Spider Physiology and Behaviour by Jerome Casas


51Jk7EGWw1L._SY291_BO1204203200_QL40_.jpg Author Jerome Casas
Isbn 9780124159198
File size 3MB
Year 2011
Pages 288
Language English
File format PDF
Category animals



 

Contributors Ingi Agnarsson Department of Biology, University of Puerto Rico, San Juan, Puerto Rico, USA Maydianne C. B. Andrade Integrative Behaviour and Neuroscience Group, University of Toronto Scarborough, Toronto, Ontario, Canada Todd A. Blackledge Department of Biology and Integrated Bioscience Program, The University of Akron, Akron, Ohio, USA Fiona R. Cross School of Biological Sciences, University of Canterbury, Christchurch, New Zealand; and International Centre of Insect Physiology and Ecology (ICIPE), Thomas Odhiambo Campus, Mbita Point, Kenya Damian O. Elias Department of Environmental Science, Policy and Management, University of California, Berkeley, California, USA Eileen A. Hebets School of Biological Sciences, University of Nebraska-Lincoln, Lincoln NE, USA Robert R. Jackson School of Biological Sciences, University of Canterbury, Christchurch, New Zealand; and International Centre of Insect Physiology and Ecology (ICIPE), Thomas Odhiambo Campus, Mbita Point, Kenya Michael M. Kasumovic Evolution & Ecology Research Centre, School of Biological, Earth, and Environmental Sciences, The University of New South Wales, Sydney, New South Wales, Australia viii CONTRIBUTORS Matjazˇ Kuntner Institute of Biology, Scientific Research Centre, Slovenian Academy of Sciences and Arts, Ljubljana, Slovenia Roger D. Santer Institute of Biological, Environmental and Rural Sciences, Aberystwyth University, Aberystwyth, United Kingdom Preface The year 2011 is a record year for the number of books devoted to spiders: the third edition of the introduction Biology of Spiders by Rainer F. Foelix and an edited book by Marie E. Herberstein Spider Behaviour were both published in the first half of this year. The present two volumes of Spider Physiology and Behaviour, totalling over 550 pages, target a somewhat more specialized public and complement nicely the above works as well as the volumes edited in the 1980s by Wolfgang Nentwig (1987), Ecophysiology of Spiders, and Friedrich G. Barth (1985), Spider Neurobiology. The gap of over 20 years between these publications was a period of intensified research on this group of organisms, interspersed by the rare publication of books and monographs, in particular, F. G. Barth’s A Spider’s World: Senses and Behaviour (2002). A similar trend for several other groups of Arachnids can be observed. The titles of these publications hint at one of the most fascinating aspect of spiders: their behaviour, its physiological basis, including the neurobiological components, and its consequences, including web construction. This fascination partly explains why many behavioural ecologists use spiders and why these arachnids became an accepted model of choice. These are relatively new trends of the past 20 years or so. Spider silk continued to raise sustained interest from a somewhat different group, in particular, from the material science quarters. The final chapter of the second volume Spider Physiology and Behaviour: Behaviour blends the two approaches of evolutionary biology and material sciences in the study of webs. This rise of spiders as studied organisms and their secured place in the pool of accepted models is highly positive, not only in terms of visibility by the notso-large community of scientists working with them but also in terms of attraction for students and of acceptance by the much larger community of ecologists: the role of spiders in nutrients flow and ecosystem services is large but under-appreciated. The planning of these two volumes identified other trends in need of attention. First, several chapters in the two edited books of the 1980s have no modern counterpart, not because the topics are out of fashion but because the expertise is lacking, worldwide, or because the field came to a full standstill. Second, the pool of tenured scientists working on these organisms is steady in comparison with other fast growing fields, with some variation between countries, if not continents. Thus, the increased visibility of spiders in mainstream journals is potentially the result of a mechanism by which a new x PREFACE generation of behavioural ecologists is replacing an older generation of physiologists and neuroethologists: more generic approaches to older problems, new journals, and an increased level of assertiveness are among the hallmarks of this evolution. Finally, because behavioural ecologists make up a good portion of the most active community of scientists working on spiders, enhanced attention must be given to processes at the physiological and cellular levels. Indeed, most behavioural ecologists are poorly knowledgeable in these matters and may underestimate their interest and complexity. I hope that the volumes in this series, in particular, the first volume of this set, contribute to their education. The splitting of a continuum from the cell to the organism is by definition arbitrary. A quick glance at the tables of contents shows that these two volumes constitute a set, not two independent books. Each chapter has been thoroughly checked by two external referees. I thank them and the authors for producing such a compelling body of knowledge. JE´ROˆME CASAS The Sensory and Behavioural Biology of Whip Spiders (Arachnida, Amblypygi) Roger D. Santer* and Eileen A. Hebets† *Institute of Biological, Environmental and Rural Sciences, Aberystwyth University, Aberystwyth, United Kingdom † School of Biological Sciences, University of Nebraska-Lincoln, Lincoln NE, USA 1 Introduction 2 2 Whip spider sensory biology 5 2.1 The antenniform legs 5 2.2 Sensory structures on other areas of the body 31 2.3 Integration of sensory information: the mushroom bodies 35 3 Whip spider behavioural biology 36 3.1 Escape and avoidance behaviours 36 3.2 Prey capture 39 3.3 Intraspecific communication 44 3.4 Sensory guidance of movement 51 3.5 Complex behaviour: sociality and individual recognition 55 4 Conclusions 57 Acknowledgements 59 References 59 Abstract Whip spiders (Arachnida, Amblypygi) comprise a small and little-studied arachnid order. They have elongated antenniform forelegs which function in a sensory capacity and are not used for locomotion. These antenniform legs are covered in large numbers of chemoand mechanosensory sensilla, and others of unknown function. The antenniform legs also contain an array of first and second order giant neurons that carry information rapidly from some of these sensilla to the central nervous system. In addition, whip spiders possess large and well-developed mushroom bodies, brain neuropils that have been associated with complex behaviour such as learning and memory in insects. In searching for the behavioural role of these and other sensory specialisations, we are slowly gaining insights into the sensory guidance of escape, prey capture, orientation, and communication behaviours in these remarkable arachnids. Here, we aim to consolidate this information and to assemble an accessible picture of the sensory and behavioural biology of this order. ADVANCES IN INSECT PHYSIOLOGY VOL. 41 ISBN 978-0-12-415919-8 DOI: 10.1016/B978-0-12-415919-8.00001-X Copyright # 2011 by Elsevier Ltd All rights of reproduction in any form reserved 2 1 ROGER D. SANTER AND EILEEN A. HEBETS Introduction Our knowledge of arachnid physiology and behaviour varies tremendously across orders. While much is now known with respect to the Acari and Araneae (e.g. see Barth, 2002 and chapters in this volume), we know less about the Scorpiones, and much less still about the Amblypygi, Schizomida, Thelyphonida, Ricinulei, Pseudoscorpiones, Opiliones, Palpigradi, and Solifugae (e.g. see Beccaloni, 2009). In this chapter, our focus is on the Amblypygi, commonly known as whip spiders. We hope to demonstrate that although many aspects of their sensory and behavioural biology are shared with their better-known cousins, there is much about them that is unique. Here, we hope to motivate neuroethological investigation of this lesser-known arachnid order, and to share something of the appeal that drew us to begin our own investigations. The Amblypygi belong to the Tetrapulmonata, an arachnid clade that also includes three other extant orders: Thelyphonida (whip scorpions), Schizomida (short-tailed whip scorpions), and Araneae (spiders) (Dunlop, 2010; Shultz, 2007). As in spiders, the body of whip spiders is divided into a prosoma ( cephalothorax) and an opisthosoma ( abdomen), separated by a narrow waist called a pedicel. Whip spiders also share with spiders a prosomal sucking stomach and some genital and sperm characteristics (e.g. Dunlop, 2010). On this basis, some authors have grouped the Amblypygi with the Araneae under the name Labellata, although this is not supported by the most recent studies (see Dunlop, 2010; Shultz, 2007; Weygoldt, 2000). Whip spiders possess neither the spinnerets nor venom glands of spiders (Weygoldt, 2000). Phylogenetic studies most commonly group whip spiders with the Uropygi (comprising Thelyphonida and Schizomida) within the Pedipalpi clade (e.g. Dunlop, 2010; Fahrein et al., 2009; Shultz, 2007). Within this clade, the pedipalps are raptorial. Furthermore, only the rearmost three pairs of legs are used in walking and the first pair has evolved into thin and elongated mechanoand chemosensory feelers. In whip spiders, these ‘antenniform legs’ (sometimes called ‘whips’) are so long that they can be 2.5 or more times the length of the walking legs (Fig. 1) and, in some large neotropical species, can have a span of nearly 60 cm (Foelix and Hebets, 2001). They are an incredible example of convergent evolution with the antennae of insects. In contrast to whip scorpions, whip spiders have no flagellum, which is why they are sometimes given the common name ‘tailless whip scorpions’ (Weygoldt, 2000). Whip spiders differ from both whip scorpions and spiders in being dorsoventrally flattened, which enables them to scuttle into narrow crevices, and by a reduction of the patellae of the legs, which are the breaking points for autotomy (a property that has pros and cons from the point of view of the experimentalist) (Weygoldt, 2000). The Amblypygi are a small order. A recent count identified 158 recognised species, divided into 17 genera and 5 families—a very small number in comparison to the 42,055 species, 3821 genera, and 110 families of Araneae THE SENSORY AND BEHAVIOURAL BIOLOGY OF WHIP SPIDERS 3 FIG. 1 The basic anatomy of a whip spider. The species shown is Phrynus marginemaculatus, a species found in the south-eastern USA and on Caribbean islands. In this species, the carapace of a large male has a width of approximately 8 mm. Note the presence of spiny, raptorial pedipalps, and hugely elongated ‘antenniform’ forelegs which are used as sensory structures and not for locomotion. recognised at the time of writing (Harvey, 2007; Platnick, 2011). The oldest fossils that can be firmly identified as whip spiders come from the late Carboniferous period (Dunlop, 2010). These fossils resemble the most basal extant species, Paracharon caecus, which has short pedipalps that articulate up and down rather than side to side like the more modern species (Dunlop, 2010; Weygoldt, 2000). This single extant species and those identified from Carboniferous fossils were grouped into the suborder Palaeoamblypygi (Weygoldt, 1996, 2000). A second suborder, Euamblypygi, comprises the more modern whip spiders, and within this, fossils from the early Cretaceous period have been assigned to the family Phrynidae, and two to the living genus Phrynus (Dunlop, 2010; Weygoldt, 1996, 2000). Whip spiders generally inhabit the tropics and sub-tropics, with a few species found in almost temperate zones, but none in regions that experience extreme cold or snow (Weygoldt, 2000). Whip spiders are not normally found in deserts, but Damon variegatus can be found in savannah-like habitats, hiding under rocks or in caves (Weygoldt, 2000), and Phrynus neomexicanus can be found in the Sonoran desert of the southern USA (Hebets, personal observation). Most whip spider species inhabit rainforests (Weygoldt, 2000). Species smaller in size tend to be found within the leaf litter, whereas the larger-bodied species (including neotropical Heterophrynus and Phrynus species which will feature heavily in this review) are found on large trees and rocky outcrops (Weygoldt, 2000). These larger species tend to prefer big trees with buttress roots (Dias and Machado, 2006; Hebets, 2002), which means that for large species like Heterophrynus longicornis, selective logging and general habitat destruction are a serious issue 4 ROGER D. SANTER AND EILEEN A. HEBETS (Dias and Machado, 2006). Most species appear to be strictly nocturnal, spending the day hidden away deep within buttress roots, in burrows, or under bark, and emerging to sit and wait for prey after dark (Hebets, 2002; Weygoldt, 2000). Our own experimental species, Phrynus marginemaculatus, can be found under limestone rocks in the pine hammock of the south-eastern USA and on Caribbean islands. Remarkably, this species can breathe under water by use of a plastron (Hebets and Chapman, 2000b), an ability that no doubt helps it to persist in these frequently inundated habitats. Weygoldt (2000) reports that many rainforest species will readily inhabit caves. For example, in Kenya, Damon diadema can be found both in coastal caves and the surrounding forest (Weygoldt, 2000). However, there are also species that have become adapted to life in caves and are found only in these habitats (e.g. Baptista and Giupponi, 2002, 2003). These may lack medial or lateral eyes (or both), but their physiology and behaviour are not yet well studied. Given that populations of some species appear to be confined to caves, whereas others are found in nearby forests, comparative studies could provide useful insights into physiological adaptations to cave living. In this review we are primarily concerned with the fascinating sensory and behavioural biology of these ancient arachnids. Before delving into this, however, we must address two important issues. Firstly, there is some confusion regarding species nomenclature. For example, much early physiological work was carried out on ‘Admetus pumilio’, a no longer recognised species that is now divided into Heterophrynus batesii and H. longicornis (Weygoldt, 1974; as described in Harvey, 2003). As such, the authors of some early physiological work state that their studies may have been conducted on representatives of both species (e.g. Foelix and Troyer, 1980; Foelix et al., 1975), but the impression from subsequent work is that the likely species identification is H. longicornis (e.g. Beck et al., 1977; Foelix and Hebets, 2001; Foelix et al., 2002; Igelmund, 1987). Here, we will follow the identifications in the original publications unless a more accurate alternative is clearly indicated. Secondly, a large volume of early literature on whip spiders was published in the German language, and is sadly not easily accessible to many. In both cases we direct readers to Peter Weygoldt’s recent volume (Weygoldt, 2000) and, for coverage of the German language work, to the review of Foelix and Hebets (2001). Our aims in this chapter are to complement these works by providing an updated review of whip spider sensory physiology and its role in behaviour, with the hope that we will contribute to an emerging accessible picture of this order that will motivate future research. Our review will broadly be divided into two sections: firstly, an account of whip spider sensory biology (Section 2), followed by a description of the state of knowledge on the roles of these adaptations in the guidance of behaviour (Section 3). We will finish by attempting to draw some general conclusions and highlighting important areas for future study (Section 4). THE SENSORY AND BEHAVIOURAL BIOLOGY OF WHIP SPIDERS 2 5 Whip spider sensory biology We will begin our account of whip spider sensory biology by describing their antenniform forelegs and the sensory structures found upon them. We will also review a number of careful and important studies describing the electrophysiology of these limbs, and in particular, the unusual giant neurons that carry information from the antenniform leg sensilla to the central nervous system. To complete our account of sensory biology, we will describe the other sensory structures of the body, which we are now finding to be almost as fascinating and behaviourally significant as the antenniform legs themselves. 2.1 THE ANTENNIFORM LEGS An alert whip spider’s antenniform legs are almost constantly in motion, gently probing and examining its environment with what appear to be very deliberate and precise movements. During locomotion, the antenniform legs are extended forwards and slightly to the sides and are used to ‘scan’ the environment in front of the whip spider—interestingly, a cockroach uses its antennae in a broadly similar way (e.g. Baba et al., 2010), and when walking in complete darkness, the wandering spider Cupiennius salei (whose first legs are not specialised like those of whip spiders), switches to a gait where it can also use its forelegs as feelers (Schmid, 1997). Weygoldt (2000) suggests that the antenniform legs of whip spiders are the ‘most important sensory structures’ for spatial orientation. Anyone who has spent time observing a whip spider would be tempted to conclude the same, but we must not underestimate the importance of the other sensory structures since studies in insects and arachnids have revealed that behaviour can sometimes be guided by unexpected sensory organs (such as visual navigation under extreme low light conditions, Nrgaard et al., 2008; Warrant et al., 2004). Nevertheless, there can be no doubt that the antenniform legs play an important role in whip spider behaviour. The morphology of the antenniform legs has been most thoroughly investigated in the large South American species H. longicornis, H. batesii, and Heterophrynus elaphus (Beck et al., 1977; Foelix and Troyer, 1980; Foelix et al., 1975; Igelmund, 1987). In H. elaphus, the antenniform legs are approximately 2.5 times the length of the walking legs and can be 26 cm long in adults (Igelmund, 1987). In this species, the tarsus and tibia are each around 10 cm in length and are divided into segments (sometimes called ‘articles’ or ‘annuli’) (Igelmund, 1987). In adults, the tarsus has 74 segments, which tend to increase in length proximally (except for the most distal segment which is long), and the tibia has 33 segments (Igelmund, 1987). By convention, antenniform leg segments are numbered from most distal to most proximal within each leg region. Prenymph whip spiders (first instars that cling to their mother’s back, also called ‘praenymphae’) possess the full number of tibial, but not tarsal, segments 6 ROGER D. SANTER AND EILEEN A. HEBETS (Igelmund, 1987). They attain the full number of tarsal segments at the moult to the first free nymph stage (second instars that leave the mother’s back, also called ‘protonymphae’), after which antenniform leg growth occurs due to lengthening of these segments (Igelmund, 1987). If an antenniform leg is damaged or trapped, autotomy occurs at the patella-tibia joint—the same is true for the walking legs. Regeneration occurs at the next moult (Igelmund, 1987), which can be brought on precociously (even adults moult, especially following damage, which is another unusual feature of whip spiders, e.g. Weygoldt, 1995). However, regenerated antenniform legs differ considerably from the originals. In a newly regenerated antenniform leg of H. elaphus, the tarsus and tibia are normally only two thirds as long as they were in the original limb, but the tarsus has 30% more segments, and the tibia 60% more segments, all much shorter than the originals and varying unsystematically in length (Igelmund, 1987). Regenerated segments get longer at future moults (Igelmund, 1987). The antenniform legs are highly mobile structures. This is especially true for the multi-segmented tarsus which has a remarkable range of movement due to flexion at each of its articulations along many possible planes. The tarsus has a prominent site of bending (equivalent to an intra-tarsal joint, Weygoldt, 2000), which is located towards the middle of the tarsus in some smaller species such as P. marginemaculatus, but much more distally in larger ones such as H. elaphus (our Fig. 1; see also Fig. 1 of Igelmund and Wendler, 1991a). The outer diameter of the tarsus in H. elaphus is greater than 300 mm proximally, but tapers down to around 180 mm distally (Igelmund and Wendler, 1991a). Cross sections of the tarsus reveal a ventral blood vessel, dorsal and ventral tendons, and two tarsal nerves inside the central lumen (Fig. 2; Igelmund and Wendler, 1991a; Spence and Hebets, 2006). In spiders, dorsal and ventral tendons raise and lower the claws, but in whip spider antenniform legs the terminal claws are much reduced, so the tendons may be involved in flexing the long tarsus in response to contraction of muscles at the tibia-tarsus joint (the tarsus itself has no internal musculature) (e.g. Beck et al., 1977 as cited in Foelix and Hebets, 2001; Igelmund and Wendler, 1991a). The anterior tarsal nerve is named N1 and the posterior N2 (Fig. 2). The axons within these nerves are presumed to be almost entirely sensory afferents (carrying impulses to the central nervous system), because the tarsus has no musculature, but does have a number of glands (Fig. 2) and many sensilla, that might be innervated (e.g. Foelix, 1975). The sensory role of the antenniform legs is clearly apparent when they are examined under the microscope. The antenniform leg tarsus is covered by a variety of sensilla, the majority of which can be found on the most distal 20 segments. Although observations have been made in a number of species, systematic SEM and TEM analyses were first conducted on specimens of H. longicornis and H. batesii (Beck et al., 1977 as cited in Igelmund, 1987; Foelix et al., 1975). A subsequent SEM analysis was carried out of H. elaphus, but internal sensillar anatomy was found to be largely identical to H. longicornis and H. batesii, with variation apparent in the positioning of some sensilla and THE SENSORY AND BEHAVIOURAL BIOLOGY OF WHIP SPIDERS 7 C G H T L N2 N1 BV T Dors. 100 µm Post. Ant. Vent. FIG. 2 The internal anatomy of the antenniform leg tarsus of Heterophrynus elaphus, shown in cross section at segment S72, two segments distal to the tibia-tarsus joint. The tarsus has no musculature, but has dorsal and ventral tendons, T, attaching to a much reduced set of terminal claws on segment S1. The tendons are thought to control movements of the tarsus somewhat like a pair of reins (e.g. Foelix and Hebets, 2001). A blood vessel, BV, supplies haemolymph to the distal tarsus, and this is returned to proximal regions through the central lumen, L. Within the tarsus are an anterior, N1, and posterior, N2, nerve (note large diameter axons within each nerve, and especially evident in the upper right-hand quadrant of N1). Also labelled are: C, cuticle; H, hypodermal tissue; and G, a gland opening. After Igelmund and Wendler (1991a, Fig. 3b in p. 66). With kind permission from Springer Science þ Business Media: Journal of Comparative Physiology A, The giant fiber system in the forelegs (whips) of the whip spider Heterophrynus elaphus Pocock (Arachnida: Amblypygi), vol. 168, 1991, p. 66, Igelmund, P. and Wendler, G., Fig. 3b. the absence of one type from H. longicornis and H. batesii (Section 2.1.1.2) (Igelmund, 1987). Together, these studies reveal seven morphological types of sensory hairs on the antenniform leg tarsus, plus a set of modified terminal claws, a pit organ, and a plate organ (Igelmund, 1987). Trichobothria are not found on the antenniform leg tarsus, but are found on the tibia (Igelmund, 1987). Since sensillar morphology is largely identical between the Heterophrynus species studied in detail, here, we provide a general description of the sensilla for this beststudied genus and identify inter-specific variation in sensillum position where it has been described. A detailed systematic study of inter-species differences in sensillar occurrence and anatomy should certainly be an aim of future work. 2.1.1 ‘Hair’-type sensilla 2.1.1.1. Bristle sensilla Bristle sensilla are the longest and most numerous sensilla on all segments of the antenniform leg tarsus (Table 1; Fig. 3A, B, and D); they are also abundant on the tibia and femur (Foelix et al., 1975; Igelmund, TABLE 1 Hair-like sensilla on the antenniform leg tarsus of Heterophrynus whip spiders Sensillum Location Number Length (mm) Diameter (at base, mm) Bristles Abundant on all segmentsa,b  1700a 200–1000a Leaflike sensilla S22–S72, regularly arrangeda (in H. elaphus only) 23a 600a 400–500 Comprising both typesc 100–150a Porous sensilla Type 1 S1–S19, most dense distallya Type 2 S1–S19, most dense distallya 100–150a Base Pores 10–15,a tapered distally 30,a Flattened distally into cuticular blade Articulateda,b Terminal pore onlya,b Articulateda Terminal pore only 6,a Tapered distally 6,a Tapered distally Fixeda,b ˚ Diameter, 400 A 20 pores/mm2;b ˚ Diameter, 7 200 A pores/mm2;b Fixeda,b Presumed modality of sensation Chemosensory (contact), mechanosensory Mechanosensory Chemosensory (olfactory) Chemosensory (olfactory) Club sensilla Rod sensilla Shorter type Longer type S1–16, Most dense distallya 500a 20–25a 4,a Widening distally into ‘club’ Fixeda,b Terminal pore, (tiny wall pores?)b Chemosensory (?) Variable, mostly distal to S3, some S8-S12 Variable, mostly distal to S3 Variable 20–25a 4–5,a Uniform diameter Fixeda,b Terminal pore onlya,b Unknown Variable 50–70a 4–5,a Uniform diameter Fixeda,b ˚ Many 300–400 A poresa,b Unknown Data are collated from a study of H. elaphus (aIgelmund, 1987) and studies of H. longicornis and/or H. batesii (bFoelix et al., 1975, c2002). No inter-specific differences are apparent except variation in the numbers and locations of rod sensilla (a qualitative description for both species is provided here, see text for detail of each species), and the absence of leaflike sensilla in H. longicornis and/or H. batesii. 10 ROGER D. SANTER AND EILEEN A. HEBETS A 200 mm Cl 100 mm b c Br C B LS a d D e LS 1 mm E d. p. PO P S1 LS LS 5 mm F L S L R S C 10 mm G 100 mm H 10 mm 25 mm FIG. 3 The antenniform leg tarsus is covered with a diverse range of sensillum types present in large number. Here, scanning electron micrographs show the tarsal sensilla of Heterophrynus elaphus. (A) Segment S1 has a set of much reduced terminal claws, Cl, that are thought to have a solely sensory function. This segment also has a number of distinct sensillum types that include bristle sensilla, Br; porous sensilla, P; club sensilla, C; rod sensilla, R; and the pit organ, PO. (B) Viewed from the distal end of the antenniform leg, bristle sensilla are arranged into five longitudinal rows that can be designated a–e and can serve as markers to describe locations on the antenniform leg. Row a is on the caudal surface, b and c dorsal to rostral, d and e rostral to ventral. (C) Detail of segments S21 (top) and S22 (bottom) showing a leaflike sensillum, LS, and the single type 1 slit sensillum, S1. (D) Segments S31 (right) to S36 (left) of the antenniform leg tarsus showing leaflike sensilla, LS, at a regular arrangement of every two segments alternately in bristle rows d and e. Also shown are the relative orientations of the bristle sensilla. At the posterior end of each segment (p), bristles are shorter and lie flatter against the cuticle; at the distal end (d), they are longer and stand more perpendicularly. (E) A single club sensillum of the antenniform leg tarsus showing the thickened terminal portion of the shaft with terminal pore. (F) Rod sensilla of the antenniform leg can be divided into THE SENSORY AND BEHAVIOURAL BIOLOGY OF WHIP SPIDERS 11 1987; Igelmund and Wendler, 1991a; Spence and Hebets, 2006). They are thick hairs with an articulated base and a terminal pore—a combined mechano- and chemosensory function can be confidently presumed from this anatomy (Foelix et al., 1975; Igelmund, 1987). Whip spiders do not possess solely mechanoreceptive bristles as seen in spiders (Foelix et al., 1975, 2002; Igelmund and Wendler, 1991a,b). Bristles are generally longer in proximal than distal tarsal segments (Igelmund, 1987). They are arranged into five longitudinal rows per segment, with the exception of the most distal bristles of segment 1 (S1), of which there are only four, arranged in a ‘square’ configuration when viewed end-on (Fig. 3B and D; Foelix et al., 1975; Igelmund, 1987). Two mechanosensory dendrites, ending in terminals with characteristic tubular bodies (a diagnostic feature of mechanosensory dendrites), connect to the articulated base of each hair (Foelix et al., 1975). A further 7–13 dendrites (in specimens of H. longicornis and/or H. batesii) run up the bristle shaft to the terminal pore and are presumably chemoreceptive (Foelix et al., 1975). Each dendrite belongs to a bipolar sensory cell, and gap junctions frequently occur between the dendrites (Foelix et al., 1975). In comparison to the contact chemoreceptors of spiders, whip spider bristle sensilla tend to have a lesser and more variable number of chemosensory dendrites (7–13 vs. 19–21 in spiders) (Foelix et al., 1975), but the functional implications of this are as yet unknown. Juvenile whip spiders have shorter antenniform legs and less bristle sensilla than adults (478 on the tarsus of first free nymph of H. elaphus vs. 1700 on the tarsus of the adult; Igelmund, 1987). As the antenniform leg grows, proximal segments gain more bristles, but the number on S1–S11 stays largely constant (Igelmund, 1987), perhaps indicating their importance in aspects of behaviour common to all instars. The shorter segments of a newly regenerated antenniform leg may have only 1–2 bristles per row, but the number increases as the segments lengthen with subsequent moults (Igelmund, 1987). The bristles of a regenerated antenniform leg are still organised into five rows, but occasionally bristles occur irregularly between the rows (Igelmund, 1987). 2.1.1.2. Leaflike sensilla Leaflike sensilla have an articulated base, a characteristic leaflike blade, and are presumed to be mechanoreceptive sensilla. They are relatively sparsely distributed on the antenniform leg tarsus (Table 1; Fig. 3C and D) and are not found in all whip spider species. Igelmund (1987) found 23 examples on the tarsi of adult H. elaphus but none were reported on longer, L, and shorter, S, types, and in H. elaphus occur largely in a dense patch on segment S1. (G) Detail of the pit organ of segment S1 (see also panel a) showing six distinct raised pore openings. (H) The plate organ of segment S12, a shallow depression with a cuticular cone (with terminal pore) rising in the distal third. After Igelmund (1987). With kind permission from John Wiley and Sons Ltd. 12 ROGER D. SANTER AND EILEEN A. HEBETS closely related specimens of H. longicornis and/or H. batesii (Beck et al., 1977; Foelix et al., 1975). Leaflike sensilla are not present in the prenymph or first free nymph stages, but develop from existing bristle sensilla in conserved locations through a process of metamorphosis over several successive moults (Igelmund, 1987). Leaflike sensilla are equivalent in length to a mid-sized bristle sensillum (Table 1), but their hair shaft forms a leaflike cuticular blade approximately 150 mm wide and 1.5 mm thick (Fig. 3C; Igelmund, 1987). The innervation pattern of the leaflike sensilla matches closely with that of the bristles. Leaflike sensilla have two mechanosensory dendrites that terminate at the hair base, and an additional ten dendrites, enclosed in a cuticular sheath, that continue to the hair tip (Igelmund, 1987). Igelmund (1987) has suggested that the flattened blade of a leaflike sensillum may act like a sail and confer air movement sensitivity. However, the articulation at the shaft base is very much stiffer than the articulation of a bristle (Igelmund, 1987), and this is atypical for an air movement sensor (e.g. Barth, 2000). The articulation is reported to be so stiff that moving a leaflike sensillum causes movements of the whole tarsus and can cause the generation of action potentials, presumably from the lyriform organ at the tibia-tarsus articulation (Section 2.1.2; Igelmund, 1987). In adult H. elaphus, leaflike sensilla have a regular spacing of one every two tarsal segments and appear alternately in the two ventral bristle sensillum rows (rows d and e, Fig. 3B) (Fig. 3D; Table 1; Igelmund, 1987). As might be expected, this pattern is disrupted in a regenerated antenniform leg. Initially, leaflike sensilla are small, but attain a more normal form with subsequent moults (Igelmund, 1987). They are still confined to bristle rows d and e, but their spacing is irregular (Igelmund, 1987). 2.1.1.3. Porous sensilla Porous sensilla are much shorter than bristle sensilla (Table 1; Fig. 3A; Foelix et al., 1975; Igelmund, 1987). They are found only on the most distal segments of the antenniform leg tarsus and decrease in density proximally (Table 1; Igelmund, 1987). Porous sensilla have wall pores and appear to be typical olfactory hairs. Such sensilla are common among insects, but not arachnids, and have not been found in spiders (see Foelix et al., 1975). There are two types of porous hair sensilla, and we describe both for specimens of H. longicornis and/or H. batesii, but their anatomy is identical in H. elaphus (Igelmund, 1987): Type 1 porous sensilla are characterised by faint, shallow grooves across their surface, and densely arranged pores without pore tubules (pore tubules are not always a feature of olfactory hairs) (Table 1; Foelix et al., 1975). Their walls are relatively thick (< 0.5 mm; Foelix et al., 1975), and enclose a lumen packed with 40–45 unbranched dendrites (Foelix et al., 1975). Some peripherally located dendrites send short processes into the pores (Foelix et al., 1975). THE SENSORY AND BEHAVIOURAL BIOLOGY OF WHIP SPIDERS 13 Type 2 porous sensilla are more deeply grooved, but have less densely arranged pores with smaller openings and pore tubules leading into a central lumen (Foelix et al., 1975). Type 2 porous sensilla have thinner walls than type 1 (0.2–0.3 mm) (Foelix et al., 1975). In the lumen there are 20–30 dendrites, which are, therefore, less closely packed than in type 1 sensilla with more surrounding fluid (Foelix et al., 1975). Type 2 sensilla have the typical structure of olfactory sensilla in insects (Foelix et al., 1975). The similarity in structure between whip spider porous sensilla and the olfactory receptors of insects are considered sufficient for both types of whip spider hairs to be considered as true olfactory sensilla (and there is some electrophysiological evidence for this, Section 2.1.4) (Foelix et al., 1975). However, both whip spider porous sensillum types have a relatively large number of sensory dendrites compared to typical insect multiporous hairs and equivalent to the individual heavily innervated units that form some composite olfactory organs (see Zacharuk, 1980). Neither the dendrites of type 1 nor type 2 porous sensilla in whip spiders branch as they do in some types of insect chemosensilla (Foelix et al., 1975; Zacharuk, 1980). Again, the functional implications (if any) of these morphological variations remain to be investigated. 2.1.1.4. Club sensilla Club sensilla are extremely short relative to the other sensillum types (Table 1), and the distal portion of their hair shaft is thickened into a club shape that bears a terminal pore (Fig. 3A and E; Foelix et al., 1975; Igelmund, 1987). Like porous sensilla, club sensilla are only found on the most distal tarsal segments and are most dense distally (Igelmund, 1987)—20% of the club sensilla in H. elaphus are found on S1 (Igelmund, 1987). In cross sections of the club sensillum shaft in H. longicornis and/or H. batesii, tiny pores appear to connect areas of the outer hair lumen with the air surrounding the sensillum (Foelix et al., 1975). In these species there are four to six dendrites encased in a thick dendritic sheath that run through the hair shaft and terminate just below the main pore opening (Foelix et al., 1975). This anatomy is typical of contact chemoreceptors (Foelix et al., 1975; Igelmund, 1987), but the club sensilla are too short to contact the substrate directly under normal circumstances due to the longer sensilla surrounding them (Table 1; Fig. 3A; Foelix et al., 1975). Weygoldt (2000) suggests that the club sensilla may be olfactory. Foelix et al. (1975) suggest that they may be humidity receptors, due to some similarity with hygro-sensitive sensilla of insects (see Altner and Loftus, 1985). 2.1.1.5. Rod sensilla The rod sensilla may be the most unusual of the morphological types on the distal tarsus (Foelix et al., 1975). They occur in short and long forms with a varying number and arrangement of pores. Their arrangement varies considerably between species, but they are always found predominantly on the most distal 1–3 tarsal segments in the Heterophrynus species studied in detail. 14 ROGER D. SANTER AND EILEEN A. HEBETS The shorter type of rod sensilla have shallow, longitudinal grooves on their surface (Fig. 3F; Beck et al., 1977; Igelmund, 1987). They have a relatively thin hair wall (approximately 0.1 mm) with thickened, cuticular ‘lumps’ attached to its inner surface (Foelix et al., 1975). Shorter type rod sensilla have no wall pores but do have a single terminal pore (Table 1; Beck et al., 1977; Foelix and Hebets, 2001; Foelix et al., 1975; Igelmund, 1987). The longer type of rod sensilla have a honeycomb patterned surface (Fig. 3F; Beck et al., 1977; Igelmund, 1987). The hair wall is uniformly thick (approximately 0.45 mm) and is perforated with many pores (Table 1; Beck et al., 1977; Foelix and Hebets, 2001; Foelix et al., 1975; Igelmund, 1987). In specimens of H. longicornis and/or H. batesii, both rod sensillum types have a single sensory cell whose dendrite branches inside the hair shaft while still enclosed by its dendritic sheath (Foelix et al., 1975; Igelmund, 1987). Foelix et al. (1975) thought that these sensilla could not be defined as olfactory (even though the smaller type has wall pores) because the dendrites remain enclosed in their sheath. The arrangement of these sensilla differs considerably between species. In H. elaphus, S1 has a prominent dorsal groove 200–300 mm long and 20–30 mm wide (Igelmund, 1987). All the longer type and most of the shorter type rod sensilla are found in this groove, which has approximately 35 sensilla and roughly equal numbers of each type (Fig. 3A; Igelmund, 1987). Additional short rod sensilla are located on the dorsal edges of S8–S12 (Igelmund, 1987). P. marginemaculatus also has a single oval-shaped patch on S1 (Spence and Hebets, 2006). By contrast, H. longicornis/batesii has more than 60 rod sensilla found in three circular patches on S1, S2, and S3 (Beck et al., 1977; Foelix and Hebets, 2001; Foelix et al., 1975; Igelmund, 1987). The function of the rod sensilla and the reasons for their differing arrangements between species are not known. 2.1.1.6. Trichobothria The medium particle displacement-sensitive filiform sensilla of arachnids are known as trichobothria (e.g. Barth, 2000). Those of whip spiders are typical in having a cup-shaped socket and a fine hair that is easily deflected by air currents (Igelmund, 1987). These sensilla are absent on the tarsus of the antenniform leg, but seven trichobothria are located on the antenniform leg tibia of H. elaphus (Foelix et al. restricted their earlier examination of H. longicornis and/or H. batesii to the distal tarsus only; Igelmund, 1987): two occur on tibial segment S1, one on S2, two on S3, one on S4, and one on S13 (Igelmund, 1987). Trichobothria are far more numerous on the walking legs, where they are predominantly located on the tibia, with two further short trichobothria on the patella (Section 2.2.3). The antenniform leg trichobothria are all 200–300 mm in length and are much shorter than those on the walking leg tibiae which can be up to 2000 mm long in the large Heterophrynus species (Igelmund, 1987; Weygoldt, 2000). The two trichobothria on tibial segments S4 and S13 have been studied electrophysiologically in H. elaphus, as movement of these hairs triggers large action THE SENSORY AND BEHAVIOURAL BIOLOGY OF WHIP SPIDERS 15 potentials that can be recorded extracuticularly from the tibia (Igelmund and Wendler, 1991a). Two types of action potentials are associated with each hair and these are elicited when the hair is deflected perpendicular to the long axis of the tibia, one for each direction of deflection from the resting position of the hair (Section 2.1.5.5; Igelmund and Wendler, 1991a). No such action potentials are recorded when the other trichobothria are deflected (Igelmund and Wendler, 1991a). The behavioural significance of the S4 and S13 trichobothria, and the large action potentials associated with them, are worthy of research. 2.1.2 Slit-type sensilla Slit sensilla consist of a slit in the cuticle associated with underlying mechanoreceptors and are unique to arachnids (Barth, 2002). Their mechanoreceptors are excited when the slit is compressed as a result of stresses in the cuticle that might result from muscle contraction, haemolymph pressure, gravity, or vibrations of the substrate (e.g. Barth, 2002; French et al., 2002). A complete description of the types and locations of these organs has only been carried out for H. elaphus (Igelmund, 1987), so our description of these sensilla is based on this species alone. Igelmund (1987) suggests that these often inconspicuous sensilla were likely overlooked in earlier investigations of H. longicornis, H. batesii, and other species. Igelmund (1987) identifies three ‘types’ of single slit sensillum in H. elaphus (based on their size), as well as a lyriform organ comprising many slit sensilla. The single slits of H. elaphus comprise: (i) type 1 slit sensilla—the largest slits (> 70 mm long), represented by only a single example found dorsocaudally, near to bristle row a on the distal edge of S22 (Fig. 3C; Igelmund, 1987); (ii) type 2 slit sensilla—relatively small slits ( 20 mm long) represented by three examples; and (iii) type 3 slit sensilla—very small slits (< 15 mm long), found on all segments of the tarsus (Table 2; Igelmund, 1987). In addition to the single slits, there is a lyriform slit sense organ, that is, a collection of many slits arranged in parallel at very close spacing so that the slits affect one another’s responses and finely tune the sensitivity of the organ (see Barth, 2002). This organ comprises seven long slits and is located on the tibia near to the dorsal condyle of the tibia-tarsus joint (Igelmund, 1987). The orientations of these slits rotate from parallel with the tibia long axis to increasing angles to it, rather like those of the walking leg lyriform organ (Section 2.2.4; Igelmund, 1987). Of these slit sensilla, the type 1 slit is best investigated. S21 has a slot enclosing an extension of S22, meaning that the articulation of the joint is stiffer in the vertical plane and that the sense organ has a degree of directionality in its response for this reason (Igelmund, 1987). As with the other sensory structures encountered so far, the position of the type 1 slit can vary between S25 and S29 in regenerated antenniform legs (Igelmund, 1987). For all single slit types, sensory dendrites attach via a coupling cylinder as in spiders (Igelmund, 1987). The position of dendrite attachment varies between

Author Jerome Casas Isbn 9780124159198 File size 3MB Year 2011 Pages 288 Language English File format PDF Category Animals Book Description: FacebookTwitterGoogle+TumblrDiggMySpaceShare This latest volume in this series contains articles on Arachnid Physiology and Behaviour.The papers in this special issue give rise to key themes for the future. Contributions from the leading researchers in entomology Discusses arachnid physiology and behavior Includes in-depth reviews with valuable information for a variety of entomology disciplines     Download (3MB) Insect Growth Disruptors Animal Behaviour: Mechanism, Development, Function and Evolution Target Receptors in the Control of Insect Pests All About Boxer Dog Puppies Thinking, Observing And Mining The Universe Load more posts

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