See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/337854621 Physical Determinants of Fluid-Feeding in Insects Chapter · December 2019 DOI: 10.1007/978-3-030-29654-4_8 CITATIONS READS 0 33 2 authors, including: Konstantin G Kornev Clemson University 161 PUBLICATIONS 1,951 CITATIONS SEE PROFILE All content following this page was uploaded by Konstantin G Kornev on 16 December 2019. The user has requested enhancement of the downloaded file. Chapter 8 Physical determinants of fluid feeding in insects Konstantin G. Kornev1 and Peter H. Adler2 1. Corresponding author: Konstantin G. Kornev, Department of Materials Science and Engineering, Clemson University, Clemson, South Carolina, 29634, USA, e-mail: [email protected] 2. Department of Plant and Environmental Sciences, Clemson University, Clemson, South Carolina, 29634, USA e-mail: [email protected] Abstract Fluid feeders represent more than half of the world’s insect species. We review current understanding of the physics of fluid feeding, from the perspective of wetting, capillarity, and fluid mechanics. We feature butterflies and moths (Lepidoptera) as representative fluid-feeding insects. Fluid uptake by live butterflies is experimentally explained based on X-ray imaging and high-speed optical microscopy, and is augmented by modeling and by mechanical and physicochemical characterization of biomaterials. Wetting properties of the lepidopteran proboscis are reviewed, and a classification of proboscis morphology and wetting characteristics is proposed. The porous and fibrous structure of the mouthparts is important in determining the dietary habits of fluid-feeding insects. The fluid mechanics of liquid uptake by insects cannot be explained by a simple Hagen-Poiseuille flow scenario of a drinking- straw model. Fluid-feeding insects expend muscular energy in moving fluid through the proboscis or through the sucking pump, depending primarily on the ratio of the proboscis length to the food-canal diameter. A general four-step model of fluid feeding is proposed, which involves wetting, dewetting, absorbing, and pumping. The physics of fluid feeding is important for understanding the evolution of sucking mouthparts and, consequently, insect diversification through development of new fluid-feeding habits. 1 1. Introduction The success of fluid-feeding insects on our “buggy” planet is unprecedented; more than half of all known insects on Earth—over 500,000 species—are fluid feeders (Grimaldi and Engel, 2005, Adler and Foottit 2009, Shaw, 2014). For about 300 million years, insects that feed on fluids have used unique feeding devices, termed “proboscises” to acquire water and nutriment ( Kingsolver and Daniel, 1995, Chapman, 2013). Anatomical features of the proboscis are detailed in Chapt. 3. Fluid feeders have evolved to exploit a remarkable diversity of food resources including nectar, phloem, and xylem of plants, and blood, carrion, dung, sweat, tears, and urine of animals (Labandeira, 1997, 2010, Misof et al., 2014). Lepidoptera provide many examples of opportunistic fluid feeding (Fig. 1). Feeding devices of insects have been popular evolutionary subjects since Charles Darwin predicted that a sphinx moth with a 30-cm long proboscis feeds from the long nectar spur of the orchid Angraecum sesquipedale ( Darwin, 1904, Arditti et al., 2012). Among the most attractive and demanding areas of research are the evolution and diversification of insect feeding organs within the context of their morphology, materials properties, and functional performance (Russell, 1916, Lauder, 2003, Krenn and Aspöck, 2012). Fig. 1. Lepidoptera feeding opportunistically from various substrates in Peru, Madre de Dios Region, Las Piedras, ca. 235–275 m above sea level. A. Euselasia sp. (Riodinidae) probing beneath the margin of a fingernail. B. Heliconius sp. gathering pollen on its proboscis from a species of Passiflora. C. Euselasia toppini (Riodinidae) probing on a leaf of the palm Geonoma sp. D. Syllectra sp. (Erebidae; identified by P.Z. Goldstein) probing on drying laundry at night. E. Ithomia lichyi (Nymphalidae) feeding on a dead caterpillar; a bead of saliva is present proximal to the “knee” bend. F. The skipper Tarsoctenus papias (Hesperiidae) feeding on antbird droppings near an army ant raid. Photos courtesy of Allison Stoiser. The feeding devices of all fluid-feeding insects consist of a proboscis paired with a sucking pump. The geometry of sucking pumps is complex and many details are poorly understood (Bennet-Clark, 1963, Davis and Hildebrand, 2006, Bauder et al., 2013, Karolyi et al., 2013, 2014,). The sucking pump, the proboscis, and their geometries exhibit a range of sizes, as represented by a selection of eight species with proboscises ranging from 0.3 mm to about 70 mm long (Table 1). Although the pump of these species is sizable relative to the head, the proboscis length varies greatly. Accordingly, the ratio of maximum size of the pump chamber to proboscis length 2 changes from infinity to zero, suggesting that the mechanism of energy dissipation changes from one species to another. Table 1. Characteristics of the proboscis and sucking pump of selected fluid-feeding insects. Species Proboscis Food canal Pump Pump Pump dp /L b c d length, 푳풑 diameter, dp length , L width , height , (mm) (µm) (µm) W(µm) ℎ (µm) Acherontia 10.1 494.6 2417.6 2030.3 765.9 0.2 atroposa Danaus 14.4 35.0 886.2 606.3 145.6 0.03 plexippuse Manduca sextae 50–70 82.5 1834.5 2272.2 1227.4 0.04 Nadata gibosa 3.58 25.4 598.3 362.8 240.4 0.04 Symmerista 0.35 17.3 298.8 358.8 91.0 0.12 albifronsf Rhodnius 5.2 8-10 3000–5000 280 160 0.02– prolixusg 0.03 Pediculus 0.4(f) 7.2 (f) 50(f) 50(f) 30(f) 0.14(f) humanush 0.4(m) 6.8(m) 43(m) 43(m) 30(m) 0.17(m) Cimex 1.23(f) 16(f) 134(f) 134(f) 75(f) 0.12(f) lectulariush 1.00(m) 14(m) 114(m) 114(m) 75(m) 0.12(m) a Data from figs. 2D, E in Brehm et al. (2015). b Longest distance within the chamber, parallel to the floor of the pump. c Greatest width within the chamber, perpendicular to the length of the pump chamber. d Greatest height, dorsal to ventral, along the mid-sagittal plane and perpendicular to the length of the pump. e Proboscis lengths for D. plexippus and M. sexta and food canal diameter for D. plexippus are from Campos et al. (2015) and Lehnert et al. (2016). f Diameter of the food canal of a single galea. The two galeae do not meet; therefore, a single food canal is not formed; the food canal is assumed to be circular. gData from Bennet-Clark (1963). h Data from Tawfik (1968); f-female, m-male. Pump height is interpreted as the “travel of diaphragm” values in this reference; the pump is considered a cylinder. Proboscises of fluid-feeding insects, such as butterflies, moths, house flies, and mosquitoes, have multiple functions enabling them to access floral nectaries, mop up liquid films and droplets, and pierce plant and animal tissues. Topographically sculptured surfaces, together with a fibrous and porous structure, are critical for multifunctionality of proboscises (Snodgrass, 1935, Schmitt, 1938, Eastham and Eassa, 1955, Hepburn, 1971,1985, Harder, 1986, Cheer and Koehl, 1987, Hainsworth et al., 1991, Koehl, 2001, Corbet, 2000, Krenn, 2010, Monaenkova et al., 2012, Abou-Shaara, 2014, Tsai et al., 2014, Chen et al., 2015, Zhu et al., 2016b). This architecture offers a large surface area, suggesting that capillary and wetting forces, which pull water into a dry sponge, should also play an integral role in the fluid uptake strategies of sucking insects. Insect evolution has involved increases and decreases of organ size (Rensch, 1948, McMahon and Bonner, 1983, Hanken and Wake, 1993, Shaw, 2014, Polilov, 2015). Accordingly, feeding devices of insects exhibit a broad range of sizes, from extremely small in insects such as aphids ( Barber, 1924, Auclair, 1963) to extraordinarily long in some sphinx moths (Arditti et al., 2012). Different behavioral strategies and physical and materials organization of the feeding devices are associated with this large size range. 3 The proboscis of fluid-feeding insects differs structurally among species. For example, the butterfly proboscis consists of two elongated components (i.e., galeae), joined together by linking mechanisms made of fence-like structures (Fig. 2, and Chapt. 3). Fluid is transported through a food canal between the galeae (Eastham and Eassa, 1955, Krenn, 2010). The proboscises of bees, house flies, and mosquitoes have different structure, often independently evolved, implying that different physical mechanisms for fluid uptake and transport might be involved (Smith, 1985, Kingsolver and Daniel, 1995, Kim and Bush, 2012). Yet, the feeding efficiency for all proboscises is remarkably high. We suggest that common principles of fluid uptake can explain the structure and function of mouthparts across fluid-feeding insect groups. The proboscises of fluid feeders, for example, share a ground plan of their materials organization: the drinking regions are fibrous and porous, pointing to the importance of capillary and wetting forces in the feeding strategies of all fluid-feeding insects (Monaenkova et al., 2012). We focus on the lepidopteran proboscis as a model to explore the physical aspects and constraints of fluid-feeding in insects. Fig. 2. Photomicrographs of butterfly proboscises (SEM). (A) Coiled proboscis of the tiger swallowtail (Papilio glaucus). (B) Cross-section of the proboscis of the monarch butterfly (Danaus plexippus) with a circular hole, the food canal, formed by the two halves (galeae). The top and bottom fence-like structures (legulae) link the two galeae together. (C) A single galea of the monarch butterfly resembles a C-shaped fiber with a semicircular C-channel, which, when united with the other half, forms a food canal (Reproduced by SPIE permission from Kornev et al., 2016).