Mechanisms of Root Herbivory Effects on Plant Performance
Mechanisms behind the root herbivory effects on plant performance
Plant growth can be retarded due to direct effects of root consumption, resulting in both losses of resources stored belowground and a reduction of the root surface area for water and nutrient uptake and/or a disruption of water and nutrient flows from roots to aboveground parts. Similar to drought stress, these processes create a water deficit that is frequently expressed in reduced water content in tissues (Andersen 1987; Goldson et al. 1987; Gange and Brown 1989). Drought stress inhibits photosynthesis mostly by decreasing stomatal conductance (Cornic 2000) to control water losses; lower stomatal conductance was also found in plants suffering from root herbivory (Riedell and Rees 1999; Diaz et al. 2006). This similarity allows making the suggestion that the mechanisms behind the decreased photosynthesis observed in plants experiencing root damage are similar to those in plants suffering from drought.
Regrowth of adventitious roots (Riedell and Rees 1999) and lateral root proliferation are considered as universal responses to root damage (Andersen 1987; Brown and Gange 1990; Rubio and Linch 2007). In general, more than 50% of the daily net CO2 fixation of a plant is allocated to the roots (Farrar and Jones 2003), indicating that it is costly to build and maintain roots. Accelerated root growth leads to an increased flow of photosynthates (assimilates) and nitrogen to the roots, at the expense of aboveground parts (Detling et al. 1980; Steiner and Müller-Schärer 1992; Borowicz 2010). In combination with decreased photosynthetic rates, the increased sink demands of regrowing roots may be especially detrimental. The similarity in the effects of root herbivory on growth and reproduction suggests that retardations of aboveground processes may be due to a general reduction of plant nutrient status caused by compensatory root growth.
Additionally, like herbivores feeding aboveground, root herbivores may induce direct and indirect defensive responses in plants (Rasmann and Agrawal 2008; van Dam 2009). The production of defensive compounds in response to root herbivory, which may co-occur with tolerance responses (van Dam 2009), is likely to imply additional costs resulting in decreased investment in growth and reproduction.
Thus, the detrimental effects of root herbivory on plant growth and reproduction result from several processes: (i) decreases in water and nutrition uptake due to direct reductions in root biomass (mostly when fine roots are consumed) or disruption of water and nutrient flows (mostly when the main root is damaged); (ii) consumption of resources stored belowground; (iii) decreases in photosynthetic rates due to water deficits imposed by root damage; (iv) translocation of assimilates to roots for root regrowth; and (v) direct costs of inducible defences.
The processes described above lead to the limitation of all types of resources, and therefore the effects of root herbivory may be very severe, leading not only to growth retardation, but even to plant death (Gange et al. 1991; Maron 2001).
References
Agrawal AA (2004) Resistance and susceptibility of milkweed: Competition, root herbivory, and plant genetic variation. Ecology 85:2118-2133
BorowiczVA (2010) The impact of arbuscular mycorrhizal fungi on strawberry tolerance to root damage and drought stress. Pedobiologia 53:265-270
Brown VK, Gange AC (1990) Insect herbivory below ground. Adv Ecol Res 20:1-58
Cornic G (2000) Drought stress inhibits photosynthesis by decreasing stomatal aperture - not by affecting ATP synthesis. Trends Plant Sci 5:187-188
Detling JK, Winn DT, Proctergregg C, Painter EL (1980) Effects of simulated grazing by below-ground herbivores on growth, CO2 exchange, and carbon allocation patterns of Bouteloua gracilis. J Appl Ecol 17:771-778
Diaz AP, Mannion C, Schaffer B (2006) Effect of root feeding by Diaprepes abbreviatus (Coleoptera: Curculionidae) larvae on leaf gas exchange and growth of three ornamental tree species. J Econ Entomol 99:811-821
Farrar JB, Jones DH (2003) The control of carbon acquisition by the growth of roots. In: de Kroon H, Visser EJW (eds) Root ecology. Springer, Berlin, pp 91-124
Gange AC, Brown VK (1989) Effects of root herbivory by an insect on a foliar feeding species, mediated through changes in the host plant. Oecologia 81:38-42
Gange AC, Brown VK, Farmer LM (1991) Mechanisms of seedling mortality by subterranean insect herbivores. Oecologia 88:228-232
Goldson SL, Bourdot GW, Proffitt JR (1987) A study of the effects of Sitona discoideus (Coleoptera, Curculionidae) larval feeding on the growth and development of lucerne (Medicago sativa). J Appl Ecol 24:153-161
Maron JL (2001) Intraspecific competition and subterranean herbivory: individual and interactive effects on bush lupine. Oikos 92:178-186
Rasmann S, Agrawal AA (2008) In defense of roots: A research agenda for studying plant resistance to belowground herbivory. Plant Physiol 146:875-880
Riedell WE, Reese RN (1999) Maize morphology and shoot CO2 assimilation after root damage by western corn rootworm larvae. Crop Sci 39:1332-1340
Rubio G, Lynch JP (2007) Compensation among root classes in Phaseolus vulgaris L. Plant Soil 290:307-321
Steinger T, Müller-Schärer H (1992) Physiological and growth responses of Centaurea maculosa (Asteraceae) to root herbivory under varying levels of interspecific plant competition and soil nitrogen availability. Oecologia 91:141-149
van DamNM (2009) Belowground herbivory and plant defenses. Ann Rev Ecol Evol Syst 40:373-391
1