Pecan is native to North America (Thompson and Grauke, 1991) and has been used since prehistoric and early historic times as an important source of food and timber (Hall, 2000). It has been commercially cultivated since the mid-1800s and is currently an important agricultural/horticultural crop. The United States is the world’s largest producer of pecans, accounting for ≈58% of the market share with an estimated annual value of ≈$400 million (U.S. Department of Agriculture, 2012). However, pecan’s pest ecology presents serious challenges to the economic success of commercial pecan production in the United States.
The pecan blotch leafminer (Cameraria caryaefoliella) is one of four species of leafmining Lepidoptera that commonly infest pecan trees in the southern United States (Heyerdahl and Dutcher, 1985). Leafminers is a generic term to describe arthropods belonging to different orders whose larvae feed or “mine” between the upper and lower epidermal leaf surfaces. The mining activity creates tiny tunnels or “galleries” in the leaf causing localized necrotic and dead areas. Leafminer injury is visually evident, but healthy plants can tolerate substantial injury although there are growth (Wagner et al., 2008) and yield penalties (Percival et al., 2011; Thalmann et al., 2003). Harris and Lee (2012) indicated that the action level for leafminers in pecan is one to two larvae per leaf; however, such thresholds may not consider physiological compensatory measures to offset injury.
The impact of leafminers and other herbivores on the photosynthetic performance of leaves is difficult to estimate because of several variables such as location of the injury (on-vein vs. between veins) (Layne and Flore, 1992; Oleksyn et al., 1998), species (Oleksyn et al., 1998), intensity of the injury, induced production of allelochemicals, and proximity to injured area (Zangerl et al., 2002). One approach to investigate the effects of foliage feeders on leaf physiology is to simulate defoliation by artificial removal of portions of the leaf lamina and study the consequences on the intact portion of the leaf. Although the approach of artificially clipping parts of the leaf lamina can be useful as a preliminary study, it may not reflect feeder injury accurately, because it fails to take into account the possible role of biochemicals secreted by the herbivores (Delaney et al., 2008; Poston et al., 1976).
Plant response to herbivory injury is highly variable across and within different plant species. During heavy leafminer infestations, leaves look bleached or faded, their physiological functions and anatomical structures are disrupted, and their aesthetic value is reduced. In some cases, the feeding galleries may become points of entry for pathogenic fungi and bacteria. Increased inoculum production and disease spread have been observed for citrus canker caused by the bacterium Xanthomonas axonopodis pv. citri after infestation by the asian leafminer (Phyllocnistis citrella) (Das, 2003).
One of the most direct consequences of herbivory attack is injury of portions of the leaf lamina, which is associated with a reduction in whole-plant carbon assimilation (Raimondo et al., 2003; Schaffer et al., 1997; Welter, 1989). The actual impact on the physiological functions of the non-injured tissue may be species-dependent. Leafminer injury to functional integrity of the photosynthetic system of horse chestnut (Aesculus hippocastanum) did not extend beyond the mines (Raimondo et al., 2003). However, a study conducted to examine the effects of caterpillar injury in wild parsnip (Pastinaca sativa) revealed that the adverse effects of caterpillar feeding on photosynthesis extended beyond the injured areas (Zangerl et al., 2002). The indirectly affected area was six times as large as the area directly injured by the caterpillars. Moreover, the size of the indirectly affected area was positively correlated with the synthesis of furanocoumarins, defense-related compounds, suggesting that the indirect effects of herbivory on plants may be related to the cost of chemical defense through increased respiration rates (Zangerl et al., 2002).
In a few cases, a compensatory increase in photosynthetic rates has been reported as a consequence of removal of a portion of the leaf lamina. Layne and Flore (1992) found that simulated removal of less than 30% of the leaf lamina of ‘Montmorency’ sour cherry (Prunus cerasus) induced higher estimated carboxylation efficiency and ribulose-l,5-bisphosphate regeneration capacity in the remaining area. Photosynthetic rate of the non-injured portion of grey alder (Alnus incana) and european alder (Alnus glutinosa) leaves grazed by the alder beetle (Agelastica alni) was increased by 10% to 50% (Oleksyn et al., 1998). Because of this compensatory increase in photosynthesis, a net reduction in photosynthesis per leaf occurred only when the proportion of leaf area grazed was greater than 40% in grey alder and greater than 23% in european alder (Oleksyn et al., 1998).
Pecan leafminers are present in the entire pecan-growing region of the United States and are usually considered a minor pest (Sutherland, 2011); however, occasional severe infestations occur (as observed in the present study). It is not known what the physiological consequences of leafminer infestation on gas exchange are and whether pecan shows any compensatory response. The objective of this study was to investigate the effects of pecan blotch leafminer on carbon assimilation and photosynthetic efficiency in pecan leaves. The hypotheses were that low-to-moderate injury induces a compensatory increase in photosynthesis and that degree of the compensation is proportional to the intensity of the injury.
Delaney, K.J., Haile, F.J., Peterson, R.K. & Higley, L.G. 2008 Impairment of leaf photosynthesis after insect herbivory or mechanical injury on common milkweed, Asclepias syriaca Environ. Entomol. 37 1332 1343
Greer, D.H. 1995 Effect of canopy position on the susceptibility of kiwifruit (Actinidia deliciosa) leaves on vines in an orchard environment to photoinhibition throughout the growing season Austral. J. Plant Physiol. 22 299 309
Harris, M. & Lee, N. 2012 Pest profiles. 3 Apr. 2013. <http://pecan.ipmpipe.org/toolbox/pest_profiles/doc_pdf/pest_profiles_sm.pdf>
Levine, A., Tenhaken, R., Dixon, R. & Lamb, C. 1994 H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response Cell 79 583 593
Oleksyn, J., Karolewski, P., Giertych, M.J., Zytkowiak, R., Reich, P.B. & Tjoelker, M.G. 1998 Primary and secondary host plants differ in leaf-level photosynthetic response to herbivory: Evidence from Alnus and Betula grazed by the alder beetle, Agelastica alni New Phytol. 140 239 249
Percival, G.C., Barrow, I., Noviss, K., Keary, I. & Pennington, P. 2011 The impact of horse chestnut leaf miner (Cameraria ohridella Deschka and Dimic; HCLM) on vitality, growth and reproduction of Aesculus hippocastanum L Urban For. Urban Green. 10 11 17
Poston, F.L., Pedigo, L.P., Pearce, R.B. & Hammond, R.B. 1976 Effects of artificial and insect defoliation on soybean net photosynthesis J. Econ. Entomol. 69 109 112
Raimondo, F., Ghirardelli, L.A., Nardini, A. & Salleo, S. 2003 Impact of the leaf miner Cameraria ohridella on photosynthesis, water relations and hydraulics of Aesculus hippocastanum leaves Trees (Berl.) 17 376 382
Schaffer, B., Peña, J.E., Colls, A.M. & Hunsberger, A. 1997 Citrus leafminer (Lepidoptera: Gracillariidae) in lime: Assessment of leaf damage and effects on photosynthesis Crop Prot. 16 337 343
Sutherland, C. 2011 Potential pecan pests to ponder—Leafminers and hickory shuckworm in New Mexico, 2010. Proc. 45th Annu. Western Pecan Growers Assn., Las Cruces, NM. p. 8–10
Thalmann, C., Freise, J., Heitland, W. & Bacher, S. 2003 Effects of defoliation by horse chestnut leafminer (Cameraria ohridella) on reproduction in Aesculus hippocastanum Trees (Berl.) 17 383 388
U.S. Department of Agriculture 2008 Official soil series descriptions. 22 Mar. 2013. <http://soils.usda.gov/technical/classification/osd/index.html>
U.S. Department of Agriculture 2012 Noncitrus fruits and nuts. 15 Apr. 2013. <http://usda.mannlib.cornell.edu/MannUsda/viewDocumentInfo.do?documentID=1113>
Wagner, D., DeFoliart, L., Doak, P. & Schneiderheinze, J. 2008 Impact of epidermal leaf mining by the aspen leaf miner (Phyllocnistis populiella) on the growth, physiology, and leaf longevity of quaking aspen Oecologia 157 259 267
Welter, S.C. 1989 Arthropod impact on plant gas exchange, p. 135–150. In: Bernays, E.A. (ed.). Insect–plant interactions. CRC Press, Boca Raton, FL
Zangerl, A.R., Hamilton, J.G., Miller, T.J., Crofts, A.R., Oxborough, K., Berenbaum, M.R. & de Lucia, E.H. 2002 Impact of folivory on photosynthesis is greater than the sum of its holes Proc. Natl. Acad. Sci. USA 99 1088 1091