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Skimming Behaviour and Spreading Potential of Stenus Species and Dianous Coerulescens (Coleoptera: Staphylinidae)

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Skimming Behaviour and Spreading Potential of Stenus Species and Dianous Coerulescens (Coleoptera: Staphylinidae) Naturwissenschaften (2012) 99:937–947 DOI 10.1007/s00114-012-0975-4 ORIGINAL PAPER Skimming behaviour and spreading potential of Stenus species and Dianous coerulescens (Coleoptera: Staphylinidae) Carolin Lang & Karlheinz Seifert & Konrad Dettner Received: 22 June 2012 /Revised: 25 September 2012 /Accepted: 3 October 2012 /Published online: 21 October 2012 # Springer-Verlag Berlin Heidelberg 2012 Abstract Rove beetles of the genus Stenus Latreille and the evolutionary aspects of the Steninae’s pygidial gland secretion genus Dianous Leach possess pygidial glands containing a are discussed. multifunctional secretion of piperidine and pyridine-derived alkaloids as well as several terpenes. One important character Keywords Stenus . Skimming behaviour . Skimming of this secretion is the spreading potential of its different velocity . Spreading potential . Spreading pressure . compounds, stenusine, norstenusine, 3-(2-methyl-1-butenyl)- Evolution pyridine, cicindeloine, α-pinene, 1,8-cineole and 6-methyl- 5-heptene-2-one. The individual secretion composition ena- bles the beetles to skim rapidly and far over the water Introduction surface, even when just a small amount of secretion is emitted. Ethological investigations of several Stenus species In 1774, Franklin (in Gaines 1966) observed first the phe- revealed that the skimming ability, skimming velocity and nomenon of spreading as he put a teaspoon of oil on the the skimming behaviour differ between the Stenus species. water surface of a pond. The ability of the oil to spread on These differences can be linked to varied habitat claims and the water surface forming a thin layer he called “spreading”. secretion saving mechanisms. By means of tensiometer With help of the applied amount of oil and the oil-covered measurements using the pendant drop method, the spreading area of the pond, he estimated that the layer must be pressure of all secretion constituents as well as some naturally monomolecular. identical beetle secretions on the water surface could be estab- Nowadays, spreading is defined generally as the expan- lished. The compound 3-(2-methyl-1-butenyl)pyridine ex- sion of a fluid or solid phase on a fluid surface establishing a celled stenusine believed to date to be mainly responsible for monolayer (Dörfler 1994). However, the phenomenon of skimming relating to its surface activity. The naturally identi- spreading can not only be found in physical chemistry cal secretions are not subject to synergistic effects of the single science of surfaces but also in the great outdoors. Small compounds concerning the spreading potential. Furthermore, staphylinid beetles of the genera Stenus and Dianous use spreading as an effective and extraordinary way of locomo- tion on water surfaces. Communicated by: Sven Thatje Rove beetles of the genera Stenus Latreille and Dianous Leach are small, slender and black insects that predominant- Electronic supplementary material The online version of this article (doi:10.1007/s00114-012-0975-4) contains supplementary material, ly inhabit wet biotopes, e.g. marshes, banks of pools and which is available to authorized users. rivers (Horion 1963; Dettner 1987). The genus Stenus is one of the species-rich genera within the animal kingdom. Till C. Lang (*) : K. Dettner Department of Animal Ecology II, University of Bayreuth, this day, 2,377 species and eight fossil species are known 95440 Bayreuth, Germany worldwide (Puthz 2008). e-mail: [email protected] The direct neighbourhood of open waters in the habitat of most Stenus and Dianous species harbours danger for the K. Seifert Department of Organic Chemistry, University of Bayreuth, beetles. While hunting for springtails, it is possible that the 95440 Bayreuth, Germany hydrophobic beetles accidently fall into water. The unusual 938 Naturwissenschaften (2012) 99:937–947 behaviour of spreading has evolved in these insects as a Jenkins (1960) investigated the spreading behaviour of mechanism to save themselves from drowning and to escape Stenus and Dianous beetles. The spreading action of these predators like water striders (Linsenmair 1963; Schildknecht two genera he named “skimming”.Besides,heobservedthe et al. 1975). For the first time, Piffard (1901) discovered that negative phototactic navigation of Stenus and Dianous on the some species of Stenus beetles are able to move over the water surface towards the dark bank of a pool. The beetles water surface in a rapid and extraordinary manner. At this, waste no time to achieve the save waterside. Schildknecht et the beetle glides on the water with high velocity without al. (1975) found that a secretion of the pygidial glands in the using its legs. A few years later, Billard and Bruyant (1905) anal region is responsible for the skimming action (Fig. 2). observed this locomotion in Stenus tarsalis Ljungh and The secretion is emitted by the everted glands as soon as the Stenus cicindeloides Schaller. They report an emission of beetle contacts the water surface and spreads on the water chemicals that interact with the water surface like a surfac- surface immediately. tant and propel the beetle fast forward comparable to a “soap The gland compounds form a monomolecular film whose boat” (Fig. 1). This locomotion is driven by the marangoni front pushes the beetle forward (Dettner 1991). By this kind propulsion (Scriven and Sternling 1960). Marangoni flows of locomotion, e.g. Stenus comma can achieve a velocity of are those forced by surface tension gradients. Surfactants 0.75 ms−1, and if the secretion is continuous, a distance up like soap and the emitted substances of the beetles are to 15 m can be covered (Linsenmair and Jander 1963). Apart molecules that find it energetically favourable to reside at from Stenus and Dianous beetles, the extraordinary move- the free surface and act to decrease the local surface tension ment is just shown by the water cricket Velia caprai Tam- (Bush and Hu 2006). anini, which uses its rostrum and as well spreading active salvia for skimming (Linsenmair and Jander 1963). No other animal is known to have this unique kind of locomotion. The driving force for skimming is the spreading potential of the gland compounds. Thereby, it is essential that the gland compounds are barely soluble in water; otherwise, it is not possible to form a monolayer. Additionally, the spread- ing agent has to exhibit a lower surface tension than the layer-carrying substance which is water in case of Stenus and Dianous (Adamson and Gast 1997). Schildknecht (1976) discovered that the Stenus secretion consists of several different compounds. Stenusine (1)is Fig. 1 Skimming procedure of Stenus comma. a Fallen on the water Fig. 2 Pygidial gland system of Stenus comma. Left side the pair of surface, the beetle is carried by the surface tension due to the hydro- pygidial glands is arranged in the abdominal tip. Right side schematic phobicity of its tarsi. b The beetle bends its abdomen and emits a small diagram of the paired pygidial glands in detail. r1 big reservoir, s1 amount of its gland secretion on the water surface. c Lying flat on the secretory cells associated to r1, r2 small reservoir, s2 secretory cells water surface due to reduction of surface tension, the beetle is pro- associated to s2, rm retractor muscle of eversible membrane parts, a1 pelled fast forward by the spreading agents in its secretion. Middle and and a2 apodemes on which retractor muscles insert, em eversible hind legs are held close to the body. The skimming direction can be membrane parts forming basal pouches; from Szujecki 1961, Whitman changed by bending the abdomen et al. 1990 and Schierling unpublished, modified Naturwissenschaften (2012) 99:937–947 939 mainly responsible for skimming because it is featured by known secretion compounds (1–7) are synthetically available, the highest spreading pressure and therefore lowers the it is first possible to measure the spreading potentials of all surface tension of water the most compared with 1,8-cineole known compounds. Over and above, we mixed artificially (6) and 6-methyl-5-heptene-2-one (7) (Schildknecht et al. natural identical secretions of some Stenus species to prove 1976). Besides, 1 forms the main component of the secre- their surface activity. tion of most Stenus species. In the course of time, many more gland compounds were identified characterizing the gland content (Fig. 3). The alkaloids 1 (Schildknecht et al. Materials and methods 1975) and norstenusine (2) (Kohler 1979), the pyridine compound 3-(2-methyl-1-butenyl)pyridine (3)(Lusebrink Collection, determination and keeping of the beetles et al. 2009) and the epoxypiperideine cicindeloine (4) (Müller et al. 2012) are stored in the big reservoirs, The Stenus beetles were collected in summer 2011 at a moun- whereas the terpenoids α-pinene (5)(Neumann1993), tain stream in the Black Forest,Germany,nearBaiersbronn 6 and 7 (Schildknecht 1970) are provided in the small (48°51′00″N; 8°31′41″E; collected species: D. coerulescens, reservoirs (Fig. 2). Stenus stigmula) and at a lakeside near Creußen, Germany The spreading pressures of the compounds can be mea- (49°52′17″N; 11°36′40″E; collected species: see all species sured experimentally for instance at an interfacial tensiom- except of D. coerulescens and S. stigmula listed in Table 1). eter (Schildknecht et al. 1976). After the measurement of the The small lake features a large marshy accretion zone with surface tension σ of the compounds against air and the plant debris. After collection, the beetles were identified by interfacial tension γ against water, the spreading pressure using the key of Lohse (1964), the additions of Lohse (1989) P can be calculated according to the following equation and additionally the new identification key of Puthz (2001, defined by Wolf (1957) 2008). After determination, the beetles were kept in Petri dishes on moist gypsum mixed with activated charcoal to prevent ¼ σ À σ þ ð Þ P water substance gsubstance= water 1 mould formation and to provide enough moisture.
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