Effective Defense of Aleppo Pine Against the Giant Scale Marchalina hellenica Through Ecophysiological and Metabolic Changes

Abstract

Aleppo pine (Pinus halepensis) is widely distributed in the Mediterranean region and in other areas of the world, where it has been introduced due to its adaptive capacity to xerothermic conditions. The giant pine scale Marchalina hellenica often infests Aleppo pine, as well as other pines, in several southeastern European countries, causing pine declines. When combined with the expected intensified heat and drought events in eastern Mediterranean, the impact of this biotic parameter on the host pines may be exacerbated. The importance of understanding the defense mechanisms of Aleppo pine is emphasized by the recent invasion of the pine scale in new regions, like Australia, lacking the insect’s natural enemies, where more intense negative effects on pine species may occur. To date, Aleppo pine’s physiological responses to the infestation by M. hellenica are largely unknown. This study aimed at assessing the responses of Aleppo pine to the giant pine scale attack, both on an ecophysiological and a metabolic level. For this purpose, gas exchange, needle water status, and carbon and nitrogen content were measured during 1 year on healthy and infested adult trees. M etabolic profiling of Aleppo pine needles was also performed before, during, and after the high feeding activity of the insect. The maintenance of stable relative water content, δ13C signatures, and chlorophyll fluorescence in the needles of infested pines indicated that infestation did not induce drought stress to the host pines. At the peak of infestation, stomatal closure and a pronounced reduction in assimilation were observed and were associated with the accumulation of sugars in the needles, probably due to impaired phloem loading. At the end of the infestation period, tricarboxylic acids were induced and phenolic compounds were enhanced in the needles of infested pines. These metabolic responses, together with the recovery of photosynthesis after the end of M. hellenica intense feeding, indicate that in the studied region and under the current climate, Aleppo pine is resilient to the infestation by the giant pine scale. Future research should assess whether these promising defense mechanisms are also employed by other host pines, particularly in regions of the world recently invaded by the giant pine scale, as well as under more xerothermic regimes.

Uncovering the Male Presence in Parthenogenetic Marchalina hellenica (Hemiptera: Marchalinidae): Insights into Its mtDNA Divergence and Reproduction Strategy

“…Although M. hellenica is associated with detrimental effects on trees at high densities, such as branch and foliage desiccation, growth decline, and crown transparency [ 15 , 16 ], it only rarely causes tree mortality, and usually only in conjunction with other biotic and abiotic secondary stress factors [ 15 , 16 ]. In regions invaded by M. hellenica , similar or greater impacts on host trees have been observed [ 14 ]. The mild adverse effects of M. hellenica on pine trees in its native region have been attributed to the impact of its natural enemies [ 11 ].…”

“…in Russia, Armenia, and Georgia [ 12 ], it was later determined that the scale-insect species encountered in these countries was Marchalina caucasica Hadzibeyli (Hemiptera: Marchalinidae) [ 13 ]. In its native range, M. hellenica is not considered a serious pest and control measures are taken only sporadically, mainly for aesthetic reasons in urban areas [ 14 ]. Although M. hellenica is associated with detrimental effects on trees at high densities, such as branch and foliage desiccation, growth decline, and crown transparency [ 15 , 16 ], it only rarely causes tree mortality, and usually only in conjunction with other biotic and abiotic secondary stress factors [ 15 , 16 ].…”

Seasonal Phenology and Climate Associated Feeding Activity of Introduced Marchalina hellenica in Southeast Australia

“…The densities of M. hellenica on Australian P. radiata were typically higher than Mediterranean conspecifics feeding on Pinus halepensis during seasonally equivalent months [ 51 ]; however, the proportion of honeydew producing insects did not reach proportions as high as those previously documented in Greece [ 50 ]. We found evidence that variation in the density of honeydew producing insects and the quantity of honeydew produced could be explained by changes in temperature, humidity, vapour pressure in the atmosphere, and solar exposure.…”

“…Since the phenological study from Greece occurred from 2001 to 2003, it is unclear whether the difference in findings between the current study and previous observations are attributable to underlying geographic differences, inherent generational variation, or host species. The insect density recorded in the current study, from 2019–2020, was only separated by six months from insect densities recorded from Greek conspecifics in 2018–2019 [ 51 ]. However, the density of Australian M. hellenica was generally higher than the density of the concurrent Greek conspecifics.…”

“…To account for combined variation in GPS [cm −2 ] and HPI [%], GPS [cm −2 ] was multiplied by HPI [%] to obtain the density of honeydew producing insects, expressed as HPI [cm −2 ]. This was used as an estimation of the density of M. hellenica producing honeydew, accounting for the decline in GPS [cm −2 ] as each generation progresses [ 51 ] and seasonal fluctuations in HPI [%] [ 50 ]. Honeydew was collected from HPI from each phenological sample.…”