape quantification. It is tempting to superimpose an herbivores’ intake target onto the nutrient
165
landscape to evaluate what choices the herbivore will make, however this is not so
166
simple. By comparing what herbivores consume and excrete, it is evident that not all
167
digestible nutrients are accessible or digested. A portion of digestible nutrient content
168
may be trapped behind indigestible cell walls [58]. Herbivores can also adjust what is
169
digested through a range of behavioral, physiological, and morphological responses
170
(reviewed by [8]). Herbivores can use these post-ingestive responses to correct for
171
shortfalls in the balance of nutrients ingested. A thorough understanding of post-ingestive
172
regulation would be required to link a nutrient landscape directly to the requirements of
173
an herbivore. At the ecological scale necessary to understand the effects of global climate
174
change via plant quality, we should first look for relationships between shifts in the
175
nutrient landscape and herbivore performance. While herbivores may use these plastic
176
responses to mitigate the effect of plant quality differences, they still show strong diet
177
selection and the nutrient landscape should therefore strongly correlate with feeding
178
behavior and subsequent performance.
cr
us
an
M
d
te
Ac ce p
179
ip t
164
While the focus in this paper has been on plant nutrient content, plant quality is
180
often dictated by interactions between nutrient content and plant defenses, especially
181
plant secondary metabolites (PSM’s). While theoretically PSM’s could be incorporated
182
as additional axes influencing the plant nutrient landscape, they are highly diverse with
183
varying modes of action and toxicities [59]. Plant chemical defenses may actually
184
increase the importance of accurate nutrient regulation by the herbivore rather than
9
Page 9 of 24
diminish it. Artificial diet experiments have shown that the deleterious effects of
186
defensive chemicals are reduced when diets match the herbivore’s intake target [60,61].
187
Along the same lines, susceptibility to the biopesticide Bt toxin was lowest in
188
Helicoverpa zea caterpillars reared on diets closest to their intake target [62,63].
189
However, plant defenses can make herbivores reluctant to consume foods that would
190
otherwise satisfy their nutrient demands [60]. The interactions of plant defenses and plant
191
macronutrient content will continue to be an exciting frontier for plant-herbivore
192
interactions.
193
LINKING CLIMATE AND HERBIVORES VIA PLANT NUTRIENT SHIFTS
194
While interacting Anthropocene drivers can be complex, their combined
195
outcomes on plant macronutrient content can be characterized and related to herbivore
196
feeding behavior, performance, and abundance. Three different fundamental shifts may
197
occur, either individually or in some combination (Figure 2). These include changes in
198
nutrient concentration, ratio, and variation. In many cases it is likely that climate change
199
will cause simultaneous shifts, especially in ratio and concentration [64,65].
cr
us
an
M
d
te
Ac ce p
200
ip t
185
Nutrient concentrations may change, becoming more nutrient concentrated or
201
dilute (Figure 2a). If the ratio of Prot:Carb remains constant but total macronutrient content
202
(calorie content) increases or decreases, the rate of herbivore consumption could change
203
to meet requirements [10,66]. In the case of nutrient dilution (Figure 2a), compensatory
204
feeding can be costly [7]. Consumers may also employ a range of post-ingestive
205
mechanisms to increase nutrient absorption rather than consumption [8]. In the case of
206
increasing nutrient concentration, herbivore performance and population density may
10
Page 10 of 24
207
increase. For example, elevated CO2 and temperature affected concentrations of multiple
208
limiting amino acids in alfalfa which strongly correlated with aphid fecundity [67]. Macronutrient ratios could shift due to changes along a single macronutrient axis
210
(Figure 2b). To maintain nutrient homeostasis, herbivores may respond in a multitude of
211
ways including switching host plants, feeding on different plant tissue, and employing
212
post-ingestive corrections for nutritional imbalances [9,68]. For example, severe seasonal
213
drought has been shown to induce this sort of shift in a grassland, decreasing forb Prot but
214
not Carb resulting in a more Carb -biased Prot:Carb ratio [26]. Polyphagous grasshoppers
215
responded to the shift along a single nutrient axis and their numbers in open drought plots
216
decreased compared to watered plots [26].
cr
us
an
The breadth or variation of a nutrient landscape may also shift either increasing or
M
217
ip t
209
decreasing the different nutrient ratios the herbivore can choose from (Figure 2c). The
219
response of consumers to variation in food nutrient content, rather than just the mean is a
220
largely ignored aspect of nutritional ecology [69]. Many studies show that insect
221
herbivores can tightly regulate their macronutrient intake by switching among foods with
222
complementary nutrient profiles, i.e. diet mixing [7,8]. While this phenomenon is likely
223
more important for mobile polyphagous species, even specialist species that feed on a
224
single plant for their development could select among tissues to reach their intake target
225
[44]. Because there are costs to over- or under-ingesting macronutrients, herbivores
226
generally benefit from diet mixing [70]. Even when consumers have similar or greater
227
mean fitness on a single optimal food, inter-individual variation in fitness is significantly
228
lower when diet mixing is possible [71].
Ac ce p
te
d
218
11
Page 11 of 24
229
Contrarily, Wetzel et al. [69] proposed that heterogeneity in plant nutrient content may be a way plants suppress herbivore populations and that pest outbreaks in agro-
231
ecosystems could be linked to homogeneity of plant nutrient content. An analysis of 76
232
studies found evidence that variation in nutrient content, either above or below a mean,
233
decreases insect herbivore performance both in terms of growth and survival [69]. The
234
study evaluated performance data from herbivores restricted to different nutrient
235
concentration levels (no-choice tests) and ‘nutrient’ was a broad category treated uni-
236
dimensionally. Considering how insects respond to nutrient regulation challenges, these
237
findings may reflect general performance costs when herbivores are restricted to foods
238
which force under- or over- ingestion of nutrients [69]. These are subject to the ‘rules of
239
compromise’ that herbivores make on imbalanced foods [9]. If plant nutrient variation
240
did reduce insect herbivore performance, we would hypothesize that herbivores given
241
food with an optimal Prot:Carb ratio would out-perform herbivores that could choose
242
between foods with complementary Prot:Carb concentrations. Diet mixing experiments
243
generally do not support this idea [70]. This hypothesis could also be evaluated using a
244
correlative approach in the field comparing variation in the multidimensional plant
245
nutrient landscape with herbivore performance and density.
cr
us
an
M
d
te
Ac ce p
246
ip t
230
247
FUTURE DIRECTIONS
248
Focusing on Anthropocene-related shifts in the plant nutrient landscape has the potential
249
to improve predictions of how insect herbivory responds to complex global climate
250
change drivers. Similar approaches in mammalian herbivore systems have already proved
251
insightful [31,32,72]. Despite decades of work teasing apart how insect herbivores
12
Page 12 of 24
regulate multiple macronutrients simultaneously, studies are still assessing plant nutrient
253
quality in a manner inconsistent with how insect herbivores forage. Specifically I
254
encourage studies of climate change and insect herbivores to 1) quantify plant nutrient
255
content using currencies and scale relevant to herbivores, 2) analyze them in a
256
multidimensional context, and 3) investigate the role of variation in nutrient landscapes.
257
In addition, insect-plant biologist must continue to study the interactions of nutrients and
258
secondary metabolites. A truly integrative approach will need to consider direct effects of
259
global climate change drivers on herbivores [3,4,73,74], and top-down effects of other
260
trophic levels [3,74,75], but a basic understanding of how complex interacting climate
261
change drivers affect the ‘buffet’ available to different insect herbivores may go a long
262
way to predicting their responses to this changing world.
M
an
us
cr
ip t
252
d
263
Acknowledgements- I thank Carrie Deans, Blanka Angyal, Jen White, and the
265
anonymous reviewers for their valuable feedback. This material is based on work
266
supported by a Texas A&M Diversity Fellowship, as well as grants from the
267
Orthopterist’s society, Texas Ecolab, and USDA NIFA AFRI (2012-67011-19930).
268 269
Annotated references:
270 271 272
[3] Rosenblatt AE, Schmitz OJ: Climate Change, Nutrition, and Bottom-Up and TopDown Food Web Processes. Trends in Ecology & Evolution 2016, 31:965-975. **This review presents a framework for understanding the responses of food webs to
273
climate change by incorporating nutritional ecology as well as the effects of top-down
274
and bottom-up processes. The authors argue that studies on a subset of climate change
275
drivers with subsets of food webs will not produce accurate predictions of climate change
276
effects.
Ac ce p
te
264
13
Page 13 of 24
277 [4] Clissold FJ, Simpson SJ: Temperature, food quality and life history traits of herbivorous insects. Current Opinion in Insect Science 2015, 11:63-70. *This review focuses on the integrative role temperature has in macronutrient regulation
281
by insect herbivores. Amounts of macronutrients digested depends on many factors,
282
notable plant cell structure, microclimate selection, gut physiology.
cr
283
ip t
278 279 280
[8] Simpson SJ, Clissold FJ, Lihoreau M, Ponton F, Wilder SM, Raubenheimer D: Recent advances in the integrative nutrition of arthropods. Annual Review of Entomology 2015, 60:293-311. *This review addresses the latest approaches to understanding multidimensional nutrient
288
regulation using the geometric framework. The authors cover nutrient relationships for
289
plant-herbivore, host-microbe, inter-individual, and food web interactions.
291 292 293 294 295
43. Deans CA, Behmer ST, Fiene J, Sword GA: Spatio-Temporal, Genotypic, and Environmental Effects on Plant Soluble Protein and Digestible Carbohydrate Content: Implications for Insect Herbivores with Cotton as an Exemplar. Journal of chemical ecology 2016, 42:1151-1163. *Quantification of the plant nutrient landscape available within one host plant, cultivated
296
cotton. Even an agricultural monoculture can provide a broad range of macronutrient
297
contents that varies with tissue type, age, environment, and to a lesser extent genotype.
te
Ac ce p
298
d
290
M
an
us
284 285 286 287
299 300 301
50. Lenhart PA, Eubanks MD, Behmer ST: Water stress in grasslands: dynamic responses of plants and insect herbivores. Oikos 2015, 124:381-390. *Quantification of the plant nutrient landscape within a herbaceous plant community fed
302
on by a diverse community of generalist grasshoppers. A seasonal drought manipulation
303
in this natural community revealed significant seasonal variation in both grasses and
304
forbs macronutrient content, and a water stress-related shift in forbs protein. These shifts
305
are compared to changes in grasshopper functional groups counts in open plots.
14
Page 14 of 24
306 [60] Couture J, Mason C, Habeck C, Lindroth R: Behavioral and morphological responses of an insect herbivore to low nutrient quality are inhibited by plant chemical defenses. Arthropod-Plant Interactions 2016, 10:341-349. *Variation in nutritional quality (along one dimension: N) induces compensatory feeding
311
in the generalist caterpillar Lymantria dispar but also interacts with plant defense.
312
Presence of salicinoids in diet had negative effects on larval performance but these were
313
most pronounced on nutritionally suboptimal foods.
us
cr
ip t
307 308 309 310
314
64. Wetzel WC, Kharouba HM, Robinson M, Holyoak M, Karban R: Variability in plant nutrients reduces insect herbivore performance. Nature 2016, 539:425427. *An analysis of 457 performance datasets from 53 insect herbivore species showing that
319
variance in plant nutritive traits around a mean reduce herbivore performance while
320
relationships with plant defense are linear. The authors conclude that this relationship
321
could play a role in suppression of herbivore populations in natural and agro-ecosystems.
324 325 326 327 328 329 330 331 332 333 334 335 336 337
M
d
te
323
Ac ce p
322
an
315 316 317 318
REFERENCES
1. Scherber C: Insect responses to interacting global change drivers in managed ecosystems. Current Opinion in Insect Science 2015, 11:56-62. 2. Waters CN, Zalasiewicz J, Summerhayes C, Barnosky AD, Poirier C, Gałuszka A, Cearreta A, Edgeworth M, Ellis EC, Ellis M: The Anthropocene is functionally and stratigraphically distinct from the Holocene. Science 2016, 351:aad2622. 3. Rosenblatt AE, Schmitz OJ: Climate Change, Nutrition, and Bottom-Up and TopDown Food Web Processes. Trends in Ecology & Evolution 2016, 31:965-975. 4. Clissold FJ, Simpson SJ: Temperature, food quality and life history traits of herbivorous insects. Current Opinion in Insect Science 2015, 11:63-70. 5. Rosenblatt AE, Schmitz OJ: Interactive effects of multiple climate change variables on trophic interactions: a meta-analysis. Climate Change Responses 2014, 1:8. 6. Houston AI, Higginson AD, McNamara JM: Optimal foraging for multiple nutrients in an unpredictable environment. Ecology letters 2011, 14:1101-1107.
15
Page 15 of 24
te
d
M
an
us
cr
ip t
7. Behmer ST: Insect herbivore nutrient regulation. Annual Review of Entomology 2009, 54:165-187. 8. Simpson SJ, Clissold FJ, Lihoreau M, Ponton F, Wilder SM, Raubenheimer D: Recent advances in the integrative nutrition of arthropods. Annual Review of Entomology 2015, 60:293-311. 9. Simpson SJ, Raubenheimer D: The nature of nutrition: a unifying framework from animal adaptation to human obesity: Princeton University Press; 2012. 10. Le Gall M, Behmer ST: Effects of protein and carbohydrate on an insect herbivore: the vista from a fitness landscape. Integrative and comparative biology 2014, 54:942-954. 11. Awmack CS, Leather SR: Host plant quality and fecundity in herbivorous insects. Annual review of entomology 2002, 47:817-844. 12. Chapman RF: The Insects: Structure and Function edn 5th edition. Cambridge, UK: Cambridge University Press; 2013. 13. Lamichhane JR, Barzman M, Booij K, Boonekamp P, Desneux N, Huber L, Kudsk P, Langrell SR, Ratnadass A, Ricci P: Robust cropping systems to tackle pests under climate change. A review. Agronomy for Sustainable Development 2015, 35:443-459. 14. Metcalfe DB, Asner GP, Martin RE, Silva Espejo JE, Huasco WH, Farfán Amézquita FF, Carranza Jimenez L, Galiano Cabrera DF, Baca LD, Sinca F: Herbivory makes major contributions to ecosystem carbon and nutrient cycling in tropical forests. Ecology Letters 2014, 17:324-332. 15. Dwyer JM, Hobbs RJ, Wainwright CE, Mayfield MM: Climate moderates release from nutrient limitation in natural annual plant communities. Global Ecology and Biogeography 2015, 24:549-561. 16. Barnett KL, Facey SL: Grasslands, invertebrates, and precipitation: a review of the effects of climate change. Frontiers in Plant Science 2016, 7. 17. Mundim FM, Bruna EM, Zuk M: Is there a temperate bias in our understanding of how climate change will alter plant-herbivore interactions? A metaanalysis of experimental studies. The American Naturalist 2016, 188:S74-S89. 18. Myers SS, Zanobetti A, Kloog I, Huybers P, Leakey AD, Bloom AJ, Carlisle E, Dietterich LH, Fitzgerald G, Hasegawa T: Increasing CO2 threatens human nutrition. Nature 2014, 510:139-142. 19. Stiling P, Cornelissen T: How does elevated carbon dioxide (CO2) affect plant– herbivore interactions? A field experiment and meta-analysis of CO2mediated changes on plant chemistry and herbivore performance. Global Change Biology 2007, 13:1823-1842. 20. Robinson EA, Ryan GD, Newman JA: A meta analytical review of the effects of elevated CO2 on plant–arthropod interactions highlights the importance of interacting environmental and biological variables. New Phytologist 2012, 194:321-336. 21. Ainsworth EA, Long SP: What have we learned from 15 years of free air CO2 enrichment (FACE)? A meta analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2. New Phytologist 2005, 165:351-372.
Ac ce p
338 339 340 341 342 343 344 345 346 347 348 349 350 351 352 353 354 355 356 357 358 359 360 361 362 363 364 365 366 367 368 369 370 371 372 373 374 375 376 377 378 379 380 381 382
16
Page 16 of 24
te
d
M
an
us
cr
ip t
22. Dai A: Increasing drought under global warming in observations and models. Nature Climate Change 2013, 3:52-58. 23. Sconiers WB, Eubanks MD: Not all droughts are created equal? The effects of stress severity on insect herbivore abundance. Arthropod-Plant Interactions 2017, 11:45-60. 24. Huberty AF, Denno RF: Plant water stress and its consequences for herbivorous insects: a new synthesis. Ecology 2004, 85:1383-1398. 25. Yamori W, Hikosaka K, Way DA: Temperature response of photosynthesis in C3, C4, and CAM plants: temperature acclimation and temperature adaptation. Photosynthesis research 2014, 119:101-117. 26. Lenhart PA, Eubanks MD, Behmer ST: Water stress in grasslands: dynamic responses of plants and insect herbivores. Oikos 2015, 124:381-390. 27. Sardans J, Grau O, Chen HY, Janssens IA, Ciais P, Piao S, Peñuelas J: Changes in nutrient concentrations of leaves and roots in response to Global Change factors. Global Change Biology 2017. 28. Gherlenda AN, Esveld JL, Hall AA, Duursma RA, Riegler M: Boom and bust: rapid feedback responses between insect outbreak dynamics and canopy leaf area impacted by rainfall and CO2. Global change biology 2016, 22:36323641. 29. Gherlenda AN, Crous KY, Moore BD, Haigh AM, Johnson SN, Riegler M: Precipitation, not CO2 enrichment, drives insect herbivore frass deposition and subsequent nutrient dynamics in a mature Eucalyptus woodland. Plant and soil 2016, 399:29-39. 30. Birkemoe T, Bergmann S, Hasle TE, Klanderud K: Experimental warming increases herbivory by leaf chewing insects in an alpine plant community. Ecology and Evolution 2016, 6:6955-6962. 31. Rothman JM, Chapman CA, Struhsaker TT, Raubenheimer D, Twinomugisha D, Waterman PG: Long term declines in nutritional quality of tropical leaves. Ecology 2015, 96:873-878. 32. DeGabriel JL, Moore BD, Felton AM, Ganzhorn JU, Stolter C, Wallis IR, Johnson CN, Foley WJ: Translating nutritional ecology from the laboratory to the field: milestones in linking plant chemistry to population regulation in mammalian browsers. Oikos 2014, 123:298-308. 33. Clissold FJ, Kertesz H, Saul AM, Sheehan JL, Simpson SJ: Regulation of water and macronutrients by the Australian plague locust, Chortoicetes terminifera. Journal of insect physiology 2014, 69:35-40. 34. Trumper S, Simpson S: Regulation of salt intake by nymphs of Locusta migratoria. Journal of Insect Physiology 1993, 39:857-864. 35. Simpson SJ, Sword GA, Lorch PD, Couzin ID: Cannibal crickets on a forced march for protein and salt. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:4152-4156. 36. Schoonhoven LM, Van Loon JJA, Dicke M: Insect-plant biology: Oxford University Press, USA; 2005. 37. Ghimire B, Riley WJ, Koven CD, Kattge J, Rogers A, Reich PB, Wright IJ: A global trait based approach to estimate leaf nitrogen functional allocation from observations. Ecological Applications 2017.
Ac ce p
383 384 385 386 387 388 389 390 391 392 393 394 395 396 397 398 399 400 401 402 403 404 405 406 407 408 409 410 411 412 413 414 415 416 417 418 419 420 421 422 423 424 425 426 427 428
17
Page 17 of 24
te
d
M
an
us
cr
ip t
38. Mariotti F, Tomé D, Mirand PP: Converting nitrogen into protein—beyond 6.25 and Jones' factors. Critical reviews in food science and nutrition 2008, 48:177184. 39. Boisen S, Bech-Andersen S, Eggum BrO: A critical view on the conversion factor 6.25 from total nitrogen to protein. Acta Agriculturae Scandinavica 1987, 37:299-304. 40. Mosse J: Nitrogen to protein conversion factor for ten cereals and six legumes or oilseeds. A reappraisal of its definition and determination. Variation according to species and to seed protein content. J. Agric. Food Chem 1990, 38:18-24. 41. Bhardwaj U, Bhardwaj A, Kumar R, Leelavathi S, Reddy VS, Mazumdar Leighton S: Revisiting Rubisco as a protein substrate for insect midgut proteases. Archives of insect biochemistry and physiology 2014, 85:13-35. 42. Mattson WJ: Herbivory in relation to plant nitrogen-content. Annual Review of Ecology and Systematics 1980, 11:119-161. 43. Zhu-Salzman K, Zeng R: Insect response to plant defensive protease inhibitors. Annual review of entomology 2015, 60:233-252. 44. Deans CA, Behmer ST, Fiene J, Sword GA: Spatio-Temporal, Genotypic, and Environmental Effects on Plant Soluble Protein and Digestible Carbohydrate Content: Implications for Insect Herbivores with Cotton as an Exemplar. Journal of chemical ecology 2016, 42:1151-1163. 45. Martínez Vilalta J, Sala A, Asensio D, Galiano L, Hoch G, Palacio S, Piper FI, Lloret F: Dynamics of non structural carbohydrates in terrestrial plants: a global synthesis. Ecological Monographs 2016, 86:495-516. 46. Barbehenn R, Karowe D, Chen Z: Performance of a generalist grasshopper on a C3 and a C4 grass: compensation for the effects of elevated CO2 on plant nutritional quality. Oecologia 2004, 140:96-103. 47. Cohen AC: Insect diets: science and technology: CRC press; 2015. 48. Hendry GA: Evolutionary origins and natural functions of fructans–a climatological, biogeographic and mechanistic appraisal. New phytologist 1993, 123:3-14. 49. Calderón-Cortés N, Quesada M, Watanabe H, Cano-Camacho H, Oyama K: Endogenous plant cell wall digestion: a key mechanism in insect evolution. Annual Review of Ecology, Evolution, and Systematics 2012, 43:45-71. 50. Watanabe H, Tokuda G: Cellulolytic systems in insects. Annual review of entomology 2010, 55:609-632. 51. Joern A, Provin T, Behmer ST: Not just the usual suspects: insect herbivore populations and communities are associated with multiple plant nutrients. Ecology 2012, 93:1002-1015. 52. Do Bae S, Kim HJ, Mainali BP: Changes in nutritional composition of soybean seed caused by feeding of pentatomid (Hemiptera: Pentatomidae) and alydid bugs (Hemiptera: Alydidae). Journal of economic entomology 2014, 107:10551060. 53. Stournaras KE, Prum RO, Schaefer HM: Fruit advertisement strategies in two Neotropical plant–seed disperser markets. Evolutionary Ecology 2015, 29:489509.
Ac ce p
429 430 431 432 433 434 435 436 437 438 439 440 441 442 443 444 445 446 447 448 449 450 451 452 453 454 455 456 457 458 459 460 461 462 463 464 465 466 467 468 469 470 471 472 473 474
18
Page 18 of 24
te
d
M
an
us
cr
ip t
54. Vaudo AD, Patch HM, Mortensen DA, Tooker JF, Grozinger CM: Macronutrient ratios in pollen shape bumble bee (Bombus impatiens) foraging strategies and floral preferences. Proceedings of the National Academy of Sciences 2016, 113:E4035-E4042. 55. Giron D, Huguet E, Stone GN, Body M: Insect-induced effects on plants and possible effectors used by galling and leaf-mining insects to manipulate their host-plant. Journal of insect physiology 2016, 84:70-89. 56. Stockhoff BA: Ontogenic Change in Dietary Selection for Protein and Lipid by Gypsy-Moth Larvae. Journal of Insect Physiology 1993, 39:677-686. 57. Schiff N, Waldbauer G, Friedman S: Dietary self selection for vitamins and lipid by larvae of the corn earworm, Heliothis zea. Entomologia experimentalis et applicata 1988, 46:249-256. 58. Clissold FJ, Sanson GD, Read J, Simpson SJ: Gross vs. net income: how plant toughness affects performance of an insect herbivore. Ecology 2009, 90:33933405. 59. Moore BD, Andrew RL, Külheim C, Foley WJ: Explaining intraspecific diversity in plant secondary metabolites in an ecological context. New Phytologist 2014, 201:733-750. 60. Couture J, Mason C, Habeck C, Lindroth R: Behavioral and morphological responses of an insect herbivore to low nutrient quality are inhibited by plant chemical defenses. Arthropod-Plant Interactions 2016, 10:341-349. 61. Behmer ST, Simpson SJ, Raubenheimer D: Herbivore foraging in chemically heterogeneous environments: Nutrients and secondary metabolites. Ecology 2002, 83:2489-2501. 62. Deans C, Sword G, Behmer S: Nutrition as a neglected factor in insect herbivore susceptibility to Bt toxins. Current Opinion in Insect Science 2016, 15:97-103. 63. Deans CA, Behmer ST, Tessnow AE, Tamez-Guerra P, Pusztai-Carey M, Sword GA: Nutrition affects insect susceptibility to Bt toxins. Scientific Reports 2017, 7. 64. Chen F, Wu G, Ge F, Parajulee MN, Shrestha RB: Effects of elevated CO2 and transgenic Bt cotton on plant chemistry, performance, and feeding of an insect herbivore, the cotton bollworm. Entomologia Experimentalis et Applicata 2005, 115:341-350. 65. Gherlenda AN, Haigh AM, Moore BD, Johnson SN, Riegler M: Responses of leaf beetle larvae to elevated [CO2] and temperature depend on Eucalyptus species. Oecologia 2015, 177:607. 66. Lee KP, Raubenheimer D, Simpson SJ: The effects of nutritional imbalance on compensatory feeding for cellulose mediated dietary dilution in a generalist caterpillar. Physiological Entomology 2004, 29:108-117. 67. Ryalls JM, Moore BD, Riegler M, Bromfield LM, Hall AA, Johnson SN: Climate and atmospheric change impacts on sap feeding herbivores: a mechanistic explanation based on functional groups of primary metabolites. Functional Ecology 2017, 31:161-171. 68. Clissold FJ, Coggan N, Simpson SJ: Insect herbivores can choose microclimates to achieve nutritional homeostasis. The Journal of experimental biology 2013, 216:2089-2096.
Ac ce p
475 476 477 478 479 480 481 482 483 484 485 486 487 488 489 490 491 492 493 494 495 496 497 498 499 500 501 502 503 504 505 506 507 508 509 510 511 512 513 514 515 516 517 518 519
19
Page 19 of 24
te
d
M
an
us
cr
ip t
69. Wetzel WC, Kharouba HM, Robinson M, Holyoak M, Karban R: Variability in plant nutrients reduces insect herbivore performance. Nature 2016, 539:425427. 70. Lefcheck JS, Whalen MA, Davenport TM, Stone JP, Duffy JE: Physiological effects of diet mixing on consumer fitness: a meta analysis. Ecology 2013, 94:565572. 71. Senior AM, Nakagawa S, Lihoreau M, Simpson SJ, Raubenheimer D: An overlooked consequence of dietary mixing: a varied diet reduces interindividual variance in fitness. The American Naturalist 2015, 186:649-659. 72. Craine JM, Elmore AJ, Olson K, Tolleson D: Climate change and cattle nutritional stress. Global Change Biology 2010, 16:2901-2911. 73. Lemoine NP, Shantz AA: Increased temperature causes protein limitation by reducing the efficiency of nitrogen digestion in the ectothermic herbivore Spodoptera exigua. Physiological Entomology 2016, 41:143-151. 74. Schmitz OJ, Rosenblatt AE, Smylie M: Temperature dependence of predation stress and the nutritional ecology of a generalist herbivore. Ecology 2016, 97:3119-3130. 75. Barton BT, Beckerman AP, Schmitz OJ: Climate warming strengthens indirect interactions in an old field food web. Ecology 2009, 90:2346-2351.
Ac ce p
520 521 522 523 524 525 526 527 528 529 530 531 532 533 534 535 536 537 538 539 540
20
Page 20 of 24
540 Figure 1. (a) The nutrient landscapes of cultivated cotton and native grassland plants.
542
Digestible protein (Prot) and carbohydrates (Carb) were quantified from bulk samples of
543
grass and forbs in a diverse community of mixed grassland plants in Texas, USA [26].
544
Grasses in this habitat mainly used the C4 photosynthetic pathway while forbs use the C3
545
pathway. Individual cultivated cotton plants (Gossypium spp.) from Texas provide an
546
even greater nutrient space based on plant tissue type [44]. Seeds were included as part of
547
the boll (cotton fruit) Prot:Carb, but separately their Prot:Carb can be over 60:20 (not shown).
548
(b) An acridid grasshopper (Melanoplus differentialis), one of 56 species in the grassland
549
[26], here selectively feeding on an aster flower. (c) A lycaenid caterpillar (Strymon
550
melinus) boring into a cotton boll.
M
d
551
an
us
cr
ip t
541
Figure 2. Various possible shifts in nutrient landscapes as a result of changing
553
environmental conditions. (a) Nutrient concentrations can change, affecting overall
554
calorie content. For example, here plant tissue (green ellipse) could become nutrient
555
dilute (orange ellipse) in both nutrient X and Y while maintaining the same X:Y ratio
556
(dashed line). (b) Absolute amounts of one nutrient can shift. In this case amounts of X
557
have decreased while Y remains constant. This shift has caused the plant tissue to have a
558
more Y-biased X:Y ratio (orange dashed line). (c) The breadth or variation in nutrient
559
space can change. Here a broad nutrient space (green ellipse) has contracted drastically
560
(orange ellipse), although the mean amounts of X and Y are only slightly reduced.
Ac ce p
te
552
561 562
21
Page 21 of 24
563 564
Highlights •
Insect herbivores selectively feed to balance intake of plant macronutrients.
566
•
Overlapping global change variables shift plant nutrient content idiosyncratically.
567
•
Shifts in the nutrient landscape may clarify climate change impacts on herbivores.
cr
ip t
565
us
568
Ac ce p
te
d
M
an
569 570
22
Page 22 of 24
i cr
(b)
(c)
Ac
ce
pt
ed
M
an
us
(a)
Page 23 of 24
ip t cr
Ac ce p
te
d
M
an
us
(b)
(c)
Page 24 of 24