Abstract
The susceptibility of plants to herbivores can be strongly influenced by the identity, morphology and palatability of neighboring plants. While the defensive traits of neighbors often determine the mechanism and strength of associational resistance and susceptibility, the effect of neighbors on plant defense phenotype remains poorly understood. We used field surveys and a prickle-removal experiment in a semi-arid Kenyan savanna to evaluate the efficacy of physical defenses against large mammalian herbivores in a common understory plant, Solanum campylacanthum. We then quantified the respective effects of spinescent Acacia trees and short-statured grasses on browsing damage and prickle density in S. campylacanthum. We paired measurements of prickle density beneath and outside tree canopies with long-term herbivore-exclusion experiments to evaluate whether associational resistance reduced defense investment by decreasing browsing damage. Likewise, we compared defense phenotype within and outside pre-existing and experimentally created clearings to determine whether grass neighbors increased defense investment via associational susceptibility. Removing prickles increased the frequency of browsing by ~25%, and surveys of herbivory damage on defended leaves suggested that herbivores tended to avoid prickles. As predicted, associational resistance and susceptibility had opposing effects on plant phenotype: individuals growing beneath Acacia canopies (or, analogously, within large-herbivore exclosures) had a significantly lower proportion of their leaves browsed and produced ~ 70–80% fewer prickles than those outside refuges, whereas plants in grass-dominated clearings were more heavily browsed and produced nearly twice as many prickles as plants outside clearings. Our results demonstrate that associational resistance and susceptibility have strong, but opposing, effects on plant defense phenotype, and that variable herbivore damage is a major source of intraspecific variation in defense phenotype in this system.
| Original language | English (US) |
|---|---|
| Pages (from-to) | 1772-1782 |
| Number of pages | 11 |
| Journal | Oikos |
| Volume | 128 |
| Issue number | 12 |
| DOIs | |
| State | Published - Dec 1 2019 |
All Science Journal Classification (ASJC) codes
- Ecology, Evolution, Behavior and Systematics
Keywords
- Solanum incanum
- associational effects
- associational refuge
- herbivory
- physical plant defenses
- spines and thorns
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Strong but opposing effects of associational resistance and susceptibility on defense phenotype in an African savanna plant. / Coverdale, Tyler C.; McGeary, Ian J.; O'Connell, Ryan D.; Palmer, Todd M.; Goheen, Jacob R.; Sankaran, Mahesh; Augustine, David J.; Ford, Adam T.; Pringle, Robert Mitchell.
In: Oikos, Vol. 128, No. 12, 01.12.2019, p. 1772-1782.Research output: Contribution to journal › Article › peer-review
TY - JOUR
T1 - Strong but opposing effects of associational resistance and susceptibility on defense phenotype in an African savanna plant
AU - Coverdale, Tyler C.
AU - McGeary, Ian J.
AU - O'Connell, Ryan D.
AU - Palmer, Todd M.
AU - Goheen, Jacob R.
AU - Sankaran, Mahesh
AU - Augustine, David J.
AU - Ford, Adam T.
AU - Pringle, Robert Mitchell
N1 - Funding Information: We found that the intensity of browsing by large mammalian herbivores on S. campylacanthum was modulated by both intrinsic (i.e. prickles), and extrinsic (i.e. associational effects) defense strategies. Despite the small size of ; Fig. A, Supplementary material Appendix 3 Fig. A5), our results suggest that prickles are an effective antiherbivore deterrent: removing prickles increased the number of leaves with browsing damage by ~25% (Fig. B), and the majority of browsing occurred on the relatively undefended tips of leaves (Fig. D). Although these results are consistent with herbivore avoidance of prickles, we are not able to conclusively rule out the (not mutually exclusive) alternative explanations that bite‐size restrictions in the smaller herbivore species (e.g. dik‐dik) and/or herbivore preference for leaf tips regardless of prickle location influenced these patterns. However, the consumption of leaf tissue that formerly contained prickles after experimental prickle removal (Supplementary material Appendix 3 Fig. A3) and the consistent location of browsing scars ~3.5 cm from the most distal prickle (regardless of the proximity of that prickle to the leaf tip) suggest that herbivore avoidance of prickles is the most probable explanation for observed patterns of leaf damage. S. campylacanthum prickles relative to the native mammalian herbivores (e.g. dik‐dik, impala, elephant) known to consume this understory species (Pringle et al. 2014, Kartzinel et al. As predicted, we also found that browsing intensity was decreased by proximity to spinescent Acacia trees: relative to conspecifics growing adjacent to tree canopies, individuals growing beneath tree canopies (and, analogously, within long‐term herbivore exclosures) experienced ~80–100% less browsing damage. Because the understory community beneath , Coverdale et al. ), these results suggest that the strength of the associational refuge provided by spinescent neighbors is greater than the potential associational susceptibility conferred by growing near attractive neighbors (Barbosa et al. 2009); indeed, experimental removal of branches leads to a rapid increase in browsing damage (Coverdale et al. 2018), suggesting that the primary mechanism of this associational refuge is the physical inhibition of large herbivores by , Cooper and Owen‐Smith , Louthan et al. 2014, Coverdale et al. ) and provide experimental evidence for the efficacy of physical defenses against large mammalian browsers in understory plants such as Acacia canopies tends to be more diverse, palatable and nutrient‐rich (Weltzin and Coughenour Acacia . Browsing damage on plants within treeless glades in contrast, was ~400% greater than in adjacent non‐glade habitat (Fig. 2). Collectively, these results are consistent with previous reports of the role of physical defenses in intrinsic and extrinsic defense strategies in African savanna plant communities (Mcnaughton S. campylacanthum . Understanding the mechanism(s) of and interactions between intrinsic and extrinsic defenses, and particularly how they influence the distribution and abundance of species among refuge and non‐refuge habitats, remains a promising area for future research. Persistent differences in browsing intensity – driven, in this case, by proximity to spinescent overstory neighbors or to short‐statured understory grasses – also appear to have exerted predictable effects on plant defense phenotype (Fig. 4). Associational resistance and associational susceptibility had strong, but opposing, effects on prickle density: associational resistance conferred by spiny trees decreased prickle density by ~80%, whereas association with grasses within glades and clearings increased prickle density by ~45–60%. Taken together, these results indicate that intraspecific variation in defense phenotype can be quite large, even over relatively small spatial scales (e.g. 5–20 m , Benevenuto et al. 2018), may be an important driver of such heterogeneity in savannas as well (Supplementary material Appendix 3 Fig. A4). 2 tree canopies) and time periods (≤3 years). These results further suggest that the identity and morphology of neighbors, which have previously been shown to affect defense phenotype in agricultural, boreal and model systems (Underwood et al. 2005, Kim Schematic illustration of the effects of associational resistance and susceptibility on browsing damage and defense investment in S. campylacanthum . Acacia trees (left) provide associational refuges against large mammalian browsers. S. campylacanthum in grass‐dominated clearings (right) suffer increased browsing damage relative to those in the matrix habitat outside glades (center). ), whereas volatile cues produced by damaged neighbors typically increase defenses through induced responses and/or defense priming (Farmer and Ryan , Arimura et al. ). Neighbors may also affect defense phenotype by reducing the frequency or intensity of the herbivory cues that are necessary for induced responses, though such indirect mechanisms have received considerably less attention than those mediated by direct plant–plant interactions (but see Kim , Benevenuto et al. 2018, Coverdale et al. 2018). Although the presence of trees is known to affect a variety of abiotic factors in savannas at the scale of individual canopies (Weltzin and Coughenour , Belsky ), we found that experimental herbivore exclusion alone was sufficient to produce strikingly similar patterns of defense investment to those observed within and outside natural refuges (Fig. 2), suggesting that associational resistance, and not changes in abiotic conditions, likely drove observed patterns of defense phenotype. However, although abiotic conditions were comparable across experimental treatments at the onset of each large‐scale manipulation (Augustine and McNaughton , Goheen et al. 2013, Ford et al. 2014), we acknowledge the possibility that years of herbivore exclusion may have resulted in differences in some abiotic conditions between herbivore‐exclusion and control plots. We attempted to minimize any such effects by selecting unassociated plants from comparable areas within and outside exclosure plots and by replicating all surveys across multiple plot pairs. We therefore believe that the primary difference between herbivore exclosure and control plots is the intensity of large mammalian browsing (Augustine and McNaughton , Young and Okello , Coverdale et al. , 2018, Wigley et al. 2019). The observed influences of neighbors on defense phenotype could in principle be caused by several mechanisms. For example, competition with neighbors often decreases plant defense investment (Stamp et al. 2004, Donaldson et al. ), our observations of defense investment by ). Collectively, the results of both exclosure experiments and experimental clearings indicate that the opposing indirect effects of associational resistance and susceptibility on focal plant defense phenotype arose from the contrasting effects of different neighbors on browsing herbivores, and are unrelated to spatial variation in resource availability in the form of light or soil nutrients (Fig. 4). Our results thus lend support to the growing body of evidence that variation in neighbor phenotype (whether intra‐ or interspecific; Underwood et al. 2014) can have marked effects on the diversity, phenotype and fitness of nearby plant (Hay , Barbosa et al. 2009, Sato and Kudoh , Kim , Benevenuto et al. 2018, Coverdale et al. 2018). Likewise, although soils and plants in glades are substantially enriched in N, P and micronutrients (Augustine and McNaughton S. campylacanthum within experimental clearings – which are dominated by grasses and support greater densities of large mammalian herbivores but have not experienced major inputs of nutrients from livestock dung and urine (Ford et al. 2014) – suggest that differences in browsing damage are the primary driver of increased defense investment in open areas (Fig. 3). Plants within glades may experience associational susceptibility as a result of two mutually compatible mechanisms: 1) increased apparency to herbivores due to the dominance of close‐cropped grasses (Castagneyrol et al. 2013), and/or 2) increased foraging intensity and/or encounter rate resulting from herbivore attraction to highly palatable neighbors (i.e. herbivore ‘spill‐over’ sensu White and Whitham The observed pattern of greater defense investment by more heavily browsed A–B, 3A–B) may result from 1) selection for defended genotypes in high‐risk areas (occurring over years or decades), and/or 2) induced responses to browsing damage (occurring over days to months). We suggest that there is little evidence for the former mechanism in this system, for several reasons. First, the timespan of our experimental exclosures and clearings is comparable to the lifespan of individual , Ford et al. 2014, Pringle et al. 2014). Additionally, we observed similar patterns of greater defense investment in the longer‐lived tree , Coverdale et al. 2018), and physical defenses are broadly inducible across species in African savannas (Wigley et al. 2019). We therefore suggest that induced responses to browsing may account for a sizeable proportion of the total observed variation in S. campylacanthum (Fig. S. campylacanthum (Augustine and McNaughton Acacia etbaica on the margins of the same experimental clearings relative to adjacent uncleared areas (see also Ford et al. 2014). Together, these results indicate that changes in defense phenotype resulting from experimental manipulations can occur within a single generation for understory and overstory plants at this site, and we therefore consider rapid induction of defenses to be the likelier driver of defense heterogeneity. Moreover, induction (or relaxation) of physical defenses in response to increased (or decreased) browsing has been repeatedly demonstrated at our study site for both overstory and understory plants within experimental and natural refugia (Young S. campylacanthum defense phenotype at our study site (Fig. 4, Supplementary material Appendix 3 Fig. A4). Similarly rapid induced responses to browsing in other members of the Solanaceae, including the congener S. carolinense (Kariyat et al. 2013), further support the inference that short‐term plastic responses are a plausible driver of observed phenotypic variation in S. campylacanthum . We quantified defense phenotype across sites that varied substantially in soil nutrient availability (e.g. glades versus experimental clearings) and found nearly identical levels of investment in carbon‐based, physical defenses. Like other Solanaceae, S. campylacanthum also produces steroidal glycoalkaloids (a nitrogen‐containing chemical defense) in fruits and leaves, yet little is known about interactions and tradeoffs between physical and chemical defenses in this (and other) species. Additional research would be required to determine whether associational effects have similar effects on chemical defenses in S. campylacanthum or, alternatively, whether resource constraints might cause chemical defenses to be down‐regulated following the induction of prickles. How variation in resource availability relates to intraspecific variation in physical versus chemical defense investment has been poorly studied, and Solanum species may be especially valuable for future investigations of tradeoffs among defense traits. ). Although many of the most prominent plant defense theories explicitly address interspecific variation in defense phenotype (Stamp , Hahn and Maron ), there is growing evidence that intraspecific variation in defense investment is widespread (Des Roches et al. ), may approach levels observed among species in plant communities or genera (Coverdale et al. 2018), and can impact the outcome of various ecological processes (Thorpe and Barbosa ). In African savannas, intraspecific variation in defense phenotype may have important implications for the persistence of plants in the face of intense top–down pressure by large mammalian herbivores: repeated browsing resulting from associational susceptibility drives a rapid accumulation of physical defenses, which in turn may reduce the proportion of plants vulnerable to herbivores. In contrast, plants within refuges invest little in intrinsic defenses, potentially allowing them to maximize fitness despite the constraints of competition with overstory neighbors. Understanding the causes and consequences of variation in plant defenses has been a central goal in the study of plant–herbivore interactions (Coley et al. 1985, Burkepile and Parker Acknowledgements – We thank A. Agrawal, J. Daskin, H. Horn, J. Farnsworth, A. Hastings and K. Holmes for conversation and insightful comments on the manuscript. V. Amaral, C. Clements, E. Coverdale, J. Echekan, M. Goat, A. Hassan, A. Ibrahim, S. Kurukura and J. Parsare assisted with field work. Funding – TCC was supported by an NSF Graduate Research Fellowship, an NSF Doctoral Dissertation Improvement Grant (DEB‐1601538), a Lewis and Clark Fund for Exploration and Field Research grant from the American Philosophical Society, a Princeton Institute for International and Regional Studies Summer Research Grant, the Caroline Thorn Kissel Summer Environmental Studies Scholarship from the Garden Club of America, and the Offices of the Provost and the Dean of the College of Agriculture and Life Sciences of Cornell University. IJM and RDO were supported by the Princeton University Office of the Dean of the College and the Princeton Environmental Institute. RMP, JRG and TMP were supported by the National Science Foundation (DEB‐1355122, DEB‐1457697, DEB‐1457679, DEB‐1556728, DEB‐1149980 and IOS‐1656527). The UHURU experiment was built with a Natural Sciences and Engineering Research Council Tools and Instruments grant and funds from the University of Florida and the Sherwood Family Foundation. The GLADE experiment was built and maintained by grants from NSF (DEB‐9813050), NERC (NE‐E017436‐1) and National Geographic (982815). Author contributions – TCC conceived the research. TCC, IJM and RMP designed the research plan. TCC, IJM and RDO performed the research and analyzed the data. JRG, TMP and RMP conceived, implemented and maintain the UHURU experiment. MS and DJA conceived, implemented and maintain the GLADE exclosure experiment. ATF conceived and implemented the artificial clearing experiment. TCC wrote the manuscript; all authors contributed edits and approved the final version. Permits – We thank the government of Kenya (NACOSTI/P/14/8746/1626), D. Martins, and Mpala Research Centre and Conservancy for permission to conduct this study. Supplementary material (available online as Appendix oik‐06644 at < www.oikosjournal.org/appendix/oik‐06644 >). Appendix 1–3.
PY - 2019/12/1
Y1 - 2019/12/1
N2 - The susceptibility of plants to herbivores can be strongly influenced by the identity, morphology and palatability of neighboring plants. While the defensive traits of neighbors often determine the mechanism and strength of associational resistance and susceptibility, the effect of neighbors on plant defense phenotype remains poorly understood. We used field surveys and a prickle-removal experiment in a semi-arid Kenyan savanna to evaluate the efficacy of physical defenses against large mammalian herbivores in a common understory plant, Solanum campylacanthum. We then quantified the respective effects of spinescent Acacia trees and short-statured grasses on browsing damage and prickle density in S. campylacanthum. We paired measurements of prickle density beneath and outside tree canopies with long-term herbivore-exclusion experiments to evaluate whether associational resistance reduced defense investment by decreasing browsing damage. Likewise, we compared defense phenotype within and outside pre-existing and experimentally created clearings to determine whether grass neighbors increased defense investment via associational susceptibility. Removing prickles increased the frequency of browsing by ~25%, and surveys of herbivory damage on defended leaves suggested that herbivores tended to avoid prickles. As predicted, associational resistance and susceptibility had opposing effects on plant phenotype: individuals growing beneath Acacia canopies (or, analogously, within large-herbivore exclosures) had a significantly lower proportion of their leaves browsed and produced ~ 70–80% fewer prickles than those outside refuges, whereas plants in grass-dominated clearings were more heavily browsed and produced nearly twice as many prickles as plants outside clearings. Our results demonstrate that associational resistance and susceptibility have strong, but opposing, effects on plant defense phenotype, and that variable herbivore damage is a major source of intraspecific variation in defense phenotype in this system.
AB - The susceptibility of plants to herbivores can be strongly influenced by the identity, morphology and palatability of neighboring plants. While the defensive traits of neighbors often determine the mechanism and strength of associational resistance and susceptibility, the effect of neighbors on plant defense phenotype remains poorly understood. We used field surveys and a prickle-removal experiment in a semi-arid Kenyan savanna to evaluate the efficacy of physical defenses against large mammalian herbivores in a common understory plant, Solanum campylacanthum. We then quantified the respective effects of spinescent Acacia trees and short-statured grasses on browsing damage and prickle density in S. campylacanthum. We paired measurements of prickle density beneath and outside tree canopies with long-term herbivore-exclusion experiments to evaluate whether associational resistance reduced defense investment by decreasing browsing damage. Likewise, we compared defense phenotype within and outside pre-existing and experimentally created clearings to determine whether grass neighbors increased defense investment via associational susceptibility. Removing prickles increased the frequency of browsing by ~25%, and surveys of herbivory damage on defended leaves suggested that herbivores tended to avoid prickles. As predicted, associational resistance and susceptibility had opposing effects on plant phenotype: individuals growing beneath Acacia canopies (or, analogously, within large-herbivore exclosures) had a significantly lower proportion of their leaves browsed and produced ~ 70–80% fewer prickles than those outside refuges, whereas plants in grass-dominated clearings were more heavily browsed and produced nearly twice as many prickles as plants outside clearings. Our results demonstrate that associational resistance and susceptibility have strong, but opposing, effects on plant defense phenotype, and that variable herbivore damage is a major source of intraspecific variation in defense phenotype in this system.
KW - Solanum incanum
KW - associational effects
KW - associational refuge
KW - herbivory
KW - physical plant defenses
KW - spines and thorns
UR - http://www.scopus.com/inward/record.url?scp=85070800938&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=85070800938&partnerID=8YFLogxK
U2 - 10.1111/oik.06644
DO - 10.1111/oik.06644
M3 - Article
AN - SCOPUS:85070800938
VL - 128
SP - 1772
EP - 1782
JO - Oikos
JF - Oikos
SN - 0030-1299
IS - 12
ER -