4. ВЛИЯНИЕ СИМБИОЗА НА РАСТЕНИЯ.
Effects of ant–hemipteran interactions on host plant damage and plant fitness

      Учитывая экологический и экономический эффект создания медвяной росы равнокрылыми, как вредителями растений, and the widespread distribution and abundance of both honeydew-producing hemipterans and ants in terrestrial communities, surprisingly few studies have investigated explicitly the consequences of ant–hemipteran interactions on plant fitness. This is not to say that the subject has not received a great deal of attention in the literature, leading to what we think is a general misconception that indirect benefits of ant–hemipteran interactions to plants are well documented. Repeated assertions that hemipteran-tending ants indirectly benefit host plants in multiple review papers (e.g. Beattie 1985; Buckley 1987; Way & Khoo 1992; Lach 2003) and in an abundance of papers investigating the effects of ants on plants in general belie the fact that relatively few studies provide a quantitative supporting evidence.

      Представляемый здесь обзор литературы, только в 22 статьях заявленная цель состояла в том, чтобы исследовать определенно эффекты взаимодействий между муравьями и создающими медвяную росу равнокрылыми. Equivalent effects could be inferred from eight additional studies of the general effects of ants on plants and associated herbivores, including honeydew-producing hemipterans. These 30 studies (summarized in table 1) examined the effects of ant–hemipteran interactions on plants by either (i) comparing plants on which honeydew-producing hemipterans and/or tending ants were naturally present or absent (correlative studies) or (ii) comparing plants on which the presence/absence of honeydew-producing hemipterans and/or tending ants was manipulated (experimental studies). We did not include in our review any studies (of which there are many) that provided only an anecdotal evidence of the effects of ant–hemipteran interactions on plants, or any studies that were not designed with a meaningful control treatment (e.g. Room 1972; Bach 1991; Fernandes et al. 2005) or that did not demonstrate a positive correlation between hemipteran density and ant density on plants (e.g. Way et al. 1999; Perry et al. 2004).

      Авторы считают, что важно обратить внимание, что из 30 статей, рассмотренных здесь, только 21 работа (70%)или учитывала методику искусственного исключения муравьев путем экспериментальных манипуляций (n=19 статей) или естественное отсутствие\присутствие муравьев на деревьях (n=2 статей; table 1). A major limitation of manipulative and natural experiments of this type is that they do not specifically test the effect of the interaction per se between ants and hemipterans on plants (i.e. whether ants have stronger effects as predators in the presence of honeydew-producing hemipterans). Муравьи фуражируют и охотятся за членистоногой добычей на деревьях, даже в отсутствии там тлей и т.д. (Holldobler & Wilson 1990). Например, фуражировочная активность рыжих лесных муравьев (F. rufa) зарегистрированная на платанах (Acer pseudoplatanus) ещё до колонизации их тлями Periphyllus testudinaceus (Skinner 1980). Similarly, wood ant predation of leafhoppers (Cicadellidae) and a non-honeydew-producing aphid species on sycamore trees has occurred at times when wood ants did not actively tend P. testudinaceus (Whittaker 1991). The interpretation of results from the studies that purport to demonstrate the beneficial effects of the interactions between wood ants and honeydew-producing hemipterans on the trees (table 1), therefore, is somewhat compromised. Indeed, in any system in which ants forage on plants in the absence of honeydew-producing hemipterans, studies relying on the presence/absence of ants to investigate the effects of ant–hemipteran interactions on plants cannot rigorously distinguish whether ant predation is independent of or truly facilitated by honeydew-producing hemipterans.

      Наоборот, семь статей (23%, table 1) или экспериментально манипулировали с плотностью равнокрылых, производящих медвяную росу (равнокрылых или удаляли или сажали на деревья где их ранее не было; n=2 studies) или использовали естественную вариацию в наличии ли отсутствии равнокрылых на деревьях (n=5 studies). These types of manipulative and natural experiments probably provide more realistic tests of the effects of ant–hemipteran interactions on plants, because ant behaviour changes in response to the presence of honeydew-producing hemipterans rather than vice versa (see Floate & Whitham 1994). Better still are the experiments that manipulate both ants and honeydew-producing hemipterans in a crossed design, because they allow a comparison of the effects of the ants alone and the hemipterans alone with the effects of the ant–hemipteran interaction specifically. Only two studies (7%) have utilized a crossed design (table 1). Thus, even though 30 studies are included in this section of the review, only four experimental studies rigorously tested for the effects of ant–hemipteran interactions on plants.

Тли и Формики.
(Фото: П.Корзунович >>>)

      (a) Net negative effects

      Несмотря на многочисленные доказательства того, что муравьи могут увеличивать численность сосущих равнокрылых (Beattie 1985; Buckley 1987; Holway et al. 2002) и что это в итоге ухудшает состояние растений через consumption of plant sap и передачу патогенов растений (Carter 1962; Buckley 1987; Delabie 2001), негативные эффекты мутуализма муравье и сосущих равнокрылых довольно редко регистрируются (n=9 studies; table 1). То есть, либо эти отрицательные эфект ы в природе очень редки, или их трудно зарегистрировать whether they have simply been assumed and, thus, not quantified remains unclear. Биологи Banks & Macaulay (1967) сообщали, что тля Aphis fabae была на 30–50% более обильна на бобах (Vicia faba), когда там были разводящие их муравьи Lasius niger, что уменьшало производительность растения и его урожайность - resulting in significantly fewer pods and seeds per plant - в сравнении с растениями где тлю A. fabae не поддерживали муравьи. Similarly, in a study of the effects of an ant–aphid mutualism on the fitness of the forb Bidens pilosa, Renault et al. (2005) reported that the aphid Aphis coreopsidis was 34% more abundant in the presence of tending Camponotus ants than in their absence. Consequently, plants hosting ant-tended aphids produced significantly fewer viable seeds than did plants from which ants were excluded. In the only study that documented the effect of an ant–hemipteran mutualism on the transmission of a plant pathogen, the presence of S. invicta caused a 240% increase in aphid abundance on tomato (Lycopersicon esculentum), resulting in a significant increase in the level of infection of plants by the aphid-vectored Cucumber mosaic virus (Cooper 2005).

      (b) Net positive effects

      Горадо многочисленнее статьи, в которых не обнаружено позитивного эффекта взаимодействий "муравьи-равнокрылые" на сами растения-хозяева (n=22; table 1). In these studies, ant–hemipteran interactions benefited plants as a consequence of increased ant predation or harassment of other, more damaging, insects, resulting in decreased plant damage by those insects and/or increased plant fitness. However, the majority of these studies (n=14, 64%) used ant-exclusion manipulations to test for the effects of ant–hemipteran interactions on plants, an experimental design that hinders distinction between the effects of ant–hemipteran interaction specifically versus the effects of the ants alone (see above). For example, Skinner & Whittaker (1981) showed that leaf damage by lepidopteran larvae was significantly reduced on sycamore trees on which wood ants (F. rufa) tended the aphid P. testudinaceus compared with trees from which wood ants were experimentally excluded. In later ant-exclusion experiments in the same system, Whittaker & Warrington (1985) showed that the radial growth of sycamore trees was two to three times greater in the presence of the ant–aphid interaction, presumably as a consequence of herbivore suppression by the aphid-tending ants.

      Другие работы (n=5 статей) использовали естественную вариацию в наличие или отсутсвии сосущих равнокрылых для тестирования эффектов их отношений с муравьями на сами растения. Treehopper-tending ants (Formica spp.) on Solidago altissima, for example, deterred feeding by the larvae of two species of leaf beetle (Messina 1981). Increased plant protection by ants in the presence of treehoppers resulted in increased plant growth and seed production relative to neighbouring plants on which treehoppers were naturally absent. Only two studies experimentally tested for the effects of ant–hemipteran interactions on plant fitness by manipulating the hemipteran densities. For example, Floate & Whitham (1994) manipulated the aphid densities to test whether a facultative mutualism between the aphid C. populicola and a Formica ant species indirectly protected cottonwood (Populus fremontii and hybrids) foliage from beetle herbivory. The addition of aphids to trees dramatically increased ant abundance, which translated into a 95% reduction in the abundance of beetle larvae and significantly less beetle damage to leaves.

      Авторы отмечают, что в 5 работах, которые зарегистрировали позитивный эффект, все работы были произведены в управляемых человеком системах (table 1), demonstrating that ant–hemipteran interactions may be exploited for biological control of more damaging pests on agriculturally important plants. In fact, arboreal ants attracted to hemipteran honeydew have long been utilized to control non-honeydew-producing herbivore pests in several tree crops (Way & Khoo 1992). For example, growers manipulate colonies of Dolichoderus ants in cocoa (Theobroma cacao) and sapodilla (Manilkara zapota) plantations in Southeast Asia, because the mealy bug-tending ants protect cocoa pods and sapodilla fruits from damage by mirids (Heteroptera; Khoo & Ho 1992) and pyralid larvae (Lepidoptera; Van Mele & Cuc 2001) without any direct yield loss caused by the mealy bugs. However, far less is known about the net effects of ant–hemipteran interactions on herbaceous crop plants in more ephemeral systems, such as row and vegetable crops. Protection by tending ants can lead to hemipteran outbreaks in agricultural monocultures of herbaceous plants, resulting in a significantly reduced yield caused by phloem loss (e.g. Banks & Macaulay 1967) and transmission of plant pathogens (e.g. Cooper 2005). If the honeydew-producing hemipterans do not vector plant pathogens to particular crop plants, and if those plants show a high tolerance to hemipteran herbivory, the ant–hemipteran interactions may still benefit plant yield. For example, in cotton, we have shown experimentally that A. gossypii attract ground-foraging S. invicta onto plants, resulting in increased ant predation of an important cotton herbivore, the beet armyworm caterpillar (Spodoptera exigua). Cotton plants hosting the ant–aphid interaction suffered less caterpillar damage to leaves and bolls (cotton fruit) and, consequently, produced significantly more bolls and seedcotton relative to plants from which A. gossypii were excluded (Styrsky 2006; Styrsky & Eubanks in preparation). We encourage additional studies of the effects of ant–hemipteran mutualisms on other annual cropping systems to further evaluate their utility for increased biological control of non-honeydew-producing herbivores (Eubanks & Styrsky in press).

Тли и Мирмики.
(Фото: П.Корзунович >>>)

      (c) Search for general patterns

      Авторы суммаризировали эффекты взаимодействий "муравьи-равнокрылые" на растения в каждой статье путем подсчета процента per cent change in plant damage and/or plant fitness associated with the presence of the interactions relative to their absence (table 1). Эти эффекты ранжировались в рамках континуума от сильного негативного до сильного позитивного эффектов. Plant damage was most often quantified as leaf damage by non-honeydew-producing herbivores. Plant fitness was quantified using a wide variety of traits that were related to both plant growth and reproduction, thus precluding the calculation of any representative average value.
      Взаимоотношения "муравьи-равнокрылые" исследовались на растениях в 18 их семействах в естественных и искусственных экосистемах в умеренной и тропической зонах климата и наблюдалось на муравьях 6 подсемейств и на равнокрылых, производящих медвяную росу в двух подотрядах (Sternorrhyncha и Auchenorrhyncha) и в двух надсемействах внутри подотряда Sternorrhyncha (Aphidoidea и Coccoidea). Given this variety in study systems, we attempted to discern the general patterns in the effects of ant–hemipteran interactions on plants based on several ecological factors. Specifically, we asked whether the frequency of negative and positive effects varied between natural and managed systems, temperate and tropical habitats, woody and herbaceous plants, ant subfamilies, hemipteran suborders, and aphids and scales/mealy bugs. We also asked whether the frequency of negative and positive effects varied between correlative and experimental studies.

      Изучение систем, использующих сельскохозяйственные виды растений-хозяев, были категоризированы как "управляемые системы" (‘managed’ systems), в то вермя как таковые, но использующие не агровиды растений-хозяев в их или естественном окружении или в нарушенных биотопах (e.g. cattle pastures, second-growth woodlands) рассматривались как ‘natural’ systems. Habitats were categorized as ‘temperate’ or ‘tropical’ based on the latitude of the study sites with respect to the tropics of Cancer and Capricorn. The frequency of negative and positive effects of ant–hemipteran interactions on plants neither varied between natural and managed systems (Fisher's exact test: p=1.0; figure 2a) nor between temperate and tropical habitats (p=0.43; figure 2b). Ant–hemipteran interactions tended to benefit woody host plants more frequently than harming them, relative to herbaceous host plants (figure 2c). However, statistically, the frequency of negative and positive effects did not vary between woody and herbaceous plants (p=0.39).

      Среди муравьев, разводящих равнокрылых как своих "коров" отмечены представители 6 подсемейств, однако большинство видов (89%) были из подсемейств Formicinae и Myrmicinae. Эти два подсемейства вместе с подсемейством Dolichoderinae, представляют большинство видов, разводящих равнокрылых (Holldobler & Wilson 1990). Ant–hemipteran interactions involving formicine ants were equally as likely to benefit plants as were interactions involving myrmicine ants (p=1.0; figure 2d). Аналогично, частота отрицательных и положительных эффектов не изменялась между подотрядами сосущих равнокрылых Sternorrhyncha (тли, червецы и щитовки) и Auchenorrhyncha (цикадки, treehoppers and planthoppers; p=0.69; figure 2e) или между надсемействами Sternorrhynchan такими как Aphidoidea (тли) и Coccoidea (червецы и щитовки, scales and mealy bugs; p=1.0; figure 2f). Наконец, частота отрицательных и положительных эффектов взаимодействий "муравьи-равнокрылые" на сами растения не изменялась между correlative (22% negative and 78% positive) и экспериментальными (31% negative and 69% positive) данными исследований (p=1.0).

      Отсутствие связи между частотой негативных и позитивных эффектов взаимодействий "муравьи-равнокрылые" на растения и экологическая переменных, проверенных выше нужно рассмотреть с предостережением. The limited amount of published data probably compromised the power of our analyses, further emphasizing the need for additional studies of the effects of ant–hemipteran interactions on plant fitness. More importantly, despite broad diversity in the geographical locations, habitats, and plant, ant and hemipteran species studied, the ant–hemipteran interactions had strong effects on plants in most studies, suggesting that ant–hemipteran interactions are important components of ecological communities.

Тли и Мирмики.
(Фото: П.Корзунович >>>)

ч.1 - Введение,
ч.2 - Методика и Влияние симбиоза "муравьи-равнокрылые" на структуру и разнообразие сообщества,
ч.3 - Влияние симбиоза на растения,
ч.4 - А что получают сами растения? Список 11 факторов,
ч.5 - Влияние инвазивных видов муравьев,
ч.6 - Выводы и литература