Исследован механизм плавания муравьёв в кувшинчиках непентеса: кинематика водной и наземной локомоции у муравья Camponotus schmitzi. Ранее, в 2005 году я уже называл это явление аквапланированием (В.К.).

      Муравьи Camponotus schmitzi живут в симбиотических отношениях с растениями рода непентес с острова Борнео (Индонезия) вида Nepenthes bicalcarata, имеющего ловчие листья-кувшинчики. Уникальные среди всех муравьёв, рабчие этого кампонотуса регулярно наряют и погружаются в кувшинчики непентеса и плавают в его пищеварительном растворе собирая там корм для своего пропитания. С помощью высокоскоростной съёмки и анализа движений было доказхано, что C. schmitzi плавают на поверхности с помощью всех шести погруженных ног, with an alternating tripod pattern. Compared to running, swimming involves lower stepping frequencies and larger phase delays within the legs of each tripod. Плавающие муравьи двигают передними и средними ногами быстрее and keep them more extended during the power stroke than during the return stroke. Thrust estimates calculated from three-dimensional leg kinematics using a blade-element approach confirmed that forward propulsion is mainly achieved by the front and middle legs. Задние ноги двигаются гораздо меньше, что говорит о их предназначении для регулирования. Experiments with tethered C. schmitzi ants showed that characteristic swimming movements can be triggered by submersion in water. Эта реакция отсутствовала в другого исследованного вида Camponotus. Данная работа демонстрирует как насекомые могут использовать сходные локомоторные системы и сходные походки для движения по земле и в воде. Авторы обсуждают адаптации насекомых к aquatic/amphibious стилю жизни и специальные адаптации муравьёв C. schmitzi к жизни на растении-хищнике, ловящем других насекомых в свои кувшинчике.

      Key words: Nepenthes bicalcarata - Camponotus schmitzi - Insect-plant interaction - Swimming - Gait analysis .

Шёл, поскользнулся, упал ... в кувшинчик Непентеса… . (Bohn, 2004)

Обзор литературы по теме "муравьи-растения"            Мирмекофитизм

 
Рис.5. Кинематика локомоции муравья Camponotus schmitzi
(по: ©Bohn & al., 2012)

      ВВЕДЕНИЕ.

      Межвидовые отношения среди организмов могут приводить к облигатному симбиозу с невероятными специализациями партнеров. Во многих взаимодействиях растения и насекомого биомеханические факторы играют важную роль. Леса и торфяные болота острова Борнео являются родиной одной такой зависимости, где оба партнера приобрели захватывающие механическии адаптации.

      Муравьи вида Camponotus schmitzi Starcke (Schuitemaker and Staercke 1933) живут в симбиотических отношениях с хищным растением с ловчими листьями-кувшинчиками Nepenthes bicalcarata Hook. f. Это растение одно из более чем 100 кувшинчиковых хищных растений, растущих в бедных по части питательных элементов условиях тропиков Старого Света. Кувшинчики растений рода Nepenthes специализированы для привлечения, поимки и переваривания, главным образом членистоногой добычи (Adam 1997).

      Муравьи Camponotus schmitzi гнездятся эксклюзивно и только в полых усиках-стебельках кувшинчиков N. bicalcarata (Burbidge 1880; Clarke and Kitching 1995). They feed on nectar secreted from the peristome and on prey items captured by their host plant, which they haul out of the pitcher fluid (Clarke and Kitching 1995; Merbach et al. 1999). In striking contrast to other ants which are regularly captured and digested in the pitchers of N. bicalcarata, C. schmitzi ants are able to run safely across the wet and slippery pitcher mouth (peristome) and never become trapped (Clarke and Kitching 1995). Moreover, they forage for food inside the pitchers. Highly unusually for ants, they are able to dive and swim in the pool of digestive pitcher fluid. On their foraging trips, they repeatedly enter and leave the fluid, apparently unaffected by surface tension forces.

      Несмотря на заметность этого взаимодействия растения и муравья, биомеханические адаптации, позволяющие этому муравью процветать в этих экстремальных условиях обитания, не были исследованы. Here we focus on the ants’ unique swimming behavior. Unlike many aquatic insects, C. schmitzi ants do not possess any apparent morphological adaptations for swimming and they are also very agile runners on land, both suggesting a relatively recent adaptation to the amphibious lifestyle.

      Плавание по поверхности воды как адаптация от случайного падения в воду или для crossing small water bodies has been reported for several ant genera, including Camponotus (DuBois and Jander 1985). While surface-swimming ants generate thrust only by moving their front legs, with the middle and hind legs acting as a rudder at the water surface, the swimming behavior of C. schmitzi ants is different in that it involves movements of all legs under water. Here we report field and laboratory observations on the aquatic foraging behavior of C. schmitzi and present a kinematic analysis of swimming locomotion in comparison with normal (terrestrial) running. We investigate (1) how gait patterns for swimming and running are related to each other and whether a different locomotor program is used for swimming, (2) whether swimming is a special adaptation of C. schmitzi and (3) how swimming ants generate thrust.

     

 
Рис.6. Кинематика локомоции муравья Camponotus schmitzi
(по: ©Bohn & al., 2012)

ДИСКУССИЯ.

      Исследователи обнаружили, что рабочие муравьи C. schmitzi плавают with a stereotyped tripod pattern similar to that used by many insects for running on land (Hughes 1952). However, there were characteristic differences between the leg kinematics of swimming and running in C. schmitzi ants. C. schmitzi ants vary velocity and leg extension between power and return stroke to generate thrust. During the power stroke, the front and middle legs were extended and moved rapidly whereas in the return stroke they moved slower and were held closer to the body. Similar asymmetries between power and return strokes are widespread among swimming animals (Alexander 1982). The hind legs contributed only little to the overall thrust, suggesting that they mainly serve for stabilization and steering.

      В то время, как многие чрезвычайно адаптированные водные насекомые обладают вытянутыми телами и специализированными ногами, приспособленными для гребли, никаких таких морфологических адаптаций не наблюдается у C. schmitzi. However, in the range of low Reynolds numbers relevant for the swimming of C. schmitzi (Re\120), the drag-reducing effect of a streamlined body shape is likely to be small (Vogel 1981).

      Кинематические различия между плаванием и управлением, вероятно, основаны на различных моторных программах ног. Это может частично отражать ограничения различных физических сред. During running, the air allows faster leg protraction than the denser water, but the ground contact constrains the extension of the legs and limits the duty factor in comparison to swimming. Legged locomotion on land often requires that the insect’s center of gravity lies within the tripod of the three legs on the ground (Ting et al. 1994). Static stability in the absence of foot adhesion requires that legs are on the ground for more than half the time, corresponding to a duty factor of at least 0.5. This constraint is relaxed during swimming, where the insect is supported by water, making smaller duty factors possible.

      Кроме возможного прямого влияния физических ограничений, the leg movements are modified for running and swimming in a segment-specific way, leading to characteristic differences in leg orientation, leg extension and duty factor. This indicates that there may indeed be different pattern generators for the different joints of each ant leg, which possess some flexibility and independence, consistent with previous findings on the locomotion and pattern generation in stick insects (BaЁssler and BuЁschges 1998).

      Несмотря на the segment-specific modifications for running and swimming, C. schmitzi ants produce a tripod-like coordination between the legs for both types of locomotion. The motor programme for each individual leg depends on the interaction of central and coordinating influences, as well as peripheral sensory input (providing information about joint positions, movements and loads) (Graham 1985; BaЁssler and BuЁschges 1998; Cruse et al. 2009). The sensory input for legs moving freely in water is obviously very different from that experienced by legs during running. This different sensory input may explain why tethered C. rufifemur ants did not show any coordinated leg movements underwater. The disposition and neuronal ability of C. schmitzi ants to perform coordinated swimming movements without any substrate contact thus appears to be an adaptation to the ants’ amphibious lifestyle. Our experiments also demonstrate that the swimming movements in C. schmitzi can be triggered by submersion. It is unclear whether the ants react to the submersion itself (using mechanical, optical or physiological cues) or whether the higher drag forces acting on the legs provide the necessary sensory input to convert the erratic leg movements performed in air to the coordinated gait underwater.

      Некоторые другие членистоногие показывают различные способы ломоции в/на воде и по земле. The patterns of leg coordination are in most cases different between aquatic/ neustic and terrestrial locomotion [например, водные жуки (Hughes 1958), клопы (Bowdan 1978; Wendler et al. 1985), прямокрылые (Pfluger and Burrows 1978), пауки (Barnes and Barth 1991)]. In some cases, intermediate types of locomotion were found (such as intermediates between walking and rowing in semi-aquatic spiders; Barnes and Barth 1991), again suggesting that the different movement patterns are produced by a flexible system capable of generating variable patterns of motor output.

      Способность быстро плавать даёт возможность муравьям C. schmitzi эксплуатировать содержание питчера (кувшинчика) как полезный источник пищи. The ants not only gain access to freshly captured, struggling arthropods but they even succeed in capturing live pitcher infauna such as rapidly swimming mosquito larvae (Clarke and Kitching 1995).

      Плавательное поведение что авторы наблюдали у муравья C. schmitzi has several similarities to the surface-swimming behavior of other ants, which was described in detail for Camponotus americanus by DuBois and Jander (1985). First, most of the thrust is produced by the front legs while the hind legs move relatively little and are held in a backwards orientation. Second, the front legs are extended during the power stroke and flexed during the return stroke. In contrast to C. americanus, however, C. schmitzi keeps all its legs underwater continuously and both middle and hind legs contribute to swimming by performing rhythmic motions, although their movements are smaller than those of the front legs. Moreover, the swimming movements of C. schmitzi appear to be much faster (step frequency 9.35 Hz in C. schmitzi vs. 1.32 Hz in C. americanus, DuBois and Jander 1985).

      Плавание это сравнительно редкое поведение среди муравьёв, обычно демонстрируемое только отдельными рабочими особями случайно упавшими в воду or when they actively cross small bodies of water (DuBois and Jander 1985). Ant species differ in their readiness to perform such surfaceswimming behavior when dropped into water (W.F., personal observation). One exception in which swimming is part of the normal behavioral repertoire is the specialized mangrove-inhabiting species Polyrhachis sokolova (Nielsen 1997; Attenborough 2005). In all these ants, however, regardless of rarity of the behavior, the hind legs are not submerged during swimming, but remain dewetted at the surface of the water. This, taken together with the 79 greater step frequency in C. schmitzi, indicates a greater degree of specialization for its amphibious lifestyle.

      Таксономия крупного подрода Camponotus-subgenus Colobopsis остаётся неразработанной (Brady et al. 2000) и ни одного близкого родственника у C. schmitzi до сих пор не найдено. Однако, уникальность этой ассоциации между родами Nepenthes и Camponotus показывает, что это сравнительно недавнее эволюционное достижение. This is consistent with our finding that C. schmitzi uses a tripod coordination for swimming, indicating a relatively simple adaptation which may have required short evolutionary periods. It appears that locomotion in water with a coordination between the legs similar to walking and running is common among terrestrial insects that only occasionally swim (Shumakova et al. 2003), whereas many truly aquatic insects have evolved more distinct ‘‘swimming gaits’’ (see overview in Shumakova et al. 2003). It seems plausible that the ancestors of C. schmitzi were able to perform a surface-swimming behavior like C. americanus and that further modifications were brought about by a change in the surface chemistry of the cuticle, making the legs more hydrophilic and allowing them to become submerged. Such a change in surface chemistry would also make it easier for C. schmitzi to enter the digestive fluid when starting to forage inside a pitcher. Indeed, we have preliminary evidence that the cuticle of C. schmitzi is more wettable than that of other Camponotus ants (D.G.T., in preparation).

      Адаптации муравьёв C. schmitzi к жизни в симбиозе с растением N. bicalcarata не ограничивается способностью плавать в пищеварительных растворах его кувшинчиков. C. schmitzi is an obligate plant-ant, и его молодые матки способны в конце брачного полёта определить местонахождение неколонизированных растений и прогрызать отверстие в домациях раздутых усиков-стебельков кувшинчиков (Clarke and Kitching 1995). У C. schmitzi также есть превосходная способность прикрепляться к поверхности перистома питчера-кувшинчика, даже когда она бывает скользкой и влажной (Bohn and Federle 2004). This not only protects them against falling into the pitcher as many other ants but it also allows them to search for prey and infauna in the pitcher’s digestive fluid (Clarke and Kitching 1995). Авторы этой работы в настоящее время исследуют захватывающую биомеханическую адаптацию C. schmitzi в его уникальной экологической нише.

     

Шёл, поскользнулся, упал ... в кувшинчик Непентеса… . (Bohn, 2004)

Составлена первая в мире карта сенсилл усиков у муравьёв.

Myrmica, Formica, Lasius, Pheidole и Camponotus