Arms race of physical defences: Hooked trichomes of Macaranga ant-plants kill lycaenid caterpillars, but one specialist has a counter-defence

Arms race of physical defences: Hooked trichomes of Macaranga ant-plants kill lycaenid caterpillars, but one specialist has a counter-defence | bioRxiv /* */ /* */ <!-- <!-- /*! * yepnope1.5.4 * (c) WTFPL, GPLv2 */ (function(a,b,c){function d(a){return"[object Function]"==o.call(a)}function e(a){return"string"==typeof a}function f(){}function g(a){return!a||"loaded"==a||"complete"==a||"uninitialized"==a}function h(){var a=p.shift();q=1,a?a.t?m(function(){("c"==a.t?B.injectCss:B.injectJs)(a.s,0,a.a,a.x,a.e,1)},0):(a(),h()):q=0}function i(a,c,d,e,f,i,j){function k(b){if(!o&&g(l.readyState)&&(u.r=o=1,!q&&h(),l.onload=l.onreadystatechange=null,b)){"img"!=a&&m(function(){t.removeChild(l)},50);for(var d in y[c])y[c].hasOwnProperty(d)&&y[c][d].onload()}}var j=j||B.errorTimeout,l=b.createElement(a),o=0,r=0,u={t:d,s:c,e:f,a:i,x:j};1===y[c]&&(r=1,y[c]=[]),"object"==a?l.data=c:(l.src=c,l.type=a),l.width=l.height="0",l.onerror=l.onload=l.onreadystatechange=function(){k.call(this,r)},p.splice(e,0,u),"img"!=a&&(r||2===y[c]?(t.insertBefore(l,s?null:n),m(k,j)):y[c].push(l))}function j(a,b,c,d,f){return q=0,b=b||"j",e(a)?i("c"==b?v:u,a,b,this.i++,c,d,f):(p.splice(this.i++,0,a),1==p.length&&h()),this}function k(){var a=B;return a.loader={load:j,i:0},a}var l=b.documentElement,m=a.setTimeout,n=b.getElementsByTagName("script")[0],o={}.toString,p=[],q=0,r="MozAppearance"in l.style,s=r&&!!b.createRange().compareNode,t=s?l:n.parentNode,l=a.opera&&"[object Opera]"==o.call(a.opera),l=!!b.attachEvent&&!l,u=r?"object":l?"script":"img",v=l?"script":u,w=Array.isArray||function(a){return"[object Array]"==o.call(a)},x=[],y={},z={timeout:function(a,b){return b.length&&(a.timeout=b[0]),a}},A,B;B=function(a){function b(a){var a=a.split("!"),b=x.length,c=a.pop(),d=a.length,c={url:c,origUrl:c,prefixes:a},e,f,g;for(f=0;f<d;f++)g=a[f].split("="),(e=z[g.shift()])&&(c=e(c,g));for(f=0;f<b;f++)c=x[f](c);return c}function g(a,e,f,g,h){var i=b(a),j=i.autoCallback;i.url.split(".").pop().split("?").shift(),i.bypass||(e&&(e=d(e)?e:e[a]||e[g]||e[a.split("/").pop().split("?")[0]]),i.instead?i.instead(a,e,f,g,h):(y[i.url]?i.noexec=!0:y[i.url]=1,f.load(i.url,i.forceCSS||!i.forceJS&&"css"==i.url.split(".").pop().split("?").shift()?"c":c,i.noexec,i.attrs,i.timeout),(d(e)||d(j))&&f.load(function(){k(),e&&e(i.origUrl,h,g),j&&j(i.origUrl,h,g),y[i.url]=2})))}function h(a,b){function c(a,c){if(a){if(e(a))c||(j=function(){var a=[].slice.call(arguments);k.apply(this,a),l()}),g(a,j,b,0,h);else if(Object(a)===a)for(n in m=function(){var b=0,c;for(c in a)a.hasOwnProperty(c)&&b++;return b}(),a)a.hasOwnProperty(n)&&(!c&&!--m&&(d(j)?j=function(){var a=[].slice.call(arguments);k.apply(this,a),l()}:j[n]=function(a){return function(){var b=[].slice.call(arguments);a&&a.apply(this,b),l()}}(k[n])),g(a[n],j,b,n,h))}else!c&&l()}var h=!!a.test,i=a.load||a.both,j=a.callback||f,k=j,l=a.complete||f,m,n;c(h?a.yep:a.nope,!!i),i&&c(i)}var i,j,l=this.yepnope.loader;if(e(a))g(a,0,l,0);else if(w(a))for(i=0;i (function(w,d,s,l,i){w[l]=w[l]||[];w[l].push({'gtm.start':new Date().getTime(),event:'gtm.js'});var f=d.getElementsByTagName(s)[0];var j=d.createElement(s);var dl=l!='dataLayer'?'&l='+l:'';j.src='//www.googletagmanager.com/gtm.js?id='+i+dl;j.type='text/javascript';j.async=true;f.parentNode.insertBefore(j,f);})(window,document,'script','dataLayer','GTM-M677548'); Skip to main content Home About Submit ALERTS / RSS Search for this keyword Advanced Search New Results Arms race of physical defences: Hooked trichomes of Macaranga ant-plants kill lycaenid caterpillars, but one specialist has a counter-defence View ORCID Profile Ritabrata Chowdhury , View ORCID Profile Ulmar Grafe , View ORCID Profile Faizah Metali , View ORCID Profile Walter Federle doi: https://doi.org/10.1101/2025.01.28.635112 Ritabrata Chowdhury 1 Department of Zoology, University of Cambridge , United Kingdom Find this author on Google Scholar Find this author on PubMed Search for this author on this site ORCID record for Ritabrata Chowdhury For correspondence: rc855{at}cam.ac.uk Ulmar Grafe 2 Faculty of Science, Universiti Brunei Darussalam , Brunei Find this author on Google Scholar Find this author on PubMed Search for this author on this site ORCID record for Ulmar Grafe Faizah Metali 2 Faculty of Science, Universiti Brunei Darussalam , Brunei Find this author on Google Scholar Find this author on PubMed Search for this author on this site ORCID record for Faizah Metali Walter Federle 1 Department of Zoology, University of Cambridge , United Kingdom Find this author on Google Scholar Find this author on PubMed Search for this author on this site ORCID record for Walter Federle Abstract Full Text Info/History Metrics Supplementary material Preview PDF Abstract The co-evolution of insects and chemical plant defences has been described as an arms-race, but it is unclear if physical plant defences can produce similar outcomes. Here we report a previously unknown interaction from the mutualism between ants and Macaranga trees. Although Macaranga trees are well protected against herbivory by aggressive ants, caterpillars of the genus Arhopala (Lepidoptera: Lycaenidae) can feed on the leaves by appeasing the ants with nectar-like secretions. One ant-plant species, M. trachyphylla , bears hooked trichomes on its green surfaces. When placed on M. trachyphylla stems or petioles, Arhopala caterpillars associated with other Macaranga species ( A. major, A. dajagaka and A. zylda ) were quickly arrested by the sharp trichomes which pierced their cuticle, resulting in rapid loss of blood and death. In striking contrast, A. amphimuta caterpillars, which occur naturally on M. trachyphylla , could easily walk over the hooked trichomes without any injury. As hooked trichomes are a novel trait within Macaranga , this interaction provides an example of de novo evolution of a physical plant defence, which in turn has been overcome by a specialist herbivore. Our study suggests that physical plant defences can lead to evolutionary arms races similar to those for chemical defences. Introduction Plants and insects have coexisted for more than 400 million years and over this period, they have developed complex interactions which play a critical role in terrestrial ecosystems ( Bronstein et al. 2006 ; Endara et al. 2017 ; War et al. 2018 ). While some of these relationships are mutually beneficial, such as pollination or seed dispersal, the majority involve insects feeding of plants, and plants defending themselves against herbivory ( War et al. 2018 ). The mutual adaptation of chemical plant defences and insect herbivores has been described as an evolutionary arms-race that has led to the diversification of both insects and plants ( Ehrlich & Raven 1964 ; Endara et al. 2017 ). Do such arms-races also occur for physical defences? One of the physical defences of plants against herbivores are trichomes, hair-like appendages produced by the epidermis. Trichomes can protect against herbivory by limiting insect access to leaf or stem tissues ( Fordyce & Agrawal 2001 ; Kariyat et al. 2019 ; Kariyat et al. 2017 ), exposing insects to toxic or sticky substances ( Hanley et al. 2007 ; Wagner 1991 ) or puncturing the insect’s cuticle ( Gilbert 1971 ; Pillemer & Tingey 1976 ). Trichomes can also decrease the rate of tissue ingestion and thereby the herbivore’s growth ( Kariyat et al. 2019 ; Kariyat et al. 2017 ), and prevent insect oviposition or reduce the adhesion of eggs to the plant surface ( Haddad & Hicks 2000 ; Handley et al. 2005 ). Sharp hooked trichomes are considered one of the most effective forms of physical defence in plants. In Passiflora vines, they can injure or kill caterpillars by piercing their cuticle ( Cardoso 2008 ; Gilbert 1971 ). Similarly, hooked trichomes on the leaves of common bean ( Phaseolus vulgaris ) can injure insects in different parts of their body, leading to their death by haemolymph loss or starvation ( Pillemer & Tingey 1976 ; Szyndler et al. 2013 ; Xing et al. 2017 ). Some insect herbivores have in turn evolved adaptations to deal with trichomes. These adaptations can be morphological, such as elongated legs to avoid contact with the sticky heads of glandular trichomes ( Voigt et al. 2007 ) or tarsal hooks for anchoring to trichomes ( Medeiros & Boligon 2007 ). Insects can also adapt behaviourally by walking “on tiptoe” between trichomes ( Voigt et al. 2007 ), removing dense trichome covers before feeding on leaves ( Shelomi et al. 2010 ), or spinning silk mats to move on trichome-bearing surfaces without being punctured ( Rathcke & Poole 1975 ). Here we report an interaction involving trichomes as a physical defence in ant-associated trees of the paleotropical genus Macaranga (Euphorbiaceae). Most Macaranga species are myrmecophilic and protect themselves against herbivory by attracting non-specific foraging ants, but ca. 30 species in South-East Asia are myrmecophytic and permanently house specialised ant partners nesting in their hollow stems. Although the ants efficiently keep away most herbivores, several species of Arhopala caterpillars (Lepidoptera: Lycaenidae) have outwitted the ants’ defences by providing them with nectar-like secretions from their myrmecophilous organs, and feed on Macaranga leaves ( Maschwitz et al. 1984 ; Shimizu-Kaya et al. 2015 ). One Macaranga ant-plant species in Borneo, M. trachyphylla , has stems and petioles densely covered by hooked trichomes, giving the surfaces a sandpaper-like feel. To our knowledge, M. trachyphylla is the only one of more than 300 described Macaranga species for which this trait is known ( Whitmore 1975 ). The functional significance of these trichomes is still unknown. We therefore investigated the effect of M. trachyphylla trichomes on Arhopala caterpillars. Results A. major caterpillars attempting to walk on petioles or stems of M. trachyphylla were rapidly arrested by the sharp hooked trichomes ( Fig.1A,B ). As soon as they became stuck on a trichome, the caterpillars could only move about 1-2mm further. The sharp trichome tips pierced the caterpillars’ prolegs and/or abdomen and thorax ( Fig.1C,D ; Fig.2B,C ; Supplementary Videos S1,S2), leading to the oozing out and rapid loss of haemolymph. All A. major caterpillars of the 1 st to 4 th instar (n=20) died very quickly, with death usually occurring within half an hour of the injury ( Fig.3 ). The only A. major caterpillar not immediately killed on M. trachyphylla stems was from the final (5 th ) instar (1 out of 5 caterpillars; Fig.3 ); it was also arrested by the trichomes, but as the piercing occurred only in the prolegs, it did not die as a result of the interaction. Download figure Open in new tab Fig 1: A,B) Scanning electron micrographs of hooked trichomes on the petiole (A) and stem (B) of M. trachyphylla ; C) Arhopala major caterpillar (2nd instar) injured by M. trachyphylla trichomes, with haemolymph oozing from the wounds (arrows), D) same as C, but 4th instar; E) 1st-2nd instar A. dajagaka caterpillar, with haemolymph oozing from the wounds (arrow); and F) 3 rd instar A. zylda caterpillar, showing proleg footpad pierced by a hooked trichome. Download figure Open in new tab Fig 2: A-C) Scanning electron micrographs of ventral side of a 3 rd -4 th instar A. major caterpillar after walking on the trichome-bearing stem surface of M. trachyphylla ; B) & C) magnified images showing several broken trichomes (arrows in B) on the surface of the cuticle, and a hooked trichome piercing the cuticle of the 3 rd left proleg footpad (arrow in C). Download figure Open in new tab Fig 3: Effect of hooked trichomes on petioles and stems of M. trachyphylla on A. major and A. amphimuta caterpillars. We found very similar effects in A. zylda and A. dajagaka caterpillars, although fewer specimens were available from these species ( Fig.1E,F ). All the caterpillars were arrested by the trichomes; A. dajagaka died due to loss of haemolymph, whereas the A. zylda caterpillars (Supplementary Video S3) could not move more than 1-2 mm, but did not die as they were only injured in their prolegs. In striking contrast, A. amphimuta caterpillars of all instars were able to move easily over the hooked trichomes on M. trachyphylla stems and petioles, and no injuries were observed in any of the caterpillars ( Fig.3 ; Supplementary Video S4). We observed that the prolegs or the body wall often caught and pulled on the hooked trichomes, but the trichomes did not puncture the cuticle. The caterpillars sometimes raised their prolegs high to free them from the trichomes, but we also observed this behaviour in the other Arhopala species tested. A. amphimuta caterpillars were always able to free their prolegs from the trichomes without being pierced. In contrast to M. trachyphylla stems and petioles, the leaves of M. trachyphylla were harmless for all the Arhopala species, probably because they contained a lower density of hooked trichomes; all caterpillars could walk on them without being injured. We tested whether A. major caterpillars would be able to cope with the mutualistic Crematogaster plant-ants living on M. trachyphylla trees. When placed on the youngest leaves, the caterpillars were mostly ignored or attended by the ants (52% and 34% of caterpillar-ant interactions, respectively); they were only occasionally attacked (14% of interactions). However, when placed on the stem, all A. major caterpillars (n=10) became stuck in the trichomes within only 5 minutes, were punctured by them and started to lose haemolymph. Once the caterpillars were injured, the ants’ behaviour changed; there were quickly many ants that attacked and removed the caterpillar (n=10), probably due to the injury and because it was no longer able to use its myrmecophilous organs. Discussion Our results show that the hooked trichomes of M. trachyphylla act as a powerful physical defence against A. major, A. zylda and A. dajagaka caterpillars, and that the Arhopala species naturally occurring on M. trachyphylla, A. amphimuta , is resistant to them. The sharp trichomes pierce the caterpillars’ cuticle, leading to rapid blood loss and death mostly occurring within minutes. The action of the hooked trichomes of M. trachyphylla against Arhopala caterpillars and the presence of a species that is immune to this physical defence represent a striking evolutionary convergence with the interaction of Passiflora trichomes and Heliconius caterpillars discovered by Gilbert (1971) . Heliconius caterpillars are also stopped, punctured and killed by the sharp hooked trichomes on Passiflora leaves, and there is one species, H. charithonia , that is resistant and capable of feeding on trichome-bearing plants ( Cardoso 2008 ; MacDougal 1994 ). However, the Arhopala-M. trachyphylla interaction discovered here differs in some important ways from the Passiflora-Heliconius system: Firstly, M. trachyphylla trees are ant-plants permanently inhabited by colonies of Crematogaster ants. These ants provide a powerful biotic defence that the herbivorous Arhopala caterpillars have to cope with. The five closely related Arhopala species associated with Macaranga (which form the amphimuta amphimuta subgroup, Megens et al. 2005 ), each occur on a non-overlapping set of Macaranga species. It is still unclear whether this host specificity is based on ant defences, or on chemical or physical plant traits. We found that A. major caterpillars were not strongly rejected by the plant-ants living on M. trachyphylla , and similar observations have been reported for A. zylda and A. dajagaka ( Inui et al. 2015 ). It is also unlikely that the specificity of A. major for M. gigantea and absence on M. trachyphylla is due to defensive plant chemicals, because A. major caterpillars can feed on M. trachyphylla leaves and successfully pupate ( Shimizu-Kaya et al. 2013 ). Our findings show that the absence of A. major, A. zylda and A. dajagaka caterpillars on M. trachyphylla can be fully explained by the sharp, hooked trichomes on the stems and petioles. A second difference to Passiflora is that the trichome defence of M. trachyphylla is restricted to the petioles and stem. A. major caterpillars can feed on M. trachyphylla leaves in the laboratory ( Shimizu-Kaya et al. 2013 ), but under natural conditions, the trichomes on petioles and stem are sufficient to prevent them from completing their development. Assuming an A. major egg is laid on a young leaf of M. trachyphylla , the emerging young caterpillar will at some point have to move to the next leaf via the petiole and stem. In this process, the caterpillar will be trapped and killed by the trichomes. It has long been proposed that there is a co-evolutionary arms race between the chemical defences of plants and insect counter-adaptations ( Ehrlich & Raven 1964 ; Endara et al. 2017 ; Howe & Jander 2008 ). Until now, it is unclear whether physical defences can trigger similar arms-races. The interaction of hooked trichomes in M. trachyphylla and Arhopala caterpillars might represent one of the first examples of such an arms-race. As the main anti-herbivore defence of Macaranga trees via their ant partners has already been overcome by Arhopala caterpillars ( Inui et al. 2015 ; Maschwitz et al. 1984 ), the isolated occurrence of hooked trichomes in M. trachyphylla suggests that they evolved as a new defence to cope with heavy Arhopala herbivory. In turn, the ability of A. amphimuta caterpillars to walk over the hooked trichomes of M. trachyphylla without sustaining any injuries could represent an adaptation in response to this new defence. However, this arms-race scenario is still speculative, as the detailed mechanisms underlying the resistance of A. amphimuta are still unknown, and it is equally possible that the relevant traits evolved as pre-adaptations for some other functions. A. amphimuta caterpillars occur not only on M. trachyphylla but also on several other Macaranga host plants that are free of hooked trichomes. Since M. trachyphylla is endemic to Borneo, populations of A. amphimuta living on M. bancana and M. hullettii on the Malay peninsula have never encountered hooked trichomes. Future research on these populations could shed light on whether the resistance of A. amphimuta to hooked trichomes is indeed a counter-adaptation or a pre-adaptation that has allowed this species to survive on M. trachyphylla . Methods Field site Arhopala caterpillars associated with Macaranga trees were studied in the Andulau Forest Reserve and the Ulu Temburong National Park in Brunei from May to June 2023 and from July to September 2024. A. major caterpillars were collected from M. gigantea trees (n=25), A. amphimuta caterpillars from M. bancana (n=17), M. trachyphylla (n=5), M. hullettii (n=4) and M. aëtheadenia (n=1; to our knowledge, this is the first report of M. aëtheadenia as host plant of A. amphimuta). A. dajagaka was collected from M. rufescens (n=1), and A. zylda from M. beccariana (n=3). Trichome morphology The morphology of hooked trichomes from leaves, stems and petioles of M. trachyphylla was studied under a Leica EZ4 stereomicroscope (Leica Microsystems, Wetzlar, Germany) and using scanning electron microscopy. For electron microscopy, leaf, petiole and stem samples were first fixed overnight in formalin-alcoholic solution (4% v/v formaldehyde, 70% v/v ethanol), followed by gradual dehydration in an ethanol series (70%, 90% and absolute ethanol). The samples were then dried in a Quorum E3100 critical point dryer, sputter-coated with 20 nm of Platinum (Quorum K575X, Quorum Technologies Ltd., East Grinstead, UK) before viewing them under the scanning electron microscope (Tescan MIRA3 FEG; TESCAN UK Ltd., Cambridge, UK) at 5eV. Effect of hooked trichomes on Arhopala caterpillars Observations of caterpillars placed on leaves, petioles and stems of M. trachyphylla were made in Brunei under a Leica EZ4 stereomicroscope (Leica Microsystems, Wetzlar, Germany) and recorded with the camera of a OnePlus 11R mobile phone (OnePlus Technology Co., Ltd, China) attached to the microscope by an adapter (Celestron 81035). 25 A. major caterpillars were studied (n=10 1 st -2 nd instar, n=10 3 rd -4 th instar and n=5 5 th instar and prepupa), as well as 27 A. amphimuta caterpillars (n=10 1 st -2 nd instar, n=10 3 rd -4 th instar and n=7 5 th instar and prepupa), three instar A. zylda (n=1 3 rd , n=1 4 th instar and n=1 5 th instar) and one 1 st -2 nd instar A. dajagaka. Each caterpillar was carefully placed on the surface using soft tweezers and then observed and video-recorded for 10 mins under the stereo microscope. One 3 rd -4 th instar caterpillar of A. major was freeze-dried after interacting with hooked trichomes on M. trachyphylla and viewed under the scanning electron microscope (see above) to visualise details of injuries. Ant behaviour towards Arhopala caterpillars Previous work showed that A. major caterpillars are able to feed on M. trachyphylla leaves under ant-free conditions in the laboratory, where they reached pupation at a rate even higher than on leaves of their natural host M. gigantea ( Shimizu-Kaya et al. 2013 ). We therefore tested whether A. major caterpillars are accepted by the Crematogaster plant-ants living on M. trachyphylla . The ants’ behavioural responses were studied by placing A. major caterpillars on ant-inhabited M. trachyphylla plants (as in Inui et al. 2015 ). 2 nd , 3 rd or 4 th instar A. major caterpillars were collected from M. gigantea in the field and kept on young ant-free leaves of their host plant in a plastic container in the laboratory for up to 2 days before the introduction. For the experiments, young M. trachyphylla trees of 1.5–2.0 m height with low herbivory damage were chosen and one caterpillar was placed on the abaxial surface of the youngest or second-youngest visible leaf of the tree. The ants’ responses to the introduced larva were recorded for 10 min after the larva was approached for the first time by a worker of the resident ant colony. The reactions of ants that approached the caterpillar were divided into the following three categories (only one interaction was scored per ant visiting the leaf): 1) ignoring: no ants attacked or touched the caterpillar; 2) attending: ants touched the caterpillar without biting near the myrmecophilous glands on the posterior-dorsal side and sometimes harvested nectar; 3) attacking: ants bit the caterpillar. Each caterpillar and each ant colony (tree) were only used once. At the end of the trials, the caterpillar, if not already killed by the ants, was placed on the first internode of the stem and the caterpillar’s movements and ant behaviour were observed qualitatively for a further 10 minutes. Author contributions Conceptualization: RC, WF; Methodology, Investigation and Visualization: RC; Supervision: WF, UG, FM; Writing – original draft: RC; Writing – review & editing: RC, WF, FM, UG Competing interests: Authors declare that they have no competing interests Supplementary Video legends Supplementary Video S1: 2 nd instar Arhopala major caterpillar being injured by M. trachyphylla trichomes, with haemolymph oozing from the wound Supplementary Video S2: 3 rd instar A. major caterpillar being injured by M. trachyphylla trichomes, with haemolymph oozing from the wound Supplementary Video S3: 3 rd instar A. zylda caterpillar, showing proleg footpad being pierced by a hooked trichome Supplementary Video S4: 3 rd instar A. amphimuta caterpillar walking over hooked trichomes on M. trachyphylla stem without being injured Acknowledgements We would like to thank Mr Federick Valentino bin Yahau for his assistance during this study and Dr Heather Greer, Department of Chemistry, University of Cambridge, for her help with Scanning Electron Microscopy. RC was funded by R. O. Whyte PhD Studentship and the Trinity Henry Barlow Studentship from the University of Cambridge, UK, the Varley-Gradwell Travelling Fellowship in Insect Ecology from the University of Oxford, UK, the Zoology Fieldwork Fund from the University of Cambridge, UK, and the Professor Hering Memorial Research Fund from the British Entomological and Natural History Society, UK. Furthermore, we would like to thank the Faculty of Science, and the Kuala Belalong Field Studies Centre, Universiti Brunei Darussalam for logistical support, the Forestry Department in Brunei for issuing the forest entry permits, collection permits and export permits and the Department of Agriculture and Agrifood, Brunei for issuing the phytosanitary certificate. References ↵ Bronstein , J. L. , Alarcón , R. & Geber , M. 2006 The evolution of plant-insect mutualisms . New Phytol . 172 , 412 – 428 . OpenUrl CrossRef PubMed Web of Science ↵ Cardoso , M. Z. 2008 Herbivore handling of a plant’s trichome: the case of Heliconius charithonia (L.) (Lepidoptera: Nymphalidae) and Passiflora lobata (Killip) Hutch. (Passifloraceae) . Neotropical Entomology 37 , 247 – 252 . OpenUrl CrossRef PubMed ↵ Ehrlich , P. R. & Raven , P. H. 1964 Butterflies and plants: a study in coevolution . Evolution 18 , 586 – 608 . OpenUrl CrossRef Web of Science ↵ Endara , M.-J. , Coley , P. D. , Ghabash , G. , Nicholls , J. A. , Dexter , K. G. , Donoso , D. A. , Stone , G. N. , Pennington , R. T. & Kursar , T. A. 2017 Coevolutionary arms race versus host defense chase in a tropical herbivore–plant system . Proceedings of the National Academy of Sciences 114 , E7499 – E7505 . OpenUrl Abstract / FREE Full Text Federle , W. , Maschwitz , U. , Fiala , B. , Riederer , M. & Hölldobler , B. 1997 Slippery ant-plants and skilful climbers: Selection and protection of specific ant partners by epicuticular wax blooms in Macaranga (Euphorbiaceae) . Oecologia 112 , 217 – 224 . OpenUrl CrossRef PubMed Web of Science Fiala , B. , Grunsky , H. , Maschwitz , U. & Linsenmair , K. E. 1994 Diversity of ant-plant interactions: protective efficacy in Macaranga species with different degrees of ant association . Oecologia 97 , 186 – 192 . OpenUrl CrossRef PubMed Web of Science ↵ Fordyce , J. A. & Agrawal , A. A. 2001 The role of plant trichomes and caterpillar group size on growth and defence of the pipevine swallowtail Battus philenor . J. Anim. Ecol . 70 , 997 – 1005 . OpenUrl CrossRef ↵ Gilbert , L. E. 1971 Butterfly-plant coevolution: has Passiflora adenopoda won the selectional race with Heliconiine butterflies? Science 172 , 585 – 586 . OpenUrl Abstract / FREE Full Text ↵ Haddad , N. M. & Hicks , W. M. 2000 Host pubescence and the behavior and performance of the butterfly Papilio troilus (Lepidoptera: Papilionidae) . Environment. Entomol . 29 , 299 – 303 . OpenUrl CrossRef ↵ Handley , R. , Ekbom , B. & ígren , J. 2005 Variation in trichome density and resistance against a specialist insect herbivore in natural populations of Arabidopsis thaliana . Ecol. Entomol . 30 , 284 – 292 . OpenUrl CrossRef ↵ Hanley , M. E. , Lamont , B. B. , Fairbanks , M. M. & Rafferty , C. M. 2007 Plant structural traits and their role in anti-herbivore defence . Perspectives in Plant Ecology, Evolution and Systematics 8 , 157 – 178 . OpenUrl CrossRef ↵ Howe , G. A. & Jander , G. 2008 Plant immunity to insect herbivores . Annual Review of Plant Biology 59 , 41 – 66 . OpenUrl CrossRef PubMed Web of Science ↵ Inui , Y. , Shimizu-kaya , U. , Okubo , T. , Yamsaki , E. & Itioka , T. 2015 Various chemical strategies to deceive ants in three Arhopala species (Lepidoptera: Lycaenidae) exploiting Macaranga myrmecophytes . PLoS ONE 10 , e0120652 . OpenUrl CrossRef PubMed ↵ Kariyat , R. R. , Raya , C. E. , Chavana , J. , Cantu , J. , Guzman , G. & Sasidharan , L. 2019 Feeding on glandular and non-glandular leaf trichomes negatively affect growth and development in tobacco hornworm (Manduca sexta) caterpillars . Arthrop. Plant Interact . 13 , 321 – 333 . OpenUrl CrossRef ↵ Kariyat , R. R. , Smith , J. D. , Stephenson , A. G. , De Moraes , C. M. & Mescher , M. C. 2017 Non-glandular trichomes of Solanum carolinense deter feeding by Manduca sexta caterpillars and cause damage to the gut peritrophic matrix . Proc. R. Soc. B 284 , 20162323 . OpenUrl CrossRef PubMed ↵ MacDougal , J. M. 1994 Revision of Passiflora subgenus Decaloba section Pseudodysosmia (Passifloraceae) . Systematic Botany Monographs 41 , 1 – 146 . OpenUrl CrossRef ↵ Maschwitz , U. , Schroth , M. , Hänel , H. & Pong , T. Y. 1984 Lycaenids parasitizing symbiotic plant-ant partnerships . Oecologia 64 , 78 – 80 . OpenUrl CrossRef PubMed Web of Science ↵ Medeiros , L. & Boligon , D. S. 2007 Adaptations of two specialist herbivores to movement on the hairy leaf surface of their host, Solanum guaraniticum Hassl (Solanaceae) . Revista Brasileira de Entomologia 51 , 210 – 216 . OpenUrl CrossRef ↵ Megens , H.-J. , de Jong , R. & Fiedler , K. 2005 Phylogenetic patterns in larval host plant and ant association of Indo-Australian Arhopalini butterflies (Lycaenidae: Theclinae) . Biol. J. Linn. Soc . 84 , 225 – 241 . OpenUrl CrossRef ↵ Pillemer , E. & Tingey , W. 1976 Hooked trichomes: A physical plant barrier to a major agricultural pest . Science 193 , 482 – 484 . OpenUrl Abstract / FREE Full Text ↵ Rathcke , B. J. & Poole , R. W. 1975 Coevolutionary race continues: butterfly larval adaptation to plant trichomes . Science 187 , 175 – 176 . OpenUrl Abstract / FREE Full Text ↵ Shelomi , M. , Perkins , L. E. , Cribb , B. W. & Zalucki , M. P. 2010 Effects of leaf surfaces on first-instar Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) behaviour . Australian Journal of Entomology 49 , 289 – 295 . OpenUrl CrossRef ↵ Shimizu-Kaya , U. , Kishimoto-Yamada , K. & Itioka , T. 2015 Biological notes on herbivorous insects feeding on myrmecophytic Macaranga trees in the Lambir Hills National Park, Borneo . Contributions from the Biological Laboratory Kyoto University 30 , 85 – 125 . OpenUrl ↵ Shimizu-Kaya , U. , Okubo , T. , Inui , Y. & Itioka , T. 2013 Potential host range of myrmecophilous Arhopala butterflies (Lepidoptera: Lycaenidae) feeding on Macaranga myrmecophytes . J. Nat. Hist . 47 , 2707 – 2717 . OpenUrl CrossRef ↵ Szyndler , M. W. , Haynes , K. F. , Potter , M. F. , Corn , R. M. & Loudon , C. 2013 Entrapment of bed bugs by leaf trichomes inspires microfabrication of biomimetic surfaces . J. R. Soc. Interface 10 . ↵ Voigt , D. , Gorb , E. & Gorb , S. 2007 Plant surface-bug interactions: Dicyphus errans stalking along trichomes . Arthrop. Plant Interact . 1 , 221 – 243 . OpenUrl CrossRef ↵ Wagner , G. J. 1991 Secreting glandular trichomes: more than just hairs . Plant Physiol . 96 , 675 – 679 . OpenUrl Abstract / FREE Full Text ↵ War , A. R. , Taggar , G. K. , Hussain , B. , Taggar , M. S. , Nair , R. M. & Sharma , H. C. 2018 Plant defence against herbivory and insect adaptations . AoB PLANTS 10 , ply037 . OpenUrl ↵ H. K. Airy-Shaw Whitmore , T. C. 1975 Macaranga Thou . In The Euphorbiaceae of Borneo , vol. 4 (ed. H. K. Airy-Shaw ), pp. 140 – 159 . London: HMSO (Her Majesty’s Stationery Office ). OpenUrl ↵ Xing , Z. , Liu , Y. , Cai , W. , Huang , X. , Wu , S. & Lei , Z. 2017 Efficiency of trichome-based plant defense in Phaseolus vulgaris depends on insect behavior, plant ontogeny, and structure . Frontiers in Plant Science 8 , 2006 . OpenUrl CrossRef PubMed View the discussion thread. Back to top Previous Next Posted January 29, 2025. Download PDF Supplementary Material Email Thank you for your interest in spreading the word about bioRxiv. 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