Functional diversity of ladder-webs: moth specialization or optimal area use?

2010·2.9 MB·English

by  Aaron M T Harmer

2010. The Journal ofArachnology 38:119-122
SHORT COMMUNICATION
Functional diversity of ladder-webs: moth specialization or optimal area use?
Aaron M. T. Harmer and Marie E. Herberstein: Department ofBiological Sciences, Macquarie University, Sydney 2109,
Australia. E-mail: [email protected]
Abstract. Ladder-websare built by several orb-web spiderspecies and can be divided into two main groups based on the
microhabitat in which they are built, either in open spaces (aerial) or against tree trunks (arboricolous). In Australian
ladder-web spiders, Telaprocera, the elongated webs are a highly plastic behavioral response to building in space-limited
conditions against tree trunks, while the aerial ladder-webs ofScoloderusare an adaptation forcatching moths. However,
therelativeimportanceofmothcaptureintheconstructionofelongatedwebsinarboricolousspiderscannotbedetermined
with existing data. We here present observational and experimental data concerning prey capture in the arboricolous
spiders T. maudaeHarmer&Framenau2008and T.joanaeHarmer& Framenau2008. Wefoundthatmothsmakeuponly
a small fraction (< 4%) of the diet of Telaprocera spiders and that the proportions of major prey orders in webs are
representative of available prey. Our experiments indicate that these webs do not function well at retaining moths.
However, furtherdata are required before more definiteconclusions can bedrawn regarding whether these webs are more
effective at retaining moths than standard orb-webs.
Keywords: Telaprocera, orb-web, moth, prey specialization
Some orb-web spiders build webs that are specifically adapted to and Robinson (1972)suggest thewebmay target insectswith variable
catch moths (Stowe 1986). Typical orbs are ineffective at retaining flight altitudes.
these prey because the scales covering a moth’s body detach upon The ladder-web spiders in the nephilid genera Herennia Thorell
contact with a web, allowing it to fall to safety (Eisner et al. 1964). 1877 (Robinson and Lubin 1979; Kuntner 2005) and Clitaetra Simon
The ladder-webs of the genus Scoloderus Simon 1887 are highly 1889 (Kuntner2006; Kuntnerand Agnarsson 2009), and thearaneids
effectivemoth-capturingdevices(Eberhard 1975; Stowe 1978). Onthe Cryptarauea atrihastula (Urquhart 1891) (Eorster and Eorster 1985)
other hand, the ladder-webs of another genus, Telaprocera Harmer and Telaprocera (Harmer 2009) build their webs almost exclusively
and Eramenau 2008, have been shown to be a response to space against tree trunks, hence we refer to them as arboricolous ladder-
limitation (Harmer 2009; Harmer and Herberstein 2009). However, webs. Webstructure varieswithin thearboricolous ladder-webgroup.
theimportanceofmothcaptureintheconstruction ofelongatedwebs Herenniaspeciescurve the web around the tree (Robinson and Lubin
in Telaprocerahasnotbeenexplored. Inthisstudyweinvestigateprey 1979)whiletheotherspeciesbuildplanarwebsslightlyoffset fromthe
capture in Telaprocera spiders for the first time. tree surface. The hub position varies from a central position (C.
Moth specialization occurs in several genera and is usually atrihastula, Telaprocera) to nearer the top [Herennia, Clitaetra).
associated with a reduction in the orb-web (reviewed in Stowe Evidenceindicatesthat theladder-websofTelaprocera(Harmer2009;
1986). The best-known example of web reduction for moth Harmer and Herberstein 2009), along with those of C. irenae
specialization occurs in bolas spiders (e.g. Mastophora Holmberg (Kuntner et al. 2008), are a response to building webs in space-
1876), which hunt using a single strand ofsilk with a sticky mass on limited conditions. As these spiders build exclusively against tree
the end and attract male moths within range by mimicking female trunks, theyarelimited in horizontal space forwebconstruction. The
pheromones (Eberhard 1977; Yeargan 1994). Extension of the orb- only way to increase capture area is to elongate the web vertically.
web to target specific prey is much lesscommon than web reduction. Whether or not the other arboricolous ladder-web species also
The exception is the ladder-web of the genus Scoloderus. Eberhard elongate their webs for this reason has yet to be tested.
(1975) suggested extreme elongation in ladder-webs assists in The differences in fine-scale web structure and web function (moth
retaining moths because as they tumble down the web they lose specialization vs. optimal area use) between aerial and arboricolous
sufficient scales to become entangled. Stowe (1978) confirmed ladder-webs suggest they are not convergent structures; however, a
Eberhard’s hypothesis by determining that the diet of S. cordatus moth-capturing function has not been ruled out for arboricolous
(Taczanowski 1879) consists ofalmost 70% moths. species. AsthehighlyelongatedwebstructureofScoloderusaidsthese
Ladder-websarebuilt byspiders in threedifferent orb-webfamilies spiders in catching moths, it is possible that the ladder-web structure
(Araneidae, Nephilidae and Tetragnathidae), yet we know remark- of arboricolous species secondarily confers an ability to retain
ably little about the foraging ecology ofthese spiders. Based on the intercepted moths. Among ladder-webs, only the prey ofthe aerially
microhabitat in which they are built, ladder-webs can be divided into building S. cordatus (moth specialist) and the arboricolous H.
twomain groupswith potentiallydifferent functions. The first group, papuana (generalist) have been surveyed, with moths making up less
which we here call aerial ladder-webs, includes the araneid genus than 70% and 10% oftheir diets respectively (Stowe 1978; Robinson
I Scoloderus (Eberhard 1975) and the New Guinean tetragnathid and Lubin 1979). Despite strong evidence for Telaprocera ladder-
Tyloridasp. Simon 1894 (Robinson and Robinson 1972). These webs webs being the result ofspace limitation (Harmer 2009; Harmer and
are built in open spaces among the vegetation. Spiders ofthese two Herberstein 2009), we cannot dismiss the possibility of a moth-
I genera build webs that may be over 1 m long (Robinson and capturingfunction in Telaprocera ladder-webswithout first surveying
Robinson 1972; Stowe 1978), although placement ofthe hub differs their prey. In this study we examined whether or not a high
betweenthetwo.ThehubofScoloderuswebsisattheextremebottom proportion ofthe prey retained by Telaprocera webs are moths. We
ofthewebandthehubofTyloridasp. isattheextremetop. Itremains also carried out preliminary experiments to see how long moths are
to beseen ifTylorida sp. is alsoa moth specialist, although Robinson retained and how farthey tumble in Telaprocera webs. IfTelaprocera
119
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ladder-webs are adapted for catching moths, we expected that moths *
wouldconstituteasignificant proportionoftheirnaturaldietandthat
a high proportion of moths that contacted the web would actually
become ensnared.
—
Telaprocemprey. ThepreyofT. inaiidaeHarmer&Framenau2008
and T. joamie Harmer& Framenau 2008 were surveyed in Famington
National Park, southeastern Queensland, Australia, in February and
July 2006, and March 2007. During the day, we searched for webs on
trees and haphazardly selected approximately 30 webs to be surveyed.
Since Telcipwcerci are nocturnal foragers, we placed a small colored
markerundereachwebsowecould relocateitat night, butthemarker
had to be removed following each night’s survey. This meant that we
may have sampled some webs more than once. However, the mean
(± SD)numberofpreyperwebpernightwas 1.18 ± 0.29, and noweb
caught more than three prey items in a night. Therefore, it is very
unlikely that a single web biased our results. For 6 h beginning at
sunset, weinspected eachweb for prey in acircuit-like fashion, so that
afterthelastwebwascheckedwestartedbackatthefirstweb(~ 1 hper
circuit). AshasbeenreportedforEriophoraedax(Ceballosetal. 2005),
preliminarysurveysalsoindicatedthatfewinsectsarecapturedbetween
midnightanddawn,soweceasedsurveysatmidnight. Werepeatedthe
—
surveythreetimesover 13mo,samplinginbothsummerandwinter.On Figure 1. Proportion of each prey order found in Telaprocera
several occasions, we opportunistically observed prey interception in webs and in traps. Double asterisks (**) indicate a significant
websduringtheday,butspidersdidnotrespondtotheseprey,sowedid difference in the proportion of prey when comparing all web prey
not systematicallysurveydiurnal preycapture. Wecollectedpreyitems with traps. A single asterisk (*) indicates a significance difference in
directlyfromwebsorfeedingspiderswithapairofsoft forceps, placed the proportion of prey when comparing only wrapped prey with
themintoavialof70%ethanol,andidentifiedthemtoorderandnoted traps. Comparisons were made using Fisher’s exact tests. Values
whetherornotthespiderhadwrappedtheprey.Foranalysis,wepooled above each bar are actual counts ofeach prey order.
prey from both T. maiidcie and T. joamie. We have previously shown
(Harmer2009) that the websofthesespeciesare indistinguishable, and
weassumedthatthetwospeciesexhibitsimilarpreyresponses.Voucher webs in frames made from a 50 cm length of PVC pipe cut in half
specimens are deposited at the Queensland Museum. lengthways. Frames were 9 cm in diameter and lined with mesh for
To compare the actual prey of Tehiprocera spiders with prey that the spiders to walk on (see Harmer and Herberstein 2009). We
was potentially available, we set up sticky traps on trees in similar removedthespiderafterit had built itsweb,andwe usedanewspider
positions as webs (as recorded by Harmer 2009). On each of the for each web tested. To test retention, we anaesthetized individual
nights we inspected webs for prey, we placed 16 traps outjust before moths (Plodia hiterpunctella; mean length 6.88 ± 0.77 mm) with CO2
sunset and collected them six hours after sunset (i.e., the same period and placed them directly on the web with the long axis ofthe body
webs were inspected). Sticky traps ofapproximately the same surface perpendicular to the capture threads (i.e., spanning several spiral
area as anadult Telaproceraweb(~ 300 cm“) weremade from an A5 turns), asclose to thetop as possible. We repeated this forfive moths
sheetofoverheadtransparencyfilmcoated inTangletrap(TheTangle in each offive T. maudae webs (« = 25). Care was taken to ensure a
Foot Company, USA). We pinned these traps to trees with a small fresh part of the web was used for each moth. Although it is not a
piece of wire that held them slightly off the bark, mimicking a very natural situation for moths to “wake up” in a web, we used this
Telaprocera web. We transferred prey on traps to vials containing method to eliminate any differences in the velocity with which prey
70% ethanol and later identified them to order. struck thewebandto standardize mothcontact with thestickyspiral.
We collected a total of 169 prey items from webs, 107 ofwhich the We then timed how long it took the moth to escape, from the time it
spiderhadwrapped,and273 preyitemsfromtraps.Preybelongedto 16 began struggling until it had either completely left the web or 1 min
different orders including insects, arachnids and isopods. Twenty-five hadelapsed. Afterward,wemeasuredthedistancethemothhadfallen
prey were unidentifiable as they had been partially digested by the down the web by measuring the length ofthe trail ofscales it left.
spiders. Weonlyincludedthemostcommontypesofprey(frequency> The median retention time ofmoths that escaped T. maudae webs
3)intheanalysesduetoverylownumbersofsomeorders.Comparisons was 2 s, range = 1-30 s. Four ofthe 25 moths did not escape after
between web and trap prey are presented in Figure 1. Diptera, 1 min. Themean (± SD) distance mothstumbled down the webswas
Coleoptera and Hymenoptera were the most common types ofprey in 4.9 ± 2.1 cm. There was no difference in the tumble distances of
both webs and traps, with Araneae, Hemiptera, Isopoda and moths that escaped from those that did not (Mann-Whitney t/-test:
Fepidopteramakingupsmall fractionsofthe total(Fig. 1). Wecarried U = 36.5, P = 0.711, —=21, Urcained = 4).
out twoseparateanalysescomparing theproportionofeach individual Discussion and conclusions. We found that Telaprocera spiders
prey order in webs to its proportion in traps using Fisher’sexact tests. catch a variety of prey orders with Diptera, Hymenoptera and
First, we compared prey in traps to all prey items collected from webs Coleopterabeingthemostcommon. Wealsofoundverylownumbers
for each order. Significantly more prey were found in webs than traps ofmoths in both webs and traps and that Telaprocera webs did not
for the orders Hemiptera {P < 0.001), Isopoda (P = 0.028) and function well at retaining moths. These results differ greatly from
Fepidoptera{P< 0.001). Wethencompared preyintrapstoonlythose those found for ScoloderiLs (Stowe 1978) and are likely due to
prey in webs that the spider had wrapped. We found a significant differences in web structure, microhabitat and foraging period
difference in the proportion of Diptera {P < 0.001), with many more between these genera. Our results suggest that moth capture has
flies in traps than webs. had little role in the evolution ofelongated webs in Telaprocera and
Moth retention. In addition to surveying T. inaudae prey, we also possiblyotherarboricolousladder-webspecies.Thisisconsistentwith
carried out preliminary observations ofmoth retention in T. inaudae previous findings that Telaprocera ladder-webs are elongated due to
webs. To do this, we allowed adult female T. maudae spiders to build space limitation (Harmer 2009; Harmer and Herberstein 2009).
HARMER & HERBERSTEIN—FUNCTIONAL DIVERSITY OF LADDER-WEBS 121
Mothscomprise<4%ofthedietofTelaprocemspidersinthisstudy, The difference in function between Telaprocera webs and Scolo-
which contrasts sharply with the almost 70% observed for S. cordatus deruswebs is perhapsdueto thevery different fine-scale architectures
(Stowe 1978).Althoughtherewereproportionatelymoremothsinwebs between these two ladder-web types. For example, the radials of
than traps, it is unlikely that this difference will have biological Scoloderus webs arecontorted into a parallel arrangement (Eberhard
significance due to the very low total number of moths over the 1975), whereas Telaprocera webs have a more typical radial
samplingperiod(sixinwebscomparedtozerointrapsinthreeweeksof arrangement (Harmer 2009). It is unclear whether this fine-scale
sampling). While moths could potentially be more important energet- difference helps to retain moths; however, web orientation is
icallyornutritionallythanotherprey,wecannotdrawanyconclusions potentially more important. Scoloderus aerial webs are nearly
on their dietary importance without first investigating the nutritional perfectly vertical, causing moths impacting from either direction to
valueofvariouspreytypes.Themostcommonpreyordersinbothwebs tumble down the web rather than falling out (Eberhard 1975).
and traps were Diptera, Coleoptera and Hymenoptera, although Telaprocera webs generally follow the slope ofthe tree on which they
Coleoptera and Hymenopteraprobablycontributed the mostbiomass. are built, and ifthe web is slanted a struggling moth will not fall into
Therewas nosignificantdifferencein theproportion oftheseorders in lower parts ofthe sticky spiral, but instead fall to safety. A further
websortrapswhenallpreywereincludedintheanalysis,indicatingthat possibility forthedifference in function isthat thecapturesilks ofthe
Telapwcerawebs are interceptingwhat is mostcommonly available. two genera differ in stickiness, thus resulting in different moth
Traps have been used extensively to assess the available prey of retention rates.
spiders(reviewedinEberhard 1990). However,therearedrawbacksin A final clue to the difference in function between aerial and
using traps to estimate available prey due to different biases between arboricolous ladder-webs is the difference in the frequency of web
traps and webs in the types and sizes of prey captured (Eberhard replacement and foraging period. Tylorida sp. and Scoloderus webs
1990). This point is illustrated in this study where we found (aerial ladder-webs) are built at night and always removed the next
significantly moredipterans in traps than webs when only comparing morning (Robinson and Robinson 1972; Eberhard 1975). On the
prey that had been wrapped by the spiders. This difference is likely other hand, Herennki, Clitaetra, Cryptamnea atrihastula and Tela-
due to the majority of unwrapped prey being tiny flies (< 1 mm in procera webs (arboricolous ladder-webs) are built at night but not
length). These flies are intercepted in webs, but they are not replaced for at least several days (Robinson and Lubin 1979; Forster
“available” to the spiders because the vibrations they produce when and Forster 1985; Kuntner 2006; Harmer 2009). This means that
struggling are likely to be below the spider’s response threshold or aerial ladder-webs are restricted to foraging for nocturnal prey such
because they are not energetically worthwhile fora spider to retrieve. as moths. Arboricolous ladder-webs can intercept prey both day and
However, spiders could still consume these small flies when recycling night (although their responsivenessto prey in theday may vary)and
the web if they do not escape beforehand. Additionally, our rate of so have access to a greater prey range.
web inspection (~ once per hour) could potentially have underesti- To conclude, the different forms of ladder-webs, both aerial and
mated the observed numbers of flies if small flies were caught and arboricolous, all share thecommon feature ofvertical elongation, yet
consumed between inspections. However, it is unlikely that spiders they appear to have divergent functions. Scoloderus webs are highly
biased the prey survey by consuming large numbers of small flies effective moth-capturing devices (Stowe 1978), while elongated
between inspections because we observed that they rarely attacked Telaprocera webs are the result of space limitation (Harmer 2009;
these small prey, although we can not completely rule this out. While Harmer and Herberstein 2009). It will be intriguing to see if the
therearelimitations incomparingpreycaptureinwebsand traps, the functional difference we observed between Telaprocera and Scolo-
lack of moths in webs in this study supports our conclusion that derus ladder-webs, paralleling their aerial versus arboricolous
Telaprocem are not specializing on these insects. microhabitats, holds for the other ladder-web building species.
Inourexperimentaltestsofmothretention,onlyfourofthe25moths
failedtoescape,andalmost60% ofmothsescaped in3 secondsorless. ACKNOWLEDGMENTS
Wthheilheubt,hisprceoyulidntsetrilclepbteedennoeuagrhttheimweefborexstpriedmeirtsiteos rmeaaychepsrceaypeclboesfeorteo We are very grateful to both Anne Wignall and Dinesh Rao for
spiders can reach them. However, data on spider attack speeds are their many long hours of assistance late at night in the field. Two
required before we can draw any conclusions. The mean tumble anonymous reviewers provided valuable feedback on the manuscript.
distance ofmoths was only ~ 25% ofweb length, and there was no The Department of Biological Sciences, Macquarie University,
difference in the tumble distances of caught or escaping moths, provided funding for this research.
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