Acta Chiropterologica, 1(1): 3-15, 1999 PL 1SSN 1508-1109 © Museum and Institute of Zoology PAS

The evolution of flight and echolocation in pre-: an evaluation of the energetics of reach hunting

JOHN R. SPEAKMAN

Department a/Zoology, University ofAberdeen, Aberdeen, AB24 217, Great Britain E-mail: [email protected]

Theories of the evolution of echolocation and flight in bats can be divided into models in which echolocation evolved first, flight evolved first, or where both evolved in tandem. The echolocation frrst hypothesis, as well as some of the flight first theories, conunonly include a hypothetical phase where the pre- hunted by intercepting insects as they flew past a perch. I have called this behavior 'reach hunting'. In the current paper I have tried to reconstruct the likely energy gains that an could achieve when using this foraging strategy. The most favorable reconstruction suggests that it would take more than a day of continuous foraging to meet a reach hunters daily energy requirement, which probably explains why no extant hunt in this manner. This modelling suggests that the evolution of bats is unlikely to have included a period of reach hunting behaviour.

Key words: Chiroptera, evolution, flight, echolocation, aerial insects, reach hunting

INTRODUCTJON forms (e.g., and - Habersetzer and Currently, the earliest known bats date Storch, 1987). Aerodynamic reconstructions from the . Several specimens of a of the bats from Green River and the Messel single (lcaronycteris index) have suggest that they were probably as capable of been recovered from the Green River forma­ powered flight as their modern day counter­ tion in Wyoming, dated to 53 mya (Jepsen, parts (Padian, 1987; Habersetzer and Storch, 1966, 1970). Examination of these fossil bats 1987, 1989; Norberg, 1989). In addition to reveals enormous extension of the digits of the fully developed wing structure the early the forelimbs. In modern bats the extended fossil bats have a rotated hip joint similar to hand digits support the wing membrane, and that found in modern bats (Simmons and it seems most likely that in lcaronycteris they Geisler, 1998). This rotation of the limb may also served this function (see Padian, 1987, be related to the orientation of the legs during for an example reconstruction). The excep­ flight and attachment of the plagioptagium tional soft tissue preservation of fossil bats (Simmons, 1995). from the in , which are A less obvious anatomical trait of these approximately 3-4 million younger early fossil bats is their enlarged cochleae than , confirms the presence of relative to the size of their skulls, since this a fully formed wing membrane in similar can only be examined by radiographic analy­ 4 1. R. Speakman f sis. The extent of enlargement is less than in the flight first hypothesis, while the tan­ t reach hunting indivic that found in modem day insectivorous bats, dem development idea suggests that the sion of the digits and but generally larger than modem megachiro­ capabilities were closely linked throughout This would extend t pterans (Habersetzer and Storch, 1989; their evolution with advances in both systems animal could reach 11 Simmons and Geisler, 1998: fig. 29). This evolving in parallel. In the present paper I of prey. Webbing lx enlargement strongly suggests that the bats will consider some problems with the echo­ improve the success, were not only capable of flying, but had also location first model for the evolution of struction of such a echolocation. developed a sophisticated echolocation illustrated in Fig. 1 system (Novacek, 1985, 1991; Habersetzer elongated arms and and Storch, 1989, 1992). Two key traits that ECHOLOCATION FIRST HYPOTHESIS would thus represer we associate with modern bats (flight and flight. echolocation) are already present in the The echolocation first hypothesis origi­ The next phase J earliest fossil representatives of this taxon nated in the 1960s and has been through involve refinement 0: (Neuweiler, 1984). several transformations as new data has the animal for echol As observed by Griffin (1958), the ab­ accumulated, and it has, at various times, 1995). Broadband l sence of any direct fossil evidence means that been modified to fit the bat diphyly and bat while targets appro we can only speculate on the process of the monophyly theories. The following account some ranging inform development of these traits. Such speculation is an attempt to synthesise previous ideas into become progressivel­ is not easy. Indeed, Darwin (1859) in the a contemporary consensus. The echolocation mal was producing' "Origin of Species" considered that the first hypothesis starts from the assumption frequency-modulated difficulty explaining the evolution of bats that the ancestral pre-bat was nocturnal, track incoming target from a quadrupedal ancestor posed a serious arboreal and insectivorous (Fenton, 1984; problem for the theory of evolution (see Hill and Smith, 1984; Fenton et al., 1995; Difficulties with the Theory section). Never­ Arita and Fenton, 1997). A good extant theless several attempts have been made to model for such an animal might be the mod­ reconstruct the process which may have led ern day tree shrews (Scandentia), which to evolution of the early fossil bats from a might also be the closest archontan relative to quadrupedal ancestral pre-bat. the modern Volitania (Novacek, 1986; There have been three major alternative Miyamoto, 1996). The hypothetical pre-bat i scenarios [reviewed in Arita and Fenton presumed to have communicated by using \ (1997) and Simmons and Geisler (1998)). broadband ultrasound calls (Sales and Pye, ~ These can be called the echolocation first 1972; Fenton, 1984). It is presumed that this I hypothesis, the flight first hypothesis and the animal fed primarily by gleaning insect pre tandem evolution hypothesis. All of the from the arboreal substrate. The prey rna models can be considered 'monophyletic' have been located by olfactory, visual hypotheses since they have generally been tactile means [for example, Simmons an developed on the a priori premise that the Geisler (1998) argued that vision was prob order Chiroptera is monophyletic (although bly well advanced in these animals]. The fi at various times in the history ofthe develop­ phase in the process of evolution wou ment of the ideas they have been modified to involve a period when the bat fed by cap fit the diphyly hypothesis of bat origins ­ ing aerial insects flying past its arbor Pettigrew et al., 1989). perches. This would involve reaching 0 The echolocation first hypothesis suggests wards from the branches to snatch the p that the pre-bats developed a fully advanced ing insects from the air (Jepsen, 1970). In echolocation system before they started to current paper I have coined the term 're fly. The situation is presumed to be reversed hunting' for this behaviour. Selection i . Reconstruction of a Evolution of flight and echolocation in pre-bats 5

while the tan­ reach hunting individual would favour exten­ evolution I suggest the animal might have sgests that the sion of the digits and forearm (Jepsen, 1970). abandoned the tops of branches in favour of inked throughout This would extend the area over which the hanging inverted below them. This might .ces in both systems animal could reach thus increasing the intake have provided two advantages. First, the . the present paper I of prey. Webbing between the digits might animal would have both hands free for prey blems with the echo­ improve the success at prey capture. A recon­ capture, and second, the branch would not 'or the evolution of struction of such a hypothetical pre-bat is cause an ultrasound shadow obscuring ap­ illustrated in Fig. 1. The development of proaching insect prey. elongated arms and digits with webbing Eventually the animal would be echo­ iYPOTHESIS would thus represent a pre-adaptation for locating on to approaching targets to track flight. their approach and sweeping them into rst hypothesis origi­ The next phase in development would greatly enlarged hand and arm webbing. As td has been through involve refinement of the ultrasound calls of the range of echolocation improved many s as new data has the animal for echolocation (Fenton et al., insects would be tracked approaching, but as, at various times, 1995). Broadband ultrasound calls made would not come within reach. The animal e bat diphyly and bat while targets approached would provide might have started to jump outwards to he following account some ranging information, and these would intercept these 'close encounters'. The se previous ideas into become progressively refined until the ani­ hand/arms would then be used to aerody­ sus. The echolocation mal was producing broad high intensity namic advantage to glide to another perch from the assumption frequency-modulated (PM) sweeping calls to from which the process could be repeated. .-bat was nocturnal, track incoming targets. During this phase of This would lead the animal to develop a IroUS (Fenton, 1984; Fenton et al., 1995; 97). A good extant ial might be the mod­ (Scandentia), which t archontan relative to a (Novacek, 1986; rypothetical pre-bat is omunicated by using calls (Sales and Pye, •is presumed that this r gleaning insect prey strate, The prey may olfactory, visual or unple, Simmons and hat vision was proba­ ese animals]. The first of evolution would the bat fed by captur­ ing past its arboreal . nvolve reaching out­ es to snatch the pass­ (Jepsen, 1970). In the oined the term 'reach .viour, Selection in a FIG. 1. Reconstruction of a hypothetical reach hunting pre-bat with elongated forearms and enlarged digits with webbing to facilitate reach distance and capture of insect prey 6 J. R. Speakman perch-hunting strategy similar to that found (pers. comm.) has suggested that nectar (Speakman et al., 1989 in modern rhinolophid bats (Schnitzler et al., feeding in the Old and New World bats may disappear during fli: 1985; Neuweiler et al., 1987; Jones and have evolved by different routes with a direct Racey, 1991) because Rayner, 1989) and many other groups (e.g., link between insectivory and nectarivory in pling of wing beat, res megadennatids, nycterids and some vesper­ the New World, but a link via frugivory in tion in bats that are fly tilionids - Simmons and Geisler, 1998; the Old World. In either case the advancing Suthers et al., 1971; Bogdanowicz et al., 1999). sophistication of flight behaviour would high costs for stationa The next stage in the process would be to allow bats to make these dietary shifts. In would be insufficient t extend the time spent in flight to intercept some instances this may have been followed perch hunting, the dii more than single insects prior to relanding. by the evolution of folivory (Kunz and location for flying a As the numbers of insects captured between Ingalls, 1994). means that the balance .landings increased, perch hunting would The final aspect of the theory is the grad­ is very likely to be WI gradually evolve into aerial hawking, with ual loss of echolocation capability and its favour of echolocatior the bat continuously in flight. The current replacement by sight as the dominant mode or in tandem with it, ra fossil evidence is suggested to start some­ ofperception in some fruit and nectar feeding The second problei where in these latter two phases. Simmons bats (the Old World megachiropterans). A significant problems, and Geisler (1998) have suggested that the parallel but not yet completed process may suggest megachiropt earliest (lcaronycteris and Archaeo­ be currently occurring in the frugivorous and ability to echolocate. , nycteris) were perch hunting forms based on nectarivorous phyllostomids, The final twist loss of sensory capab: their short wings and lack of uropata­ in the story is the re-evolution of echoloca­ animal kingdom, for gia/calcars, while later fossils were aerial tion using completely different sound pro­ cave fish and reptiles hawkers. Norberg (1989) also stated that duction mechanisms among some of the and fossorial animals these species may have been perch hunters, megachiropterans (Rousettus spp. using 1965), and these have although she clearly considered them capable tongue clicks and Eonycteris spelaea using sent analogies to the of continuous flight, rather than being re­ wing clapping - Griffin et al., 1958; Rob­ (Simmons and Ge stricted to hunting from perches, as implied erts, 1975; Gould, 1988). Arguments sup­ Hutcheon, pers. com by Simmons and Geisler (1998). Norberg porting this pattern of sensory modality these analogies to th (1989: 205) for example states: 'There is swapping were presented by 1. M. Hutcheon echolocation in ances nothing in the wing shape which indicates the at 11th International Bat Research Confer­ questionable. Loss 0 ancient bats included here were poor fliers' . ence in 1998. fish and fossorial ar Others have suggested that they were all there is no light availa aerial hawking bats (Habersetzer and Storch, PROBLEMS WITH THE ECHOLOCATION FIRST thus vision is a supe 1989) based on their wing loading and pre­ MODEL cost energy to maint dicted aerodynamic performance relative to vision in this situati modern aerial hawking bats. I think that there are at least three majo fitness benefit comi Once aerial hawking had evolved as a flaws with the echolocation first model :D retain their visual cap foraging strategy the sophistication of flight the evolution ofbats. Two of these argumen from the hypothesise performance would improve in some forms, have been presented elsewhere. The thir capability in mezacl allowing them to glean insects from surfaces argument will be developed in this pap highly sophisticat:d a while remaining themselves in flight. This First, it has been suggested (Jones, 19 location) is suggestec would allow bats to take insects from sites Speakman, 1993) that the echolocation y another equally sc where ground based gleaning animals would model, as presented above, is unreali ve system (vision). have no access, because of their body because it ignores observations that sh cd that there are weights, such as from the corollas offlowers. there are significant energy costs associ P of sensory r This in turn might lead to the evolution of with the production of echolocation voc 3). This is bee, nectar feeding and fruit feeding. S. Vogel tions for animals that are statio ume (Martin, 19E Evolution of flight and echolocation in pre-bats 7

led that nectar (Speakman et al., 1989). However, such costs and/or metabolites that can be devoted to .;World bats may disappear during flight (Speakman and sensory systems, means that an intermediate .routes with a direct Racey, 1991) because of the observed cou­ animal possessing both an inferior echo­ y and nectarivory in pling of wing beat, respiration and vocalisa­ location and inferior visual system, compared L link via frugivory in tion in bats that are flying (Schnitzler, 1968; to specialised alternatives, would always be ier case the advancing Suthers et al., 1971; Kalko, 1994). While out competed by animals with the specialised iht behaviour would high costs for stationary echolocation alone alternatives (Speakman, 1993). This makes it lese dietary shifts. In would be insufficient to prevent evolution of unlikely that if megachiropterans ever had iy have been followed perch hunting, the different costs of echo­ the capability to echolocate that they would folivory (Kunz and location for flying and perching animals lose it to replace it with a complex visual means that the balance of costs and benefits system (Rayner, 1991). More probable that the theory is the grad­ is very likely to be weighted much more in they never had the capability in the first ion capability and its favour of echolocation evolving after flight, place. This argument receives substantial is the dominant mode or in tandem with it, rather than preceding it. support from the observed success of the ruit and nectar feeding The second problem is that there are also megachiropteran groups that have evolved a megachiropterans). A significant problems with the scenarios that rudimentary form of echolocation. A third impleted process may suggest megachiropterans have lost the argument against the echolocation first hy­ in the frugivorous and ability to echolocate. Although it is true that pothesis, developed here, concerns the ener­ omids. The final twist loss of sensory capability is common in the getic feasibility of 'reach hunting' as a forag­ .volution of echoloca­ animal kingdom, for example among blind ing strategy. different sound pro­ cave fish and reptiles (e.g., Halpern, 1973) among some of the and fossorial animals (e.g., Lund and Lund, ENERGETICS OF REACH HUNTING ousettus spp. using 1965), and these have been claimed to repre­ iycteris spelaea using sent analogies to the loss of echolocation In the remainder ofthis paper I propose to 'fin et al., 1958; Rob­ (Simmons and Geisler, 1998; J. M. evaluate the energy gains that a hypothetical 188). Arguments sup­ Hutcheon, pers. comm.), the relevance of 'reach hunting' animal might be expected to of sensory modality these analogies to the hypothetical loss of obtain by using this foraging strategy and ted by J. M. Hutcheon echolocation in ancestral Megachiroptera is how such gains might depend on the length­ 3at Research Confer­ questionable. Loss of vision in blind cave ening ofthe arms and digits and the inversion fish and fossorial animals occurs because of posture. To evaluate the energy returns there is no light available in their habitats and that reach hunting would provide it is neces­ ~CHOLOCATION FIRST thus vision is a superfluous trait that must sary to quantify several key parameters. The cost energy to maintain. Animals that lose first parameter is the distance that an animal vision in this situation therefore derive a can reach, which provides an estimate of the 'e at least three major fitness benefit compared to animals that area surrounding the animal within which cation first model for retain their visual capability. This is different any passing insect would be vulnerable to wo ofthese arguments from the hypothesised loss of echolocation capture. The second paramter is the likeli­ elsewhere. The third capability in megachiropterans where one hood of an insect flying into this area of eloped in this paper. highly sophisticated and useful system(echo­ vulnerability, which will depend on the gested (Jones, 1993; location) is suggested to have been replaced density of insects and their activity (flight the echolocation first' by another equally sophisticated but alterna­ speeds and flight patterns). The third parame­ above, is unrealistic tive system (vision). I have previously sug­ ter is the probability that an insect will be servations that show gested that there are difficulties with such a detected and captured once it enters the zone iergy costs associated swap of sensory modalities (Speakman, of vulnerability. Finally, we must calculate -cholocation vocalisa­ 1993). This is because the limited brain the energy content of the prey that can be that are stationary volume (Martin, 1981) processing capacity extracted by the animal in question. I will 8 1. R. Speakman consider each of these parameters in tum and the second arm minus the digits (which are then synthesise this information to recon­ utilised in holding on to the branch to form struct the probable energy gains that an the second point of attachment). Using the A: animal could obtain by employing this forag­ tree shrew (Tupaia pieta) as a model, I mea­ Hypothetical Arboreal ing strategy. sured the lengths of the major limb bones and Predator digits of a museum specimen (University of REACH D1STANCE AND AREA OF VULNERA­ Aberdeen, Natural History Museum: unnum­ BILlTY bered display specimen). The measurements were: body width, 50 rnm; humerus, 25 mm; A dorsal view of a model pre-bat, such as ulna/radius, 35 rnm; hand incl. digits, 15 mm. a tree shrew, reveals that the animal has two Applying the above formula gives an esti­ points of attachment to the arboreal habitat. mated maximum reach distance of 175 mm. These are located approximately below the It seems very unlikely that the animal could pelvic and pectoral girdles (Fig. 2A). Assum­ make such a reach in all directions (for exam­ ing that the animal uses the forelimbs to ple vertically upwards). However, I will B: Reach capture its prey (Fig. 1), there are two ways make the generous assumption that this to envisage the reach distance. In the first would in fact be possible, so the area of reconstruction the centre of the body remains vulnerability for this model pre-bat animal over the forward point of attachment and the describes a sphere of radius 175 mm and a forelimb is extended to one side (Fig. 2B). volume of 0.024 m' (which is approximately However, the animal can extend the reach equivalent to a square box with sides 28 em substantially by leaning outwards, so that the across). centre of the body lies to one side of the branch at the same time as extending the LIKELIHOOD OF AN INSECT ENTERING THE forelimb in the same direction (Fig. 2C). AREA OF VULNERABILITY Leaning and reaching gives the maximum rear, area of vulnerability. This fact suggests two Imagine a cube measuring 1 m on each things. Selection will favour reducing the side. Inside this cube, in the middle, is an­ angle between the body and the forelimbs other cube measuring 28 em on each side. c: Lean and and thus will not only favour extension of the There is a single insect flying around at Reach arms and digits to effect prey capture but will random inside the big cube. How long would also promote selection of extended body it take before the insect would pass through length. In addition, adopting an inverted the smaller cube? The solution to this prob­ posture, and releasing both forelimbs from lem would be the answer to the likelihood of· the perch, actually reduces rather than in­ an insect entering the area of vulnerability, at creases the area of vulnerability. The sugges­ a density of I insect/nr', If we could answer tion that an inverted posture might increase this question the general solution would be prey capture would only occur ifby releasing applicable to all insect densities and the both limbs the increased probability of a encounter rate of our hypothetical pre-bat successful capture offset the reduced volume with prey could be evaluated from knowl­ of air in which passing insects would be edge of its prey density. vulnerable. Unfortunately, a simple mathematical The maximum reach distance for a lean­ solution to the problem is not tractable. In FIG. 2. Schematic view: (A) ing and reaching animal is approximately general we might expect the answer to be a girdle; (B) of a hypothetical ' equal to the length of one arm plus digits, distribution approximating something like a branch; (C) of a 'lean and re" plus the width of the body, plus the length of Poisson distribution. But deriving parameters Evolution of flight and echolocation in pre-bats 9

.rigits (which are ne branch to form chment). Using the A: Hypothetical a) as a model, I mea­ Arboreal front anchor point Dorsal view ~ major limb bones and Predator pecimen (University of story Museum: unnurn­ en). The measurements mm; humerus, 2S rnm: iand incl. digits, 15 mrn. rear anchor point formula gives an esti­ .h distance of 175 mm. y that the animal could t11 directions (for exam­ ••- -»-.-.------.-~••-... area of vulnerability .ds). However, I will B: Reach "'."\~~' assumption that this //__ -/ lnsects .ssible, so the area of

model pre-bat animal I " . radius 175 nun and a rfront anchor point \ vhich is approximately ~ box with sides 28 cm \, .. \ "." " <,

NSECT ENTERING THE .. ~ -c-,... _ITY rear anchor point easuring 1 m 'On each , in the middle, is an­ -... -...... --­~ --_...--..- -_..------...- 28 cm on each side. ~~;~~n and _///-­ sect flying around at cube. How long would / ct would pass through / .. ... solution to this prob­ .er to the likelihood of· ! rea of vulnerability, at ( 3• 1 If we could answer \ \ ) ral solution would be ... :' .ct densities and the \ j'/ \\. rear anchor point-~l. hypothetical pre-bat ..,//' reach distance ..../ raluated from knowl­ -," -._-­ f· -- .. _~---- simple mathematical n is not tractable. In FIG. 2. Schematic view: (A) from above of an arboreal showing locations of the pelvic and pectoral ct the answer to be a girdle; (B) of a hypothetical 'reach' to one side, retaining the centre of the pectoral girdle over the centre of the ting something like a branch; (C) of a 'lean and reach'. By displacing the pectoral girdle away from the centre of the branch the total It deriving parameters length of the reach is greatly extended 10 J. R. Speakman

of such a solution depends on several un­ involved an equal probability of moving to 400.,------­

knowns such as the directionality ofthe flight each of the nine alternatives (rule A: 350 •

path. To derive a solution to the insect in two equiprobable movement). The second move­ 300

cubes problem I used a computer simulation. ment rule (B) was weighted against diagonal ~ 250 • (The simulation was written in BASIC and movements. Thus each of the four corner t:: ~ 200 • copies are available from the author on re­ alternatives had a probability of 0, and the 0" £ 150 quest). In the simulation an insect is moving remaining five alternatives were equiprob­ 100 • around a cube with sides measuring 1 m. The able. The third movement rule (C) was 50 large cube is subdivided into small cubes weighted against directly forward movement • 0.1...------­• measuring 1 em on each side. The insect or remaining stationary. Both these possibili­ a 2000 4000 SI moves between the 1ern cubes in single steps ties were given a probability of 0, and the taking one time unit to travel one step. One remaining 8 alternatives were equiprobable. way to imagine this scenario is to imagine In all cases, the program iterated move­ 350 ;------­ that wherever it is the insect is in the centre ments until the insect entered a cube of given 300 • of a virtual Rubik cube. The virtual Rubik dimensions located centrally in the larger 250 • >. cube consists of 26 1-cm cubes surrounding cube. The number of 1ern steps before enter­ u :;; 200 a central l-cm cube. In a given time unit the ing the central box (which mimics the area of ::J 0" • insect in the middle of the Rubik cube can vulnerability) was recorded and the program E 150 move to any of the immediately adjacent 26 iterated 1,000 times to generate a distribution - 100 l-crn cubes (or stay where it is) - making a of interception distances. The results of three • • 50 total of 27 movement possibilities. Once it simulations using different movement rules • has moved it is then considered to be the are shown in Fig. 3A-C. In these simulations, oJ.-..-~-_-- central point of another virtual Rubik cube the central cube had dimensions of 20 em on a 2000 4000 with a further 27 movement options open to each side. The pattern of distances in all

it, and so on. The insect can enter the large these cases was remarkably similar. How­ 350 r------­ 1m cube at any point on its surface and can ever, the actual means differed by about 25% 300 • also exit at any point. Ifit exits then another between the shortest and longest. The short­ insect immediately enters the 1m cube some­ est interception on average for an intercep­ 250 • ~ t:: 200 where else completely at random. In other tion cube of this size occurred with the Q) ::J words there are no edge effects for the large equiprobable movement rule (A) and was go 150 • cube. 1,676 steps (16.76 m). On average, at a ~ • 100 I used three different movement rules to density of 1 insect/m' each insect would fly describe the insect flight behaviour. In all 16.76 m within the 1 m cube before flying 50 • three cases I made the a priori assumption into the area of vulnerability. It is necessary 0'-1-----­ a 2000 4000 that the insect would fly forwards with much to know the flight speeds of insects to con­ em steps before ent greater probability than backwards. The vert this into a time. probability of entering one of the 9 1-cm Johnson (1962) reported flight speeds for FIG. 3. Distributions of t: cubes in front of the insect was set at 0.75, insects of different sizes, and found that the thetical fly inside a 1 m and for moving into the 9 cubes behind was majority of small insects « 1.5 ern body entering a zone of vulne the cube measuring 20 set at O. Thus the animal had a probability of length), which dominate the aerial insect three different movement 0.25 of staying in one of the 9 cubes at the fauna (see below), fly at speeds of around text for ill~ centre of its direction of travel. Having de­ 1 mls. Larger insects such as and fmed whether the insect would move for­ dragonflies can fly much faster than this, but movement rule that ~ wards or not, I then used several alternative are very rare components of the aerial insect distance suggests thar rules defining to which of the 9 cubes the community. Using a mean flight speed of sect/nr' one insect WOl insect would move. The simplest of these 1 m/s, in our hypothetical example, the vulnerability about e Evolution of flight and echolocation in pre-bats 11

l' moving to 400 ,------, evaluate how realistic the computer simula­ .es (rule A: 350 • A tions were, I constructed a cube with sides of c second move­ 300 20 em using plastic drinking straws and

.against diagonal ~ 250 • placed it at a height of 1.5 m on a warm l: If the four comer ~ 200 sunny afternoon near Aberdeen and observed ility of 0, and the C' • for 20 minutes the numbers of insects that £ 150 es were equiprob­ flew through it. I estimated by eye that 100 • ent rule (C) was around the immediate vicinity of the box the 50 'orward movement • • aerial insect density was around 1.5 oth these possibili­ insects/nr'. On average, I recorded 4.2 insects ility of 0, and the passing through the box each minute - while rere equiprobable. the computer simulation at a density of 1.5 am iterated move­ 350 r------, insects/nr' predicts (17/1.5) an insect every red a cube of given 300 • B 11.2 seconds or 5.2 per minute. Given the 'ally in the larger arbitrary nature of the flight rules used in the 250 • >. steps before enter­ CJ model, and probable inaccuracies in the ; 200 mimics the area of :I evaluation of insect density by eye, I am C' • ~d and the program ~ 150 struck by the similarity of these values and erate a distribution therefore feel the computer simulation af­ 100 I'he results of three • • fords a reasonable approximation (perhaps It movement rules 50 • slightly generous) of the likely interception l these simulations, • • • • rates that hypothetical reach hunting animals nsions of 20 em on 2000 4000 6000 8000 10000 12000 might have with P9tejJt!a!.prey.J,Jsing if distances in all hypothetical cUcpe witb s~i:ies Qt28'YJ;l:r(see

bly similar. How­ 350.,...------, above) to simulate a tree-shrew like animal~ ered by about 25% and using the equiprobable moveqientJ3,l.le, 300 longest. The short­ • C the average time to interception at a density 250 ?e for an intercep­ >. • of 1 insect/nr' and a flight speed of 1 m/s was CJ t: 200 occurred with the Q) 10 seconds. :I rule (A) and was C' 150 Two questions remain. What was the e • On average, at a .... • density of aerial insects in the late Creta­ 100 :h insect would fly ceous/early Tertiary when these animals were 50 cube before flying • • • • • evolving, and second, to what extent is den­ lity. It is necessary sity reduced inside the canopy of a tree adj­ a 2000 4000 6000 8000 10000 12000 , of insects to con­ acent toa branch, when compared with the em steps before enters area of vulnerability density measured in free field sites? In the edflight speeds for FIG. 3. Distributions of the distances that a hypo­ absence of any information I have made the and found that the thetical fly inside a I m cubed box covers before assumption that modem day insect densities .s «1.5 em body entering a zone of vulnerability in the centre of matched those in the period when the hypo­ the cube measuring 20 em'. Simulations under : the aerial insect three different movement rules are illustrated (see thetical reach hunting pre-bat was alive. speeds of around text for more details) Johnson (1952) has reviewed estimates of ich as moths and aerial insect density. The maximum densities faster than this, but movement rule that generates the shortest occur in locust and aphid swarms when of the aerial insect distance suggests that at a density of 1 in­ between 11 and 14 individuals/rrr' have been an flight speed of sect/nr' one insect would fly into the area of reported. Generally, however, maximal den­ ical example, the vulnerability about every 17 seconds. To sities average between 1 and 3 per nr', and l

12 J. R. Speakman

these are sustained for relatively short peri­ mal that has not developed a specialised ing animal need to fe: ods. We might imagine that for short periods sensory system for tracking incoming insects daily energy require the pre-bats could intercept insects at rates of and is relying on vision, I have assumed that based on Tupaia picta. 1 insect every 10 seconds. However over the animal only detects larger insects with imately 160 g. The da much longer periods average insect densities wings measuring greater than 1 em across predicted for a marnn are considerably lower. Rydell (1989) esti­ (see Brigham and Barclay, 1995, for biased approximately 150kJ/ mated aerial insect densities in the early size selection towards larger insects by night Consequently, with aJ evening in southern Sweden were 0.15 to foraging Caprimulgiformes, which are con­ 0.34 Watts it would 0.30 insects/rrr' and Johnson (1950) reported strained by light levels). Insects over 1 ern average a predicted slimmer densities in the temperate zone long are actually a relatively rare component hunt foraging to take average 0.15 per nr' over the entire diel of the aerial fauna, which tends to be domi­ requirement. cycle. Densities of aerial insects in the tem­ nated by very small insects. Speakman et al. Itshould be remem perate zone during summer generally exceed (In press) found that insects with wings is based on several v those in the tropics (Johnson, 1962). Since greater than I em comprise only 4.2% of the tions: the interceptic bats are believed to have evolved in sub­ total aerial insects in Norway during the equiprobable movem tropical and tropical habitats the assumption summer. This is not an exceptional figure. slightly generous inti based on aerial insects from the temperate Johnson (1962) quotes various values be­ with reality, the captu zone is probably generous. tween 2 and 5% for similar sized insects from cally high (100%), it Insect densities are generally measured at various sites around the world. I will assume the digestive efficiem free-field sites and not within the canopies of that the same size distribution of insects assumed aerial insect trees. To evaluate the difference in insect pertained in the late . This is a 24h was 30% higher t density between a free-field site and within a reasonable assumption given the similarity of value for present day j tree canopy I made observations of the num­ modern insects to those trapped in amber least generous assurm bers of insects flying through a 20 em' straw from this time period (Ross, 1997). Moreover mals only detect insec box located inside a tree (adjacent to a the rates at which insects were trapped in ing more than 1 em branch), at the same site and immediately amber relative to the trapping rates of mod­ assumption however r after the free field observations detailed ern sticky traps suggests the assumed density ence to the calculatic above. The average number of insects within of ancient insects is also not unrealistic. contents of much s the tree was only 16% of the average num­ I will make the generous assumptions that dominate the fauna is bers passing through the same box at the if any insect of this size entered the zone of mass of modern insee free-field site. Using a generous average vulnerability, the success rate of capture was ing less than 1 em in insect density over 24 h of 0.2 insects/rrr' and 100%, and once ingested the digestive effi­ (Speakman and Rae a reduction from free-field to inside the ciency was also 100%. The average mass of animal would need tl canopy of 84% yields an interception rate insects with wings measuring greater than small insects to mate with insects for the hypothetical animal based 1 em is assumed to be 100 mg (based on my single large insect. B on the tree-shrew (with a 0.0224 nr' intercep­ own unpublished observations of insects detects all aerial insec tion area) of one insect intercepted every collected around Aberdeen) and they are daily energy requirerr 312.5 seconds. assumed to have an energy content of25 kJ/g approximately 20%. To evaluate the energy intake of the (Kunz, 1988). Each insect therefore was A key factor in t] animal it is necessary to make some assump­ assumed to contain 2,500 J of available sumed density of ir tions about the probability that the animal energy. Using these values, the interception animals might be a1 would detect these prey, the probability that rates with insects in the appropriate size class attracted to certain lot once detected they would be captured, their would be one insect every 7,440 seconds, or exuding sap, becau energy content, and the digestive efficiency giving the animal an energy ingestion rate of prey density might m. of the animal once it had eaten them. Since 0.34 Watts. Given this energy intake rate, startegy. Although thi we are presumed to be dealing with an ani­ how long would the hypothetical reach hunt­ for the evolution of n Evolution of flight and echolocation in pre-bats 13

, a specialised ing animal need to feed each day to meet its probable precursor to the evolution of flight .ncoming insects daily energy requirements'? The model is and echolocation. This is because animals .iave assumed that based on Tupaia picta, which weighs approx­ exploiting such a resource would not need to larger insects with imately 160 g. The daily energy requirement develop sophisticated echolocation to track er than 1 ern across predicted for a mammal of this body size is the flight paths of the insects or need to leap lay, 1995, for biased approximately 150 kJ/day (Speakman, 1997). out and catch them, because the insects arger insects by night Consequently, with an energy intake rate of would always predictably come to the attrac­ mes, which are con­ 0.34 Watts it would take this animal on tant, where they might be captured. .). Insects over 1 em average a predicted 122.5 hours of reach­ ively rare component hunt foraging to take in a single days food CONCLUSIONS ch tends to be domi­ requirement. The inevitable conclusion of this model­ ects. Speakman et al. It should be remembered that this estimate ling is that reach hunting is not a viable insects with wings is based on several very generous assump­ foraging strategy. Animals may have in the rise only 4.2% of the tions: the interception rate, based on the past, and may still, occasionally and opportu­ Norway during the equiprobable movement rule may predict nistically snatch insects from the air when 1 exceptional figure. slightly generous intercept rates compared stationary on the ground or a perch (Courts, ; various values be­ with reality, the capture success is unrealisti­ 1997). The contribution of these insects to lar sized insects from cally high (100%), it was also assumed that the total energy budget however is likely to world. I will assume the digestive efficiency was 100%, and the have been (and be) trivial. Given that elon­ stribution of insects assumed aerial insect density averaged over gated limbs and webbed elongated digits (as 'retaceous. This is a 24h was 30% higher than the literature cited envisaged in Fig. 1) would probably have ~iven the similarity of value for present day insect populations. The reduced the efficiency of other activities, se trapped in amber least generous assumption was that the ani­ such as locomotion, it seems very improbable ass, 1997). Moreover mals only detect insects with wings measur­ that natural selection would favour develop­ .cts were trapped in ing more than 1 em across. Relaxing this ment of such traits. apping rates of mod­ assumption however makes very little differ­ I suggest that this conclusion is consistent ; the assumed density ence to the calculation because the energy with the fact that currently there are no J not unrealistic. contents of much smaller insects which known vertebrates that employ reach hunting .ous assumptions that dominate the fauna is very low. The average as a foraging strategy (either with or without ~ entered the zone of mass of modem insects with wings measur­ the aid of echolocation). The only animals, ss rate of capture was ing less than 1 em in length averages 1 mg which employ similar tactics to intercept ed the digestive effi­ (Speakman and Racey, 1989). Thus the flying insects, are web spiders. Web spiders The average mass of animal would need to take in 100 of these are only capable of doing this because the asuring greater than small insects to match the intake of only a web is a massive trapping surface relative to 00 mg (based on my single large insect. By assuming the animal the animals own body size. Only by having ervations of insects detects all aerial insects the time to meet the trap, which extends 20-50x greater than its deen) and they are daily energy requirement is reduced by only limb length, can a spider trap sufficient 'gy content of25 kJ/g approximately 20%. insects to meet its energy requirements. As nsect therefore was A key factor in this analysis is the as­ reach hunting is not a viable foraging strat­ ,500 J of available sumed density of insects. Reach hunting egy, and because it forms a major stage in the lues, the interception, animals might be able to exploit insects hypothetical scenario for pre-adaptation of appropriate size class attracted to certain locations such as flowers the limbs of pre-bats for flight, this paper very 7,440 seconds, or exuding sap, because the locally elevated provides further evidence that the 'echo­ ergy ingestion rate of prey density might make it a more profitable location first' route is less realistic than the energy intake rate, startegy. Although this is a potential scenario flight first and tandem evolution scenarios for iothetical reach hunt­ for the evolution of reach hunting it is not a the evolution of bats. 14 J. R. Speakman

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